Evaporitic source rocks: mesohaline responses to cycles of ...haline in saline brines and the...

Evaporitic source rocks: mesohaline responses to cyclesof “famine or feast” in layered brines

JOHN K. WARREN

International Master Program in Petroleum Geoscience, Department of Geology, Faculty of Science, ChulalongkornUniversity, 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 sedimentsbeneath adensity-stratifiedmass of salinewaterwhere layeredhydrologies are subject tooscillations in salinity and brine level. Organic matter is not produced at a constant ratein such systems; rather, it is generated in pulses by a halotolerant community inresponse to relatively short times of less stressful conditions (brackish to mesohaline)that occur in the upper part of the layered hydrology. Accumulations of organic mattercan occur in any layered brine lake or epeiric seaway when an upper less-saline watermass forms on top of nutrient-rich brines, or inwetmudflats wherever waters freshen inand above the uppermost few millimetres of a microbial mat. A flourishing communityof halotolerant algae, bacteria and archaeal photosynthesizers drives the resultingbiomass bloom. Brine freshening is a time of “feast” characterized by very high levelsof organic productivity. In a stratified brine column (oligotrophic and meromictic) thetypical producers are planktonic algal or cyanobacterial communities inhabiting theuppermesohaline portion of the stratifiedwatermass. Inmesohaline holomicticwaters,where light penetrates to the water bottom, the organic-producing layer is typically theupper algal and bacterial portion of a benthic laminated microbialite characterized byelevated 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 columnand/or the enhanced construction of benthicmicrobialmats in regionswhere freshenedwaters reach the hypersaline base of the column. With the end of the freshening event,ongoing intensely arid conditions mean that salinity, temperature and osmotic stressincrease rapidly in thepreviously freshenedwatermass. This leads to a time ofmass die-off of the once flourishing mesohaline community (“famine”). First, these increasinglysalty waters no longer support haloxene forms. Then, halotolerant life dies back, andfinally by the halite precipitation stage, only a few halophilic archaea and bacteriaremain in the brine column (typically acting as heterotrophs and fermenters). Repeatedpulses 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 orfeast” 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-filledperennial saline lacustrine basins; (4) closed seafloor depressions in halokinetic deep-water marine slope and rise terrains. An inherently restrictive hydrologymeans that thesame mesohaline settings show a propensity to evolve into regions characterized bythe accumulation of widespread evaporite salts. If this happens soon after deposition ofa layer of organic-rich sediment there is an increased likelihood of evaporite pluggingin the source-rock layer, this in-turn decreases expulsion efficiency anddowngrades thelaminite bed’s ability to act as a prolific source rock.

Keywords: Oil and gas, source rocks, halobiota, hypersaline, salinity

� 2011 International Association of Sedimentologists and published for them by Blackwell Publishing Ltd 317

Int. Assoc. Sedimentol. Spec. Publ. (2011) 43, 315–392

INTRODUCTION

Back in 1988, Evans & Kirkland made the observa-tion that some 50% of the world’s oil may havebeen sourced in evaporitic carbonates. Heresy ornot, the notion that much of the oil sealed byevaporite salts may also have also been sourcedin sediments deposited in earlier less saline, butstill related, evaporitic (mesohaline) conditions, isworthy of consideration. The association betweensaline waters, the accumulation of organic-richsediments and the evolution of the resultingevaporitic carbonates into source rocks has beennoted by many, including: Woolnough (1937),Sloss (1953), Moody (1959), Dembicki et al.(1976), Oehler et al. (1979), Malek-Aslani (1980),Kirkland and Evans (1981), Hite et al. (1984),Jones (1984), Eugster (1985), Sonnenfeld (1985),ten Haven et al. (1985), Warren 1986, 2006,Busson (1988), Evans & Kirkland (1988), Edgell(1991), Hite & Anders (1991), Beydoun (1993),Benali et al. (1995), Billo (1996), Carroll (1998) andSchreiber et al. (2001). The current paper draws onmaterial and references discussed in greater detailin Warren (2006).

As long ago as the middle of the last century,Weeks 1958, 1961 emphasized the importanceof evaporites as caprocks to major hydrocarbonaccumulations.Weeks 1958, 1961 pointed out thatmany of the cycles of deposition that involveorganic-rich carbonate marls or muds also endwith evaporites.Manyauthors havenoted the asso-ciation of Type I–II hydrogen-prone kerogens inevaporitic source rocks and related their occur-rence to the ability of1 halotolerant photosyntheticalgae and cyanobacteria to flourish in saline set-tings (Fig. 1A). Such kerogens tend to be oil-pronerather than gas prone (Fig. 1B). This paper exam-ines chemical pathways and the conditions thatfavour various species that live in hypersalineenvironments. It compares modern saline settingswith ancient systems and attempts to define thoseancient saline settings that facilitated depositionof organic matter and subsequent evaporiticsource rocks.

First, usage of the terms hypersaline and meso-haline in saline brines and the associated mineralprecipitates is defined (Table 1). For seawater-derived and thalassic (seawater-like) brines the

use of the term “hypersaline” encompasses allwaters more saline than seawater (mesohaline,penesaline and supersaline). There is an associ-ated predictable suite of evaporite minerals, start-ing with carbonate (usually aragonite) in modernmesohaline waters, and evolving through gypsumand halite in penesaline waters, into bitterns fromsupersaline waters. However, ionic proportions inseawater have changed over time (Warren 2006).Accordingly, some ancient evaporite primary car-bonates were dolomitic, especially in the Precam-brian (although reflux dolomite has always beena widespread early diagenetic evaporite precipi-tate), and Archaean water probably precipitateda trona-halite-dominated set of salts rather then thehalite-gypsum salts of the Phanerozoic.

Bittern salts frommodern seawater concentratesshow a carnallite-MgSO4 association and a pro-pensity to accumulate aragonite in the early stagesof concentration, as they did also in the Permian

Oil-generating kerogen(sapropelic)

(Type I and II)

Gas-generating kerogen(humic)(Type III)

20

50

100

150

200

Tem

pera

ture

(ºC

)

ThermalCH4

ThermalCH4

C2H6+CO2 CO2

H2S H2S

N2 N2

Relative yield of gas from organic matterin fine-grained sediments

Sapropelicsource

Humicsource

Diagenesis(Eogenesis)

Ro<0.5%

Catagenesis0.5%<Ro<2.0%

Metagenesis2.0%<Ro<4.0%

A

B

BacterialCH4 CH4

Bacterial

Fig. 1. Organic matter and source rocks. (A) Molecularstructure of typical oil-generating (sapropelic) and gas-generating (humic) organic matter showing the greater pre-ponderance of long-chain hydrocarbons in the sapropelicmaterial (after Hunt, 1996). (B) Relative volumes of gasesand liquids derived from a sapropelic and a humic sourcerock (after Hunt, 1996). Evaporitic source rocks tend to besapropelic and contain less iron as a reductant so they arealso likely to generate more H2S.

1 (seeGlossary at the endof this article for explanation of thespecialist terminology used herein).

318 J. K. Warren

(icehouse climate mode). Bitterns at other times inthe Phanerozoic (greenhouse climate mode) tendto lack the MgSO4 minerals and have a propensityto form Mg-calcites in the mesohaline phase.

Use of the term hypersaline inmodern continen-tal (non-marine) waters is much less well definedand is variably applied to waters with total dis-solved salt contents (TDS) that are more salinethan 3 to 5‰. Nonmarine or continental waterscan have ionic proportions considerably differentto seawater (athalassic), and so a broader rangeof minerals can precipitate at all stages of brineconcentration.

METABOLISM IN PRODUCERSAND CONSUMERS

Cyanobacteria and algae are the dominant pri-mary producers in most mesohaline waters, alongwith lower and varying inputs from the higherplants and photosynthesizing bacteria. Algae andcyanobacteria typically make up the bulk of theplanktonic biomass in the upper layer of a strati-fied mesohaline brine column and construct theupper parts of microbial mats in oxygenated set-tings where light penetrates to the water bottom.Cyanobacteria are prokaryotal (cell lacks anucleus) bacteria and, like eukaryotic (cell withnucleus) algae and higher plants, are photoauto-trophic and require oxygen to photosynthesize.The typical aerobic photosynthetic reaction for allthree groups is:

CO2 þ 2H2O ¼ CH2OþH2OþO2 ð1ÞThat is, carbon dioxide and water react in thepresence of chlorophyll and sunlight to form car-bohydrate plus water plus oxygen.

All aerobic photosynthesizing organisms con-tain the pigments chlorophyll-a and phycobilinand use water as their electron source in reactionsthat generate oxygen. Chlorophyll-a is a greenpigment that absorbs red and blue-violet light,hence the typical green colour of photosynthesi-zers (Fig. 2A, B). It is made up of molecules thatcontain a porphyrin ‘head’ and a phytol ‘tail’(Fig. 2A). The polar (water-soluble) head is madeup of a tetrapyrrole ring and a magnesium ioncomplexed to the nitrogen atoms of the ring, itsphytol tail typically extends into the lipid layer ofthe thylakoid membrane. Phycobilisomes (phyco-cyanin, phycoerythrin) are proteins that absorblight of more energetic wavelengths than chloro-phyll and are widespread pigments in the cyano-bacteria and red algae (Fig. 2B). Their presenceallows some members of the halotolerant com-munity to photosynthesize into deeper brine andsediment depths, where light with longer wave-lengths is less transmitted and therefore less avail-able directly to chlorophyllic photosynthesizers(blue-green spectrum). Phycobilisome moleculesare linear tetrapyrroles and are structurally relatedto chlorophyll-a, but lack the phytol side chainand the magnesium ion. In chlorophyll-richoxygen-evolving reaction centres in a cell (chlor-oplasts) the phycobilisomes help transmit photicenergy and in cyanobacteria they are located inchloroplasts in an extensive, intracellular systemof flattened, membranous sacs, called thylakoids,the outer surfaces of which are studded withregular arrays of phycobilisome granules. Cyano-bacteria are the only prokaryotes that containchlorophyll-a in their chloroplast and so showstrong affinity with the algae and the greenplants. In the pre-genomic era of microbial studiesthis meant they were typically classified as

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

Brine Stage Mineral precipitate Salinity(‰)

Degree ofevaporation

Water loss(%)

Density(g cm�3)

Brackish None <35 <1 0 1.000–1.040Normal marine

seawaterAlkaline earth carbonates

(aragonite, Mg-calcite)35 1 0 1.040

Hypersaline Mesohalineor vitahaline

Alkaline earth carbonates(aragonite, Mg-calcite,dolomite)

35–140 1–4 0–75 1.040–1.100

Penesaline CaSO4 (gypsum/anhydrite) 140–250 4–7 75-85 1.100–1.126CaSO4�halite 250–350 7–11 85–90 1.126–1.214

Supersaline Halite (NaCl) >350 >11 >90 >1.214Bittern salts (K-Mg) Extreme >60 �99 >1.290

Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 319

“blue-green algae.” However, in terms of theirgenomic signature and the fact that the cell lacksa nucleus, they are better classified as prokaryoticbacteria.

In contrast to the cyanobacteria, all other photo-synthetic bacteria in saline waters are anaerobesand utilize a single type of photosynthetic reactioncentre with a different pigment (bacteriochloro-phyll). When compared to chlorophyll and phy-cobilin, bacteriochlorophyll can absorb light withlonger, less energy-rich wavelengths that extendsinto the infrared spectrum. Such light-requiringbacteria (e.g. purple bacteria) live in anoxic con-ditions and their ability to utilize the infraredspectrum means they can thrive deeper in a sedi-ment or water column than aerobic photosynthe-sizers (Figs 2B and 13). The green sulphur bacteria(Chlorobiaceae) and purple sulphur bacteria(Chromatiaceae) use elemental sulphur, sulphide,thiosulphate, or hydrogen gas as the electron

donor, whereas the purple and green nonsulphurbacteria use electrons from hydrogen or organicsubstrates (Table 2). As in aerobic photosynthesis,the resulting electrons (derived from the “lightreaction” of photosynthesis) are stored in glucoseand then used for CO2 fixation (aka the “darkreaction” of photosynthesis).

The following simplified equation typifiesanoxic photosynthesis of purple sulphur bacteria:

CO2 þ 2H2S ¼ CH2OþH2Oþ 2S ð2Þ

That is, carbon dioxide and hydrogen sulphidereact with bacteriochlorophyll and sunlight toform a carbohydrate (such as glucose) as well aswater and sulphur. The light-absorbing pigmentsof the purple and green bacteria consist of bac-terial chlorophylls and carotenoids. Phycobilins,characteristic of the cyanobacteria, are not foundin these bacteria. All photoautotrophs (including

Bacteriochlorophylls (anoxic photosynthesis)

OO

O

phytyl

OMeO

BChl b

O

OO

O

phytyl, geranylgeranyl

OMeO

BChl a

O

OO

O

famesyl

N

BChl e

OH

R1

R2

R1 = Et, n-Pr,isobutyl

R2 = Me, Et

O

OO

O

famesyl

BChl d

OH

R1

R2

R1 = Et, n-Pr,isobutyl, meopentylR2 = Me, Et

OO

O

famesyl

BChl c

OH

R1

R2

R1 = Et, n-Pr,isobutylR2 = Me, Et

Chlorophylls (oxic photosynthesis)

CH2CH3

O

H

CH3

H2C=CH

C

CH3 CH3

HCH2CH3CO2CH2CH=C(CH2CH2CH2)3CH3

H

CO2CH3

CH3

O

H

Chlorophyll β(mostly in land plants)

CH2 CH3

CH3 CH3

CO2CH3

H2C=CH

H3C

CH3

O

H

Mg

HCH2CH3CO2CH2CH=C(CH2CH2CH2)3CH3

H

CH3

Chlorophyll α(universal in plants,

algae & cyanobacteria)

A

C

B

BChl a (purple sulphur bacteria)BChl b (purple sulphur bacteria)BChl c (green sulphur bacteria, chloroflexi = filament. green)BChl d (green sulphur bacteria)BChl e (green sulphur bacteria)

250 300 400 500 600 700350 450 550 650Red

Chlorophyll

Chlorophyll α

β-Caroten

Phycoerythrin Phycocyanin

Abs

orpt

ion

Absorption spectra of photosynthetic pigments

800750Ultraviolet

Infrared

Bacteriochlorophyll

Porphyrin head Phytyl tail

Violet Blue Green Yellow Red

Wavelength (nm)

N N

NN

N N

N NMg

N N

N

N N

N NMg Mg

N N

N NMg

N N

N NMg

N N

N NMg

Fig. 2. Structures and features of the main photosynthetic pigments. (A) Chlorophyll-a and -b showing porphyrin head andphytyl 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.

320 J. K. Warren

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

Phylum orfamily

Informal group Metabolic lifestyles (selected halophilicspecies)

Prokaryotes Halo-adaptedbacteria

Cyanobacteria Cyanobacteria Aerobic photoautotrophwith chlorophyll-aplus phycobilicins, split water andgenerate oxygen (Arthrospira platensis,Dactylococcopsis sauna, Aphanothecehalophytica, Microcoleuschthonoplastes)

Proteobacteria Purple sulphurbacteria

Anaerobic obligate photoautotroph – useH2S or sulphur as electron donor(Halorhodospira halophila may be asignificant primary producer in somesettings, e.g. at a halocline; Chromatiumglycolicum, Ectothiorhodospiramarismortui)

Purple non-sulphurbacteria

Anaerobic photoautotroph (tolerate lowoxygen levels) – use hydrogen, but notfrom water, as the electron donor (e.g.Rhodospirillum sp.)

Chlorobiaceae Green sulphurbacteria

Anaerobic obligate photoautotroph – useH2S or sulphur as electron donor(Chlorobium limicola)

Flexibacteria Green non-sulphurbacteria

Anaerobic (thermophilic) photoautotroph –use hydrogen, but not from water, as theelectron donor (Chloroflexusaurautiacus)

Spirochetes Spirochetes Free-living obligate anaerobe (Spirochetehalophila oxidizes Fe and Mn).Chemolithotrophic, some species can besymbiotic or parasitic

Bacteriacea Flavobacteria Anaerobic organotrophs andchemoautotrophs, some species can beparasitic (Flavobacterium gondwaneseand F. salegens are psychrotoleranthalophiles isolated from Antarctic Lakes)

(Salinibacter ruber is phylogeneticallyaffiliated 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(sulpho-archaea)

Thermophile Anaerobic chemoautotroph(Crenarchaeota-domain clone sequencesdocumented in hypersaline sedimentsincluding Shark Bay stromatolites,anthropogenic salterns and sediments ofLake Qinghai, China)

Acidophile Aerobic- anaerobic chemoautotroph(as above), organotroph

Nanoarchaeota Symbiont onIgnoccus

Hosted on hot vent Archaea in Iceland. Itscell is only 400nm long

Korarchaeota New group ofextremethermophile

Only described from RNA samples (if it is areal phylum then it is the closest to life’suniversal ancestor of the earliestArchaean �3.7Ga)

See Fig. 3 for additional information.


higher plants, cyanobacteria and bacteria) containcarotenoid pigments, which are red-orange andyellow in colour as they absorb the blue-violet andblue-green wavelengths missed by chlorophyll(Fig. 2B). The green sulphur bacteria are probablythe most energetically efficient of all phototrophicorganisms and can live in environmentswith long-term light intensities that are less than 0.01% oftypical daylight. Many purple and green sulphurbacteria store elemental sulphur as a reserve mate-rial that, like glucose, can be further oxidized, inthis case to SO4, and so act as a photosyntheticelectron donor.

Modern chemoautotroph communities in salinemicrobial communities generally form a metabo-lizing layer beneath the photosynthesizers (inbothmats and stratified brine columns) and on topof the methanogens; some species in the chemo-autotrophic layer are lithotrophs. Lithotrophicsulphur oxidizers active in saline environmentsinclude a number of species of both bacteria (e.g.Thiobacillus) and archaea (e.g. Sulfolobus sp.).Thiobacillus iswidespread inmarine andhypersa-line microbialites and oxidizes thiosulphate andelemental sulphur to sulphate. Other lithotrophicbacteria use substances such as nitrate and reduceit to nitrite and include at least two species(Nitrobacter akalicus and Nitrosomas halophila)that flourish in the freshened water stages in theKenyan soda lakes (Sorokin & Kuenen, 2005).Sulfolobus sp. tend to be hydrothermal vent dwell-ers that prefer settings characterised by hot, salineand acidic waters (see later).

Sulfolobus is a species within the archaealdomain (formerly known as the archaebacterialdomain), which constitutes the “third domain oflife” (see Glossary). While members of the archaearesemble bacteria in morphology and genomicorganization, they resemble eukarya in theirmethod of genomic replication. The archaealdomain is further subdivided into two kingdoms:the Crenarchaeota, of which all members pres-ently isolated are extreme thermophiles, and theEuryarchaeota, a diverse group, that includes thehalophilic order Halobacteriaceae, certain thermo-philes and all members of the methanogen group(Table 2). All archaea are characterized by: (1) thepresence of characteristic tRNAs and ribosomalRNAs; (2) the absence of peptidoglycan cell walls;(3) the presence of ether-linked lipids built frombranched-chain subunits; and (4) their occurrencein unusual habitats (that seem extreme from ananthropocentric worldview).

Archaea are mostly extremophiles, that is theythrive in extreme conditions including: extremelysaline (halophile), extremely hot (thermophile),extremely dry (xerophile), extremely acid (acido-phile), extremely alkaline (alkaliphile), and extre-mely cold (psychrophile) environments. Someextremophiles are capable of surviving the multi-plicity of extreme conditions that characterizearid environments and are known as polyextremo-philes (Kates et al., 1993).

Archaea and bacteria that require extreme sali-nities to metabolize are called halophiles, thosethat can tolerate salinities in excess of 25% aretermed hyperhalophiles, and almost all docu-mented modern hyperhalophiles are archaea.One of the more impressive halophilic archaea isHalobacterium lacusprofundi; it is both a halo-phile andapsychrophile, it thrives inbottomwatersof the supersaline (�350‰) and cold (<0�–11.7 �C)Deep Lake, Antarctica (Franzmann et al., 1988).The lake is too saline to freeze over, is thermallystratified and lies in an endoheic depression in theVestfold Hills with a water surface that is some50 m below sea level.

Throughout this paper, it will be discussed indetail why microbes (archaea and bacteria) in sal-ine waters are halophilic, but it is notable thatmany halophiles are also thermophiles. World-wide, aerobic halophilic archaea of the orderHalobacteriales tend to have high growth optimaat warm temperatures, typically between 35� and50 �C and sometimes even higher (Oren, 2006).This may be an adaptation to the elevated temp-eratures that characterize stratified heliothermicwaters in salt lakes worldwide. Likewise, withinthe anaerobic halophilic bacteria of the orderHaloanaerobiales there are several moderately ther-mophilic representatives. Halothermothrix orenii,the first truly thermophilic halophile discovered,was isolated from Chott El Guettar, a warm salinelake in Tunisia. It grows optimally at 60 �C and upto 68 �C at salt concentrations as high as 200‰(Cayol et al., 1994). The halophilicAcetohalobiumarabaticum strain Z7492 has a temperature opti-mumof 55 �C, can grow at salinities between 100‰and 250‰ with an optimum around 150–180‰and, like the halophilic archaea, has adapted tohigh salinities via the uptake of intracellular KCl(Zahran, 1997).

Even more extreme in its environmental prefer-ences is the archaea Sulfolobus tokodaii; it is a hotspring dweller and intracellularly transformsH2S to elemental sulphur. It flourishes at

322 J. K. Warren

temperatures in excess of 90 �C and can live insaline environments where pH hovers around 1.Many such sulphur-dependant archaea are anae-robic chemoautotrophs that live in the vicinity ofhydrothermal/volcanogenic vents in saline lacus-trine rifts, or inmarinehydrothermal brine springs,or in the basal waters of density-stratified brinelakes and seaways. They also inhabit deep seafloorbrine pools on top of dissolving salt allochthonsand they can survive and possibly metabolizehundreds of metres below the surface in bathy-phreatic halite beds and sulphate caprocks (Grantet al., 1998). Like these archaea, some chemoauto-trophic bacteria can survive in extreme conditions,even living in saline subterranean settings, asevidenced by the recovery of viable halophilicchemolithotrophic bacteria (Haloanaerobium sp.)from highly saline oil fields brines in Oklahomawhere pore-water salinities are �150–200‰(Bhupathiraju et al., 1999).

Many halotolerant and halophilic bacteria andarchaea are heterotrophs feeding on the remains ofother organisms that had flourished in the samewatermass at lower salinities. Heterotrophicmeta-bolism shows variation in the terminal electron

acceptor. In aerobic respiration it is oxygen and thebreakdown product is CO2, in anaerobic respira-tion it may be sulphate or nitrate and the break-down product is H2S or nitrite.

Halotolerant bacteria isolated from mesohalinesettings tend to be anoxygenic photosynthesizerssuch as Chromatium salexigens, Thiocapsa halo-phila, and Rhodospirillum salinarum, with opti-mal growth in these species between 60 and 110‰(Fig. 3; Caumette, 1993). In contrast to the cyano-bacteria, which are oxygenic phototrophs, theseanoxic phototrophs use H2S, organic compoundsor sulphur compounds as electron donors to pro-duce various oxidized sulphur metabolites, thefinal product being sulphate. These anoxygenichalotolerant to halophilic photobacteria createdense biogenic laminae in a variety of anoxic,generally poorly lit environments. Phototrophicsulphur-oxidizing bacteria inmany salt lakes growin narrow niches defined by interfaces that arelit and also contain sulphide. In microbial matsthey grow below the cyanobacterial and the photo-trophic bacterial layers, while in stratified brinecolumns they inhabit waters of the halocline.Intense blooms of purple or green sulphur bacteria

50 100 150 200 250 300 NaCl (‰)

Marine to slightly halophilic(15 to 60‰)

Chromatium buderiChloroherpeton thalassiumEctothiorhodospira mobilisRhodobacter sulfidophilusPelodictyon phaeumRhodopseudomonas marinaEctothiorhodospira vacuolataProsthecochloris phaeoasteroideaThiorhodovibria winogradskyiChlorobium chlorovibrioidesChromatium purpuratumRhodobacter adriaticusProsthecochloris aestuariiChromatium vinosum HPC#Desulfobacter halotolerans

Rhodospirillum mediosalinumRhodospirillum salexigensEctothiorhodospira marismortuiThiocapsa halophilaChromatium salexigens

Ectothiorrhodospira abdelmalekiiRhodospirillum halophila

#Desulfovibrio halophilus#Desulfohalobium retbaense

Moderatelyhalophilic(30 to 150‰)

Halophilic(sensu stricto)(90 to 240‰)

Ectothiorhodospira halochlorisHalorhodospira halophila Salinibacter ruber

Extremelyhalophilic(180 to 300‰)

Fig. 3. Salinity tolerances of phototrophic halophilic bacteria, sulphate-reducers (#) and Salinibacter ruber. Star on barindicates the salinity for optimal growth (after Ollivier et al., 1994; Caumette, 1993; Imhoff, 1988; Ventosa, 2006).


can form brightly coloured water masses or sedi-ment layers. Most of the H2S they metabolizeis biogenic rising from below and generated bymicrobial sulphate reduction, except around brinesprings and hydrothermal vents where there canbehigh levels of abiogenicH2S (Knauth, 1998). Thebiodiversity of bacterial photosynthesizers fall offas higher salinities are reached (Pedr�os-Ali�o, 2005).

Purple and green bacteria growth is only possi-ble in settings where the chemical gradient ofsulphide is stabilized against vertical mixing. Inlayered microbial mats this occurs at the interfacebetween the oxygenated layer createdby thephoto-synthesizing cyanobacteria and the underlyinganoxic layer created by the sulphate reducers. Instratified brine columns, chemical gradients arestabilized by density and temperature differencesbetween the cooler less saline surface waters andthe warmer more saline bottom layers and so theytend to inhabit the halocline. Examples of sulphur-oxidizing bacteria in hypersaline settings includeAtium volutans from Solar Lake, Beggiatoa albafrom Guerrero Negro, and B. leptiformis fromSolarLake (DasSarma&Arora, 2001).Aunicellularhalophilic, chemoautotrophic sulphur-oxidizingbacterium, Thiobacillus halophilus, has also beendescribed in a hypersaline Western Australia lakewhere it grows in waters with salinities of up to240‰ (Wood & Kelly, 1991).

All modern halophilic sulphur-oxidizing bac-teria are filamentous, CO2-fixers, typically motileand utilize sulphide as an electron donor for theirphotosynthesis. Purple sulphur bacteria seem toflourish across a broad range of continental brinesalinities. For example Ectothiorhodospira halo-philic speciesdominate in themicrobial sedimentsof alkaline soda lakes in Egypt and Central Africa,while the moderate halophile Ectothiorhodospiramarismortui is a strict anaerobe found in thewaters of hypersaline waters (170‰) of sulphursprings in the Dead Sea, where spring waters had apH around 5.2 and a temperature of 40 �C (Fig. 3).Isolates of this species grew poorly at a pH or5.5 but thrived in the neutral pH range between7 and 8 (Oren et al., 1989). Another extremelyhalophilic sulphate-oxidizer Ectothiorhodospirahalochloris was isolated from Wadi Natrun in1977, in the laboratory it showed optimal growthin salinities in the range 140–270‰, a pH-rangebetween 8.1 and 9.1 and temperatures between47�C and 50�C (Fig. 3).

Dissimilatory sulphate reduction can occur upto quite high salt concentrations and black,

sulphide-containing sediments formon the bottomof modern coastal salinas and salt works well intothe penesaline salinity range (Oren, 2001).Amongst the bacteria, most salt-tolerant halophilicsulphate-reducer thus far found is Desulfohalo-bium retbaense; it is a lactate oxidizer and wasisolated from Lake Retba in Senegal. In the labora-tory it remained viable at NaCl concentrations ofup to 240‰, with a growth optima of 100‰ (Olli-vier et al., 1994). Two other sulphate-reducinghalophilic isolates are Desulfovibrio halophilusand Desulfovibrio oxyclinae, which can tolerateperiodsofNaClconcentrationofup to225‰ (Fig. 3;Caumette, 1993; Krekeler et al., 1997). Anotherisolate, similar to Desulfovibrio halophilus hasbeen identified in brine pool samples collected inthe allochthon-associated deep-water brine lakeson the floor of the Red Sea where it grows insalinities up to 240‰, but only slowly.

In sulphate reduction, the oxidation of acetateand CO2 yields more energy per cell compared tothe precursor oxidation of lactate. Recently thefirsthalophilic acetate-oxidizing sulphate-reducingbacterium was isolated: Desulfobacter halotoler-ans (or Desulfohalobium utahense). It was col-lected from the hypersaline bottom sediments ofthe North Arm of Great Salt Lake, Utah, and wasfound to have a rather restricted salinity tolerance,it grows optimally at 10–20‰ NaCl, does not growabove 130‰ and is unable to survive above 240‰NaCl (Fig. 3; Brandt & Ingvorsen, 1997; Jakobsenet al., 2006). Even so, it possesses the highestNaCl-tolerance reported for any member of thegenus Desulfobacter. In terms of metabolic path-ways in the various salt-tolerant or halophilicsulphate reducers, it seems species that oxidizelactate, such as Desulfovibrio halophilus, can tol-erate higher salinities of up to 250‰ than thosespecies capable of oxidizing acetate, such asDesul-fobacter halotolerans,whichdobest in salinities ofless than100–120‰ (Figs 3and4). In contrast to thesulphate-reducers, it seems no viable sulphur-oxi-dizing communities can survive at similar extremesalinities compared to the lactate oxidizers (Fig. 4).

Living below or among the sulphate-reducercommunities in both microbial mats and stratifiedbrine columns are the fermenters and the metha-nogens. One group of halophilic bacteria espe-cially well adapted to the fermentative lifestyleis the Haloanaerobiales (Oren, 1992). Fermenterslive in anaerobic saline conditions when there isno electron acceptor, and different sugars and insome cases amino acids are fermented to products

324 J. K. Warren

such as acetate, ethanol, butyrate, hydrogen, andcarbon dioxide. Fermentation breaks down anorganic compound, such as a sugar or an aminoacid, into smaller organic molecules that thenaccept the electrons released during the break-downof the energy source.When glucose is brokendown to lactic acid, each molecule of glucoseyields only two molecules of ATP, and consider-able quantities of glucose must be degraded toprovide sufficient energy for microbial growth.Fermentation means only a relatively small out-put of energy per glucose molecule consumed asany organic molecule is only partially oxidized.Fermentation tends to be the sole metabolicmechanism in the well-adapted halotolerant andhalophilic species of the Haloanaerobiales thatinhabit the lowers parts of a microbial mat or brinecolumn. It can be an emergency metabolic systemin other microbes that find themselves in thissame environment. The presence of biomarkersof fermentativemicrobes in saline and hypersalinePhanerozoic sediments or oils indicates deposi-tional conditions that were anoxic and highlystressed with respect to higher life forms. Suchbrine- and pore-water conditions tend to facilitate

the preservation of hydrogen-prone organic end-products (proto-kerogens).

Methanogens are archaea that create methanegas as they remove excess hydrogen and fermenta-tion products produced by other forms of anaero-bic respiration. The methane then rises throughthe sediment or brine column to be utilized by thesulphate-reducers. Today some two-thirds to threequarters of the biogenic methane passed intothe atmosphere worldwide is the work of a fewdozen species of methanogenic archaea most ofwhich live in relatively low salinity environments.The remainder of the world’s methane comes fromhigher plants (Keppler et al., 2006; Houwelinget al., 2006). Allmethanogenic archaea are obligateanaerobes thriving in three habitats: (a) bodies ofanoxic fresh to hypersaline surface and subsurfacewater (e.g. the bottom brines of Solar Lake; (b) thevicinity of thermal brine springs; and (c) the diges-tive tracts of ruminants).

The main methanogenic processes in freshwaterenvironments and in the guts of ruminants are thereductionofCO2withhydrogenand theaceticlasticsplit mechanism where organic matter is split byoxido-reduction into methane and carbon dioxide,

Salinity (‰)

0 100 200 300

?

?

Autotrophic ammonia oxidation

Methanogenesis from acetate

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

Autotrophic nitrite oxidation

Fig. 4. Approximate upper salinity limits of selectedmicrobialmetabolic pathways (afterOren, 2001 and references therein).Values presented are based on laboratory studies of pure cultures (solid brown bars) and on activitymeasurements of naturalcommunities in hypersaline environments (graded-colour extensions to bars).


but neither of these reactions has been shown tooccur at high salt concentrations (Oren, 2006 andreferences therein). It seems thatoxidationoforgan-ic matter is incomplete in settings with high levelsof NaCl when compared with that in other ecosys-tems (temperate lacustrine andmarine ecosystems)where acetate, H2 þ CO2 are efficiently metabo-lized to produce CH4, or are oxidized by sul-phate-reducing bacteria whenever sulphate isavailable. At salinities higher than 150‰, themineralization of organic compounds is limitedby poor rates, or the complete absence, ofmicrobialsulphate reduction of acetate and the inherentlyslow rates of methanogenesis utilizing H2 (Fig. 4).The highest salt concentration at which suchmethanogenesis (from H2 þ CO2) occurs in natureis in the 88‰ bottom waters of Mono Lake, Cali-fornia (Fig. 4: Oremland & King, 1989). The result-ing accumulation of hydrogen and volatile fattyacids (VFA) in saline sediment beneath brine col-umnsmore saline than this, implies that catabolismvia interspecies hydrogen transfer hardly occurs atall in more hypersaline environments (Ollivieret al., 1994). Hence sediment from the floor of theGreat Salt Lake contains up to 200mMdissolvedH2.Similar results were obtained from Dead Sea sedi-ments stimulated to reduce sulphate with H2 andformate, although the same sediments did notrespond with acetate, propionate, or lactate treat-ments. Energetic constraints may explain theapparent lack of truly halophilicmethanogens cap-able of growing on H2 þ CO2 or on acetate, as thesemethanogens use the energetically more expensiveoption of synthesizing organic osmotic solutes (seelater, “low salt in” discussion).

Methanogenesis occurs at much higher salt con-centrations but only via a less productive meta-bolic pathway that utilizes methylated amines,methanol, anddimethylsulphide substrates (Fig. 4;Oren, 2001, 2006). The most salt-tolerant metha-nogens known are Methanohalobium evestigatumand M. portucalensis, which grow in up to250–260‰ NaCl. Additional moderately halophi-lic methanogens have been isolated, growing opti-mally at 40–120‰ salt (e.g. Methanohalophilusmahii,M.halophilus,M.portocalensis,M.zhilinae).Modern halophilic methanogens can form richmicrobial communities in the density-stratifiedwaters of deep-seafloor brine lakes, includingsuprasalt allochthon areas on the deep Mediter-ranean seafloor where some anoxic bottom brineshave evolved to the bittern stage (MgCl2 saturation;van der Wielen et al., 2005). It may well be that

Earth-bound primordial life first evolved as meth-anogens in hypersaline waters (Dundas, 1998;Knauth, 1998).

Fermenters live in anaerobic saline conditionsusing a metabolic pathway where there is no elec-tron acceptor, where different sugars, and in somecases amino acids, are fermented to products suchas acetate, ethanol, butyrate, hydrogen and carbondioxide (Hite & Anders, 1991). When evaporitesalts precipitate, these liquid organics are oftenencased as brine inclusions in halite and other saltcrystals and so are not picked up in standard TOCdeterminations. Their relative contribution to anysource rock potential is poorly understood in sub-surface evaporitic systems where cross-flowingbasinal brines are dissolving buried halite beds.They may be locally significant contributors volu-metrically to the hydrocarbons moving in carrierbeds in contact with dissolving evaporites.

The last groupings to be considered in this dis-cussion of the various metabolic pathways activein hypersaline settings are the haloviruses andbacteriophages that must infect the haloarchaeaand bacteria. Compared to the literature-base forthe halophilic archaea and bacteria little is knownand most published studies to date deal with thehaloviruses infecting the haloarchaea (Ventosa2006; Dyall-Smith et al., 2005). Nonetheless, giventhat in the natural world virus populations aregreater than those of their prokaryotic hosts andthat each host species is susceptible to infectionby several different viruses, it may be deducedthat a great diversity of such viruses must existin hypersaline environments.

Electron microscopy of hypersaline watersshows that they maintain high levels of virus-likeparticles (about 10 times higher than the cell popu-lation), with recognizable morphotypes includinghead–tail and lemon-shaped particles (Ventosa,2006 and references therein). Guixa-Boixereuet al. (1996) determined the abundance of virusesin twodifferent salterns in Spain andobserved thatthe number of viruses increased in parallel to thatof prokaryotes, from 107mL�1 in the lowest sali-nity ponds to 109mL�1 in the most concentratedponds (crystallizers), thus maintaining a propor-tion of 10 virions per prokaryotic cell throughoutthe salinity gradient. A lemon-shaped virus wasfound infecting square archaea; its abundanceincreased along the salinity gradient together withthe abundance of the square archaea. Followinga Dunaliella sp. bloom in freshened surface watersof the Dead Sea, Oren et al. (1997) observed the

326 J. K. Warren

presence of large numbers of virus-like particles inwater (up to 107 virus-like particles mL�1), with avariety of morphologies, from spindle-shaped topolyhedral and tailed phages. Details of the halo-biotal bloom in the Dead Sea will be discussedlater. It may be concluded that viruses and bacter-iophages are abundant in the archaea and bacteriathat inhabit hypersaline waters, but the variousmetabolic pathways operating within this infest-ing community have yet to be fully established andawait further study.

In summary, halophilic bacteria as a group arecapable of using severalmetabolic styles and so aremore biochemically divergent than the halophilicarchaea. Some purple bacteria and gram-positivebacteria are chemoautotrophic halophiles, whilehalophilic cyanobacteria are oxygenic photoauto-trophs. Under suitably stressed conditions manyhalophilic bacteria become heterotrophic, utilizingeither anaerobic or aerobic respiration pathways.By evolving oxygen respiration some 2.5 billionyears ago, the cyanobacteria came to flourish andultimately displace the archaea. Ancient cyano-bacteria lived in symbiosis with early eukaryotes;by the Mesoproterozoic this had allowed eukaryo-tic photosynthesis to develop and ultimately ledto the evolution of the higher plants and animals.Once oxygen was plentiful in the atmosphere(�2.2Ga), it was difficult for anaerobes (includ-ing photosynthesizing archaea and bacteria) toflourish in most surface waters. Some retreatedto anaerobic environments, some acquired aerobicbacteria as endosymbionts, and some continuedto thrive in aerobic/dysaerobic conditionsthat typify the hypersaline bottom waters of mostdensity-stratified brine bodies.

BIOADAPTATIONS TO INCREASINGSALINITY

In 1957, in his classic book on evaporites, Lotzemade the statement: “Nicht das Leben, sondern derTod beherrscht die Salzbildungsst€atten” (Not life,but death rules the locales of salt deposition).Saline environments were considered biotaldeserts, largely devoid of biological activity andhence were considered to be sedimentary systemswith little source rock potential. The followingdiscussion shows that this is not the case. Rather,saline environments and water bodies are sites ofperiodic but intense organic activitywhere numer-ous highly specialized algal, bacterial and archaeal

species grow and die (cycles of “famine or feast”).They can leave behind substantial volumes of oil-prone organic residues in the bottom sediments,especially in laminated mesohaline carbonates,which on burial can evolve into prolific sourcerocks. Even inmodern saline environments, whereevaporite depositional settings are not as diverse orwidespread as those ofmuch of the past, conditionsare such that mesohaline carbonates can preservehigh levels of total organic carbon (TOC; Fig. 5).

Salinity ranges of the modern halobiota

Progressive brine concentration leads to sequentialblooms of a macro and microbial biota adapted todifferent ranges of salinity in both marine andcontinental settings (Fig. 6A and B). As a modernsurface brine is concentrated from 60‰ to around200‰, dense eukaryotic algal and cyanobacterialpopulations appear, grazed by ostracods, brineshrimp and brine fly larvae. Halotolerant protozoacan be found feeding in this salinity range, as canyeasts and other fungi (Gunde-Cimerman et al.,2005). Halotolerant microbial mats cover the bot-tom of many hypersaline ponds and shallow lakesin this salinity range. In anoxicwaters in this salin-ity range there are a variety of sulphur-oxidizing,sulphate-reducing, homoacetogenic,methanogenicand heterotrophic bacteria and archaea, especiallynear the base of stratified brine columns or in thelower parts of mesohaline microbial mats.

From about 240‰ to more than 320‰, red-orange haloarchaea (halophilic and hyperhalophi-lic archaea) and halobacteria (e.g. Salinibacterruber) come to dominate, mostly living on theproducts of decomposing organic matter left overfrom an earlier lower salinity time (Pedr�os-Ali�o,2005). At the elevated salinities where these halo-philes and hyperhalophiles flourish, only a feweukaryotes such as brine shrimp (Artemia andParartemia sp.) can survive to graze on the remain-ing species of cyanobacteria and algae, especiallyDunaliella sp. – a unicellular green alga (Fig. 6A).Above 300‰ no aerobic photosynthesis occurs, orat least is not known to occur based on the absenceof chlorophyll-a in the brines. As ever more ele-vated salinities are attained, most other microbialactivity first slows and then ceases.

A variety of obligate and facultative halophyticplants can survive in the moderate-to-high salin-ity soils that surround saline pans and lakes, e.g.Atriplex halimus, Mesembryanthemum crystalli-num and Salicornia sp. Only a few species of


animal can tolerate hypersaline conditions(Fig. 6A and B; DasSarma & Arora, 2001). Thehighest salinity at which viable vertebrates havebeen observed is around 60‰. For example, thewhite-lipped or alkaline tilapid fish (Oreochromisalcalica) flourishes in themesohalinewaters of theAfrican rift lakes. This setting includes thermalspringwaters at 36–40 �Calong themoat-like edgesof Lake Natron and Lake Magadi, where waterscan have a pH as high as 10.5–11 and salinities inexcess of 65–70‰.

Large numbers of invertebrates can survive inlow to moderately mesohaline environments.Examples include salt-tolerant rotifers (aka wheelanimalcules) such as Brachionus angularis andKeratella quadrata, and tubellarian worms (flat-worms) such as Macrostomum sp. Insects fromhypersaline environments include halotolerantbrine flies, such as Ephydra hians and E. gracillis,which feed and lay their eggs in microbial matsand organic scum about the strandlines of modernsaline lakes. Likewise, brinefly larva are adapted tosaline conditions, Ephydrellamarshalli larvae col-lected from commercial salt work lagoons on PortPhillip Bay, Victoria, have survived several daysimmersed in hypersaline sodium chloride mediaat an osmotic concentration of 5848mOsmL�1

(175‰ NaCl; Marshall et al., 1995).Halotolerant crustaceans include ostracods such

as Cypridis torosa, Paracyprideinae sp., Diacypris

compacta andReticypris herbsti, copepods such asNitocra lacustris and Robertsonia salsa, and brineshrimps such as Artemia salina, Parartemia ziet-zianis and other related species. Brine shrimp sur-vive awide range of salinities from25 to 240‰withtheir optimal range around 60–100‰; they arewell adapted to the fluctuating oxygen and salinitylevels that characterize many mesohaline ecosys-tems. Geddes 1975a–1975c argued that increasedosmotic stress, not oxygen level, is the dominantlimit on the upper salinity tolerance of Australianbrine shrimp (Parartemia zietzianis), and this isprobably also true for Artemia sp. (Geddes, 1981).

Halotolerant ostracods and brine shrimp feed onplankton living in the upperwatermass of density-stratified brine columns and ingest benthic matswhere this less-saline water mass intersects thelake margin or when bottom-water salinities aresuitably lowered (de Deckker, 1981; De Deckker &Geddes, 1980). They produce pelleted carbonatedetritus, which is a common component ofmany modern and ancient evaporitic laminites(Warren, 2006).

Diatoms (halotolerant bacillariophytal yellow-green algaewith siliceous tests) are commonplank-tonic forms in mesohaline and penesaline waters.They flourish at times of bloom in freshened salt-lake waters or in zones of perennial seepage anddissolution ponds (posas) about the edges of somesalars. Their siliceous tests become a major detrital

Salt Flat Playa, west Texas (continental dry mudflat)Dead Sea (continental transform lake)

Lake Van, Turkey (continental collision lake)Lake Urmia, Iran (continental collision lake)

Lake Rukwa (rift valley lake)Lake Nakuru (rift valley lake)

Lake Natron ("moat" facies in rift valley lake)Lake Kivu (rift valley lake)

Lake Tanganyika (rift valley lake)

Coriaco Trench (deep marine)Offshore Peru below upwelling (deep marine -15°S)

Gulf of Bacabano (Caribbean marine platform)Bahamian ooids (Caribbean marine platform)

Red Sea (silled sea)Black Sea (silled sea)

Abijan lagoon, Ivory Coast (restricted coastal lagoon)Abu Dhabi mats (saline mudflat)

Laguna Lejia, Antofagasta, Chile (restricted coastal lagoon)Harbour Is. Texas (restricted coastal lagoon)

Coast Lake, Ross Is. Antarctica (cryogenic coastal salina)Kleberg Point lagoon, Baffin Bay (coastal salina)

Lake Haywood, Australia (coastal salina)Coorong ephemeral lakes, Australia (coastal salina)

Laguna Guerro Negro, Baja California (coastal salina)Solar Lake, Gulf of Aqaba (coastal salina)

0 5 10 15 20 25 30 35

Total organic carbon (% dry weight)

MA

RIN

EN

ON

- M

AR

INE

Con

tinen

tal

Per

ital o

r se

epag

eO

pen

mar

ine

Fig. 5. Total organic carbon (TOC, drywt%) inmodern saline settings. Compiled from sources listed inWarren (1986, 2006).

328 J. K. Warren

component in some lacustrine stromatolites(Winsborough et al., 1994). Some halotolerantvarieties of diatoms live in mesohaline lake brineswith salinities around 120‰, while the upperlimit for diatom growth is around 180‰ (Clavero

et al., 2000). The most halotolerant diatom taxain the saltern ponds of Guerrero Negro, BajaCalifornia Sur, Mexico, are Amphora subacutius-cula,Nitzschiafusiformis (bothAmphora taxa), andEntomoneis sp.; all grow well in salinities ranging

Evaporation 1ratio (Vi/Vo)

36-70‰

Carbonatedomain

70-140‰

Transition

140-220‰

Gypsumdomain

220-300‰

Halitedomain>300‰

A

B

Methanopyrus

Methanothermus

Methanobacterium

The

rmoc

occu

s

Met

hano

coss

us ja

nnas

chii

Met

hano

cocc

us v

anni

elii

Arch

aeog

lobu

s Ther

mop

lasm

aHalobacte

riales

Methanospirillum group

Thermophilum

ThermoproteusDesulfurococcus

Sulfolobus

Pyrodi

ctum

Flavobacte

rium group

Flexibacte

r

Plan

ctom

yces

g-P

rote

obac

teria

b-P

rote

obac

teria

a-P

rote

obac

teria

d-P

rote

obac

teria

Cyanobacteria

ChlamydiaChlorobiumSpirochetes

ClostridiumBacillus

Heliobacterium

High-HC gram-positive bacteria

Thermomicrobium

Thermus

Thermotoga

Aquifex

EUBACTERIA ARCHAEA

EUKARYA

Halophilic members

C

Salinity (‰)

Fish &mangroves

Bio

mas

s

35

Red halophiliceubacteria & archaea

Brine shrimp &brine fly larvae

Seagrass &seaweeds

Microalgae, cyanobacteriaeubacteria & protozoa

100 150 200 250

1/2 1/4 1/7 1/11

diatomscyanobacteria

green algaephototropic sulphur bacteria

Artemia salina

DunaliellaHalophilic archaea & eubacteria

Parartemia zietziania

Fig. 6. Salinity tolerances of key biota. (A) Typical salinity ranges of the halotolerant biota where Vi is the volume of inflowto the basin and Vo is the volume of outflow (includes evaporation and reflux; after Barb�e et al., 1990). (B) Typical salinityranges and biomass proportions of the biota in modern marine saltwork ponds. (C) Phylogenetic tree of the bacteria andthe archaea, based on 16S rRNA sequencing comparisons. Thick red lines indicate branches containing representativesable to grow at or near optimal rates at NaCl concentrations exceeding 15% (after Ventosa et al., 1998).


from 5 to 150‰, Three strains of the diatom Pleur-osigma strigosum are unable to grow in salinities ofless than 50‰ and so are true halophilic alga.

In most moderately hypersaline (mesohaline topenesaline; 60–200‰) settings halotolerant cyano-bacteria and green algae, rather than diatoms, arethe dominant primary organic producers and greenalgal densities can be more than 105mL�1. Theseplanktonic blooms can support many birds; one ofthemost spectacular examples is the pink flamingopopulation of African rift lakes. Mesohaline algaeare mostly obligately aerobic, photosynthetic, uni-cellular microorganismswith some species produ-cing large quantities of orange-coloured b-carotenepigment. Planktonic blooms in saline lakes cancolour saline waters pink or red, especially at thehigher end of this salinity range. Green algae of thegenus Dunaliella (e.g. Dunaliella salina, D. parva,and D. viridis) are ubiquitous in modern NorthernHemisphere brine lakes, such as Great Salt Lakeand the Dead Sea, and are the main source of foodfor brine shrimp and larvae of brineflies (DasSarma& Arora, 2001). Most species of green algae aremoderate halophiles, with only a few extremelyhalophilic species (e.g. Dunaliella salina andAsteromonas gracilis) that survive in marginwardrefugia, even when the upper and lowwater layersin the Dead Sea are NaCl-saturated (see later).

Protozoa occur in most mesohaline waters, theyare chemoheterotrophic protists that lack a cellwall and typically ingest algae and bacteria (Hauer& Rogerson, 2005). Identified species includethe moderate halophile Fabrea salina from a westAustralian salt lake and the extreme halophilePorodon utahensis from the Great Salt Lake. Thenumber of known protozoan species identified inhypersaline waters (at salinities ranging from 90‰to 220‰) has grown from<50 in the 1970s to morethan 200 today, and include a range of amoebae,ciliates and flagellated protozoa. Fungi, mostlyyeasts, are another heterotrophic component of amodern saline salt lake biomass (DasSarma &Arora, 2001; Gunde-Cimerman et al., 2005). Theyare chemoheterotrophic eukaryotes, some of whichare well adapted to tolerate markedly hypersalineenvironments. They grow best in aerobic con-ditions on carbohydrate substrates at moderatetemperatures and in acidic to neutral pH brines.Debaromyces hansenii is a halotolerant yeast that,when isolated from seawater, can grow aerobicallyin salinities up to 250‰ and is capable of assim-ilating hydrocarbons. Another saprophytic hypho-mycete (fungi), Cladosporium glycolicum, was

found at a salinity exceeding 260‰ growing onsubmerged wood panels in the Great Salt Lake.Halophilic fungi (e.g. Polypaecilum pisce andBasipetospora halophila) have also been isolatedas a cause of spoilage in salted fish and bacon,but their distribution in hypersaline waters is notwell known.

Above200–240‰most photosynthetic algae andhalotolerant cyanobacteria cease to function andthe halophilic archaea and bacteria come todominate, mostly as decomposers (Fig. 6A and B;Pedr�os-Ali�o, 2005). The transition into a morearchaeal-rich biota means that while eukaryoticmetabolic pathways and biochemistry dominatesmesohalinewaters, prokaryotic and archaealmeta-bolisms come to dominate at higher salinities(see later biomarker discussion).

“Halobacteria” flourishing in supersalinewatersbelong to the archaeal family Halobacteriaceae.All known extremely halophilic archaea staingram negative, do not form resting stages or spores,and reproduce by binary fission (Oren, 2006).They are highly specialized micro-organisms,most of which will not grow at total salt concen-trations below 2.5–3M (145–175‰ NaCl) and aredestroyed by lower salinities (see cellular adap-tations). At present with the archaeal familyHalobacteriacea there are 14 known genera and35 validly described species. Six of these generaare monotypic: Halobacterium; Halobaculum;Natrosomonas; Natrosobacterium; Halogeometri-cum; Haloterrigena. The other genera (Table 3;Oren, 2006) are: Natrialba (2 species); Natrono-coccus (2 species);Natrinema (2 species);Natror-ubrum (2 species); Halococcus (3 species);Haloferax (4 species); Halorubrum (7 species),Haloarcula (7 species). Halococcus sp. are strictaerobes, their name reflects their coccoid cellshapes and they form pairs, tetrads, sarcinae orirregular clusters. Cells produce several orangeor red carotenoid and retinal pigments needed tobetter cope with high levels of ultraviolet lightthat characterize supersaline brine settings.Haloferax prefers high-Mg waters and is a majorconstituent in the halophilic biota of the DeadSea. The various Halococcoid species, along withHaloferax and Haloarcula, flourish worldwide inhypersaline lakes, coastal salinas and brine lakeson the deep sea floor.

Most interesting, but most problematic, are thesquare-shaped archaea growing in many halite-precipitatingbrines. In1980,A.E.Walsbydescribedthe abundant presence of “square bacteria” in

330 J. K. Warren

a small, halite-saturated brine pool, in the SinaiPeninsula (Walsby, 1980). These micro-organismswere collected from the surface of the pool, hada large number of gas vesicles, and presentedunique cell morphologies never observed pre-viously in the microbial world. The cells aresquares and very thin, with sizes from 1.5 to11 mm and a thickness of about 0.2 mm. Divisionplanes were observed, with an arrangement indi-cating that division occurred in two planes alter-nating at right angles, so that each square grows toa rectangle which then divides into two equalsquares, producing sheets divided like postagestamps (Walsby, 1980). In addition, different gasvesicles were observed, from spindle-shaped tocylindrical with conical ends and, in many cases,they were concentrated at the cell periphery.Ultrastructure studies confirmed that the square

cells observed by Walsby were micro-organismswith a typical prokaryote structure.

Direct observations of brines of salterns andother hypersaline environments showed that thesesquare cells were very abundant in such habitats,especially in the most concentrated ponds withsalinities higher than 3–4M NaCl (at halite satura-tion, 175–233‰ NaCl), and they have beenreported to occur in many geographical locationsin both the Northern and Southern Hemispheres(Oren, 1999a). For more than 20 years these wereconsidered uncultivable, until the work of Burnset al. (2004) and Bolhuis et al. (2004), who inde-pendently cultivated what Bolhius and coworkersinformally named “Haloquadratum walsbyi”. Theisolation of the square archaea by two independentresearch groups introduced a new methodologythat nowpermits the isolation of new fresh isolates

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. sodomenseH. lacusprofundiH. corienseH. distributumH. vacuolatumH. trapanicum

Haloarcula Haloarcula vallismortisT

H. marismortuiH. hispanicaH. japonicaH. argentinensisH. mukohataeiH. quadrata

Natronomonas Natronomonas pharaonisT

Halococcus Halococcus morrhuaeT

H. saccharolyticusH. salifodinae

Natrialba Natrialba asiaticaT

N. magadiiNatronobacterium Natronobacterium gregoryiT

Halogeometricum Halogeometricum borinquenseT

Natronococcus Natronococcus occultusT

N. amylolyticusHaloferax Haloferax volcaniiT

H.x gibbonsiiH. denitrificansH. mediterranei

Natrinema Natrinema pellirubrumT

N. pallidumHaloterrigena Haloterrigena turkmenicaT

Natronorubrum Natronorubrum bangenseT

N. tibetense

T¼ type genus of the family or type species of the genus.


of square archaea from various areas. Future workwill establish whether they are represented by asingle or several novel haloarchaeal species cap-able of living amongst halite crystals. Work to datesuggests that it is a new genus of the Halobacter-iaceae, rather than a species within the existinggenera of the order. The question arises as towhether the square cellular shapes of this archaealgroup, and the cubic outline of pores and inclu-sions in and amongst the halite meshwork it inha-bits, are more than fortuitous. Two haloarchaealgroups live only in high-pH high salinity waters ofsoda lakes such as Wadi Natrun and Lake Magadi;these are Natronobacterium and Natronococcus.They grow only in hypersaline waters with highpH (8.5–11.0) and very low levels of Mg (<0.024 gL�1), and so are known as alkaliphiles. They havenot been found in marine-fed salterns or less alka-line continental systems. However, the precisedefinition of genome systematics in halophilesliving in soda lakes is still in a state of flux (Grantet al., 1999).

Haloarchaeal species growing at salt concen-trations above 150–200‰ characterize not onlythe Halobacteriaceae but also moderately halo-philic methanogenic archaea, such as species ofMethanohalophilus and Methanococcus (Table 2;Pfl€uger et al., 2005). The existence of methano-genic archaea in hypersaline environments isrelated to the presence of noncompetitive organicsubstrates such as methylamines, which origi-nated mainly from the breakdown of osmoregula-tor amines, rather than the presence of carbondioxide, acetate and hydrogen (Fig. 4). The extre-mely halophilic methanogen, Methanohalobiumevestigatum, with a NaCl optimum of 260‰, isalso a thermophile with a temperature optimumof 50 �C. Halophilic methanogens are commoncontributors to the biota of methane hydrates asso-ciated with saline seeps and deep-sea brine poolsabove salt allochthons in the Gulf of Mexico(Lanoil et al., 2001). Interestingly, unlike the Halo-bactericaea, these various methanogenic speciesseem to adapt to the increased salinity by a buildup of osmolytes in the cell, and so are not obligatehalophiles.

As well as halophilic archaea, there are halo-philic bacteria flourishing in waters with sali-nities in excess of 240‰. One of the most inter-esting is Salinibacter ruber; which can constitutebetween 5 and 25%of the prokaryotic communityin a number of halite-saturated settings world-wide (Ant�on et al., 2005; Bardavid et al., 2007).

Until the late 1990s, when Salinibacter ruberwas first isolated and cultured from samples inanthropogenic salterns, the microbial popula-tion of halite-saturated waters was thought to bemade up of a few species of archaea, includingthe distinctive archaeal phenotypewith its squarecell, which because of its unique four-sided mor-phology is widely known as the SHOWphylotype(Square Haloarchaea Of Walsby; Bolhuis, 2005;Dyall-Smith et al., 2005).

It now seems that Salinibacter ruber is ubiqui-tous (some 5–25% of the biomass) in halite-saturated waters worldwide, and is typically com-mingled with the SHOW phylotype (Ant�on et al.,2005). Most workers now agree that S. ruber andthe square haloarchaea are the dominant microbialspecies at these elevated halite-saturated salinities(Ventosa, 2006). Once isolated in pure culture, itwas evident that the similarity of S. ruber to manyhaloarchaea could have hampered the isolationof the bacterium. Both types of prokaryotes areextremely similar at the phenotypic level: both areextreme halophiles, aerobes, and heterotrophsand pigmented by carotenoids. S. ruber, like manyhaloarchaea, accumulates high concentrations ofKþ to counterbalance the osmotic pressure of themedium, has a high proportion of acidic aminoacids in its proteins, as well as enzymes functionalat high salt concentrations and even has a highproportion of GþC in its genome (65–70% forS. ruber, in the range of 59–70% for haloarchaea;Ant�on et al., 2005.). All these similarities, togetherwith the fact that S. ruber and “Haloquadratumwalsbyi” dominate the biota in halite-saturatedwaters whenever prokaryotic density is high, poseinteresting questions as to the evolutionary pro-cess. For example, what environmental conditionsin the Precambrian led to such a high degree ofmetabolic similarity between two groups that nowoccur in very genetically separate domains of life?It also shows that S. ruber is a bacterium that is ashalophilic and as salt dependant as anymember ofthe Halobacteriaceae.

Other than Salinibacter ruber, two groups ofhalophilic bacteria are well represented in salinityranges in excess of 150‰; the fermentative bacteriabelonging to the family Haloanaerobiaceae andthe phototrophic sulphur-oxidizing bacteria of thefamily Ectothiorodhospiraceae (Figs 3 and 6C).Both groups are mostly made up of moderatehalophiles. Phototrophic halophilic bacteria arefurther divisible into purple and green bacteriaaccording to their respective bacteriochlorophylls

332 J. K. Warren

and carotenoids (Fig. 2C). For example, the shal-low parts of soda lakes in the Wadi Natrunmay be intensively red coloured due to the devel-opment of Halorhodospira halophila (purplesulphur bacteria), while green non-sulphur bacter-ia dominate the photosynthesizing layer of thehypersaline microbial mats in brines of similarsalinity in Guerrero Negro, Baja Mexico (see “redwaters and brines” in Glossary). Small brine pud-dles in many hypersaline locations may showseparate development of green- and red-colouredspecies of Halorhodospira, while top layers of thesediments of Wadi Natrun lakes (Egypt) showseparate layers of the green-coloured and thered-coloured Halorhodospira species (Imhoffet al., 1979). Halorhodospira abdelmalekii, Halor-hodospira halochloris, and in particular Halorho-dospira halophila are among the most halophilicphototrophic bacteria known (Imhoff, 1988). Iso-lates ofHalorhodospira halophila from soda lakesin the Wadi Natrun have salt optima of 250‰total salts and can survive in halite-saturatedsolutions (Fig. 3).

Oren (2001) has shown that in general in salineecosystems the bioenergetic constraints of vari-ous metabolic pathways at the cellular level definethe upper salinity limit at which the differentdissimilatory processes can occur (Fig. 4). Dissim-ilatory sulphate reduction of a lactate substrateprovides relatively little energy, and so the needto spend a substantial part of the cell’s availableenergy for the production of organic osmotic sol-utes probably sets the relative low upper limit tothe salt concentration at which sulphate-reducingbacteria can grow (Oren, 2001).

Our understanding of which microbial speciesdominate the halobiota at elevated salinities isnot yet fully developed. As Ventosa (2006) empha-sized, numerous ecological studies have demon-strate that haloarchaea may reach high cell densi-ties (>107 cellsmL�1) in such hypersaline waters.Traditional microbial studies based on cultivationof viable cells from samples collected in suchwaters suggested that the predominant speciesfound in most neutrophilic hypersaline environ-ments were related to the genera Halobacterium,Halorubrum,Haloferax andHaloarcula.However,more recent molecular ecological studies based oncultivation-independent methods indicate that, inmost natural hypersaline environments, membersof these now well-documented halophilic generaconstitute no more than a small proportion of themicrobial biomass. They are seen more often

because they are more readily cultivated. Severalmore recent studies carried out in actual hypersa-line environments and not the culture dish haveallowed some general conclusions to be drawn(Ventosa, 2006): (a) square haloarchaea are veryabundant, but they have not been isolated (culti-vated) until recently; (b) many environmentalclones within the haloarchaeal group are alsoobtained from natural hypersaline settings that arenot phylogenetically closely related to previouslydescribed cultivated species of archaea and bacter-ia. In other words, the search to define the numberof halophilic species and their relative contri-bution to the biomass made up haloadaptivemicrobes has only just begun.

Cellular biochemical adaptations to hypersalinity

Halotolerant and halophilic species have devel-oped special biochemical mechanisms to copewith life’s fatal propensity to desiccate inmesoha-line and hypersaline waters, namely; motility,slime, osmolytes and halo-adapted cellular mem-branes and proteins. Many of the halotolerantcyanobacteria (still called “blue-green algae” bymany geologists) form a significant componentof photosynthesizing microbial mats in modernsabkhas and shallow brine lakes subject to bothperiodic desiccation and hypersalinity. Suchmicrobial mats show a worldwide recurrenceof a few cosmopolitan cyanobacterial species:Microcoleus chthonoplastes; Lyngbya sp.; Ento-physalis sp.; and Synecococcus sp. All of thesemat-forming taxa are embedded in matrices ofextracellular polymeric mucous (slime), whichhold large amounts of water to protect the photo-synthesizing cell from osmotic stress and act asa buffer against extreme temperatures and ultra-violet rays (Gerdes et al., 2000a, 2000b).

Aside from a greater likelihood of subaerialdesiccation, one of the effects of increasing salinityis to increase osmotic pressure on all cellular lifefloating in a brine column. It may well be that thedominant biomass control in subaqueous hyper-saline and supersaline environments is not low-ered oxygen levels but increased osmotic pressure.At a concentration of 300‰, a sodium chloridebrine exerts an osmotic pressure on a cell of morethan 100 atmospheres (Bass-Becking, 1928; Reedet al., 1984). Cells of haloxene species that typi-cally inhabit marine or brackish waters quicklydesiccate in such brines, leading to rapid death(e.g. Geddes, 1975b).


Accidental exposure of pelagic and bottom-living metazoans to osmotic stress and anoxiaassociated with hypersaline bottom waters hascontributed to many ancient lagerstatte associa-tions (fossil “death communities”), along with theinherent excellent preservation of fine details ofthe entrained largely undecomposed fossil forms.For example, there are the numerous “death-dance” trackways in the Cretaceous Solnhofenmicritic plattenkalk of Bavaria. The tracks leadto the fossil remains of intimately preserved mar-ine crustaceans that once wandered into the highosmotic pressures associated with hypersalineand anoxic bottom-waters of the lagoon that nowpreserves their remains (Viohl, 1996). Likewise,the feathers and skeleton of the bird-like dinosaurArcheopteryx were well preserved by the sameanoxic hypersaline bottom waters.

Communities of haloxene chemosynthetic mus-sels, which inhabit nutrient-rich deep dark bot-toms about the edges of modern anoxic brine lakesatop dissolving salt allochthons, can suffer massextermination and immaculate preservation whensediment slumps occur and these mollusc bios-tromes are carried into lethal anoxic H2S-richhypersaline waters of the brine lake on the deepseafloor (MacDonald, 1992). Rich fossil-fish layerscharacterize subaqueous lacustrine laminatedsediments of the Laney Shale Member of EoceneGreen River Formation. Almost all the fish in thelagerstatte are freshwater species, and this deathassemblage indicates the presence of inimicalbottom waters tied to a salinity-stratified watercolumn. This stratified column formed during thefreshened highwater stage of the lake when dis-solution of the underlying sodic evaporites of theWilkins Peak Member released brines that createda condition of perennial anoxia in the deeper partsof lakewater column (Boyer, 1982). A similar brinecolumn stratification probably favoured the pre-servation of organic matter in the muddy lacus-trine/lagoonal sediments that overlie theMesozoicPurbeck evaporites that crop out along the Dorsetcoast (Schnyder et al., 2009).

Microbes that flourish inhypersalinewaters haveadaptedat the cellular level to survive the increasedosmotic stress that accompanies increased salinity.At the intracellular molecular level, Dunaliellaparva, a halotolerant unicellular green alga thatflourishes in mesohaline waters worldwide (opti-mum �120‰, survival 20–340‰), distributes gly-cerol throughout its cytoplasm. This increases thetotal solute concentration in the cell and so the

algae can better cope with the high osmotic pres-sure of its high salinity surrounds. Glycerol is anosmotically active substance (osmolyte) that takesup space in the cellular fluids. It lowers the relativewater content of the cell and so raises the internalosmotic pressure. Cytoplasmic concentrations ofglycerol in Dunaliella parva can reach 7mol L�1

and can constitute over 50% of the dry weight ofcells growing in salinities �280‰. Glycerol is alsoused as an osmolyte by other halotolerant andhalophilic algae, as well as yeasts, fungi and brineshrimp. Halotolerant and halophilic prokaryotescan use a variety of other sugars, sugar alcohols,amino acids and compounds derived from them(such as glycine, betaine and ecotoine) as osmo-lytes, leading to characteristic biomarker assem-blages in ancient saline sediments.

In contrast to an osmolyte solution, halophilicarchaea have two main defence mechanisms tocope with the extreme osmotic gradients inducedbyhypersaline to supersalinewaters.One is amodi-fication of the plasma (cell) membrane; the other isan adaptation the protein structure itself. Unlikemost cell membranes, the plasma membrane ofhalophilic archaea is dominated by rhodopsins andthe cell membrane does not actively exclude salts,so the overall internal salt concentration in halo-archaeal cytoplasm is high. This adaptive mech-anism is sometimes called the “salt-in” strategy.However, the cellmembrane is selective, it tends toexclude sodium, while actively pumping potas-sium into the cell against a thousand-fold concen-tration gradient. The total ionic strength remainsthe same on both sides of the plasma membrane,but the ratios of specific ions differ inside andoutside the cell wall. Potassium is the dominantcation within the cell, many cell functions requirepotassium, but would be disrupted by high levelsof sodium. Cells of halophilic archaea can con-tain up to 4mol L�1 of potassium chloride, whichis eight times its concentration in seawater. Anae-robic bacteria of the order Haloanaerobiales usea similar “high potassium in the cell” strategy, asdoes Salinibacter ruber (Oren, 1999b).

Halobacterium halobium is a well-studiedexample of a well-adapted halophilic archaea; itscell carries a combination of orange-red carotenoidpigments, mostly b-carotene (C-40), and bacterior-uberins (C-50). It is an aerobe-facultative anaerobe.When oxygen levels fall, but light penetrates thebrine, photophosphorylation takes place in theabsence of chlorophylls and redox carriers, sowaters and sediments where it flourishes can take

334 J. K. Warren

on a blue or purple tint. Bacteriorhodopsin’scharacteristic purple colour has led to manyhaloarchaea in their photo-active stage beingdescribed historically (pre-genomic) as purplebacteria, not archaea. The main cellular metabo-lism of Halobacterium halobium is heterotrophicin brines with higher oxygen levels, and itflourishes in such conditions in Great Salt Lake,Solar Lake and Lake Magadi.

Cells in the heterotrophic mode are mostlycoloured by carotenoids, and waters where it isthriving appear red. This normal respiratory meta-bolic chain depends on b and c cytochromes aswell as cytochrome oxidase to create ATP. This isnot a particularly unusual metabolic pathway formost life forms, except that in this case the cellitself is halophilic. As a result, in brines withrelatively high levels of oxygen, these highlysalt-adapted halophilic cells respire and produceATP using their red membrane (carotenoids).Under anaerobic conditions they can survive butproduce lesser volumes of ATP, either by fermen-tation of arginine or by anaerobic respiration withfumarate as an electron receptor. It means that theycan still live, although at lower metabolic rates,in well-lit dysaerobic to anoxic hypersaline con-ditions as they utilize their purple membranepatches to pump protons and so maintain theircellular metabolism (Oesterhelt & Marwan, 1993;Kates et al., 1993).

Some halophilic archaeal strains, includingHalobacterium, contain another rhodopsin pig-ment in their purplemembrane calledhalorhodop-sin. This acts as a Cl-pump, once again suitable forgenerating energy in highly saline conditions. Itis usually present in the cell membrane in muchsmaller amounts than bacteriorhodopsin, but con-tains the same retinal pigment. It too absorbs light,which it converts to an ion gradient. However,instead of pumping protons out, like bacteriorho-dopsin, it pumps chloride ions inwards, whichhelps maintain osmotic balance in highly salineconditions. Since chloride ions have a negativecharge, moving chloride inwards is equivalent interms of energy tomoving a proton outwards. Thushalorhodopsin generates a chloride ion gradient,which also supplies energy to the cell.

Membrane adaptation shifts the osmotic balanceproblem from the cellular to the molecular level.Ions within the cell’s cytoplasm still compete withproteins and other biomolecules for that universalsolvent, water. In order to cope with high osmoticstress at the molecular level, halophilic archaeal

proteins have evolved so as tomaintain a high neg-ative charge on the protein surface. This attractswater molecules and envelops the protein in aprotective shroud of bound water.

Consider the halophilic archaea Haloarculamarismortui, which flourishes during times offreshened surface waters in the Dead Sea. Proteinsof its metabolic enzyme (malate dehydrogenase)and its electron transfer protein (ferredoxin) arewrapped in coats of acidic amino acid sidechainsso that both proteins carry a negative charge inneutral media. A predominance of charged aminoacids on the surfaces of cellular enzymes andribosomes better stabilizes the hydration shell ofthe various cytoplasm molecules, even when theextracellular brines are well into the halite satura-tion field. This high-density surface charge bindswater molecules to the protein surface much moreeffectively than any mesophile protein. Hence,Haloarcula proteins do not dehydrate or unfold(denature) even when exposed to extremely highsalinities. However, the high levels of shieldingcations are lost by diffusion in low salinity envir-onments and an excess of negatively chargedions then destabilizes the molecular structureby ionic repulsion and so intracellular proteinstend to lyse or disintegrate. This means any spe-cies using a “salt-in” cytoplasm strategy has aninnate restriction to highly saline environments(obligate halophiles) and does not cope well withrapidly oscillating schizohaline waters. Ironi-cally, intracellular acids that unfold normal pro-teins in non-halophiles counteract this tendencyin the halophiles.

In summary, bioadaptations at the cellular levelto highly saline conditions can be divided into twogroups of responses (Oren, 2001):

(a) The “high-salt-in” optionAccumulation of salts in the cytoplasmare maintained at concentrations equal to orhigher than those of the outside medium.Generally KCl is used as the main intracellularsalt. Aerobic halophilic archaea (familyHalobacteriaceae) utilize this strategy, as dofermenting bacteria, eubacterial acetogenicanaerobes (Haloanaerobium, Halobacteroides,Sporohalobacter, Acetohalobium), the extre-mely halophilic Salinibacter ruber and somesulphate-reducers. Energetically, this strategyis relatively inexpensive, but requires far-reaching adaptations of the intracellular enzy-matic machinery to the presence of high salt


concentrations. Cells utilizing this strategyshow limited adaptability to changing salt con-centrations (obligate halophiles) and do bestin environments where long-term salinitiesremain elevated. That is, they do best in theperennial hypersaline portions of salt lakessuch as the upper water mass of the Dead Seaand do not do as well in parts of the deposi-tional setting characterised by rapid and fre-quent bouts of schizohalinity.

(b) The “low-salt-in” optionExclusion of salts from the cytoplasm and theaccumulation of organic osmotic “compatible”solutes (osmolytes) may be employed to pro-vide osmotic balance. This strategy is used byhalophilic and halotolerant eukaryotal micro-organisms, by most salt-requiring and salttolerant bacteria, and also byhalophilicmetha-nogenic archaea. This strategy is energeticallyexpensive; the energetic cost depends on thetype of organic solute synthesized. No majormodification of the intracellular machinery isneeded compared to non-halophiles, and inmost cases cells can rapidly adapt to changesin salinity. As such, they do better than the“salt-in” biota in conditions of rapid and fre-quent schizohalinity.

As Oren (2001) clearly illustrated, organismsliving in increasingly high salinity environmentshave to devote increasing large proportions of theirbioenergetic budgets to osmoregulation, either tosynthesize organic solutes or to activate and main-tain ionic pumps. This creates a natural salinity-related control over various metabolic pathwaysand their energy efficiencies and hence to biomar-ker distributions in the resulting sediments. Thefollowing metabolic adaptations and groups func-tion best at high salinities (Fig. 4):

(1) Processes that use light as energy source andare generally not energy-limited;

(2) Heterotrophs (bacteria as well as archaea) thatperform aerobic respiration, denitrification,and other dissimilatory processes that yieldlarge amounts of ATP;

(3) All types of metabolism performed by organ-isms that use the “high-salt-in” strategy, even ifthe efficiency and amount of ATP obtained intheir dissimilatory metabolism is low.

Thus, the growth of phototrophic microorgan-isms in hypersaline surface waters is generally

limited by the availability of inorganic nutrientsandnot by lackof light energy (Oren, 2001).Accord-ingly, both oxygenic (Dunaliella, cyanobacteria)and anoxygenic phototrophs (Halorhodospira,Thiohalocapsa, Halochromatium) produce organicsolutes for osmotic stabilization.Theymaybe foundup to very high salt concentrations and in severalcases survive well into the halite-saturation field.However, in the case of chemolithotrophs and anae-robic heterotrophs, the amount of energy generatedin the course of their dissimilatory metabolism isoften insufficient to supply the demands of cellgrowth, osmotic adaptation, and life maintenance.Long-term growth and survival in hypersalineenvironments is not possible in such species. The“high-salt-in” strategy is preferable for stronglyenergy-limited organisms (haloarchaea) as it isenergeticallymuch less costly than the productionof organic osmotic solutes. Oren (2001) documen-ted an excellent correlation between the amountof energy generated in the course of the differentdissimilatory processes and the salinity-relatedoccurrences of various metabolic styles (Fig. 4).Clearly the resulting biomarkers from the variousmetabolic pathways will likewise preserve sali-nity-related indicator markers in the rock record.

Biomarkers and microbial responsesto salinity changes

The salinity-controlled transition between a halo-tolerant and halophilic biota can been seen in theirorganic residues and subsequent biomarkers pre-served in evaporitic source rocks. Biomarkerscan be thought of as molecular or chemical fossilswhose basic carbon skeleton is derived from once-living organisms and are found in modern sedi-ments, as well as in petroleum and rock extracts.They can provide information about species diver-sity, depositional environment, thermal maturity,migration pathways and hydrocarbon alteration(Peters et al., 2005a, b).

Commonly accepted environmental generaliza-tions based on biomarkers include the notion thatvariation in the ratio between the isoprenoidspristane and phytane indicates oxidizing versusreducing conditions (pristane and phytane areboth breakdown products of chlorophyll). In anoxidizing environment the cleavage of the phytolside chain of chlorophyll is followed by decarbox-ylation to produce phytane. In a reducing envi-ronment the sidechain cleavage of chlorophyll isfollowed by its reduction to ultimately produce

336 J. K. Warren

pristane. Low pristane/phytane ratios in marineand terrestrial settings are thought to indicatereducing conditions, while higher values (>1)indicate oxidizing conditions (Table 4). Philp &Lewis (1987) have shown that the chemistry ofchlorophyll breakdown ismuchmore complicatedin many natural systems, and that variations inthe ratio may also indicate varying inputs fromarchaeal membranes, which contain much higher

levels of phytane chains than bacteria and candominate the halobiota at higher salinities.Phytane can also come from bacteriochlorophyll-aand tocopherols, which can also be locallycommonplace (Peters et al., 2005a, b; Koopmanset al., 1999).

Likewise, differences in the distribution ofn-alkanes are thought to indicate depositionaldifferences 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 underhypersaline depositional conditions. High values indicate stratifiedwatercolumn during source deposition (Sinninghe Damste et al., 1995).

Pristane/phytane Very low values (<0.5) in oils derived from source rocks deposited underhypersaline conditions, indicates contribution of phytane fromhalophilicbacteria/archaea (ten Haven et al., 1987, 1988).

Acyclic isoprenoids Acyclic isoprenoid hydrocarbons are the predominant components in theorganic matter extracted from sedimentary cores and oils of varioushypersaline settings (Wang, 1998).

Low diasteranes Oils from the hypersaline sources typically have very low amounts ofdiasteranes, which commonly suggests a source rock that has low contentof catalytic clays, consistent with carbonate or evaporite source rocks(Mello & Maxwell, 1991; Peters & Moldowan, 1993). The amount ofdiasteranes in oils also decreases in highly reducing noncarbonateenvironments with increasing salinity (Philp & Lewis, 1987).

Other biomarkers Even-over-odd dominance in the n-alkanes, presence of b-carotene andc-carotene, dominance of the C27 steranes.

Organic sulphurcompounds

There is a high abundance of organic sulphur compounds (thiolanes,thianes, thiophenes and benzo-thiophenes) in many anoxichypersaline settings (Wang, 1998). The distributions of the C-20isoprenoid thiophenes in combination with those of the methylated2-methyl-2-(4,8,12-trimethyltridecyl) chromans can be used todiscriminate non-hypersaline from hypersaline paleoenvironments(Sinninghe Damste et al., 1989)

Carbon isotopes Heavy 13C values (�20 to �30‰) are consistent with typical saline lakeenvironments 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 depositedunder anoxic conditions (Peters & Moldowan, 1993). Abundance of C35

homohopanes in oils (relative to C31–C34 homopanes) is correlated withsource rock hydrogen index (Dahl et al., 1994).

Pristane/phytane >1.0 can indicate anoxic conditions, but the ratio is affectedby many other factors.

Isorenieratane &derivatives

Presence in oil indicates anoxic photic zone during source rockdeposition, these compounds are biomarkers for green sulphur bacteria(Summons & Powell, 1987).

V/(V þ Ni) Porphyrins High¼ 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 Presence¼ lacustrine source. Absence¼meaningless (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).


higher plants have significant concentrations of thelong chain C22–36 alkanes with a pronounced odd/evendistribution (Fig. 1A).Suchorganics tend toberelatively rare in evaporitic source rocks, unlesssurface waters were periodically freshened by run-off from the land. Much of the terrestrial organicmaterial entering an evaporitic depressionhas beenoxidized and biodegraded before it makes it to thefinal site of deposition on the brine pool floor. Incontrast, a high algal input is thought to be char-acterized by n-alkanes in the C16–18 region.

Waples et al. (1974), along with ten Havenet al. (1986), noted that Tertiary sediments depos-ited in saline evaporitic lagoons possess high con-centrations of regular C25 isoprenoids (Table 4).The activities ofChlorobiaceae, an anaerobic greensulphur bacteria, thought to flourish inmesohalineto hypersaline seaways, leads to the preservationof a series of 1-alkyl-2,3,6-trimethyl benzenes,thought to be derived from the breakdown ofaromatic carotenoids in sulphate- and sulphide-rich brines (Summons & Powell, 1987). ten Havenet al. (1988) went on to propose a number ofbiomarker indicators of hypersalinity, includingshort-sidechain steranes and5a(H), 14b(H), 17b(H)pregnanes and homopregnanes, as well as highgammacerane indices (gammacerane/C30 hopane).Gammacerane is a pentacyclic C30 triterpanethought to be a diagenetic alteration product oftetrahymenol, a natural product produced by bac-tiverous ciliates, such as Tetrahymena (Table 4).

At its simplest, much of the utility of biomarkersin saline environments comes fromsalinity-relateddifferences in contribution to organic matter ofthe general categories of primary producers (auto-trophs), namely prokaryotes (cyanobacteria andbacteria) and eukaryotes (higher plants, algae) andthe archaea. Most triterpanes are associated withprokaryotic sources, whereas eukaryotic organismsproduce steranes. Thus, the triterpane/steraneratio can be a rough measure of the prokaryote/eukaryote contribution to the organic material. Assalinity increases, the less salinity-tolerant eukar-yotic organisms (mostly sterane-producing greenalgae) give way to more halotolerant bacteria andcyanobacteria (tricyclic and hopane producers)with a corresponding increase in the triterpane/sterane ratio. Thus high alkalinity/salinity settingsare characterized by tricyclics (C20–C24; m/z 191),b-carotene (C40H56 compound; m/z 125), gamma-cerane (C30 triterpane; m/z 191), all with prokar-yote sources. Hence, high levels of gammaceraneand b-carotene are typically associated with

non-marine highly saline environments (Peters &Moldowan, 1993).

For archaea, the cell membrane itself, due to itsinherent high thermal stability, is a very goodcandidate for a biomarker. Archaeal cytoplasmicmembranes do not contain the same lipids thatprokaryotes and eukaryotes do. Instead, theirmembranes are formed from isoprene chains(ether lipids) made up from C5 isoprenoid units(as for the side chains of ubiquinone) rather thanC2 units (ester lipids) in the normal fatty acids ofthe non-archaea (Fig. 7A). Moreover, the isopre-noid chains are typically attached to glycerol byether linkages instead of esters. Thus the cell wallof archaea is constructed of lipids, mainly ofglycerol, connected to phytanyl chains 20 carbonsin length by ether bonds to form phytanylicdiether. Typically these are organized in bilayers.In the case of archaea living in extreme con-ditions, two glycerol molecules can be connectedto a double chain of phytanol to create a tetra-ether structure of forty carbons (Fig. 7B). Iso-prene derivatives indicative of ancient archaeahave been found in Mesozoic, Palaeozoic, andPrecambrian sediments (Hahn & Haug, 1986).Interestingly, their chemical traces have evenbeen found in sediments from the Isua districtof West Greenland, the oldest known sedimentson Earth, some 3.8 billion years old.

Lipids entrained as organic residues in modernevaporitic carbonate and gypsum from modernsaline pans (mesohaline and lower penesalinewaters), aremostlyderived fromcyanobacteria andheterotrophic bacteria. Their n-alkane distributionsshow a high predominance of n-docosane. Thus,in the evaporitic carbonate domain (mesohalinewaters), the presence of the C20 highly-branchedisoprenoid olephines, tetrahymanol and largeamounts of phytol constitute precursors to mostlipids found in buried evaporitic sediments. Incontrast, the main lipid contributors in organicsaccumulating in halites and bittern beds can be theextremely halophilic archaea and their organicsignatures are enriched in the isoprenoids, espe-cially phytane (Barb�e et al., 1990; Wang, 1998).However, both archaea and halophilic bacteriacan flourish in upper penesaline and supersalinewaters at salinities higher than 200–250‰, so thebiomarker signatures are not mutually exclusive(Caumette, 1993; Ollivier et al., 1994). Any high-salinity biota also includes the metabolic productsof fermentators, homoacetogens, sulphate-reducersand methanogens.

338 J. K. Warren

A predominance of degraded green algal andcyanobacterial biomarkers in mesohaline settingsis indicated by biomarkers preserved in organi-cally immature, evaporitic mesohaline laminatesat the base of the Permian Zechstein evaporitesuccession in NW Europe (Bechtel & Puttmann,1997; Pancost et al., 2002). There the degree ofmethylation of 2-methyl-2-trimethyl-tridecylchro-mans (MTTCs) and the abundance of maleimidesand bacteriochlorophylls in the organic-richKupferschiefer shales at the base of the Zechstein

evaporite succession implies a subaqueous euha-line to mesohaline (�30–40‰) transition into ahypersaline marine-fed drawdown basin. Thesebiomarkers are thought to have been derived fromgreen/purple sulphur bacteria (decomposers)within organic-rich laminites and suggest that thebottom waters were saturated with H2S at the timeof deposition. Maximum water depths were prob-ably less than 100 metres (it was a stratified meso-haline drawdown basin at the onset of Zechsteinsalinity; Warren, 2006). Decomposers probably

Biphytanyl glycerol

Diacyl glycerol

HeadgroupHeadgroup Hydrophobic core

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OH

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Lacustrine CretaceousBucomazi Formation

Angola

Fig. 7. Biomarkers: lipid structures and some rock characteristics. (A) Lipids fromarchaea andbacteria.Upperportion showshowphosphatidylanolamine forms a bi-layer lipid in bacterial cells. The acyl chain is usually, but not always straight. Somebacterial lipids have a methyl branch of a cyclohexal group at the end of the acyl chain, other lipids have one or moreunsaturated bonds and the connection of glycerol to the acyl chain is via an ester linkage. The lower part showshow lipids aremonolayers in archaea and the phytanyl chain contains isoprenoid-like branches. An ether linkage connects the phytanylchain. Archaeal membranes also contain bilayer-forming diether lipids. (B) Relationship between pristane/phytane and themethyltrimethyltridecylchhroman (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 thegammacerane index for oils from lacustrine source rocks in Angola (inset shows gammacerane structure). Independentbiomarker evidence suggests a marine source for the point that lies off the shaded trend (after Peters et al., 2005a).


lived near the brine boundary between the photiczone and the anoxic (euxinic) bottom water attypical water depths of 10–30 metres below thewater surface, as in modern marine-fed density-stratified systems, much like in Lake Mahoneytoday (Overmann et al., 1996). Primary productionin the upper water column was dominated byphotosynthetic cyanobacteria or green algae,whilesulphate reduction in the sediment was tied tothe availability of abundant sulphate and organicdetritus from the overlying water column.

Methanogenesis was also active in or at thebase of the water column during Kupferschieferdeposition. This is reflected in the light carbon-isotopic composition of organic matter that hadoriginated via recycling of CO2 generated bymethane-oxidizing bacteria in the water column(Bechtel & Puttmann, 1997). Saccate pollen is theonly morphologically preserved body fossil inorganicmatterwithin the laminatedKupferschiefersediment, all other traces of cellular morphologiesare gone. Euxinic (anoxic) conditions were con-firmed by Pancost et al. (2002) over a much largerarea of Kupferschiefer deposition than studiedby Bechtel and Puttmann (1997). They concludedthat almost all of the Kupferschiefer seaway wassubject to periods of photic zone stagnation andstratification during the early mesohaline historyof the Zechstein Sea.

By themselves, high pristane/phytane ratios,high amounts of gammacerane, and high MTTCratios are not totally reliable indicators of hyper-salinity.More reliable determinations can bemadewhen two or more of these biomarkers are cross-plotted and the resulting output shows a consis-tent trend. Figure 7B plots pristane/phytane ratioagainst the MTTC ratio in the Jurassic Malm Zetalaminites of eastern Bavaria in SW Germany(Schwark et al., 1998). The plot shows a covariantdecrease in the twomeasures, which is interpretedas indicating a trend from normal marine to meso-haline deposition.

A similar covariant trend can be seen in salinelacustrine source rockswhen the pristane/phytaneratio is crossplotted against the gammaceraneindex inMesozoic source rocks from offshoreWestAfrica (Peters et al., 2005a). Figure 7C plots varia-tions in pristane/phytane (a redox and archaealindicator) and gammacerane index for oils froma set of lacustrine source rocks. Increasing salinityin the depositional setting explains the covari-ant trend in the plot, whereby higher salinitywas accompanied by density stratification and

associated reduced oxygen-levels in bottomwaters.Independent biomarker evidence suggests a mar-ine source for the point that plots off the shadedsalinity trend in this figure.

Although the levels of entrained organics arevery low, similar covariant trends in pristane/phytane and gammacerane occur in C21–25 isopre-noids, along with relatively heavy d13C signatures,in biomarkers extracted from the Miocene halitesof the halokinetic SedomFormation in Israel. Theyindicate a predominance of halophilic archaeawhen the salt was deposited in a CO2 limitedsystem (Grice et al., 1998; Schouten et al., 2001).

Light and sulphide inmodernhypersaline envir-onments typically occur in opposing gradients,so the growth of halotolerant andhalophilic photo-trophic sulphur bacteria is confined to narrowzones of overlap in stratified brine or water col-umns. In Precambrian sediments bacterial lifeforms were much more widespread in any watermass as the column was mostly anoxic. For exam-ple, in Neoproterozoic and early Cambrian hyper-saline settings such as the Ara Salt Basin ofOman there were no higher life forms present inthe depositional setting, and so this possibly nor-mal-marine setting, and the subsequent encase-ment in salt, led to preservation of a unique setof bacterial biomarkers in blocks of salt-encasedmarine platform source rocks (Terken et al., 2001;Schoenherr et al., 2007).

The presence of mesohaline and marine carbo-nate muds, rather than aluminosilicate clays, inthe matrix of many buried organic-rich evaporiticsource rocks can change maturity and migrationparameters comparedwith shale source rockswithnon-carbonate matrices. For example, mesohalinecarbonate source rocks are susceptible to earlygeneration of bitumens and volatiles comparedwith terrigenous shales (ten Haven et al., 1986;di Primio & Horsfield, 1996). The proportion ofbitumens (extractables) in the organics of carbo-nate source rock is high compared with that ofshales, as most mesohaline carbonates are largelyisolated from high levels of terrigenous influxand the associated load of “spent” or oxidizedterrestrial organic matter (Warren, 1986). Forthe same reason, much of the early asphaltic(hydrogen-prone) product in a mesohaline carbo-nate laminite begins to migrate early in the burialhistory, driven in-part by recrystallization of thecarbonate matrix, whereas similar materials areheld to greater burial depths in the lattice of alu-minosilicate clays (Warren, 1986; Cordell, 1992).

340 J. K. Warren

Espitalie et al., (1980) showed that carbonatesource rocks are likely to provide larger volumesof hydrocarbons for pooling compared with analo-gous terrigenous shales for the same levels of TOC.Geochemical analyses show that heavy oils fromcarbonate source rocks can form at marginallymature stages and at lower temperatures thanrequired for oil generation from terrigenous shales(Jones, 1984).

Lastly, some widely-used biomarker-derivedmaturity indicators formulated in marine sedi-ments, are not as reliable in relatively young sal-ine-lacustrine basins or in hypersaline oils withhigh sulphur contents, such as those sourced fromhypersaline Oligocene laminites in the northernQaidam Basin, China or the Miocene mesohalinecarbonates of the Mediterranean (Hanson et al.,2001; di Primio & Horsfield, 1996). The discre-pancy between mature indications coming fromvitrinite in these very young evaporitic sourcerocks and the immature indications derived fromvarious sterane isomerization ratios or other stan-dard source rock evaluation techniques, are in partexplained by a lack of time for various steraneequilibria to develop and by the complicatingeffects of high sulphur levels on reaction kineticsin systems with high levels of early asphaltenes.Some of these hypersaline heavy oils in Chinacome from hydrogen-rich type-I lacustrine sourcesthat may be as little as 3 million years old in theQaidam Basin.

LAYERED BRINES AND ORGANICSIGNATURE

So far the biological factors and metabolic path-ways that control the type and volume of organicmatter accumulating in saline settings have beendiscussed,withoutmuch consideration of the phy-sical conditions or hydrologies that control thecondition or position of the brine and pore fluidsin which the organics accumulated. The presenceor absence of organics in an evaporite basin ispredicated on suitable hydrologies to manufacturethe requisite factors to create anoxia. Penecontem-poraneously, the hydrological conditions of earlyburial control whether organics are to be preservedin its evaporitic matrix until any protokerogen issufficiently buried to evolve into a source rock.Brine density increases with increasing salinity,so influxes of less dense brines into an evaporiticdepression create a layered system where lower

salinitywaters tend tofloat on topof higher salinitywaters. Depositional hydrologies in all modernand ancient evaporite systems are accordinglylayered and, as will be demonstrated below, thestability, temperature and salinity range of thislayering largely controlswhether andwhere organ-ic matter accumulates in an evaporitic depression.

Almost all primary organic matter in an evapori-tic source rock was first photosynthesized insurface brines outcropping at the top of the activephreatic zone or its capillary fringe. An activephreatic flow regime encompasses the zones ofseepage outflow, brine/seaway ponding, brinereflux and meteoric flow. The brine surface of aperennial brine lake or seaway is the outcroppingexpression of the regional water table, and inmarine-drawdown basins is by definition lowerthan sea level. In the surrounds,where the regionalwater table comes near the landsurface, the top of acapillary fringe may be the outcrop expression ofthe same regional water table and so is the depo-sitional area where sabkhas dominate (Warren,2006). Solar evaporation concentrates waters inboth ponded and vadose settings to form matricesof bottom-nucleated and sabkha salts, respectively.Depressionswith surface andnear-surface brines inarid settings indicate groundwater discharge zonesand their long-term outcropping creates dischargeplayas and ancient evaporite seaways.

Where areas of strong topographic relief definethe margin of a modern evaporite basin, bothunconfined and confined meteoric waters typi-cally discharge into the edges of a brine-saturateddepression, as inmodern continental rift valleys ofthe East African rift, or in a transtensional basin-and-range setting of the American southwest, orin the Dead Sea of the Middle East. Farther out,beneath the more central and topographicallylowest parts of the evaporite depression, density-induced brine reflux, andnotmeteoric throughput,is the dominant process driving shallow-subsur-face brine flow. The saline water mass driving thisreflux may be an ephemeral or perennial holomic-tic surface water. Which hydrological style of sur-face water dominates in an evaporite basin(ephemeral versus perennial) is in part related tothe steepness of the surrounding topography andthe presence or absence of a hydrological conduitfor water outflow (Warren, 2006).

In a large evaporite drawdown basin, such as inthe Mediterranean in the Late Miocene, the basintypically had no surface connection to the ocean,and the level of the discharge zone and the water


surface of the perennial brine discharge lakewas attimes thousands ofmetres belowsea level. Gravity-induced seepage and associated evaporation ofsurface waters cycled huge volumes of marine/meteoric waters through the depression’s sur-rounds and into the drawdown depression. Refluxbeneath a stratified perennial meromictic watermass is at its maximum when the brine columnis holomictic (Warren, 2006).

Hydrologies in saline basins

Hydrological settings that allow most evaporiticcarbonates and associated organics to accumulatecan be divided into two end member situations:

(1) a perennial seawayor a brine lake that at times isdensity stratified; and (2) an evaporitic mudflat(sabkha) with a surface defined by the top of thecapillary fringe and itsmost salinewater lying at orjust below the sediment surface. A common inter-mediary stage is anevaporiticmudflat occasionallycovered by thin sluggish brine sheets (salt pan).The hydrology of an evaporitic mudflat and itslandward surrounds is controlled by the positionof the water table in the sediments (Fig. 8A). Poresbelow the water table are filled by brine and makeup the phreatic or saturated zone where the water-volume saturation is total (equal to 1 or 100%). Thephreatic zone is the region where gravity-drivengroundwaters seep down the potentiometric slope

Unsaturatedzone

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halocline thermocline

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hypersaline

hypersaline

bottom nucleates

pelagic cumulates

Holomictic

A

B

Capillaryfringe

Fig. 8. Hydrological classification in saline settings. (A) Hydrological zonation in an evaporitic mudflat (sabkha) and itslandward surrounds. (B) Water mass zonation in a perennial brine lake or seaway (after Warren, 2006).

342 J. K. Warren

toward discharge zones (forced-convection) anddense free-convecting brines sink into underlyingstrata. Above the water table is the vadose zone,where pores are filled by a combination of soil airand varying levels of water and brine and water-volume saturation is less than one.

Vadose hydrologies

The vadose zone in dry mudflats contains anuppermost interval where the water content andthe oxygen/CO2 content of the porewaters can varyconsiderably and is known as the soil moisturezone. Light rains on a dry mudflat typically pene-trate the soil moisture zone but are not sufficient involume to saturate the pore space of the wholevadose zone, and so are returned to the atmospherevia evapotranspiration without ever replenishingthe water table (Wood et al., 2002). Fluctuatingevapotranspiration levels in this zone vary widelybetween storms, driven in part by the metabolicactivities of the soil biota, by mean moisture con-tents, and by varying O2 and CO2 levels. Pedogeniccarbonates and more soluble salts are precipitatedas surface crusts and near-surface cements as aresult of these fluctuations.

Ongoing and periodic oxidation of this vadosehydrology means any hydrogen-rich microbialmaterial tends to be decomposed/oxidized priorto burial. Dry mudflats in saline depressions arenot areas with any potential for long-term preser-vation of elevated amounts of hydrogen-proneorganics. With the next heavy rain the less solublecarbonate precipitates remain, while the moresoluble salts tend to be flushed through a now-saturated vadose profile to enter the water table.There they continue to flow as dissolved phreaticsalts into the discharge depression where evapora-tive concentration once again reprecipitates themas wet sabkha and brine pool salts.

The lower part of the vadose zone beneath a drymudflat is made up of the capillary fringe. In partsof an evaporitic mudflat (sabkha) depression thatare actively accumulating displacive salts, the topof capillary fringe is at or above the land surface(Fig. 8A). This allows the concentration of porebrines to the attain hypersaline levels needed toprecipitate the nodular and displacive salts thattypify wet sabkhas and salinemudflats. Unlike thedry parts of a playa or mudflat, the inherently wetcapillary surface facilitates long-term evaporativeconcentration of the near-surface pore brines andthe ongoing crossflow of dense brine into

sediments below the water table (sabkha-drivenbrine reflux). As long as brine can be supplied froman updip source, closed cellular flow beneath thewet sabkha flat is the result. In a capillary zone-bound system that is also subsiding, such wetsabkha hydrologies can retain continual hypersa-line brine saturation with associated dysaerobia oranoxia, and so sequences of hydrogen-pronemicrobial organic matter can accumulate as matsand so be preserved into the burial environment.

Given enough time, waters in a brine plumebeneath a wet sabkha or a periodically holomicticbrine lake will reach the bottom of the basin fill orbe dispersed back into the regional cross flow ontop of any aquiclude it intersects on its way down(Wood et al., 2002; Warren, 2006). In either case,the refluxed waters start to spread laterally andback out toward the basin fringes, so mixing withfresher forced-convection waters beneath the lake,playa or seaway margin. Ultimately this brinereturns to the playa surface, usually in a dilutedform as a component of water-edge spring or seepwaters. This convective flow is an effective way ofmoving salt load through largevolumes of thebasinsediments beneath an accumulating salt bed, andyet still maintain anoxic pore waters beneath awetsabkha or salt lake (see discussion of brine curtainsinWarren 2006).Ongoing recycling of anoxic brinebeneath a salt lake or seaway in-turn aids in thepreservation of organic material. Thus, organicsdeposited in a perennial wet sabkha or salinemudflats with a long-term reflux curtain have thepotential to be preserved as hydrogen-prone organ-ics until the sediment passes into the zone ofcatagenesis.

Even so, outcropping capillary-fringe areaswhere brine-saturated microbial mats reside aboutthe edge of a saline water body, can be subject toepisodes of water table lowering or to flushing byfresh oxygenatedmeteoric waters. Then themicro-bial organic matter may be intermittently strippedof its hydrogen by aerobic decomposers that willflourish on top of andwithin themats during timesof exposure or pore-water freshening.

Perennial phreatic hydrologies

Permanent brine lakes and ancient epeiric seawayswith variably holomictic water columns drivingstable long-term reflux curtains or plumes, aremuch more likely than wet sabkhas to preservehydrogen-rich organics into the zone of catageneticburial. Surface water-masses within perennial


brine lakes or seaways routinely fluctuate betweenstratified and nonstratified conditions, while thebottom waters typically have a greater propensityto maintain long-term anoxia (Warren, 2006). Anupper fresher (less dense) water layer sits on topof a more saline (denser) lower water mass in astratified system in a perennially brine-filleddepression (Fig. 8B). The narrow zone of transitionin the brine column between the two waters iscalled a halocline or pycnocline. Often a stratifiedsaline lacustrine/seaway system is also thermallystratified and heliothermic, with warmer watersconstituting the lower water mass. The zone oftransition separating the upper and lower watermasses is the called the thermocline, or the che-mocline, or the halocline, or the pycnocline. Ther-mal stratification of brine masses with a cool topand a hot base is opposite to that found seasonallyinmany temperate freshwater lakes and so is some-times called reverse thermal stratification, butheliothermal is a more appropriate term.

Heliothermy is a result of the contrast in specificheat response between less saline and more salinewaters. Specific heat of a brine decreases as thesalinity increases (Kaufmann, 1960). Specific heatis the amount of heat needed to raise one gram of asubstance by1 �C.For a given amount of heat input,a unit volume of hypersaline water will show agreater increase in temperature than a less salinewater. The resulting greater increase in tempera-ture in a lower hypersaline water mass, comparedto an upper less-saline water for the same degreeof insolation, makes brine lakes and seawaysheliothermic; independent of any salinity (osmo-tic) or oxygen stresses, heliothermy can inducepronounced heat stress in any benthic halobiota.Modern heliothermal lakes occur in appropriatelystratified saline water bodies on all continents andinclude numerous saline lakes on the steppes ofRussia, Siberia and Canada, Solar Lake in theMiddle East (Fig. 11B), numerous coastal salinasin Australia, Lake Meggarine in Algeria, Hot Lakein Washington State and Red Pond in Arizona(Hammer, 1986). One of the more unusual exam-ples is Lake Vanda in Antarctica, which has amaximum water temperature of 25 �C below thechemocline (at a depth of 64 m in the water col-umn), yet the water surface remains ice-covered.

Dissolved gas levels and temperature changesassociated with periodically heliothermal bottomwaters create extreme levels of environmentalstress in bottom communities attempting to copewith hypersalinity. For example, oxygen is

supplied to any water body via exchange with theatmosphere and as a byproduct of photosynthesisof the biota living in thewaters. Inwell-oxygenatedwater columns most of the organics produced byprimary production the upper water mass aredestroyed bymicrobial respiration and the conver-sion of organic matter back to CO2. Much of theimproved preservation potential associated with“higher than marine” bottom salinities in layeredmesohaline to hypersaline settings reflects theeffect on biotal diversity of increasingly low levelsof dissolved oxygen and CO2 in the bottom andpore waters on biotal diversity.

Oxygen levels in natural brines tend to decreasewith increasing salinity, independent of biologicalrespiration. If not enhanced by the activities ofbottom-living photosynthesizers, natural bottombrines will be dysaerobic to anaerobic by the timesalinities reach halite saturation (Fig. 9; Kinsman,1973;Warren1986).DissolvedCO2 shows a similardepletion; dissolved CO2 levels in marine-fedmodern salt pans decrease to around 50% of theoriginal value when the brine concentrationsincrease from 1.5 to 4 times that of seawater (Lazar& Erez, 1992). CO2 concentration in brine is alsopH dependent; at a pH of 9 (reached by concentrat-ing seawater to around 70‰) the CO2 content isnear zero (Moberg et al., 1932). Those algae and

BBB

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Fig. 9. Oxygen levels in present-day surface brines underincreasing salinity. Oxygen content of modern seawater is�5.4mgL�1 (after Warren, 1986).

344 J. K. Warren

cyanobacteria, which are dependant on dissolvedCO2 for photosynthesis, will suffer or die at highersalinities.

Stability of brine stratification and anoxiain modern stratified brine lakes

Brine stratification occurs today in all perennialsaline lakes, including many coastal salinas inAustralia, rift valley lakes of theAfricanRift Valleyand the Dead Sea, Israel and most are meromicticand oligomictic (Warren, 2006). Lake Hayward, acoastal salina in Western Australia, typifies suchstratified brine system. It is a sub-sea-level water-filled marine seepage depression with bottombrines possessing ionic proportions similar to thatof seawater (thalassic). The seawater seeps intothe basin as groundwater and there is no hydro-graphic (at-surface) connection to the nearby

ocean. Gypsiferous carbonate muds with organiccontents of 1–5% accumulate on its microbially-bound floor beneath its small shallow perennialbrine pool (0.6 km2 and less than 2–3m deep). Inthe permanently inundated centre of the lake,where waters are 1–2m deep even in late summer,laminated benthic microbial mat communitiesflourish and are dominated by photosynthesizingcyanobacteria (mostly Cyanothece sp.). Filamen-tous Microcoleus sp., along with coccoids,dominate the laminated to pustular mats in theseasonally-desiccated strand zone. Sediments inthe lake centre accumulate under a limnology thatis density-stratified and heliothermal for much ofthe year (Rosen et al., 1995). Meteoric winterinflow creates a well-defined long-term mixolim-nion (Fig. 10A) where an upper, less dense andcooler water mass has salinities ranging from 50 to210‰. It exists from late autumn to early summer

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1985 162 - 187 30.0 - 35.0 200 - 330 0

1986 176 - 210 22.0 - 39.5 41 - 250 0

1987 178 - 184 33.0 - 34.6 140 - 250 0

30 Nov 1988 222 42.4 0 35.4

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

23 Sep 1993 160 28 378 0

Site 2

30 Nov 1988 216 43.2 0 23.8

1989 180 - 192 24 -36 50 -137 0 - trace

Fig. 10. Brine stratification in Lake Hayward waters, West Australia. (A) Seasonal hydrogeochemical evolution. Uppermostplot 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 bicarbonateconcentration decreases, suggesting precipitation of calcium carbonate (aragonite; after Rosen et al., 1995). Lower plotshows saturation state of waters with respect to gypsum. The monimolimnion was saturated with respect to gypsum forsummer 1991–1992 and was near saturation at the start of summer 1992–1993. The mixolimnion is only saturated when thelakewater is homogeneous (afterRosen et al., 1996). (B) Effect of gypsumprecipitationonbenthicmicrobial communities andassociated oxygenation in Lake Hayward, West Australia (compiled from data in Burke & Knott, 1997).


(May to February) as it floats on top of a lowerdenser and warmer water mass (monolimnion)with salinities in the range 150 to 210‰.

Stratification disappears for a few months eachyear from mid-summer to mid-to-late-autumn.During summer thewaters of the upper watermassevaporate and concentrate as their bicarbonatecontent steadily increases. From the onset of stra-tification in late autumn, acrossmid-winter and oninto to early summer the temperature trends of thetwowatermasses are parallel (Fig. 10A). They forma heliothermic systemwhere the lower water massis some 15–20 �C hotter than the upperwatermass.By mid-summer (e.g. January 1992) lower watermass began to cool, while the temperature of theupper water mass continued to rise. Once thetemperatures (and densities) of the two watermasses equalize, they mix as the lake overturns(holomixis) and waters of the lower water mass(the monolimnion) came into contact with theatmosphere once more.

While the water masses are stratified, the che-mocline and the thermocline are sharply definedacross a 10 cm interfacewith a salinity contrast thatmay be as much as 135–140‰ and a temperaturedifference of up to 19 �C. The time of mixing isimmediately preceded by a sharp fall in the level ofbicarbonate in the mixolimnion, suggesting thatfrom late summer to autumn the precipitation ofpelagic calcium carbonate (mostly aragonite) thengypsum occurs in the upper water mass (Fig. 10A,upper plot; Rosen et al., 1995). For example, theupper water mass in Lake Hayward was super-saturated with respect to gypsum and anhydritefrom October 1991 to February 1992 (Fig. 10A,lower plot; Rosen et al., 1996). When the lakemixed from March 1992 until early May 1992, theentire water body was at gypsum saturation, butslightly undersaturated with respect to anhydrite.

A ‘whiting’ (a cloudy white appearance to thewater body)was observed in the lake inMarch, justat the time of first mixing of the lake waters.Analysis by scanning electron microscopy of thecollected filtrate indicated that the “whiting” wascomposed of gypsum and silica from diatom tests.At that time, there was a thin (10–20mm) crustof gypsum accumulating on the lake bottom. Afterthe “whiting”, when the water was unstratified(holomictic), both the monimolimnion and mixo-limnion were near saturation with respect to gyp-sum. Aftermixing, with the next influx ofmeteoricwaters building across the lake water surface, sali-nity stratification re-established itself. Prior to the

long-term stratification that defined the wintermonths, brine layering in the transition to stratifi-cation was not stable as the upper and lower waterbodies remixed a number of times extending overperiods of days before stable stratification set inbymid-winter (Fig. 10A,May–June 1992;M.Rosenpers. comm., 2006).

Lake Hayward bottom sediments also illustratean aspect of pelagic evaporite precipitation thatis probably true for many ancient “deep water”density-stratified saline settings. Namely, thatwhile precipitation of pelagic evaporitic sedimentis seasonal, and it occurs in the surface water masseven as the lake waters are density stratified, bot-tom salts can only accumulate when the wholebrine column is saturated and unstratified (holo-mictic). This is so even if the chemistry of the lowerwatermass is at gypsumor halite saturation almostall year round. Only pelagic sediments (includingcarbonates and organic residues) and terrigenousdetritus (including eolian dust) make it to thebottomwhen a saline lake is perennially stratified,as was the case in the Dead Sea for the 400 yearsprior to 1979 (Warren, 2006).

Intensity of light penetration to the subaqueousbottom of an evaporite-accumulating depressionis a significant control on how much photosyn-thetic oxygen can be generated by the bottom-living microbial community. In Lake Hayward ahealthy mat of photosynthesizing halotolerantcyanobacteria drastically alters the levels of anox-ia in shallow bottom brines. Photosynthesis, viaits benthic microbial mat community, is normallysufficient to maintain supersaturation of the LakeHayward bottom waters with dissolved oxygen,even during periods of brine column stratification(Fig. 10B).

Burke & Knott (1997) found that after anunusually dry year in 1987, the salinity of LakeHayward increased to 260‰ as gypsum precipi-tated throughout the lake waters. Brine turbiditygenerated by the markedly increased pelagic crys-tallization of gypsum in the surface waters in thatyear was sufficient to obscure the benthos comple-tely, despite the shallowness of the lake.As a resultthe amount of oxygenic photosynthesis and aero-bic decomposition was greatly reduced in thebenthic mats and they degraded. During brinestratification in the following winter (1988),bottom waters became anoxic and sulphurous.During the next few years, after each subsequentbrine column overturn, healthy microbial matswere re-established across the lake floor and they

346 J. K. Warren

were able to again supersaturate the bottomwaterswith oxygen year round, as was seen in 1992,which was the time of the Rosen et al. (1995,1996) study.

Development of a healthymat community in theLake Hayward salina prevents periodic bottomanoxia. Nearby lakes, that do not contain a healthymicrobial benthos, tend to anoxia during stratifica-tion. Comparisons between Lake Hayward andnearby lakes clearly show that healthy microbialmats function as a strong homeostatic mechanismin the lake hydrology. Shallow meromictic butperennial salt lakes, with long-term stability ofphotosynthetically elevated oxygen levels in thebottom, tend to have lower levels of preservedTOCdue to the higher efficiencies of halotolerant aero-bic decomposers acting on the benthic organicmatter. This can be seen when comparing TOClevels in the microbial laminites of Lake Haywardand Solar Lake (Fig. 5).

Solar Lake in the Middle East is another smallmeromictic hypersaline lake (coastal salina) with

a well-documented heliothermal hydrology. It islocated on the Sinai coast of the Gulf of Aqaba(Cytryn et al., 2000) and is separated from theocean by a narrow permeable sand barrier. Thebarrier allows seawater to seep into the sub-sea-level hydrographically-isolated lake depressionand so replace waters lost to evaporation. See-page-derived seawater can then pond on top of thelake floor, along with lesser volumes of waterssupplied by occasional winter rains (Fig. 11A).Brine depth in the lake centre fluctuates between4 and 6 m, driven by seasonal changes in theintensities of evaporation and the related levelsof seawater seepage and brine reflux.

Thick cyanobacterial mats carpet much of theSolar Lake sediment surface and contain a highlydiverse microbial community of cyanobacteriaand haloarchaea. Unlike the microbial laminitesof LakeHaywood, a structureless organic-rich gyp-siferous mush constitutes the sediment across them-deep bottom of the anoxic lake centre (Fig. 11A;seeWarren, 2006 for geological detail). Fluctuating

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planktonic microbial activity mirrors seasonalchanges in brine column layering by exportingvarying volumes of oxygen, sulphide, andmethaneinto the brine column as this mush accumulates(Fig. 11B).

High evaporation and aridity in the summermonths raises Solar Lake salinity to 200‰. At thattime the brine column is completely mixed (holo-mictic) and the entire water column is oxygenated(Fig. 11B, September, 1997). Temperature and sali-nity in the holomictic state vary little throughoutthe water column and sulphide and methane con-centrations are very low. By autumn, the watercolumn becomes stratified as a newly introducedseawater brine (50‰) layer overlies the residual,highly saline bottom water (180–200‰). A well-defined density gradient (halocline or pycnocline)separates an upper oxygenated cooler (16 �C) brinemass (epilimnion) from the lower hotter (45–55 �C)anoxic sulphide-rich brine mass (hypolimnion;Fig. 11b, December 1997). A high sulphide con-centration develops in the anoxic waters belowthe halocline and comes from the activities ofsulphate-reducing bacteria both in the water col-umn and in the underlying degrading cyanobac-terial mats. Crossing the halocline into the lowerbrine there is a rapid downward increase in sul-phide concentration, which reaches a maximumvalue of 1240mM near the sediment-brine contact(Cytryn et al., 2000). At the same time a peak inmethane concentration develops directly belowthe halocline, where a maximum value of 6.5 mMwas measured in the December 1997 profile andwas in-part a reflection of the decomposer activ-ities of the methanogenic haloarchaea.

As winter passes into spring gradual heating,along with an increase in the salinity of the upperwatermass, degrades thehalocline (Fig. 11B).Thusthe June 1997 data portray a transitional statebetween late stratification and the beginning ofholomixis. Salinity and temperature gradientsacross the halocline are more gradual and deeperin the water column than those observed in theDecember 1997profile. Thedeepeninghalocline ofJune 1997, when the chemocline was located3.25m below the water surface, allowed oxygento penetrate much deeper into the brine column,and so extend farther out across the subaqueouslake bottom than it had in the earlier stages ofstratification. Oxygen concentration in the upperwatermass in June 1997 reached amaximumvalueof 300 mMat a depth of 1mbelow thewater surface.These supersaturated values of oxygen imply

intense oxygenic photosynthetic activity at thebrine surface and in underlying shallow salinawaters. Deeper in the brine column, and wellbelow the chemocline, a sharp rise in sulphideconcentration occurs reaching a maximum valueof 2150 mMat thewater-sediment interface (Cytrynet al., 2000). Methane concentration increaseslinearly below the brine surface and reaches amaximum value of 17 mM adjacent to the lakebottom, implying methane, like the bacteriallyderived H2S, is escaping from the sediments.Increased evaporation rates in the mid- to latersummer further increase the salinity of the surfacelayer and ultimately disrupt the stratification andso lead into summer holomixis (as seen in theSeptember 1997 profile). Unlike Lake Hayward,conditions beneath the perennial lakefloor of SolarLake are anoxic for longer periods, oxygenic spe-cies, including cyanobacteria, tend not thrive inbottom waters for long periods, especially in thedeep central parts of the lake, where levels ofpreserved organics tend to be higher (5–20% ver-sus 1–5% TOC in Lake Hayward; Fig. 5).

Substantial density differences between theupper and lower masses in most density-stratifiedsystems means diffusive mixing across any halo-cline is insignificant. When a hypersaline watermass is density stratified there is no mechanism todrive changes in saturation state and so there is nowidespread bottom nucleation of salts. Sedimen-tation on the floor of the lower water layer (espe-cially if it is below the euphotic zone) is mostly bya pelagic rain of organics and evaporite crystallitesformed in the upperwatermass at the halocline viabrine mixing. There may also be local changes inbrine chemistry and the associated mineral preci-pitation driven by local influxes of spring and seepwaters. In contrast, when the upper and lowerwater masses equilibrate and homogenize, bottomnucleation of salts is possible even at the base ofdeep brine columns, as is occurring with the pre-cipitation of coarsely crystalline halite at the baseof the 350m holomictic brine column in the DeadSea today (Warren, 2006). In some perennial salinelakes in more temperate climates the holomicticstage is seasonal and so the sediment layers arevarves (e.g. Lake Hayward, Solar Lake, Lake Van,Lake Urmia), in others, holomictic mixing of sur-face with bottom water masses occurs across alonger time frame (e.g. the 400 year stability of thelower water layer in the Dead Sea driving episodesof laminite versus coarse crystalline halite bedson the deep lake floor).

348 J. K. Warren

Whenever a homogenized brine mass restrati-fies, the lack of ongoing concentration in the lowerwater mass means the rate of brine reflux throughbottom sediments beneath the sediment brineinterface slows and ultimately stops. Hypersalinepore brines remain but in a stagnant condition asthere is no ongoing mechanism to resupply brinesdenser than existing pore waters in the columnsubstrate. High pore water salinities, a propensityfor anoxia, anoxic pore brines and elevated bottomtemperatures, all tend to exclude aerobic burrow-ing and grazing animals from evaporite bottomsediments beneath a stratified brine column. Thisminimizes the effects of oxygenic biota that wouldotherwise oxidize and destroy mesohaline micro-bial debris, as in sediments deposited in less salinesettings.

Although the daily temperature/stratificationrecords of Lake Hayward and Solar Lake are prob-ably the best documented examples of the long-term hydrological cycling of a naturally stratifiedbrine pool, they both have a number of limitationswhen attempting to use them as direct analoguesfor the hydrology of ancient stratified brine sea-ways. Unfortunately, neither lake can act as asame scale hydrological analogue for ancient eva-porite seaways, intraplatform depressions or evensome of the larger ancient evaporitic lakes. Theysuffer from the scaling limitations that enfeebleall modern marine-associated evaporite analogues(Warren, 2006). Although hydrographicallyisolated and marine-seepage fed, neither lake issituated in a hydrological setting where enoughtime or aerially extensive drawdown stability hastranspired to allow substantial thicknesses ofmesohaline carbonates, halite or gypsum to accu-mulate. Their small aerial extents (�0.6 km2) andtheir centripetal meteoric inflow hydrologies (dri-ven by winter rains, a marked seasonal lowering ofevaporation intensity, and a high-relief hinterlandimmediately adjacent to the water body) meansthey cannot be directly compared to ancient meso-haline epeiric brine seaways where inherentlylow-relief topographies meant strandlines movedup to hundreds of kilometres in a wet-dry cycle,and where unfractionated meteoric runoff fromthe hinterland was much less significant in thefreshening process.

Biological responses to layered hydrologies

Brines in modern evaporitic depressions are typi-cally layered in terms of the annual or longer-term

hydrological cycle, with densermore salinewaterssupporting an ephemeralmass of less dense inflowwater. The lower, denser part of the water masstends to be more stable and its physical conditionschange less. In contrast, the conditions in thefloating less-dense layer are much more variableand its physical chemistry tends to oscillate. Thisupper layer periodically freshens to where it sup-ports awidespread planktonic bloom (feast). Then,as ongoing evaporation concentrates the upperlayer, conditions become increasingly less suitablefor life (famine) and a mass die-off occurs, first ofthe haloxene species, then the halotolerants, thenthe halophiles.

The die-back creates a pulse of organic matterthat can swamp the abilities of the decomposers inthe water column to strip it of its hydrogen, and soit can reach the sediment interface with its long-chain alkanes still intact. Even in conditionswherelight penetrates to the bottom of the brine columnand the bottomwaters immediately above the sedi-ment surface are oxygenated, the halotolerant pri-mary producers can be sufficiently productive andthe underlying anoxic decomposers sufficientlyinefficient that substantial volumes of hydrogen-rich microbial mater can be retained into burial.Somemodern examples of hydrologically inducedcommunity layering in modern evaporitic settingswill now be considered.

Halotolerant plankton and watercolumn layering

The significance of periodic freshening on biomassin stratified waters in creating conditions of“famine or feast” for halotolerant and halophilicspecies is clearly seen in the present productivitycycle of the Dead Sea (Fig. 12; Oren 2005; Oren &Gurevich, 1995; Oren et al., 1995). The main com-ponent of the halobiota in the Dead Sea waters isa unicellular green alga, Dunaliella parva beingthe sole primary producer in the lake. Severaltypes of halophilic archaea of the family Halobac-teriaceae then metabolize the glycerol and otherorganic compounds produced by the alga. As inall ecosystems, producers and consumers in thebrine-stratified water columns are codependent.Halophilic archaea (Halobacterium and Halo-coccus) survive into much higher salinities thanDunaliella parva as they decompose the glycerol-rich remains.

Three distinct periods of organic productivitywere seen in thirteen years of quantitative studies


of Dead Sea microbiology starting in 1980 (Oren,1993). Unlike more temperate lakes, organicblooms in the Dead Sea are not an annual event.Mass developments of Dunaliella (up to 8800 cellsmL�1) and red halophilic archaea (2� 107 cellsmL�1) were observed in 1980, following a dilutionof the saline upper water layers by rain floods and

an associated rise in lake level of 1.5m. This bloomhad disappeared at the end of 1982, followingcomplete mixing of the water column and theassociated salinity increase in the upper watermass (holomixis).

During the period 1983–1991 the Dead Sea washolomictic, and noDunaliella cellswere observed.

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350 J. K. Warren

Viable halophilic and halotolerant archaea werepresent during this period, but in very low num-bers. Then heavy rain floods during the winter of1991–1992 raised the lake level by 2m and causednew salinity stratification as the upper five metresof the water column was diluted to 70% of thenormal surface salinity (Fig. 12A). Themeromicticphase lasted until 1996 when the current holomic-tic conditions with seasonal stratification wereestablished, clearly illustrating the oligotrophichydrology of the Dead Sea brine column. Duna-liella reappeared in the upper less saline waterlayer (up to 3� 104 cellsmL�1 at the beginningof May 1992, rapidly declining to less than40 cellsmL�1 at the end of July), while the bloomof the archaea (3� 107 cellsmL�1) continued andimparted a reddish colour to the Dead Sea brines(Fig. 12B). The reddish hue of the surface waters atthis time was due to elevated levels of the carote-noid pigment bacterioruberin, which absorbs lightat wavelengths between 420–550nm.

Archaeal numbers in the Dead Sea decreasedonly a little after the July 1992 decline of theDunaliella bloom, and most of the haloarchaealcommunity was still present at the end of 1993.However, the amount of carotenoid pigment percell decreased 2–3-fold between June 1992 andAugust 1993 (Fig. 12B; Oren & Gurevich, 1995).No new algal and archaeal blooms developed afterthe winter floods of 1992–1993, in spite of the factthat salinity values in the surface layer were suffi-ciently low to support a new algal bloom. A rem-nant of the 1992 Dunaliella bloom maintaineditself at the lower end of the pycnocline (halocline)at depths between 7 and 13 m (September1992–August 1993). Its photosynthetic activitywas small, and very little stimulation of archaealgrowth and activity was associated with this algalcommunity (Fig. 12B). This pattern suggests thatthe photosynthetic activity of the algae may havebeen limited by a lack of nutrients in the upperbrine column.

Colouration of the Dead Sea waters from theinitial algal bloom allowed Oren & Ben Yosef(1997) to use Landsat images, collected in May1991 and in April and June 1992, to plot thedevelopment of the Dunaliella parva bloom. Incontrast, the carotenoids of the subsequent archaeabloom did not produce a recognizable signal in theLandsat images. The April 1992 image obtained atthe time of the onset of the algal bloom, prior to itslake-wide spread, suggested it originated in theshallow areas near the shore of the lake, where

light penetrated to the bottom of the brine columnandanewlyestablished freshenedwater layer inter-sected the lake floor. The resulting algal blossomingwas instigated by resting cells that had survivednear the sediment surface around the lakemargin orin species refugia around freshwater springs.

The decline of the lake-wide bloomof halophilicarchaea in the Dead Sea appears to be related toviral infection (Oren et al., 1997). For example, inOctober 1994, therewere between 0.9 and7.3� 107

virus-like particles per mL of brine during declen-sion of halophilic archaea in the upper 20m oftheDead Seawater column and virus-like particlesoutnumbered archaea by a factor of 0.9–9.5 (aver-aging 4.4). By 1995 all water samples containedlow numbers of both archaea and virus-like parti-cles; 1.9–2.6� 106 and 0.8–4.6� 107mL�1 respec-tively in April 1995. Viral numbers declined evenfurther so that byNovember 1995–January 1996 allsamples contained less than 104 particlesmL�1.Oren et al. (1997) further suggested that virusesplay a major role in the decline of halophilicarchaeal communities in many other hypersalinesettings at salinities where protozoa and fungi areabsent.

Community layering in mesohaline microbialites

Laminated organic-rich sediments that typifymany evaporitic microbial carbonates (possiblepetroleum source rocks) and described by sedi-mentologists using the general, and perhaps dated,terms algal mats and cryptalgal-laminites, are ineffect microbial “high rises,” as are many livingstromatolites. They, and their entrained biomar-kers, indicate the activities of an ecologicallylayered microbial community that can thrive inboth subaerial and subaqueous settings. Likemicrobial layering in the Dead Sea brine column,layering in a microbial mat is divisible into anupper aerobic community and a lower layer ofanaerobic decomposers (Fig. 13). As a microbialmat accretes, its organic constituents are buried.The biochemical make-up of the initial halobiota,which flourished in the hypersaline conditions(typically oxygenic) at or above the mat surface,is altered by the metabolic activities of variousdecomposers flourishing below.

In order to investigate early or syndepositionalchanges in the dominant organic constituents andthe main diagenetic processes influencing organiccharacter, Grimalt et al. (1992) studied organicprofiles in cross sections through two different


subaqueous cyanobacterial mats in a moderncoastal salina. Changes in lipid composition werecompared with the vertical distributions of thevarious microbial populations. Vertical distribu-tions in the lipid patterns were defined usingenrichment cultures from typical species of cya-nobacteria, diatoms, purple bacteria, sulphate-reducers and methanogens obtained from thelayered mats. Cyanobacteria Phormidium valder-ianum and Microcoleus chthonoplastes were thedominant primary producers in the sampled mats,they occurred almost asmonocultures in the upper6mm of themats (Fig. 13A). Worldwide, these andother cosmopolitan filamentous cyanobacterialphotosynthesizers are the most obvious organismsin most mesohaline algal mats. Their chlorophyllcreates a green layer with a sticky or slimy surfaceand defines the upper few millimetres of the matcommunity. As layers of mucilaginous sheathsaggrade via periodic growth spurts, it createsbiolamination.

Below the photosynthesizing cyanobacteria isa layer of aerobic heterotrophs (bacteria andarchaea), which in the presence of oxygen breakdown organics produced by the cyanobacteria(mostly abandoned algal sheaths and slime). How-ever, because oxygen is only produced by photo-synthesis, these organisms can only perform thisprocess during daylight. The next layer below isdominated by chemolithotrophic sulphur-oxidiz-ing bacteria. These are life forms that use the redoxenergy contained in the biochemical gradientbetween reduced sulphur compounds producedby sulphate reducers (below) andoxygenproducedby the cyanobacteria (above). They are anaerobic

photosynthesizers that fix sugars by utilizingthe infrared portion of the light spectrum as theyconvert H2S to SO4. Infrared radiation penetratesdeeper into microbial sediment than the visiblelight usedby the cyanobacteria (Fig. 13B).Utilizingthe redox gradient these purple sulphur-oxidizingbacteria synthesize organic matter and create thecharacteristic purple-orange layer seen belowthe green layer in an aggrading microbial mat. Thesulphur-oxidizing bacteria can only metabolize ina suitable redox gradient, and they need to locatethemselves exactlywithin this gradient, so they aretypically the most motile forms in a microbial mat.The redox gradient lies deeper in the mat commu-nity during the day due to oxygen production bythe cyanobacteria, but it rises and can even reachthe mat surface in the dark of night (Fig. 13B).

Below the phototrophic sulphur-oxidizing bac-teria are the sulphate reducers, the fermenters andthe methanogens (Fig. 13C). In saline settings theyare relatively inefficient decomposers and tend tobe active at salinities that are less than150‰ (Figs 3and 4; Ollivier et al., 1994). During the day thesulphate-reducers metabolize organics deep in themicrobial mat via anaerobic respiration, utilizing avariety of chemical constituents including manga-nese, nitrate, sulphate and even CO2. At night theyrise somewhat with redox gradient and at times ofprolonged bottom-brine anoxia and brine-columnturbidity can even reach the mat surface or enterthe lowerparts of adensity-stratifiedbrine column.They are very important decomposers in mostmesohaline microbial mats and give the lowerparts of a mat its characteristic “rotten egg” smell.They generally consume up to one third of the

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352 J. K. Warren

organic carbon present in a typical mesohalinemicrobial mat and are most efficient at salinitiesthat are less than 120–140‰.

Fermenters and reducers do not completelybreak down the organics but create alcohols, lac-tates and other organic compounds (Ollivier et al.,1994). The other group of anaerobic decomposersdeep in the mat is the methanogens. They arearchaea and utilize simple compounds createdby the fermenters (CO2 and hydrogen, along withorganic components such asmethanol, acetic acid,formic acid and methylamines) to producemethane. This metabolic pathway produces littlebiochemical energy and is usually the “last resort”community that makes up the lowermost livinglayer in the microbial high-rise community thatinhabits a microbial mat or a stratified brinecolumn.

Stratification of the microbiota in response to,and in biofeedback with, oxygen levels has impor-tant implications in terms of the biomarkers foundin preserved saline sediments (and source rocks).Grimalt et al. (1992) found that although theupper-most layers of salinemicrobial mats are dominatedby cyanobacteria, they typically leave no morethan minor traces in the solvent-extractable lipids(biomarkers) in the buried sediment. Rather, thepredominant fatty acid distributions in the lowerparts of mesohaline mat sediments parallel thecompositions observed in the enrichment culturesof sulphur-oxidizing bacteria, and appear to bemixed with acids characteristic of heterotrophicbacteria, including purple bacteria and sulphate-reducers. In other words, the retained organic sig-natures, even as themat laminawere accumulatinga few millimetres above, were those of the decom-posers, not the primary producers (Fig. 13C). Thisimplies thatmany biomarkers used to typify organ-ic production in modern and ancient hypersalinesediments typically do not come from organics ofthe primary producers but from the products of thedecomposer community.

The overprinting effects of the decomposers inmicrobial laminites are clearly seen when mole-cular characteristics of recent hypersaline sedi-ment from the Ejinur salt lake (northern China) arecompared to Tertiary (Eocene) core samples fromthe Qianjiang Formation (hypersaline lacustrine)of the Jianghan Basin, central eastern China(Fig. 14; Wang et al., 1998). N-alkanoic acids insediments from both areas (Ejinur and Jianghan)show a pronounced even-over-odd predominanceand a bimodal distribution. In the lower molecular

weight range, the C16 and C18 components areprominent, with the former dominant. For higherhomologues (greater than or equal to C20), docosa-noic (C22) and tetracosanoic (C24) acids dominatethe n-alkanoic acid homologues for the Jianghanand Ejinur samples, respectively. Alkanoic acidswith an isoprenoid skeleton are more abundantin Jianghan samples, including C20, C21, C24, C25

and C30 homologues, with a C25 component(3,7,11,15,19-pentamethyleicosanoic acid) mostpronounced in the lower part of the QianjiangFm.The carbon skeletons of these isoprenoid acidsare attributed to archaeal decomposers. Iso andanteiso branched carboxylic acids are prevalentin both the Lake Ejinur samples and the upperportion of the Qiangiang Formation. (Wang, 1998).They derive from bacteria, probably sulphate-reducing bacteria, and their abundances clearlyshow again the importance of bacterial decompo-sers, along with haloarchaea as contributors to thebiochemical signature of organic matter in bothmodern and ancient saline lake sediments. Thepresence of hopanoid acids and a 3-carboxy ster-oidal acid in both further attest to contributionsfrom bacterial and eukaryotic sources, respec-tively. The occurrence of particular carboxylicacids in the Jianghan samples illustrate these com-pounds, indicators of halotolerant and halophilicdecomposers, can survive as biomarkers in sourcerocks deposited in hypersaline settings.

Defining where ancient halotolerant and halo-philic decomposers lived (“in brine column” or “inmat”) is not possible from an analysis of sediment

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biomarkers. It requires sedimentological interpre-tation of the rock matrix, which typically is alaminite. As discussed in Warren (1986), anyassumption of “lamination indicating deeperbrines” is fraught with difficulty, as ancient eva-poritic laminites and biolaminites were subaqu-eous sediments with near-identical mm-scaletextures accumulating beneath stratified andunstratified perennial brines columns at depthsranging from less than one metre to hundreds ofmetres. Determination of water depth requiressedimentary analysis of evaporitic sediments thatare intercalated with the laminites.

ORGANIC ENRICHMENT

At the broader scale of petroleum source rockcreation, the amount of organic matter preservedin evaporitic sediment, which becomes a potentialsource rock, is a functionof three factors that canbeexpressed in the equation (Bohacs et al., 2000):

Organic Enrichment ¼ ðP-DeÞ=ðDiÞ ð3Þwhere P is production, De is destruction (oxidationand biodegradation and Di is dilution (detritalinflux and matrix precipitation). Maximumenrichment occurswhen production ismaximizedand destruction and dilution are minimized.

Production atmesohaline salinities ismostly viaphotosynthetic fixation of CO2. It includes auto-chthonous organicmatter, formedat ornear the siteof accumulation and derived from algae, bacteriaand aquatic plants, aswell as allochthonous organ-ic matter carried in during floods (Bohacs et al.,2000). Katz (1990) showed that varying levels ofsolar input andwater chemistry/stratificationexertthe largest effects on overall primary production inmesohaline settings. Initial destruction of organicmatter is mostly a function of the efficiency of thevarious scavengers and grazers, which is typicallya function of the availability of oxygen (Demaison& Moore, 1980). In higher salinity settings thescavenger/decomposer population is dominatedby bacteria and archaea, while the density of themetazoan grazers is largely inhibited by the samehigher salinities. Dilution by an influx of mineralprecipitates to possible areas of organic enrich-ment can limit levels of organic enrichment bydecreasing the proportion of organic matter rela-tive to inorganicmatrix. The source of dilution canbe detrital siliciclastics or precipitates of gypsumand halite.

Salinity controls on organic productivity: theflamingo connection

When biodiversity is low and salinity is high, aproliferation of well-adapted mesohaline speciescan generate organic productivity levels in surfacewaters that aremuch higher than those observed inmost non-evaporitic settings. These saline systemsare indicative of general principles seen in stressedecosystems, namely, as the harshness or abioticstress in a system increases, the biotic stressdecreases on a few well-adapted species (as thereare fewer predators and grazers). The total biodi-versity (number of species) decreases, while at thesame time the biomass (total mass of organisms inthe system) initially increases (e.g. Garcia & Niell,1993). Ultimately, as salinity rises further, biomassdeclines as conditions become unsuitable for anylife. One of the most visually impressive indica-tions of periodic very high levels of organic pro-ductivity in a modern salinity-stressed water bodyresides in the “flamingo connection”, a connectionbetweenflamingos,mesohalineplanktonic bloomsand saline lakes, well documented in Lake Nakuruby Vareschi (1982) and first noted in the geologicalliterature by Kirkland & Evans (1981).

Flamingos are filter feeders thriving on the densecyanobacterial blooms in the shallows of salinelakes around the world. For example, two speciesof flamingo intermittently occur in huge numbersin the various East African rift lakes. These are thegreater and the lesser flamingo (Phoenicoptusruber roseus and P. minor); the lesser flamingo isthe birdwith the spectacular pink-red colouration.These bright pink birds feed and breed in rift lakeswhere cyanobacterial blooms can be so dense thata secchi disc disappears within a few centimetresof the lake’s water surface (Warren, 1986). LakeNatron is a major breeding ground for flamingos inEast Africa and is the only regular breeding site forthe lesser flamingo in Africa (Simmons, 1995). Infact, Lake Natron has the highest concentration ofbreeding flamingos of any lake in East Africa. Boththe greater and the lesser flamingo are found there,with the lesser flamingo outnumbering the greaterby a hundred to one. Lesser flamingos bred at LakeNatron in9out of 14years from1954 to1967.WhileLake Natron (a trona lake) is an essential breedingsite, it is not a focal feeding site forflamingos.Majorfeeding sites in the rift valley are LakesNakuru andBogoria in Kenya, which are somewhat less salinethan Lake Natron and so have a greater abundanceof mesohaline plankton.

354 J. K. Warren

The main phytoplankton component in LakeNakuru waters is the cyanobacterium, Arthrospiraplatensis (previously known as Spirulina platen-sis), it forms themain food component of the lesserflamingo. In Nakuru it is also consumed by onespecies of tilapid fish and one species of copepodand a crustacean. Rotifers, waterboatmen, andmidge larvae also flourish in the waters of LakeNakuru. Themouth-breeding tilapid fish Sarother-odon alcalicum grahami was introduced to thelake in the 1950s to control the mosquito problemand they have flourished ever since, at times dis-placing the flamingos as the primary consumers ofplanktonic algae. Their introduction also increasedthe number of fish-eating birds residing in the lake(Vareschi, 1978).

In a good year more than a million flamingosconsume more than 200 tons of plankton per dayfrom Lake Nakuru, a shallow saline soda lake witha pH �10.5 and a typical annual salinity range of10–120‰. The lake measures some 6.5 km by10 km, with waters up to 4.5 m deep in the lowerparts of the lake during a “lake-full” period. Lakelevels are subject to change, both annually and ona longer time scale, with permanent eutrophicwaters developed in the lake centre duringtimes of higher water (Fig. 15A and B; Vareschi,1978–1982).

The feeding style of the birds is to wade throughthe shallows, with heads upside down and beakswaving side to side across the water surface. Fla-mingo beaks have evolved to skim plankton fromsaline to brackish surface waters and are equippedwith a filter-feeding system unlike any other birdon Earth and more akin to feeding apparatus of thekrill-ingesting Great Whales. Flamingos siphonthe lake water through the beak filters to trapA. platensis and other plankton by swinging theirupside-down heads from side to side and usingtheir fat tongues to swish water through theirbeaks. They can filter as many as 20 beak-fulls ofplankton-rich water in a second. Spacings of thefilters in the beak of the greater flamingo are widerthan those in the beaks of the lesser flamingo.Greater flamingos feed mostly on zooplankton,while lesser flamingos feed almost solely on Spir-ulina, thus in any saline lakewhere the two speciesco-exist they do not compete for the same foodsource.

Arthrospira platensis provides high levels ofthe red pigment phycoerythrin to the food chainand it accumulates in flamingo feathers to give thebirds their world famous colouration (hence the

“flamingo connection”). This is the same pigmentthat turns waters red in Lake Natron and LakeMagadi, but in this case it comes mostly from thehalophilic archaea. Lesser flamingos, with theirnarrower spacings of beak filters, survive solelyon Arthrospira and so have a more intense pinkcolour than greater flamingos, a species that sitshigher in the lake food chain and get its feathercolour second-hand from the lake zooplankton.

As well as possessing very high levels of phy-coerythrin in its cytoplasm, Spirulina is also unu-sual among the cyanobacteria in its unusually highprotein content. In Lake Chad and in some salinelakes inMexico it accumulates as a lake edge scumthat is harvested by the local people and used tomake nutritious biscuits. In the 16th century it wasmentioned in the diary of one of Cortez’s soldierswho described how the Aztecs sold hard flat cakesmade from the dried remains of Arthrospira. TheAztec word for it was Tecuitlatl, which translatesliterally as “excrement of stones.” The lack ofcellulose in the A. platensis cell wall means it isa source of plant protein readily absorbed by thehuman gut, making it a potentially harvestablefood source in water bodies in regions of deserti-fication and it has become a popular alternativeprotein source in the developed world.

In 1972, Lake Nakuru waters held a surfacebiomass of 270 gm�3 and an average biomass of194 gm�3 but, as in most hypersaline ecosystems,Nakuru’s organic production rate varies drasticallyfrom year to year as water conditions fluctuate(Fig. 15C; Vareschi, 1978). Arthrospira platensiswas in a long-lasting bloom in 1971–1973, andaccounted for 80–100%of the large phytoplanktonbiomass in those years. In 1974, however, it almostdisappeared from the lake and was replaced bycoccoid cyanobacteria such as Anabaenopsis sp.,Chroococcus sp. and by diatoms, all species thatdealt betterwith elevated salinities. This change inbiota was tied to a serious reduction in biomass,which in 1974 was down to 71 gm�3 in surfacewaters, and averaged 137 gm�3 in the total watermass. As a result, the flamingo population in thelake declined from 1 million to several thousands(Vareschi, 1978).

The lower salinity limit forArthrospira platensisgrowth is �5‰ and in terms of water conductivityit does best in the range 10–50mScm�1. The driv-ing mechanism for the change in biomass in LakeNakuru in the mid-1970s was not clearly docu-mented. It was thought to be related to increasedsalinity and lowering of lake levels, along with


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356 J. K. Warren

the growth and bottom shading by planktonicalgal species that were better adapted to highersalinity. These better adapted were present in les-ser volumes and with lower per cell protein cells(Fig. 15C; Vareschi, 1978).

During the mid- to late 1970s and in the 1980sLake Nakuru returned from a relatively saline dryphase to more typical annual schizohaline oscilla-tions in water level and salinity (Fig. 15A). Sea-sonally, in the 1980s, theA. platensis and flamingopopulations returned to impressive numbers.From the 1990s more reliable long-term data onphysical lake condition and flamingo numbershave being compiled (Fig. 15E). In 1995 and1998 feeding flamingo populations in LakeNakuruwere once again at very low levels and the remain-ing population was stressed (Fig. 15E). In 1998,unlike 1974, the stress was related to fresheningdriving a decrease in A. platensis biomass, notincreased salinity anddesiccation. This fresheningof the lakewaters favoured a cyanobacterial assem-blage that alsoproduced toxins (seeCyanobacterialtoxins in Glossary). In the preceding bountifulyear (1996), the A. platensis-dominated biomasshad bloomed at times when salinities were favour-able, and died back at times of elevated salinitiesand lake desiccation, as in 1974. By 2000, thesomewhat lower salinity cycles had once againincreased, making surface waters suitable foranother widespread A. platensis bloom and theassociated return of high numbers of feedingflamingos.

It seems that breeding flamingos come to LakeNakuru to feed in large numbers when there iswater in the lake with appropriate salinity andnutrient levels to facilitate an A. platensis bloom.In some years when heavy rains occur, lake levelsrise significantly and the lake waters, althoughperennial, stay in the lower salinity tolerance rangefor A. platensis, as in the El Ni~no period betweenOctober 1997 andApril 1998.Once lake levels start

to fall, salinities and rates of salinity change returnto higher levels, then water conditions once againbecome appropriate for A. platensis. Environmen-tal stress on the flamingos also comes with drierperiods that elevate lake salinities into the upperend of A. platensis tolerance. Ongoing droughtultimately leads to lake desiccation and the com-plete loss of the food supply in the lake.

One of the reasons why Lake Nakuru is sosuitable for cyanobacterial growth at times ofA. platensis bloom, is the maintenance of suitabletemperatures and associated oxygenation in theupper water mass. The lake develops a remarkabledaily thermocline in the upper 1.5m of the columnthat dissipates each day via wind mixing in thelate afternoon, and so recycles nutrients back tothe oxygenated surface waters to facilitate theongoing plankton bloom of the next diurnal cycle(Fig. 15D).

Some environmentalists have argued in the pop-ular press that lower numbers of flamingos in LakeNakuru, such as occurred in 1995 when more than50,000 birds died, are an indicator of: uncontrolledforest clearance; an uncontrolled increase in sew-erage encouraging eutrophication; an increase inheavymetals from increasing industrial pollutantsin the lake; and general stress on the bird popula-tion from tourists and the drastic increase in localhuman population centered on the town ofNakuru(now the third largest in Kenya). Numbers of peo-ple in the town, which is the main city in the riftvalley, have grown by an average of 10% everydecade for the past 30 years.

Likemany environmental doomsday arguments,the above are more based on opinionated predic-tion than on scientific fact. Rise and fall of lakelevels, drastic changes in salinity, a periodicallystressed biota, and a lack of predictability in watercharacteristics are endemic to saline ecosystems(cycles of “famine or feast”). Oscillations in oneor more of these factors are not necessarily

Fig. 15. Physical and chemical characteristics, algal biomass and flamingo numbers of Lake Nakuru, Kenya. (A) Lake levelsfrom 1930 to 1999. Data are not sufficiently detailed to record times of complete lake drying or drought, and there are alsosubstantial timeswhennodatawere 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 tocentre these are: December 1979; January 1969; January 1967; and January 1961. Dashed isopleths are based on soundingstaken inDecember, 1971. Two sewage plants are located at a and b. (C) Trends of algal biomass and conductivity of lakewaterduring 1972–1978. The percent contribution ofArthrospira platensis (formerly Spirulina platensis) to the total algal biomassis 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 tomid-2001.Water depth andflamingodata only available from1994 tomid-2000 (data are digitized and replotted to a common timescale from a number of figures and pdf reports downloaded from http://www.worldlakes.org on 2 February 2004).

3


anthropogenically induced. For example, theamounts of most heavy metals (Cd, Cr, Cu, Hg,Ni, Pb, Zn) in the lake sediments were found tobe in the typical range of metals in natural lakesworldwide (Svengren, 2002). The exception wascadmium, which is elevated in the lake sedimentand could perhaps be assigned to anthropogenicpollution. All other metals are present at lowlevels, especially if one considers that LakeNakurulies within a labile catchment where bedrock isan active volcanogenic-magmatic terrane. At thepresent time, sufficient base a scientificdata arenotyet available in Lake Nakuru, and so scientificallyaccurate determinations cannot be made of therelative effects of humanity verses natural baselineenvironmental stresses on bird numbers in thisschizohaline ecosystem.

Nearby lakes Magadi and Natron have extensivetrona platforms covered with brine sheets that arecharacterized by short periods of high productivityand times of bright red waters. In this higher sali-nity ecosystem, the dominant producers of thebrine colour are haloalkaliphilic bacteria andarchaea. Archaeal species belonging to the generaNatronococcus, Natronobacterium, Natrialba,Halorubrum, Natronorubrum and Natronomonas,all occur in the lakes. Lake centre brines when thisbiota flourishes are at trona/halite saturation, witha pH �12. Stratified moat waters around the tronaplatform edge are at times almost as chemicallyextreme, and the moat bottom sediments are madeup of aragonite/dolomite/detrital laminites thatcan preserve elevated levels of organics (�6–8%).As well as algae and cyanobacteria, Lake Magadiand Natron moat waters also harbour a variedanaerobic bacterial community including cellulo-lytic, proteolytic, saccharolytic, and homoaceto-genic bacteria (Shiba & Horikoshi, 1988; Zhilina &Zavarzin, 1994; Zhilina et al., 1996). When thehomoacetogen Natroniella acetigena was isolatedfrom Lake Magadi its pH growth optimum wasfound to be 9.8–10.0, and it continued to grow inwaters with pH up to 10.7, making it an exemplaryalkaphile (Zhilina et al., 1996).

Regionally, salinities in the East Africa rift-val-ley lakes range from around 5‰ total salts (w/v) inthe more northerly lakes (Bogoria, Nakuru, Elmen-teita, and Sonachi) to trona and halite saturation(>200‰) in lakes to the south (Lakes Magadi andNatron). Yet across this salinity range, a combina-tion of high ambient temperature, high light inten-sity and a continuous resupply of CO2,makes thesesoda lakes amongst the highest in the world in

terms of their seasonal planktonic biomass (Grantet al., 1999) and also places them among theworld’s most productive ecosystems (Melack &Kilham, 1974). As demonstrated above, the lesssaline soda lakes are dominated by periodicblooms of cyanobacteria, especially Arthrospiraplatensis, while the hypersaline lakes, such asMagadi, can on occasion support blooms of bothcyanobacteria and alkaphilic phototrophic bacter-ia belonging to the genera Ectothiorhodospira andHalorhodospira (Jones et al., 1998).

The halotolerant and halophilic biota livingin the layered water columns of these soda lakesconstitute small-scale “famine or feast” ecosys-tems, which at times of “feast” are far more pro-ductive than zones ofmarine upwelling (Fig. 16A).A general observation of short periods of enhancedorganic productivity between somewhat less andsomewhat more saline episodes in schizohalinelake waters worldwide, reflects the general ecolo-gical principle that increased environmental stressfavours the survival of a few well-adapted haloto-lerant species, to the detriment of others bettersuited to life in a less saline environment (see insetin Fig. 16A). Ultimately, abiogenic stresses asso-ciated with more elevated salinity means all life,including the halophiles, ceases to function.

The same general principle that schizohalineecosystems encourage dominance by a few better-adapted species can be clearly seen in the decreasein invertebrate species (grazers and predators) withincreasing salinity in the carbonate lakes of theCoorong of Southern Australia, where only brineshrimp remain alive in waters with salinities inexcess of 200‰ (Fig. 16B). It reflects a general trendof decreasing faunal biomass with increasing sali-nity (Fig. 16C). A decreased level of biomass in amesohaline system does not necessarily mean lesssource rock potential in the resulting sediments.Preservation levels of organicmatter and suitabilityof the protokerogen (type I to type III) depends onwhat biotal contributors constitute the biomasspreserved in the sediment.

Examples of “famine or feast” productivity haveso far focused on continental salt lakes. Similarenhancements of primary productivity can occurin modern coastal salinas during episodes of per-iodic freshening as blooms of haloxene and halo-tolerant microbes (oxygenic photosynthesizers)takeplace across formerly exposedmats. For exam-ple, a study of biolaminites collected from a mod-ern salina (Storr’s Lake in the Bahamas) showedthat a reduction in brine salinity from 90 to 45‰

358 J. K. Warren

significantly enhanced CO2 and N2 fixation rates,but additions of inorganic nutrients and dissolvedorganic carbons did not show any significantlyenhanced rates compared with the salinity con-trols (Pinckney et al., 1995). That is, dissolvedorganic carbon/dissolved organic nitrogen uptakewas not influenced over the entire range of sali-nities (45–90‰) seen in this study of mesohalinemat growth.

In other words, abiotic stress, induced by hyper-saline conditions in theBahamian lagoons, createdlower productivity in the saline-tolerant microbialmats, even when nutrient levels were high. Oncethe osmotic stress on the biota was relieved by alowering of salinity, mats underwent enhancedprimary production and nitrogen fixation as halox-ene producers could once again photosynthesize.Changing nutrient levels were far less significant

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than changing salinity levels as controls on matproductivity in this stressed setting. Salinity-induced stress in these halotolerantmicrobialmatsoutweighs typical limiting factors regulating pri-mary production in phototrophic communities atthe lower salinities that typifymarine and brackishwaters.

Organic production in saline waters

When surface water salinities are suitable, evapor-ite basins have some of the highest measured ratesof organic productivity in the world (Fig. 16A;Warren, 1986). Times of elevated primary produc-tion (“feast”) in density-stratified hypersalinebrine lakes and evaporitic seaways appear to becontrolled by two factors: (1) the ephemeral pre-sence of a less saline surfacewater; and (2) a supplyof nutrients (nitrate/ammonia and phosphate)from the lower hypersaline water mass. The biotacontributing the organics that ultimately reach thebottom sediments to form organic-rich laminae(and so control their future biomarker signature)are largely dependent on the timing of photosyn-thetic activity. Perennial saline lakes subject to anannual freshening of surface waters will depositvarved carbonates (e.g. LakeTanganyikawithup to7–11% TOC in deep bottom laminites; Cohen,1989), while other saline lakes and seaways withless predictable stratification may form similarcarbonate laminites, but the organic layering maynot be annual, and the resulting organic biomar-kers contain elevated levels of isoprenoids due tothe greater contribution from the haloarchaea.Microbial mats in some shallower saline lakesmay be subject to short periods of photosyntheticoxygenation and even subaerial exposure, yet stillpreserve elevated levels of hydrogen-prone organ-ics (Warren, 1986).

Once brinemoves into the gypsum precipitationfield and beyond, the amount of organics accumu-lating on the bottom is diluted by inherently rapidrates of crystal precipitation and accumulation,especially if the bottombrine is photosyntheticallyoxygenated by its microbial community. Hypertro-phication, in combination with shading by pelagiccrystallites, can overwhelm the delivery of oxygento the bottom, as in Solar Lake and in Lake Hay-ward in the late 1980s. Evaporitic systems subjectto longer-term eutrophication can facilitate highlevels of pelagic organic delivery to bottom sedi-ments, even beneath shallow penesaline waters(Horsfield et al., 1994; Warren 1986). In a study

of eutrophication in man-made saltfields, Javor(2000) found that in shallow gypsum and pre-gypsum ponds there was an interesting inverserelationship between the level of nutrients(nitrates and phosphates) in the brine column andthe development of microbial mats on the watercovered pan floor. In a high-nutrient brine system(eutrophic or “well-nourished pan”) the algaeand bacteria flourished as planktonic forms andthe biomass buildup in the upper parts of thebrine column tended to shade the sediment sur-face. There was little or no development of anoxygenated microbial mat and bottomwaters weredysaerobic to anoxic. In a low nutrient system(oligotrophic or “poorly-nourished pan”) therewas little or no planktonic development of algaeor bacteria and microbial mats tended to flourishon the perennial pond floor. Benthic mats formedfrom salinities of 50‰ to gypsum saturation inthe poorly-nourished pans. In pans at even lowersalinities the benthic mats were destroyed by thefeeding activities of invertebrates and fish.

Preservation of microbial mats into early burialin hypersaline systems depends, in large part, onthe efficiency of nutrient recycling by the bacterialand archaeal decomposers that making up theunderside of the living part of a mat. Even if nitro-gen and phosphorus levels are low in the overlyingbrine, theremay be sufficient recycling of nutrientswithin themat community to allow thebenthicmatto continue to grow. Javor (1989) found that oncea gypsum crust becomes well established over thefloor of a crystallizer pond, there was little recy-cling of nutrients from beneath the crust to theuppermost photosynthesizers, and from this pointdownstream in the crystallizer pans, nitrate andphosphate nutrients were concentrated by eva-poration and recycled into the biomass living inthe brine column. In oligotrophic gypsum pondsthegypsumcrust is stableand thebottomwatersareoxygenated. In eutrophic gypsum ponds at thesame salinities, the bottom waters become anoxicand sulphate-reducing bacteria flourish. In thesesystems,gypsumdissolvesandablackslimyorgan-ic-rich carbonate/detrital mud (a potential sourcerock inancient counterparts) covers thebottomandcontains no more than a few embayed and dis-solved gypsum remnants. If portions of this slimybottom become suspended and are flushed intothe next stage of crystallizer they create a problemin the final salt product known as “black spot”.

The difference in organic levels between oligo-trophic systems such as Lake Hayward and

360 J. K. Warren

perennial eutrophic systems like Solar Lake prob-ably explains why the latter retains much higherlevels of hydrogen-prone organic material in itspreserved bottom sediments (Fig. 5). Javor’s workalso demonstrated that as higher salinity brinestend to concentrate nutrients, they will supplythese nutrients at times or at interfaces wheresupersaline waters in a natural schizohaline sys-tem are subject to periodic freshening or mixing.

Proximity of organic-rich mesohaline laminitesto bedded evaporites in ancient successions hasled some geologists to postulate that bedded saltsare potentially also organic-rich sediments, withthe same level of source potential as mesohalinecarbonates. This is not borne out by TOC analysisof evaporitic salts; total organic matter levels inancient CaSO4 and NaCl lithologies tend to benormal or depleted (Katz et al., 1987), althoughlevels of dissolved organicmatter and volatile fattyacidsmay behigh in the entrained brine inclusions(Hite & Anders, 1991). The typically low organicmatter levels in bedded gypsum and halite mayreflect the higher depositional rates of evaporiticsalts when compared with evaporitic carbonates(dilution effect). Only in settings where bottomwaters are anoxic in the gypsum stage can thebuild up of H2S from sulphate reduction becomehigh enough to remove CaSO4 minerals and soallow preservation of elevated levels of partiallydegraded organics (as in Solar Lake today).

That organic enrichment mostly occurs in themesohaline carbonate stage in an evaporite basin isclearly seen in organic contents of the evaporiticmarls and salts of the Oligocene Mulhouse Basin(Fig. 17; Hofmann et al., 1993a, b). This deposit isone of a few ancient evaporites where organicchemistry has been studied in a logical anddetailed fashion. Organic matter occurs mostlyin finely laminated carbonate marls (varves),which can contain up to 7% TOC, anhydrite bedscontain 0.08–0.78% TOC, halite beds 0.01–0.25%TOC and the potash beds <0.1% TOC. The marlsare characterized by thin, continuous beddingparallel laminae that are not disturbed by anybioturbation. They are interpreted as seasonalvarves with the clay and carbonate forming alter-nate layers in the couplet (Fig. 17, inset). In springand summer the increased temperature in surfacewaters favoured precipitation of micritic carbo-nate, in autumn and winter the phytoplanktondied back and rainfall/runoff transported silici-clastic debris into the basin. On the basis that thelaminar couplets are varves,Hofmann et al. (1993a)

were able to plot the relationship between sedi-mentation rate and TOC content in the marls(Fig. 17). Marls deposited during times of lowsedimentation tend to be organic-rich, while marlsdeposited with higher sedimentation rates tendto contain lower amounts of organics. They extra-polated that the even lower levels of organics inthe more saline salt beds (anhydrite and halite)indicate greater dilution because of the inherentlyhigher sedimentation rates of halite and gypsumcompared to mesohaline carbonate.

Salinity-induced environmental stress (“famineor feast”) facilitates organic preservation

Organic matter in modern saline systems tend toaccumulate in bottom sediments beneath density-stratified saline water and sediment columns inevaporitic settings where layered hydrologies aresubject to oscillations in salinity and brine level.Organicmatter is not produced at a constant rate insuch systems, rather, it is produced as pulses by ahalotolerant community in response to relativelyshort times when less stressful conditions occur inthe upper part of the layered hydrology (Fig. 18A).This happens when an upper less-saline watermass forms on top of nutrient-rich brines or withinwet mudflats when waters in and on top of theuppermost few millimetres of any microbial matfreshen. The resulting bloom (a time of “feasting”)by halotolerant algae and cyanobacteria is a timecharacterized by very high levels of organicproductivity. In mesohaline waters where lightpenetrates to the bottom, the organic-producing

5

4

3

2

1

0

TOC

(w

t %)

0 20 40 60 80 100Sedimentation rate (cm kyr-1)

WinterAutumn

WinterAutumn

SummerSpring

SummerSpring

Micriticcarbonate

Mineral detritus,pyrite, algae, layers ofamorphous OM

50 µm

Fig. 17. Sedimentation rate versus percent of total organiccarbon (TOC) in laminite marls from the Oligocene evapor-ites of the Mulhouse Basin, France. Inset shows the scaleand mineral/organic distribution in the laminae (varvecouplets) of the sampled intervals (after Hofmannet al., 1993b).


layer is generally the upper algal and bacterialportion of benthic laminated microbialites (typi-cally characterized by elevated numbers of cyano-bacteria). In stratified brine columns, the typicalproducers are the planktonic algal or cyanobacter-ial community inhabiting the upper water mass.Halotolerant autotrophic microbial communities,living off the remains of this plankton, float mid-water at the halocline of the density-stratifiedbrine columns. Similar aerobic decomposers canalso constitute bottom-layer communities in zonesof oxygenated oligotrophic waters.

Short pulses of extremely high organic produc-tivity during times of freshened mesohaline sur-face waters in-turn create a high volume of organicdetritus settling through the water column and/orconstruction of benthicmicrobialmats. Then,withthe end of the freshening event, the ongoing inten-sely arid climate that characterizes evaporiticdepressions means that salinities, temperaturesand osmotic stresses increase rapidly in the pre-viously freshened water mass. This leads to atime of mass die-off, in the once flourishing meso-haline community (“famine;”Fig. 18B). First, these

Permanent

Hab

itiat

sta

bilit

y

Environmental adversityincreases

Short-livedspecialists(very highproductivity& biomass)

Temporary

Tolerance ofadverse

conditions(lowest active

biomass)

Long-termhaloid specialists,fewer trophic andcommunity webs,( lower biomass)

Complexly tierednormal marine& lacustrinecommunities(high biomass)

Haloxenes,high speciesdiversity and bioticinteraction

Halophiles,moderate

biodiversity(osmolytes and anion adaption)

Halotolerants,halophiles, lowestbiodiversity, most

hostile to life

Blooms ofholotolerants(moderate tolow biodiversity)

Mass die-back

“FAMINE”“FEAST”

Stress on biota increasesdue to osmotic stress, anoxia,

temperature, salinity

Hab

itiat

perm

anen

ce

High

Low

Increasing biotic effects on preservation oforganic remains ofhaloid community

“FAMINE”“FEAST”

A

B

Abu

ndan

ce

Environmental stress(salinity, temperature, exposure)

Biodiversity

Biomass

Bio

tic s

tres

s

Abi

otic

str

ess

Environmental harshnessN

umbe

r of

via

ble

halo

tole

rant

cel

ls

Decline anddeath

FAMINEStationary

Exponentialexpansion

FEASTLag

Time

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

Low

Sou

rce

rock

pot

entia

l

High

Onset of freshening

SchizohalineSchizohaline

Perennialstable

Perennialstable

Sigmoidalgrowth

Fig. 18. Life in saline systems. (A) General ecological principles in stressed saline ecosystems. Sigmoidal growth curve oflife moving into a newly created niche (as created by a freshening event setting up a layered brine). As environmentalharshness increases due to abiogenic stress factors (such as increasing salinity, osmotic stress and temperature) the level ofbiogenic stress (predation or grazing decreases, allowing a few well-adapted species to flourish, leading to a decrease inbiodiversity anda short-term increase inbiomass. (B)Schematic summaryof the inter-relationships betweenhabitat stability,environmental stress or adversity, biodegradation, anoxia and source rock potential in an evaporite basin, showing whyschizohaline environmentally stressed mesohaline systems tend to favour the accumulation of organic matter in bottomsediments.

362 J. K. Warren

increasingly salty waters can no longer supporthaloxene forms. Then halotolerant life dies backand finally, by the halite precipitation stage, onlya few halophilic archaea and bacteria remain inthe brine column (typically acting as heterotrophsand fermenters). Repeated pulses of organicmatter created during a freshening event in a stra-tified brine column thus create laminated bottomsediment.

Hydrogen-rich algal and eubacterial debris isbest preserved within sediments where porewaters are anoxic and remain so until the resultingkerogen is sufficiently buried for it to generateliquid and gaseous hydrocarbons (Demaison &Moore, 1980). Thus the preservation of organicswith long-chain hydrocarbons intact is most likelyin settings characterized by long-term anoxia(less efficient decomposers). This tends to occurbeneath stratified eutrophic saline brine columnswith a permanent anoxicmesohaline bottomwatermass and a transiently freshened upper watermass. Preservation is also possible in benthic matsin shallow oligotrophic systems with permanentlyhypersaline pore waters, but the propensity forperiodic bottom oxygenation means preservationpotential of oil-prone mats is less likely in thissetting, as is also the case inmats of the strandzone.

Increasing rates of mineral precipitation athigher salinities means levels of hydrogen-proneorganics are highest in sediments deposited inschizohaline waters that remain in themesohalinefield. Once ambient salinities pass into the penesa-line and supersaline, the proportion of organics inthe sediment becomes insignificant as it is rapidlydiluted by large volumes of gypsum and halite(or trona and glauberite in some continental pene-saline/supersaline waters).

Feast and famine cycles are a biotal response toenvironmental salinity conditions that at first areeminently suitable and then increasingly adverseto life. It reflects the typical biological response torapid niche creation and expansion as the fresh-ened water layer sets up in the evaporitic depres-sion, and is known as the sigmoidal growthresponse (Fig. 18A). Freshening of surface waterscreates a vacant ecological niche intowhichmicro-bial life rapidly expands, flourishes and then oncemore dies back as drying or brine concentrationshrinks suitable niche space.

Long-term stability in any ecosystem leads todomination by “specialist” species that are welladapted, diverse and efficient in terms of energyflow-nutrientutilization (Fig. 18B).This biodiverse

community takes up and recycles carbon veryefficiently through the system and the potentialfor large volumes of carbon passing into the burialrealm is low and hence source potential is also low(a good example in the marine realm is a tropicalcoralgal reef).

In contrast, a schizohaline system is one definedby high habitat instability, its lack of habitat per-manence encourages opportunistic lifestyles(cycles of “famine or feast”). Opportunist speciesexpand rapidly into any suitable niche space, butthen just as quicklydiebackor encyst as conditionsbecomeadverse. Such systemsare characterisedbyhigh biomass pulses and low species diversity,leading to pulses of organics accumulating inthe evaporitic depression, with the remains likelyto be buried and “pickled” beneath anoxic bottombrines and pore waters, giving such systems ahigher source rock potential (Fig. 18B).

Some hypersaline settings are intermediates inthat their waters are constantly hypersaline, stress-ful to most life, but suitable to a few well-adaptedspecies. These regions are usually populated bya few very specialized species (e.g. “high-salt-in”halophiles) that can survive and flourish in con-ditionswheremost life dies. Theyphotosynthesizeand metabolize successfully in these hypersalineconditions (often for example living near halo-clines), but do so at rates that are much slowerthan the growth rates attained by halotolerant“opportunists” at times of “feast.” The long-termcycling of organic materials means bottom sedi-ment layers tend to have lower levels of entrainedorganics preserved compared to the schizohaline-mesohaline.

To take an understanding of community andcontrols from the modern into ancient saline sys-tems, it is necessary to account for changes in bothscale and diversity when comparing the style andsetting of “famine or feast” in modern saline set-tings to those of the past. Put simply, there are nomodern same-scale analogues for ancient marine-fed evaporite depressions, and so there are nomodern same-scale marine-fed evaporitic sourcerocks (Warren 2006, 2010).

ANCIENT EVAPORITIC SOURCE ROCKS

The common theme to deposition of all prolificsource rocks, both evaporitic and non-evaporitic,is that they require anoxic conditions to accumu-late and preserve their organics (Demaison &


Moore, 1980). This in-turn requires some way ofrestricting the influx of oxygenated waters and isusually accomplished by thermal or density stra-tification of a water body, in a setting where plank-tonic-producers flourish periodically in the upperwatermass. This iswhy somanyancient evaporiticsettings are also places where organics tend toaccumulate. By definition, evaporites requirerestricted inflow conditions to accumulate, theyare also typically areas of density-stratified waterswith long-term elevated salinities in the lowerdenser water mass. Levels of dissolved gases arenegligible to non-existent in the lower brine body,as it does not easily exchangewith the atmosphere,so encouraging long-term bottom anoxia.

This doesnotmean that all of theworld’s anoxia-associated source rockswere deposited in evapori-tic settings, only that the restricted conditionsthat favour the accumulation of evaporites are intheir early stages similar to conditions that favourthe accumulation of organics. In arid climates anyminor changes in inflow conditions can easilyforce a transition from one into the other. Hencethe common association of source rocks with thefreshened, typically early phases of the onset ofevaporitic sedimentation in many modern andancient lacustrine settings (Table 5). In the marinerealm, the sameneed for tectonicor eustatic restric-tion to create basins suitable for source rock accu-mulations (intrashelf, circular or linear sags) alsoexplains why, if further restriction and isolationfrom surface connections to the oceans ensue,the same regions are easily covered by a sequenceof salts (Fig. 19).

Tectonic and eustatic styles in ancientevaporitic basins

Almost all of the information that has been gath-ered and analyzed so far in this paper comes fromorganic accumulations in saline Quaternary lacus-trine and marine-margin settings. Likewise, allthe largest and thickest examples of Quaternarysabkhas, saline pans and salinas are continentaldeposits (Warren, 2006). Quaternary saline sys-tems only define same-scale analogs for ancientcontinental lacustrine deposition and are notsame-scale analogues for ancient marine-fed epei-ric and basin-centre salt basins, or their entrainedsource rocks (Fig. 19; Warren 2006, 2010). Yetcompared to lacustrine sediments, these ancientmarine-associated deposits entrain and seal fargreatervolumesofevaporitic source rocks (Table5).

Most ancient marine-fed evaporite deposits areone or two orders of magnitude larger than today’smarine-fed hypersaline systems and accumulatedin huge marine-seepage fed sub-sea-level tectonicdepressions with no surface connection to theocean (Fig. 19). Well-documented source rock-entraining ancient basinwide evaporite depositsinclude the Jurassic Hith, Permian Zechstein andMiocene Messinian evaporites, but none have asame-scale modern counterpart. Likewise, nowidespread marine-fed platform evaporites haveaccumulated since the Eocene. TheMediterraneanMessinian salts (�5.5Ma) are the youngest knownbasinwide evaporite. Well-documented marine-fed platform evaporites include the evaporite-capped cycles of the Jurassic Arab Formation inSaudi Arabia and the United Arab Emirates, thePermian Khuff Formation in the same region, andthe evaporite-capped Permian backreef strata ofGuadalupian age in West Texas and New Mexico.

Although platform and basinwide evaporitesmay have no Quaternary counterpart in terms ofscale or thickness, they can be interpretedusing process models that are combinations of thehydrologies of Quaternary sabkhas, saline pansand salinas. Accumulations of thick evaporiteaccumulations (continental or marine) and asso-ciatedmesohaline stages require a stable long-termbrine curtain (�100 kyr–1 Myr) to accumulateto substantial thicknesses and lateral extents(Warren, 2003, 2006). The hydrological positionof the active top of an aggrading brine curtain, withrespect to the evaporite depositional surface, inboth platform and basinwide settings, defines thedominant textural signature of the resulting saltsequence (saline-pan, evaporitic mudflat/sabkha,saltern, deeper slope and basin).

High amplitude, high-frequency 4th-order sea-level oscillations of the current “icehouse” climatedo not allow the set up of stable brine curtainsbehind laterally-continuous seepage shoals in pre-sent-day carbonate platforms, and so there are noNeogene examples of platform evaporites withstable intrashelf depressions. Platform evaporitesrequire greenhouse eustacy to form. Nor are theresuitable sub-sea-level rift-induced intracratonicsags or soft-collision belts in arid marine-fedsettings where conditions are suitable for the crea-tion of basinwide marine drawdown deposits(Warren, 2006).

The need for sub-sea-level tectonically-inducedbasins explains why times of worldwide conti-nent-continent collision followed by continental

364 J. K. Warren

Table

5.Characteristicsandsettingsofevaporiticsourcerocks.Basinstyles:1=basincentre;2=intrash

elf;3=lacustrine.SeeW

arren(2006)forfurtherdetailonthe

significanceofdifferentbasinstyles

Form

ation/G

roup

locality

andage

BasinStyle

Characteristicsanddepositionalsetting

Reference

Messiniancarbonates

LorcaBasin,Spain

UpperMiocene

1a

Basinwideevaporite

marginalbasin

Organic-richlaminatedmudstonesdepositedin

pre-evaporitic

mesohalinemarginalbasinswithdensity-andsalinity-stratified

brinecolumns.

Thebasinunderw

entsp

oradic

phasesof

circulatory

restrictionwithmarkedproductionand

preservationoforganic

matter,culm

inatingin

evaporative

sedim

entation(latest

Miocene).Asthewaterin

this

basin

evolvedtoward

evaporativeconditions,

anumberoforganic-

richdepositionalphases(>

25wt%

TOC)occurred.Duringthe

earlypartsofthese

phases,

theupperwaterwasnutrientrich

andcomparatively

norm

almarine,andthebottom

waterwas

anoxic

andmore

saline.T

hiswasfollowedbyrisingsalinitiesin

thesu

rfacewaters,holomixis

andsh

ort

phasesofevaporite

form

ation.

Benalietal.,1995

Russelletal.,1997

Rouchyetal.,1998

Gessoso-Solfifera

Form

ation,Sicily

UpperMiocene

(Messinian)

1a

Basinwideevaporite

marginalbasin

Biomarkercompositionsfrom

immature

organic

sulphur-rich

marl

samplesfrom

10ofthe14evaporite

cyclesin

anItalian

Messinianevaporiticbasin(V

enadelGesso)indicate

large

variationsin

thecompositionofsp

eciesin

thewatercolumn

(e.g.dinoflagellates,

diatomsandotheralgae,cyanobacteria,

methanogens,greensu

lphurbacteriaandbacterivorousciliates)

andin

contributionsfrom

thecontinent(i.e.landplants)within

eachmarl

bedandbetw

eenmarl

beds.

Themarl

bedswere

depositedwithin

astratifiedlagoonwhere

anoxic

conditions

extendedinto

thephoticzoneformuchofthetime.

Damsteetal.,1995

Keely

etal.,1995

Luglietal.,2007

Organic-richmarls,

Rudeis,Kareem

and

Belayim

Fms.

Gulfof

SuezMiocene

3 Riftbasincontinentalto

transitionalmarine

Inclusionstudiessh

ow

evaporiticenvironmentofdeposition

(reducingconditionsandhighsalinities),favouredoil-

generatingkerogen.Carbonate

mineralsandinclusionstrapped

ingypsu

mindicate

possible

mixingofmarinewaterwithabrine

ofrestrictedoccurrenceatthetimesourcerockswere

deposited.

Kholief&Barakat,1986

Rouchyetal.,1995

Barakatetal.,1997

Alsharhan,2003

BresseandValencesalt

basins,

France

Paleogene


transitionalmarine

Organic

matterismostly

immature

andoccurs

inintercalatednon-

halite

beds.

Type-IIIkerogenis

tiedto

terrigenousdeposition.

Type-Ikerogenis

abundantin

mesohalineevaporiticlaminites

ofValencebasin.Type-IIis

more

abundantin

BresseBasin.

Organicsaccumulatedbeneath

aperenniallystratifiedbrine

columnofupto

tensofmetres.

Syndepositionaldissolution

ofhalite

mayhaveaidedtheaccumulationofsignificant

amounts

ofoil-proneorganic

matterin

non-soluble

brecciatedresidues.

Curialetal.,1990

(continued)


Table

5.(C

ontinued)

Form

ation/G

roup

locality

andage

BasinStyle


Reference

SaltIV

Form

ation,

Mulhouse

SaltBasin,

EuropeLower

Oligocene


transitionalmarine

Biomarkerassemblagesare

dominatedbyacyclicisoprenoids,

esp

eciallyphytane(0.13<Pr/Ph<0.52),n-alkaneswith

specificdistributionpatterns,andsteranes.Largedifferencesin

distributionindicate

changesin

paleoenvironment.Thelargest

changesare

indesm

ethyl-andmethylsteranedistributionsand

are

probably

linkedto

occasionalreconnectionofthestratified

evaporite

basinto

thesea,leadingto

adinoflagellate

bloom

intheupperwaters

ofadensity-stratifiedbrinecolumn.

Damsteetal.,1993

Hofm

annetal.,1993a,b

Hollanderetal.,1993

Keely

etal.,1993

EoceneQianjiangand

LowerEocene-

PaleoceneXingouzhui

Form

ationsof

Jiangling-D

angyang

area,JianghanBasin,

Northwest

China

Eocene-Paleocene

3 Forelandflexure

basins,

mountain-frontfault

depressions

Anoxic

evaporiticlacustrinesourcerocksgeneratedmost

ofthe

crudeoils.

Highsalinityandlow

Ehenhancedpreservationof

oil-proneorganic

matterandfacilitatedincorporationof

sulphur.Anoxiaandtheunusu

alp

resenceofabundantsulphate

asgypsu

mresu

ltedin

microbialreductionofsu

lphate

tosu

lfide

andincorporationofthis

sulphurinto

thekerogen.Biomarkers

inQianjiangForm

ationsh

ow

thatsomesourcerocks(Sha13

well-1322m)wasdepositedundermore

saline,lowerEh

conditionsthanothers)Ling80well-1808m).Sha13sample

ismore

organic-rich(6.62vs1.27wt%

TOC),hasahigher

hydrogenindex(794vs501mgHCg�1TOC)andfasterreaction

kinetics.

Kerogenfrom

theSha13sample

isTypeI.

Jiang&Fowler,1986

Huang&Shao,1993

Peters

etal.,1996

Ritts

etal.,1999

Hansonetal.,2001

GreenRiverForm

ation,

WyomingandUtah

Eocene

3 Forelandflexure

basin

from

Laramide

orogeny

Laminatedorganic

mudstonesandoilsh

alesdepositedin

deeper

anoxic

bottom

waters

ofaperennialsalineanddensity-stratified

alkalinelake.Gilsoniteandtabbyitebitumensare

associated

withParachute

CreekMember,depositedduringamajor

expansionandfresh

eningofancientLakeUinta.Compound

specificisotopic

analysesofb-caroteneandphytane

(d13C=�3

2.6

to�3

2.1‰)from

these

bitumensreflectinputfrom

primary

photosyntheticproducers

suchascyanobacteria.

Steraned13C

values(�

34.5

to�2

9.2‰)reflectcontributions

from

lacustrinealgae,whileextremely

depletedd13Cvaluesfor

methylhopanes(�

58.1

to�6

1.5‰

)su

ggest

inputfrom

methanotrophic

bacteria/archaea.Variationsin

thed13Cvalues

ofthea�b

-hopanes(�

51.4

to37.7‰)im

ply

additionalinput

from

otherbacterialsources.Thewurtzilitebitumengenerated

from

thesalinefaciesoftheGreenRiverForm

ationwas

depositedduringalaterregressionofLakeUinta.Compound

specificisotopic

analysesofphytane(d

13C=�3

0.1‰)and

steranes(d

13C=�2

9.6

to�2

6.7‰)from

this

bitumenindicate

continuedinputfrom

primary

producers

andeukaryotes.

The

higherrelativeconcentrationsofgammacerane(d

13C=�2

6.9‰)

indicate

increasinginputfrom

aerobic

species.

Slight

enrichmentin

d13C

inthewurtziliteextract(andseveral

biomarkers)su

ggestssu

lphate-reducingbacteriaoutcompeted

methanogens,

thereby,eliminatingtheinfluenceof

methanotrophsin

this

latersalinestageofdeposition.

Ruble

etal.,1994

Katz,1995

366 J. K. Warren

KongdianForm

ation

(Ek)andEs4

member

oftheShahejie

Form

ation

Zhaolanzhuangfield,

Jizhongdepression,

BohaiBayBasin,

China

Eocene–Oligocene

3 Continentalhalf-graben

Palaeogeneriftwith

Neogenesu

bsidence

Naturalgascontainsthehighest

proportionsofH

2S(40–92%

)amongthesourgasesencounteredin

China.Thesedim

entary

sequenceconsistsofhalite,anhydrite,carbonate,sandstoneand

shale

interbedsdepositedin

theevaporativebrackishwater

lacustrine-saltlakesetting.InthedeepestpartoftheJinxiansag,

thetotalthickness

ofevaporitesis

more

than1000m,ofwhich

halite

accounts

forover40%

.Variousorganic-richmudstones

intercalatedwiththeevaporitesare

currentlywithin

the

conventionalhydrocarbonwindow

(withadepth

of

2500–3500m),andlikely

thesourcefortheoilandsourgasin

theZhaolanzhuangfield.Thetemperaturesofthegasreservoirs

rangefrom

75to

100

� C,toolow

forsignificanttherm

ochemical

sulphate

reduction.Theco-occurrenceofabundantelemental

sulphurwiththesourgasandthed34Svaluesofthevarious

sulphur-containingcompoundsindicate

thattheH2Sgases

were

most

likely

derivedfrom

muchdeepersourcekitchens

where

significanttherm

ochemicalsu

lphate

reductionhas

occurred.

Chenetal.,1996

Zhangetal.,2005

BucomaziForm

ation,

Cabinda,offsh

ore

Angola

Cretaceous


transitionalmarine

TheLowerCongohydrocarbonhabitatis

dominatedbythe

Pre-SaltBucomazipetroleum

system.These

lacustrine,often

super-rich,laminatedevaporiticsedim

ents

revealconsiderable

organofaciesvariationsbetw

eentheirearlylacustrinebasinfill

andlatersh

eetdrapedevelopmentwiththreemajor

depositionalregim

esreflectingsalinityandwaterdepth

control.

13C

depletedbasalsedim

ents,sh

owingstronggammacerane/

4-m

ethylsteranesignatures,were

segregatedasseenbyamajor

isotopic

excursion.Thiseventrepresents

thetransitionfrom

an

earlysalineplayalaketo

adeeperwatersalinity-stratified

mesohalinelakesu

pportingahighlevelofbottom

anoxia.For

theinterm

ediate

sedim

ents,steraneandtricyclicditerpane

abundances,

plussterane/hopaneratios,

hadmarine

connotationsandcanbeinterpretedastheresu

ltofinterm

ittent

marineincursions.

Foresh

adowingirreversible

oceanic

ingression,aresu

rgenceofgammaceraneabundancein

the

upperm

ost

sedim

ents

typifiedlittoral-sh

allow

marine

depositionalconditions.

Burw

oodetal.,1995,

1992

Burw

ood&Mycke,1996

Schoellkopf&Patterson,

2000

LagoaFeia

Form

ation,

CamposBasin,Brazil

LowerCretaceous


transitionalmarine

Rift-stagelacustrinesedim

entsare

thesourcerockofallpetroleum

sofardiscoveredin

theCamposBasin,themost

prolificoil

provincein

Brazil.These

organic-richsh

aleswere

depositedin

anoxic

brackishto

salinelakes.

Petroleum

migrationpathways

involvedirectcontactbetw

eensourceandreservoir

rocks

within

theriftsequence.L

atermigrationto

themarinesequence

reservoirsis

relatedto

windowsin

thehalokineticsaltlayer

connectedto

growth

faultsandunconform

ities.

Trindadeetal.,1995

Mello&Maxwell,1991

(continued)


Table

5.(C

ontinued)

Form

ation/G

roup

locality

andage

BasinStyle


Reference

MuribecaandMacei� o

Form

ations,

Sergipe

Basin,Brazil

LowerCretaceous


transitionalmarine

Most

hydrocarbonaccumulationsdiscoveredin

theSergipe

subbasinare

sourcedbytheprotomarineAptianmarlsand

calcareoussh

alesoftheMuribecaandMacei� o

form

ationsboth

below

andabovetheAptiansalt(Ibura

Member).These

source

rocksaverageabout6%

TOCandare

composedmainly

of

hydrogen-richtypeIIkerogen.

Melloetal.,1988

Kim

meridgianShale,

NorthSea

UpperJurassic

1b

Sedim

ent-starveddeep

marinebasincentre

generatedbyongoing

Perm

ian-M

esozoic

riftingandsu

rrounded

byPurbeckevaporite-

carbonate

platform

Seawaterflowedsouthwardsfrom

BorealOceaninto

Tethyan

Oceanbutevaporationin

thesh

allow

waters

ofthearchipelago

ofislandsandsh

oalscreatedwaters

ofincreasedsalinityandin

somecaseslocalstrongbrinesandevaporites,

whichsankand

flowedassalinebottom

currents

(from

34–42‰)into

deeper

water.Areasofpondeddeepermesohalinewaterwere

commonplacein

themore

rapidly

subsidinggrabens,separated

bysills,denserwaters

accumulateduntiltheywere

able

tosp

ill

overthesills.In

this

waymore

salinewaters

migratedalongthe

seabottom

depressions,

their

pathsbeingdeterm

inedbylocal

tectonic

features,

butmostly

inanorthto

south

direction.

Astable

waterstratificationensu

ed,thehaloclinebeingatabout

50m

waterdepth

andperiodsofwidesp

readincreasedsalinity

are

markedby“hot”

shales.

Cooperetal.,1995

Miller,1990

Purbeckianlacustrine

beds,

Dorsetcoast

UK,

LowerCretaceous,

3 Continentallagoonsand

lakesin

sea-m

argin

positionatedgeof

carbonate

platform

Within

these

beds,

whichim

mediately

overlie

thePurbeck

evaporites,

alargeOM

accumulationis

recorded,withtotal

organic

carbon(TOC)ofupto

8.5wt%

.Highhydrogenindex

(HI)values(upto

956mgHCg�1TOC)pointto

aTypeIOM,

generallyconsideredasderivedfrom

algal-bacterialbiomass.

This

contrastswiththeOM

presentin

theunderlyingand

overlyingintervals,displayingin

generallowerTOCandHI

values,andconsistingofdegradedalgal-bacterialmaterialwith

higherproportionsofterrestrialOM.This

organic-rich

accumulationcanbeinterpretedasaperiodofenhanced

primary

productivitywithin

coastallagoonal/lacustrine

settingsattimesoflow

sealevelandhasstrongaffinitiesto

modern

CoorongLakesin

Australia.

Schnyderetal.,2009

Shelfmargin

laminites,

ArabianGulffrom

NW

Iraqthroughthe

ArabianGulfto

central

Oman(e.g.Diyab,

Tuwaiq

andHanifa

Form

ations)

UpperJurassic

2 Density-stratified

intrash

elfbasins

surroundedby

evaporiticplatform

.Somelowsare

possibly

tiedto

saltwithdrawal

Organic-richlaminatedmudstonesandwackstonesdepositedin

pre-saltintrash

elf,mesohalinebasinsonagentlydownwarped

epeiric

platform

.Intrash

elfbasinsthatretain

organicsallhavea

density

andsalinitystratifiedwatercolumnwithmesohaline

bottom

carbonates.

These

basinssourcemore

than90%

ofthe

hydrocarbonsin

theMiddle

East.Theyare

argillaceous

dolomitic

limestonesthatfeedthemost

prolificpetroleum

system

intheworldandunderlie

theworld’srichest

reservoir:

theArabDin

theArabForm

ation.O

neofthemostprolificsource

unitsis

theHanifaFm.in

theArabianBasinofSaudiArabia.

Inthedeeperpartsoftheintrash

elfArabianBasin(w

aters

�30m

deep)theHanifaiscomposedoflaminitemudsandmarls,while

Ayresetal.,1982

Palacas,

1984

Evans&Kirkland,1988

Droste,1990

Beydoun,1993

Carriganetal.,1995

Whittle&Alsharhan,

1996

Ibrahim

etal.,2002

368 J. K. Warren

inthesu

rroundingsh

elfitis

dominatedbygrainstonesand

packstones.

Within

theHanifalaminitesthere

are

discrete

but

minorprimary

laminaeofanhydrite(originallygypsu

m),aswell

asearlydiageneticanhydrite

nodules,

both

indicators

of

occasionalhypersalinity.There

are

alsolaminaeoffibrous

calcite,whichsomeauthors

haveinterpretedasanother

indicatorofhypersalinity.TheHanifais

awidesp

readand

prolificsource,itcanentrain

more

than30metresoflaminites;

totalorganic

carbonexceeds1%

,withsomesectionshaving

more

than5%

.Thekerogenispredominantlyhydrogenrich,the

generatedoilshaveahighsu

lphurcontent,aPr/Py<1,and

apredominanceofeven-numberednorm

alalkanes.

Smackovertrendof

Mississippi,Alabama

andFlorida,

northeastern

Gulfof

Mexico

UpperJurassic

2 Shallow

restricted-

circulationsalinity

stratifiedintrash

elf

basinonabroad

carbonate

platform

Oilandgasin

thistrendare

generatedfrom

algal-richlight-brown

toblacklaminatedlimemudstones(argillaceouscontent<6%

)oftheLowerSmackoverForm

ation.Depositionoccurredin

intraplatform

depressionssu

rroundedbyabroadcarbonate

platform

.Bottom

waters

were

stratifiedwithslightlysaline

waters

suppliedfrom

thebroadplatform

surroundsandthe

shoalingcarbonate

system

wassealedbythesu

lfate

evaporites

oftheBucknerAnhydrite.

Oehler,1984

Sassen,1990

Mancinietal.,2003

Todilto

Form

ation

Todilto

Basin,USA

Middle

Jurassic

3 Forelandflexuralbasin

(lacustrine?)

TheLim

estoneMemberoftheTodilto

Fm.is

awidesp

read

carbonate

laminiteupto

3m

thick,o

verlain

inthesu

bsu

rfaceby

upto

30m

ofCaSO

4knownastheGypsu

mMember,althoughit

ismostly

anhydrite.TheLim

estoneMemberis

thesourcerock

for6knownhydrocarbonaccumulationsin

thesandsofthe

underlyingEntradaFm,w

hileitandtheoverlyingCaSO

4are

the

seal.Thequantity

ofTOCis

low

(�1%

)forsu

chathin

source

rockandithassomeunusu

alcharacteristicscomparedto

most

evaporiticsourcerocks.Laminitecoupletsare

0.15mm

thickyet

are

laterallycontinuousforupto

3.7

km

andform

widesp

read

cohesive“sh

eets”,whichinvariably

contain

remnants

of

vascularplants.TheTodilto

isprobably

lacustrinewitha

marineseephydrology,similarin

hydrologyto

thecoastal

salinasofsouthern

Australia.Theorganicsreflectthegrowth

of

ahealthyconifercoverin

itssu

rroundsanditswaters

were

density-stratifiedlacustrine,probably

fedvia

amarineseepage

inflow

andperiodic

seasonalrunoff.T

hismaintainedadensity-

stratifiedbrinecolumn,firstatcarbonate

saturationduring

depositionoftheLim

estoneMember,thenatgypsu

msaturation

duringthedepositionoftheGypsu

mMember.

Vincelette&Chittum,

1981

Evans&Kirkland,1988

Organic

mudstones

intercalatedwith

evaporites,

Mandawa

Basin,Tanzania

Triassic


transitionalmarine

Totalorganic

carbon(TOC)valuesrangefrom

1.23to

7.41wt%

of

kerogenTypeII/III.Theevaporite

(hypersaline)influenceis

indicatedbythepresenceofC-24-tetracyclicterpanes,

gammaceraneandC-35-homohopanes.Therelativeabundance

oftricyclicterpanes(C-19-C-28+)withresp

ectto

pentacyclic

terpanes(C-27-C-35,)seemsto

changewithdepth,whereby

Kagya,1996

(continued)


Table

5.(C

ontinued)

Form

ation/G

roup

locality

andage

BasinStyle


Reference

thetricyclic/hopanesratioapparentlyincreaseswithdepth.T

he

mixedorganic

inputfrom

marineandterrestrialprecursors

are

indicatedbymixedabundancesofC-27-,C-28-,C-29-steranes.

Subsalt-allochthonoil

seeps,W

indsorGroup,

NovaScotia,Canada

Carboniferous


transitionalmarine

Theoilseepsare

eitherassociatedwithupperHortonGroup

(Ainslie

Form

ation)orbasalW

indsorGroup(M

acumber

Form

ation)sedim

ents.Thebiomarkerdistributionsofthe

samplesare

similarto

StoneyCreekoilsandtheir

lacustrine

carbonate

sourcerock(A

lbertShale)oftheMonctonSub-basin,

NewBrunsw

ick,asare

oilsfrom

seepsin

thePugwash

Saltmine.

Fowleretal.,1993

Blacksh

alesin

the

ParadoxMemberofthe

Herm

osa

Form

ation,

ParadoxBasin,USA

Carboniferous

(Pennsylvanian)

1a

Forelandflexuralbasin

Organic-richblacksh

ales(inform

allyknownastheCaneCreek,

Chim

neyRock,Gothic

shales)

form

acarbonate

laminitebasal

sequenceto

anumberofsalting-upward

evaporite

cyclesin

the

ParadoxMember.Mineralogicallythesh

alesare

betw

een

30–50%

calciteordolomitewithclaysandquartzsandform

ing

theremainderofthematrix.TOCvaluesof5%

ofhydrogen-

proneorganicsin

theblacksh

alesare

usu

al,withvaluesof10%

notuncommonandthehighest

valuesmore

than20%

.The

organicsare

mixturesofhalotolerantdebrisandmarine-style

organicsform

edwhensu

rfacewaters

were

atmarinesalinities,

aswellasoccasionalterrestrialorganicswash

edinto

thebasin

from

thesu

rroundinghinterland.

Evans&Kirkland,1988

Hiteetal.,1984

OilShales,

Junggar

Basin,NW

China

UpperPerm

ian

3 Controversial,with

tectonic

interpretations

rangingfrom

foreland

flexure

toregional

transtensionalbasin

Junggar

Basin

isoneofthelargestoil-producingbasinsin

China,its

Upper

Perm

ianoilsh

alesareamongthethickest

andrichest

lacu

strinesourcerocksin

theworld.TogethertheJingjingzigo

u,

Lucao

gou,andHongy

anch

iForm

ationsofthesouthern

Junggar

Basin

comprise

over1000m

oforganic-richlacu

strinefacies.

They

reco

rdanevolutionfrom

relativelysh

allow,evaporative

lakesto

freshwater

lakes

withfluvialsystems.

Jingjingzigou

Form

ationwasdepositedin

aperennialsalinelakecharacterized

bylow

TOCandHI,andbiomarker

features(suchas

abundan

tb-carotane)

consistentwithasp

ecializedsalineorhypersaline

biota.Biomarker

distributionsin

JingjingzigouForm

ation

extracts

most

closely

resemble

oilsfrom

thegian

tKaramay

oilfield.OverlyingLucao

gouForm

ationrepresents

oneofthe

rich

estan

dthickestlacustrinesourcerock

intervalsin

theworld,

yet

itcontrad

icts

conventional

lacu

strinesourcerock

modelsin

atleasttw

oim

portan

tasp

ects.First,dep

ositionoccu

rredat

middle

palaeo

latitudes

(39–43� N

)ratherthan

inthetropics.

Second,limited

nutrientsu

pply

inadrainage

basindominated

byinterm

ediate

volcan

icrock

sappearsto

hav

ecau

sedlow

tomoderate

primary

productivities.

Stable

salinitystratification

andlowinorgan

icsedim

entationratesin

adeeplakenonetheless

resu

lted

indep

osits

withupto

20%

TOCandHInear800.

Carroll,1998

Carrolletal.,1992

Tangetal.,1997

370 J. K. Warren

OverlyingHongyan

chiF

orm

ationhas1–5%

TOCbutlowHI,an

dwas

dep

ositedin

freshwater

oxic

tosu

b-oxic

lakes.

Ravnefjeld

Form

ation,

East

GreenlandUpper

Perm

ian


transitionalmarine

TheRavnefjeld

Form

ationissu

bdividedinto

fiveunitsthatcanbe

tracedthroughouttheUpperPerm

iandepositionalbasin.Two

oftheunitsare

laminatedandorganic

rich,andwere

deposited

underanoxic

conditions.Theyare

consideredgoodto

excellent

sourcerocksforliquid

hydrocarbonswithinitialaverageTOC

(totalorganic

carbon)valuesbetw

een4and5%

andHI

(hydrogenindex)betw

een300and400.Thecumulativesource

rockthickness

isbetw

een15and20m.Thesourcerocks

are

separatedandenclosedbythreeunitsofbioturbated

siltstonewithaTOCofless

than0.5%

andanHIofless

than100.

These

siltstoneswere

depositedunderrelatively

oxic

conditions.

Theorganic

geochemistryofthesourcerocksis

typicalformarinesourcerockswithsomefeaturesnorm

ally

associatedwithcarbonate/evaporite

riftenvironments

[low

Pr/Ph(pristane/phytane),low

CPI(carbonpreference

index),distributionoftricyclicandpentacyclicterpanes].

Theestablish

mentofanoxic

conditionsandsu

bsequentsource

rockdepositionwascontrolledbyeustaticsealevelchanges.

Christiansenetal.,1993

Phosp

horiaForm

ation,

LittleSheepCreek,

Montana

Perm

ian

1b

Forelandflexure

basin

Correlationsbetw

eenbiomarkerindicators

ofanoxia

andsalinity

suggest

thatanoxia

wasin

part

theresu

ltofachemocline

separatingnorm

almarinewaters

abovefrom

more

salinebottom

waters.A

noxia

andsalinityin

thebottom

waters

increasedwith

timemakingconditionsin

thebasinprogressively

more

hostile

tobenthic

organisms.

Dahletal.,1993

Kupferschiefer

Form

ation,

NW

Europe

Perm

ian

1a

Riftbasin,restricted

marine

Thin,widesp

readorganic-richlaminatedmudstonedepositedin

shallow

mesohalinemarginalsea-lakeswithwaters

whichwere

<100m

deepandmostly

10–30m

deep.Surfaceexchangewith

Zechstein

oceanwasrestrictedbypalaeohighs.

Bechtel&Puttmann,

1997

Anhydriticlacustrine

beds,

East

Shetland

Platform

,NorthSea

Middle

Devonian

3 Riftbasin,restricted

marine

TheUKCSwell9/16-3

drilledonthewestern

flankoftheBeryl

Embaymentindicateslocaldevelopmentofhypersaline

environments

equivalentto

theAchanarras/Sandwickfish

bed.

Showsclose

affinitywithcontemporaneousMiddle

Devonian

sourcerocksoftheInnerMorayFirth

andcrudeoilin

Beatrice

oilfield.

Duncan&Buxton,1995

MuskegForm

ationand

LowerKegRiver

Member,Alberta,

Canada

Devonian

1a


marine

Laminatedorganic-richbituminousmudstonesdepositedin

pre-evaporiticdensity

stratifiedwatercolumns.

Vertical

migrationfrom

theMuskegform

ationto

theMuskegReservoirs

mayhaveoccurredthroughlocalfracturingofanhydritesdriven

bythedissolutionofBlackCreekHalite.

Clark

&Philp,1989

Stasiuk,1994;Chenet

al.,2005

Laminatedevaporitic

A-1

mudstones,

MichiganBasin

Silurian

1a


marine

Biomarkercharacteristicsindicate

acarbonate/evaporite

source

rockdepositedunderhypersalineconditionsin

astrongly

reducingenvironment.Thesourcerocksoccurin

thebasin

centrein

organic-richlaminitesoftheinter-reefA-1

Salina

Gardner&Bray,1984

Oberm

ajeretal.,1998,

2000

(continued)


Table

5.(C

ontinued)

Form

ation/G

roup

locality

andage

BasinStyle


Reference

Form

ation,a

mesohalinecarbonate

depositedbeneath

adensity

stratifiedbrinecolumn.

ChandlerForm

ation,

AmadeusBasin,

AustraliaLower

Cambrian

1a

Forelandflexure,

Restrictedmarine

Thin

bituminouspre-evaporiticcarbonate

mudstonedeposited

subaqueouslyin

arestrictedbasinim

mediately

priorto

the

depositionofthethickhalitesoftheChandlerForm

ation.

Bradsh

aw,1988

Horm

uzSeries,

Arabian

Gulfandcounterparts

inOman,India

and

Pakistan

Neoproterozoic

toEarly

Cambrian

1 Forelandflexure,

restrictedmarine

Alm

ost

allthePersianGulfandlargeareasofsouthern

Iranand

northeastern

Arabia

are

underlain

byathicksequenceof

sedim

ents,knownastheHorm

uzSeries,

ortheHuqfGroupin

Oman.Itis

madeupofinterbeddedsalt,anhydrite,dolomite,

shale

andsandstone.Itisnotonly

thecause

ofmanysalt-dome-

relatedoilandgasfieldsbutis

alsoconsideredto

havebeena

majorsourcerockforhydrocarbonsin

Ordovician,Devonian,

Carboniferous,Perm

ianandperhapsyoungerreservoirs.These

oilshavecharacteristic

biomarkers

andhighly

depletedcarbon

isotopessignaturesindicativeoftheir

prokaryoticprecursor.

Amthor,2000

Edgell,1991

Grantham

etal.,1988

Peters

etal.,1995

Terken&Frewin,2000

Schoenherr

etal.,2007,

2009

372 J. K. Warren

rifting (“zip then split”) tectonics encourage theaccumulation of substantial volumes of salts andorganic-rich evaporitic sediments in sub-sea-leveltectonic depressions (Fig. 19). In the past 800 Myrthere have been two such tectonic cycles definedby supercontinent accretion and disaggregation(i.e. the accretion and disaggregation of Phanero-zoic Pangea and Neoproterozoic Rodinia). Marine-fed evaporitic source rocks tend to form at timeswhen the tectonic depression is undergoing hydro-graphic isolation from the open ocean. The basinstill has a surface (hydrographic) connection tothe ocean, but inflow is restricted and the basinis typically surrounded by widespread saltyplatforms with sheets of salterns and evaporiticmudflats (Fig. 19). When the surface connectionto the open ocean is completely cut-off, thebasin becomes a marine-fed sub-sea-level seepagedepression and widespread thick salts precipitate

in the lower parts of the basin floor in watersranging from hundreds of metres deep toephemeral.

Ancient mesohaline source rocks

Worldwide, studies of ancient evaporitic basinshave shown that organic-rich mesohaline sedi-ments accumulate in ephemeral surface brines,saltern sediments, or basin and slope settings inboth marine and continental regimes (Evans &Kirkland, 1981; Oehler, 1984; Warren, 1986; Bus-son, 1988; Kirkland & Evans, 1988; Rouchy 1988).The most prolific accumulations of organics inancient evaporitic sediments tend to have beendeposited as laminated micritic carbonates thataccumulated beneath density-stratified moder-ately-saline (mesohaline) anoxic water columnsof varying brine depth. There are three, possibly

Sea Level

3

-5

Axial riftsubsealevel seepage basin

Continental Terrace(hinge zone) Alluvial fan &

lake deposits

0Brine level

sealevel

Marine source rocks in rift to incipient marine evaporite stageAulocogen and intracratonic sag

(no Quaternary counterparts)

Hot Spot / Thermal Doming continental hydrology, supra-sea-level setting means marine seepage not possible). Wilson Cycle early Stage B

3

-3

Volcano: mafic if from hot spot. Felsic if frommelting of continental crust

Felsic batholiths from fractionalmelting of lower continental crust

Normal faults

Horst Graben

0sealevel

Continental lacustrine source rocks(Quaternary with ancientcounterparts)

sea level

Continent-Continent Collision (periods of marine seepage coincidentwith hydrographic isolation). Wilson Cycle Stages later E & F

Ancient continental marginsediment wedge (thrust-faulted & folded)

Ancientaxial graben

Foreland basin(sub-sea-level)

Volcanic front Suture zoneBackarc

(marginal)basin

Hinterlandthrusts

g r e e n s c h i s t

a m p h i b o l i te

g r a n u l i t e

Continental lacustrine source rocks & evaporites(Quaternary with ancient counterparts)

Collision and/or sag belt evaporites(no Quaternary counterparts)

Stage BEarly rifting

Stage CFull Ocean basin

Stage DSubduction Zone

Ocean begins to close

Stage EClosing Remnant

Ocean basin

Stage GPeneplainedmountains

Stage FContinent-Continent

Collision

Contin

ent-to-continent proximity

Stage AStable craton

Continentsfarapart

WILSONCYCLEIs

olat

edsu

b-se

a-lev

el seepage basins possible

Foundering of Rift Valley transition to restricted marine (stepped marine invasionvia seepage spillover). Wilson Cycle later Stage B or early C.

Epeiric seaway

Peric

onco

ntin

enta

l

seaw

ay

Openmarine

Evaporiticmudflat

sabkhasalina

mudflat

Intrabasinaldepression(stratified,

anoxic

Increasingly restricted hydrographic entrance to a closing seaway. The restriction is 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 isolation and onset of long-term sub-sea-level seepage.

Organic-rich laminites in bottom depressions of a stratified mesohaline marine-fed basin

500 km

Periplatform depression(potential source rock sitewith increasing restriction

of shelf waters)

Elevation (km)

Elevation (km)

A

C

B

500

m

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


four, major mesohaline density-stratified settingswhere organic-rich laminites (source rocks) accu-mulate in saline settings that are also associatedwith, or evolve into, evaporite deposits (Fig. 20;Table 5). These are:

(1) Basin-centre lows in marine-fed evaporiticdrawdown basins:(a) evaporite-pluggedmesohaline basin centre;(b) evaporite platform rim surrounding

restricted and stratifiedslightly-mesohalinecarbonate basin centre.

(2) Mesohaline intrashelf lows on top of epeiricevaporitic platforms;(a) intraplatform depressions with layered

mesohaline brines;

(b) shelf-edge depressions with layered meso-haline brines.

(3) Saline-bottomed lows in perennial underfilledsaline lacustrine basins.

(4) Closed seafloor depressions in halokineticdeep-water marine slope and rise terrains.

Basin Setting 1

There are two depositional styles for basin-centreor basinwide mesohaline source rocks: (a) basin-centre drawdown laminites intercalated andoften sealed by basinwide salts; (b) basin-centrelaminites where the basin margin is a shallow,restricted, at times evaporitic platform that sur-rounds a slightly mesohaline deep-water starved-

1aD

raw

dow

n2a

Intr

apla

tform

2bP

latf.

edg

e

Set

tin

g 1

B

asin

wid

e se

tting

Set

tin

g 2

E

peiri

c pl

atfo

rm lo

ws

Set

tin

g 3

S

alin

e la

cust

rine

Set

tin

g 4

H

alok

inet

ic lo

ws

1bS

trat

ified

mar

ine

Lake water surface

≈10s-100s m

Pre-drawdownsea level

Brine surface

Basinwide evaporites

≈10s-100s m

sea level

sea level

Progradingdelta/platform

≈10s-100s m

salt allochthon

sea level

Marine-hypersaline across a restricted,in part evaporitic, arid platform

Deep basinwidemarine sediments

Open sea

Brine≈10s-100s m

≈10s-100s m Upwelling(Nutrient-rich)

Shelf edge algal bloom

Phosphoria style

Kimmeridge style

Messinian style

Intraplatform depressions

Restricted shallow epeiric seaway,at times evaporitic

≈10 mHanifa-Arab style

Green River style

Gulf of Mexico style

(Quaternary analogues)

(Quaternary analogues)

Fig. 20. Dominant depositional styles for evaporitic source rocks (dark green).All thewater bodies showevidence of salinity-related density stratification (indicated by dashed line); this is also reflected in an associated heliothermic stratification(after Warren, 2006).

374 J. K. Warren

basin centre. Bottom waters in this deeper part ofthe basin were never drawndown or concentratedto salinities where basinwide salts precipitated.Matrices in Setting 1b basin-centre laminites rangefrom limestones through marls to siliciclastics(Fig. 20).

Basin Setting (1a) In this setting the basin islargely isolated from a surface marine connectionand high levels of organics accumulate as “blackshales” (typically carbonate laminites), which areintercalated with, and overlain by, basinwide eva-porite salts (typically gypsum/halite). These lami-nites accumulate on the bottom of mesohalinedensity-stratified pools in topographically closedparts of the basin floor during the early stagesof isolation and drawdown. Inactive, typicallysubaerial, shelf margin reefs and pinnacles typi-cally lay updip or encircled the basin-centre lows(Warren, 2006). Subsequent encasement of theseplatform buildups and other potential reservoirsby “fill and spill” evaporites means these basinseasily become highly focused hydrocarbon flowsystems. Hydrocarbons accumulate in the reefsor shelf margin shoals beneath basinwide evapor-ite seals. Such systems typify themarine-fed Silur-ian reef/salina salt association in the MichiganBasin, USA (Gardner & Bray, 1984), the DevonianRainbow Reef reservoirs of the Black Creek/Musk-eg Basin of Alberta (Clark & Philp, 1989), and theMessinianmarls of the Lorca Basin, Spain (Russellet al., 1997).

Expulsion efficiencies suffer from encasementand widespread salt plugging of the potentialsource rocks in many evaporite-rich Setting 1abasins. This style of deposit tends to retain vola-tiles in the source beds until the whole systembecomes overmature. For example, in the GibsonDome No. 1 well in the Paradox Basin, almost allof the black shales in the Upper CarboniferousParadox Member are mature enough to have gen-erated oil (Hite et al., 1984), but the hydrocarbonshave been largely retained in this mature sourcerock, reflecting the highly efficient sealing effectof the intercalated evaporite beds and salt plugs(mostly halite). Only where the black shales areintercalated with porous carbonates have thehydrocarbons escaped. The source potential ofthese shales is very high; the “Gothic shale” mem-ber is capable of generating almost 5000 barrels peracre. But that potential is nevermore than partiallyrealized. Paradox “shales” are responsible foran accumulative production of a little more than

400 million barrels of oil and about 1 TCF of gas inthe Paradox Basin in fields such as Ismay andAneth (Peterson & Hite, 1969).

Theproblemof evaporitepluggingplaguesmanybasinal source rocks where the basin centreevolved to accumulate basinwide evaporates, andis one of the main reasons for the dearth of largeonshore oilfields beneath bedded salt or withinintrasalt carbonates in the Zechstein Basin ofNW Europe. Organic-rich source intervals suchas the Stinkdolomit, Stink-kalk, and Stinkscheiferare widespread, but the associated oil accumula-tions are never more than localized and are smallscale. This setting also created the salt-encasedself-sourced low-permeability reservoirs in theCambrian Ara Group platform carbonate stringersand basin centre silicilytes of the South OmanSalt Basin (Al-Siyabi, 2005; Amthor et al., 2005;Schoenherr et al., 2007, 2009). Very rich organicsource beds can characterize Setting 1a sediments,but the intercalated seals prevent most of the vola-tiles from ever escaping into a reservoir. Some-times, as in the silicilytes of Oman, the source bedscan become self-reservoiring. In later burial diag-enesis the trapped hydrocarbons can play animportant role as a reductant and metal fixer asongoing burial dissolution of salt interbeds focuseslong-term contact with basinal waters carryingCu, Pb and Zn (Warren, 2000).

Basin Setting 1b Basin-centre mesohaline accu-mulations in this setting are much more efficientpetroleum producers than Setting 1a as they lackintercalated beds of basinwide gypsum or halite,which otherwise create salt-plugged and salt-cemented source intervals. Setting 1b source rocksdevelop where dense mesohaline bottom-waterspond on the bottom of a deep density-stratifiedrestricted-marine basins. Slightly elevated bottom-brine salinities are maintained by a series of densebrine underflows, fed from nearby shoalwater eva-poritic platforms (Fig. 20). Such basins are typifiedby a deep-water “marine” centre and the presenceof widespread evaporitic and shoal water carbo-nate sediments in the surrounding platforms andshelves. Setting 1b basins are best thought of asstunted or underdeveloped basinwide evaporitesystems. Development of the basinwide evaporitehydrology was suspended prior to the basincentre drawdown reaching the state of sea-surface(hydrographic) isolation, which is needed forwidespread salt precipitation across the basin cen-tre. Nonetheless, evaporitic conditions dominated


in isolated platform depressions about the basinmargin. Typical examples of this style of associa-tion are the Upper Jurassic Kimmeridge shales ofthe North Sea (Miller, 1990; Cooper et al., 1995),the organic-rich laminites of the Cherry CanyonFormation in the Permian Delaware Basin of WestTexas (Jones, 1984), and possibly the JurassicLower Smackover Formation in the Proto-Gulf ofMexico (Sassen, 1990).

In Setting 1b, the deep-water basin centreremains “sediment starved” and density-stratified,with the upper less-saline part of thewater columntypified by normal marine water, maintainedthrough surface connections to the open ocean.The little sediment matrix that does accumulatein the basin centre settles into an anoxic thermally/density stratified bottom, so that the sedimentmatrix of the source laminites is dominated by aplanktonic or nektonic biota and a more or lessconstant elevated organic content. Carbonatebanks or reefs in the surrounding platform gradelandward through lagoonal and evaporitic plat-form facies into terrestrial siliciclastics. At timesof slightly lowered sea-level these epeiric plat-forms can go evaporitic and so deposit widespreadplatform salts (Warren, 2006). Such basins show acentrifugal salinity gradient where the highestsalinity areas are the shallow evaporite platforms,which supply dense saline waters that trickle andseep basinward to pond in seafloor lows at theanoxic base of a density-stratified water column.

With Setting 1b, the formation of evaporites andsaline waters about the basin edge is not typicallyfollowed by the deposition of basin-centre evapor-ites. At the time the deep-water organic laminitesare accumulating, the deep basin-centre waters lieat the bottom of the thick density-stratified watercolumn in a semi-enclosed seaway, and bottombrinesmay be nomore than 3–5‰more saline thanthe normalmarinewaters. For example, at the timethe Upper Jurassic Purbeck evaporites were accu-mulating on the platforms of northern Europe, theanoxic bottom waters in the marine basin centrewhere theKimmeridge Claywas accumulating hadsalinities around 42‰, temperatures �30�C anddensities �1.027. The overlying near-normalmarine waters had salinities of 34–39‰, surfacetemperatures of 26�C in the south and as low as 6�Cfarther north in the region of the Boreal Oceaninflow, and densities around 1.0267 (Miller, 1990).As the Kimmeridge Clay source rocks accumu-lated, halokinesis and salt solution of Zechsteinmother salt probably also played a role in

generating local briny anoxic bottoms on the dee-per parts of the basin floor (Clark et al., 1999).

Basin Setting 2

Upper Jurassic source rocks of the Middle East arewell-studied examples of the epeiric shelf or mar-ine evaporitic platform settings and typify Setting2a source rocks, which are deposited within localsomewhat deeper, density-stratified mesohalineintrashelf lows (Figs 19, 20 and 21; Table 5; Ayreset al., 1982; Evans & Kirkland, 1988; Droste, 1990;Warren, 2006). In the Tethyan of the Middle Eastthis style of source rock feeds a petroleum systemthat is probably the most efficient in the world.It evolved from Upper Jurassic source rock accu-mulators (typically with TOC’s�1%, occasionallyup to 13%) into evaporitic mudflats sealing themostly bioclastic carbonate reservoirs of the ArabFormation cycles, into the regional HithAnhydriteseal, which was deposited on a saltern-coveredplatform.

The laminite source rocks in the various intra-shelf depressions were deposited at times of wide-spread epeiric carbonate deposition and stagnantoceanic circulation. It was a time when a warmshallow greenhouse sea covered much of the Ara-bian platform and was precipitating carbonatesand evaporites over much of its extent. Denserwarmer waters, generated by evaporation of theseepeiric waters, along with waters supplied by thesurrounding evaporitic mudflats, were concen-trated to where they were somewhat more salinethan normal seawater. These dense brines thentrickled and seeped over the shallow seafloorinto the lower parts of restricted intrashelf basinsto create density-stratified bottom waters thatwere not more than tens of metres deep and nomore than 10–30‰ more saline than seawater(Ayres et al., 1982). Ongoing mixing and dilutionof the bottom-hugging brines during their passageto the lows meant that the basal waters on theintrashelf lows, although saline, rarely attainedgypsum saturation (mostly mesohaline anoxicbrines). The overlying column was typically atnear-normal marine salinities. Salt withdrawaland dissolution of salt diapirs and allochthons,sourced in the Precambrian Hormuz salt, perhapshelped create the intrashelf depressions and mayalso have played a role in generating a portion ofthe bottom brines.

One of the most prolific intrashelf source rocksin the Middle East is the Upper Jurassic Hanifa

376 J. K. Warren

Formation deposited in the intrashelf ArabianBasin of Saudi Arabia (Fig. 21; Droste, 1990; Car-rigan et al., 1995). It sources most of the hydro-carbons reservoired in the Arab cycles of SaudiArabia and is regionally sealed by the Hith Anhy-drite. The organic-rich portions of the Hanifaand its equivalents elsewhere in the Middle Eastwere deposited in the “deeper” parts of a numberof Jurassic intrashelf basins (waters �30m deep).Sediments accumulating beneath the slightly

mesohaline layered bottom waters are composedof organic-rich laminite muds and marls, whilesediments of the surrounding Arabian shelf aredominated by grainstones and packstones. As thevarious intrashelf depressions filled with lami-nites they shallowed to where the stratificationwas lost and the sediment became an open-marine packstone-wackestone equivalent to sedi-ments deposited over the rest of the ArabianPlatform.

100 0 100GR (API)

6200

ft

WBasin centre

0 GR (API)

Juba

ilaH

anifa

For

mat

ion

Tuw

aiq

6300

ft

5450

ft

EBasin margin

Juba

ilaH

anifa

Tuw

aiqPeak source

rock development

Peak source rock development

10 ft

5 m

SWQatar

MarginHanifa intraplatform

basin centre Margin

NEArabian Gulf

Arabian Basin

Organic-rich lime mud/wackestones

Bioturbated lime mud to peloidal packstones

Anhydrite (some with gypsum ghosts)

Dolomite of NE basin margin

Grainstones of Tuwaiq Formation

Hardground

30 m

100 km

Fig. 21. Correlation and lithofacies of the Upper Jurassic Hanifa Formation, Saudi Arabia. This Setting 2 intraplatform basinsource rockwasdepositedbeneath relatively shallowandanoxicmesohaline bottomwaters in a slight depressionon the shelfand 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).


Successive platform isolation, via buildups ofa transgressive platform rim and a slight fall insea level, then drove deposition of anhydritic salt-ern or mudflat caps of the various Arab cycles(Cycles A–D; Warren, 2006). Within the Hanifalaminites, there are discrete laminae and thin bedsof primary anhydrite, as well as early diageneticanhydrite nodules, both indicators of periodichypersalinity even as the laminites were accumu-lating. Likewise, the evaporitic cap to each of thesource cycles in the Hanifa Formation in theArabian Basin preserves aligned gypsum ghostsindicating a subaqueous gypsum precursor. Simi-lar, but volumetrically less prolific, intrashelfsource rocks characterize the Lower SmackoverFormation (Upper Jurassic) of the northeasternGulf of Mexico (Oehler, 1984; Sassen, 1990) andthe Cretaceous Sunniland Formation of Florida(Palacas et al., 1984).

A variation on this density-stratifiedmesohalineplatform-depression style of source rock accumu-lation is the phosphate and organic-rich Setting 2bsource rocks sediment of the Phosphoria Forma-tion in the USA (Stephens & Carroll, 1999). Thisunit sources much of the oil in Wyoming and wasdeposited in somewhat-saline shelf-edge depres-sions of the Phosphoria Sea adjacent to an area ofmarine upwelling. The nutrient-rich waters facili-tated algal blooms near and above the shelf edge,while bottom-hugging brines, seeping seawardfrom the evaporitic hinterland, ponded in stagnantshelf-edge depressions.Overlap of the two systemscreated local anoxic bottom-waters in the shelf-edgedepressions thatpreserved theorganics fedbythe detritus of the overlying algal blooms (Fig. 20).

Basin Setting 3

These source rocks accumulated in sediment-starved or underfilled saline lakes in arid climates.The laminites typically accumulated in the earlycontinental stage of infill in an opening rift, prior toits opening into a marine-fed marginal evaporitebasin (Figs 19 and 20), or in the restricted lacus-trine stage of a foreland flexure in a collision belt.Modern underfilled saline rift lakes have some ofthe highest rates of organic productivity knownand can accumulate high levels of organics withincarbonate laminites. Someof these lacustrine lami-nites accumulate beneath deep density-stratifiedwater columns, while others accumulate as “moatfacies” or microbial mudflats around lake margins(Fig. 20; Table 5).

The likelihood of numerous water level changesduring the life of a saline lake especially affectslaminites deposited in shoal-watermoats andmar-gin mudflats and so can lower their preservationpotential (Bohacs et al., 2000). Most oil-proneSetting 3 lacustrine source rocks were depositedat the bottom of perennial salinity-stratified hydro-logies, with water column depths measured inmetres to tens ofmetres, not as subaerially exposedalgalmudflats. Examples include theWilkins PeakMember of the Eocene Green River Formation,USA, the Lower Cretaceous Lagoa Feia Formationof the Alagoas portion of the Campos Basin inBrazil, and the Permian Jingjingzigou Formationin the Junggar Basin, China (Table 5).

Desiccation needed to form an underfilled lacus-trine succession typically means that saline lacus-trine phases have lesser aerial extents comparedto units deposited at times of fresher water in thelake depression. This does not necessarily meanthe evaporitic lacustrine source rocks are less pro-lific than their freshwater counterparts.Within theGreen River Formation there are two associations(fresh and saline) of lacustrine organic laminitesexemplified by the Luman Tongue and the LaneyMember (Fig. 22;Horsfield et al., 1994).TheLumanTongue consists of organic matter-rich mudstonesdeposited as profundal sediments at a time whenlake waters were relatively fresh (Fig. 22A). Prox-imal organic matter-poor sediments, as well ascoals and thin sandstones, were deposited on thelake plain. The highest levels of TOC in the LumanTongue occur in lake-margin deposits, which con-tain a mixture of alginite and vitrinite, but theyhave a low hydrogen index and a low petroleumgeneration potential (Fig. 22B, C). In fact, the pet-roleum generation potential of these freshwaterdeposits is no more than moderate.

In contrast, the organic percentages of the carbo-nate laminites of the evaporitic Laney Shale aremuch higher (6–22%) and these are hydrogenprone (Fig. 22B, C). Themost organic-rich sampleswere deposited in the lowest parts of the lake andare composed mostly of alginite with relativelyminor contributions from higher plants. Themuchhigher petroleum potential of the Laney Shalereflects the marked density stratification of LakeGosiute waters at the time the Laney was accumu-lating. At that time bottom anoxia was stabilizedby the perennial highly saline bottom waters(Boyer, 1982; Fischer & Roberts, 1991). The dis-solution of underlying evaporites to createdensity-stratified lacustine waters also characterized the

378 J. K. Warren

Cretaceous Purbeck strata of Dorset, although inthis case the underlying evaporites were marineand the depositional setting was akin to the sea-margin meteoric lakes of today’s Coorong region ofAustralia (Schnyder et al., 2009).

Basin Setting 4

This is an increasingly documented open-marineevaporite-associated source rock setting wheredensity-stratified saline bottom brines and

1000

800

600

400

200

0

Hyd

roge

n In

dex

(mg

HC

g-1

TO

C)

Oxygen Index (mg CO2 g-1 TOC)

0 40 80 120 160 200

I

II

III

S2

rock

(m

g g-

1 )200

100

020100

TOC (wt %)

B

C

A

Laney Member (evaporitic)

Luman Tongue (deltaic)

Luman Tongue(vitrinite-rich)

Wilkins Peak Member

Laney Member

Green RiverBasin

Rock SpringsUplift

WashakieBasin

UpperEocene

MiddleEocene

250 km

fresh

saline

evaporitic

saline

fresh

Lakechemistry

2500 m

West East

Luman Tongue

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


organic-enriched laminites accumulate in brine-bottomed depressions on top of and adjacent toshallow and dissolving salt allochthons (Fig. 20).With burial these laminites may act as sourcerocks, but unlike the restricted settings of the pre-ceding three styles, deposition typically occurs inopen-marine waters in continental slope and riseenvironments. The laminites accumulate on thefloor of deep brine pools that form on or nearthe margins of actively flowing and dissolvingshallow salt allochthons (Warren, 2006). This isalso a significant setting for the formation of basemetal-hosting laminites as in Tunisia and theRed Sea (Warren, 2000). As yet it is not a widelydocumented environment for hydrocarbon sourcerocks, but it may in-part explain the higher thanexpected source potential of many prodelta andslope muds in the passive margin fill of evaporite-floored halokinetic rifts.

Source rocks of settings 1a, 2 and 3 are typifiedby the accumulation of mm-scale layers of oil-prone organics typically in a matrix of fine carbo-nates. Setting 1b typically contains higher levels ofsiliciclastic fines and in many cases the host to theorganics is a basinal marl or less often a laminatedcalcareous shale. The matrix of Setting 4 laminitestends to be composed of whatever detrital sedi-ment is accumulating above the salt allochthon.In many situations, such as the Gulf of Mexicoand the Mediterranean allochthon terranes, thismatrix is a siliciclastic mud/clay laid down at thedistal ends of prodelta wedges. In others, such asthe Jurassic and Cretaceous of the ArabianGulf and the Triassic of Tunisia, the matrix iscarbonate.

CONCLUSION

It seems that there are no same-scale “famine orfeast” analogues for modern and ancient salinelacustrine settings (Table 6, Setting 3). Organic-rich carbonate laminites forming in the African riftvalley lakes have been documented and similar-scale counterparts exist in the Mesozoic sourcerocks found for example in the Cabinda Basin ofAngola and the lacustrine basins of South America(Table 5). Likewise,Quaternary examples of supra-allochthon brine lakes with anoxic bottoms richin organics are now being documented (Table 6,Setting 3).

However, there are no modern counterparts formost ancient large-scale marine evaporite

depressions with mesohaline “famine or feast”laminites (Table 6, settings 1 and 2). These Pre-Quaternary evaporitic source rocks generated fargreater hydrocarbon volumes than all lacustrinesource rocks combined, yetmany source rockmod-els for evaporitic mesohaline carbonates still drawstrong comparisons to underfilled Quaternarylacustrine settings. Such “strict” uniformitariancomparisons lead to the conclusion that evaporiticmesohaline source sources areprobably not all thatsignificant as contributors to the volume of exploi-table hydrocarbons in the world.

It is the author’s opinion that depositional set-tings in arid environments are still being consid-ered in the same way that Lotze (1957) viewedthe abundance of life in modern deserts. Organicaccumulations in ancient evaporitic source rocksshould be seen as biological responses to the “feastor famine” cycles that still characterize life in ariddepositional settings. Formation of ancient mar-ine-fed mesohaline depressions required varyingcombinations of greenhouse eustacy (epeiric sea-ways) and tectonics-climate, which are alsoneeded to create huge sub-sea-level depressionsfillingwithevaporites (epeiricplatformevaporites,marine-seepage rifts, soft collision belts and far-field intracratonic sags). These systems do nothave same-scaleQuaternary counterparts (Warren,2010). Yet, it was in salinity-layered intraplatformepeiric depressions and restricted tectonicallyinducedmesohaline basin centreswhere the requi-site schizohaline water columns and stable long-term brine bottoms occurred. They did so acrosstime scales and across areas that not only allowedwidespread periodic halotolerant blooms in thesurface waters of whole mesohaline-floored sea-ways, but also formed in settings that facilitatedlong-term stable anoxic bottom brines. This anoxicbrine-soaked bottom in-turn allowed widespreadmesohaline source rocks to accumulate and to bepreserved across the areally-extensive depressions(Figs 19 and 20; Table 5).

As for most ancient evaporite styles, the presentis not a suitable time for studying scales of marinemesohaline source rock development. However,process and texture relevant to these ancientmesohaline source rocks can be seen in “famineor feast” cycles in small-scale Quaternary conti-nental deposits. Rather than the words ofLotze (1957), a more apt aphorism to describe lifein modern and ancient saline systems is found inthe words of John Morley, a 19th Century Scottishstatesman (1838–1923), agnostic, and the First

380 J. K. Warren

Table

6.Summary

ofevaporiticsourcerockassociations

Setting

Othersignificant

characteristics

Someancientexamples

Quaternary

counterparts

Tectonic/eustatic

associations

Setting1.Basin-centre

lowsin

marine-fed

evaporiticdrawdown

basins,

typicallywith

evaporite

platform

rim

1a.Drawndownevaporite-

sealedandplugged

mesohalinebasincentre

carbonates

CambrianAra

stringerandsilicilytes,

Oman;Silurianreef/SalinaSalt,

MichiganBasin,USA;Devonian

Rainbow

Fm

oftheBlackCreek/

MuskegBasin,Canada;Perm

ian

StinkdolomitZechstein

Basin,

Europe;CarboniferousGothic

Shales,

ParadoxBasin,USA;

Messinianmarls,

LorcaBasin,

Spain

None

Rifts,collisionbeltsand

intracratonic

sagswith

complete

hydrographic

isolationofmarine-

seepagebasincentre

1b.Density-stratified

restricted-m

arine

slightly-m

esohaline

basincentreswithno

immediately

overlying

evaporite

seal

Perm

ianCherryCanyonFm,

Delaware

Basin,USA:Jurassic

Kim

meridgesh

ales,

NorthSea;

Jurassic

EgretMember,Jeanne

d’A

rcBasin,offsh

ore

Canada;

CretaceousSirte

Shale,Sirte

Basin,

Libya

Partial

Oftentiedto

earlyopening

stagesofriftsin

semiarid

climaticsettingsin

greenhouse

climate

mode.Someasp

ects

of

RedSea/G

ulfofSuezare

similar,buthigharidity

andicehouse

eustacydo

notallow

adirect

comparison

Setting2.Mesohaline

intrash

elflowswithin

anepeiric

evaporitic

platform

2a.Intraplatform

lows

withadjacentepeiric

mesohalinesh

oals

HanifaForm

ationin

theintrash

elf

ArabianBasin,S

audiArabia

andits

equivalents

throughouttheMiddle

East;LowerSmackoverForm

ation

(UpperJurassic)ofthenortheastern

GulfofMexico;Cretaceous

SunnilandForm

ationofFlorida

None

Greenhouse

eustacycreates

continuoussh

elf-or

ramp-edgerim,the

dissolutionofthecrestsof

nearbyactivehalokinetic

structuresmaycontribute

brinesto

theseafloorlows

2b.Platform

edgelow

with

epeiric

mesohaline

hinterland

1b:Phosp

horiaFm,USA

None

Greenhouse

eustacycreates

continuoussh

elf-or

ramp-edgerim

Setting3.Mesohaline-

uppercolumnin

perennialsaline

lacustrinebasins.

Underfilledstages

alternatingwithbalanced

fillstagesin

resp

onse

totectonic/climaticchanges

Perm

ianJingjingzigouForm

ationin

theJunggarBasin,China:Eocene

GreenRiverForm

ation,USA;

CretaceousLagoaFeia

Form

ation,

CamposBasinin

Brazil;Tertiary

salinelacustrinebasins,

China

East

AfricanRift

Valleylakes;

LakeVan,

Turkey;Lake

Urm

ia,Iran

Enhoheic

basinsin

riftor

continent-continent

collisionsettings

Setting4.Closed

mesohaline-bottomed

deepseafloor

depressionsin

halokineticbelts

Brineseepsthatcreate

the

stratifiedbrinelakesare

tiedto

ongoingsalt

dissolutionandsh

allow

subseafloorsaltflows

Possible

explanationforthe

enhancedsourcepotentialof

marinedeep-w

atersh

alesin

variouscircum-A

tlantic

halokineticbasins

Poorlydocumented

stratifiedbrine

lakesin

suprasalt

allochthon

provinces

Halokineticprovincesin

the

deepwaters

ofthepassive

margin

slopeandrise

of

theGulfofMexicoand

theMediterraneanRidge

collisionbelt

SeeFig.20.


Viscount of Blackburn, who once said: “The greatbusiness of life is to be, to do, to do without, andto depart.”

GLOSSARY

Aerobes are organisms that can survive andgrow inan oxygenated environment.

Aliphatic hydrocarbons are any chemical com-pound belonging to the organic class in which theatoms are not linked together to form a ring. Theyare divided into three main groups according tothe types of bonds they contain: alkanes, alkenes,and alkynes. Alkanes (n-alkanes) have only singlebonds and a continuous chain structure, alkenescontain a carbon-carbon double bond, and alkynescontain a carbon-carbon triple bond. Aromatichydrocarbons are classified as either arenes, whichcontain a benzene ring as a structural unit, or non-benzenoid aromatic hydrocarbons,which are char-acterized by stability in burial but lack a benzenering as a structural unit.

Anaerobes are organisms that do not require oxy-gen for growth and may even die in its presence.Obligate (or strict) anaerobes are unable to live ineven low oxygen concentrations. Facultative anae-robes are able to live in low or even normal oxygenconcentration as well. All anaerobes are simplemicroorganisms such as bacteria, archaea andsome fungi. Archaea are usually strict anaerobes.

Autotrophs (literally “self-feeders”) are organismscapable of producing organic compounds fromsimple inorganic compounds.

Basinwide evaporites are one of the two majorstyles of ancient marine-fed salt accumulationsknown as: (1) marine-fed basinwides and (2) mar-ine-fed platform evaporites. Neither setting isactive anywhere on the world’s current landsur-face. Basinwide salt fills tend be thick (>100m)and relatively pure with deposits accumulatingrapidly across time frames of less than one millionyears. Basinwide evaporites are most likely toaccumulate on the floors of isolated sub-sea-leveldepressions at times of close proximity of driftinglandmasses (Warren 2006, 2008, 2010).

Catabolism is the breakdown in livingorganismsofmore complex substances into simpler onestogether with a release of energy.

Cellulolytic bacteria decompose cellulose; proteo-lytic bacteria breakdown proteins into simpler,soluble substances such as peptides and aminoacids; saccharolytic bacteria breakdown sugars,while homoacetogens are obligately anaerobic bac-teria that make acetate from either (H2 þ CO2) orfrom the fermentation of sugars.

Chemoautotrophs use endogenous light-indepen-dent reactions to obtain energy, these reactionsinvolve inorganicmolecules and an electrondonorother than water and do not release oxygen.

Cyanobacterial toxins. Intoxication of lesser fla-mingo flocks by cyanobacterial toxins, and some-times even mass fatalities have occurred in nearbyLake Bogoria when the birds ingest detachedcyanobacterial cells from cyanobacterial matsflourishing in the vicinity of hot springs (Krienitzet al., 2003). This is because the flamingos feedingat night on plankton blooms in a saline lakes needtodrink freshorbrackishwater after feeding, and towash their feathers daily. They tend to do this inwaters in the vicinity of the hot springs, wheresalinities are lower than in the main waterbody ofthe lakewhere they have been feeding.Mycosystinheptatoxins can characterize the benthicmicrobialcommunity in those hot spring mats and waterscan be dominated by the potentially toxic cyano-bacterial association of Phormidium terebriformis,Oscillatoria willei, Spirulina subsalsa and Syne-chococcus bigranulatus.

Denitrification is the microbial process by whichnitrates are removed from an aqueous liquid.

Dissimilatory metabolic processes drive the con-version of food or other nutrients into productsplus energy-containing compounds.

Dissimilatory sulphate reduction. Sulphate-redu-cing bacteria gain energy for cell synthesis andgrowth by coupling the oxidation of organic com-pounds or molecular hydrogen to the reduction ofsulphate to sulphide (H2S, HS�). This process iscalled “dissimilatory sulphate reduction”, to allowclear differentiation from assimilatory sulphatereduction. Assimilatory sulphate reduction gener-ates reduced sulphur for biosynthesis (e.g. ofcysteine). It is a widespread biochemical capacityin prokaryotes and plants and does not lead to theexcretion of sulphide. Only upon decay (putrefac-tion) of the biomass is the assimilated reducedsulphur released as sulphide.

382 J. K. Warren

Endosymbionts are organisms that live within thebody or cells of another organism without deleter-ious effects.

Extremophiles are organisms that thrive in extremeconditions including: extremely saline (halo-phile), extremely hot (thermophile), extremely dry(xerophile), extremely acid (acidophile), extre-mely alkaline (alkaliphile), and extremely cold(psychrophile) environments.

Fermentation is of a series of anaerobic transforma-tion processes whereby organic matter is brokendown into compounds of smaller size, which aremore reduced or more oxidized and eventuallymore assimilatable by livingmatter. When fermen-tation leads to organic acids and a lowering of pH,it is called acidogenesis. The microorganismsresponsible for this are called acidogens.

Gram-negative and Gram-positive are responses totheGramstaining techniquewherebymicro-organ-isms are first stained with crystal violet,then treated with an iodine solution, decolourizedwith alcohol, and counterstained with safranine.Gram-positive bacteria retain the violet stain;Gram-negative bacteria do not.

“Halobacteria”. Prior to hybridization studies andgenomemapping, classificationwas based onmor-phology and staining, the evolutionary relation-ships among various members of the bacterial andarchaeal domains were contradictory and poorlydefined. Today some of these contradictions andconfusions remain in microbial taxonomy of thegroup of microbial organisms broadly known ashalobacteria, as distinct from the archaeal groupHalobacteriales.

Halophilic organisms thrive at very high saltconcentrationsandcanbekilledbylowersalinities.

Halotolerant (aka halovariant) organisms can tol-erate high salt concentrations but grow better atsomewhat lower salinities.

Haloxene organisms cannot tolerate high concen-trations of salts.

Heterotrophs (literally “feeders on others”) useorganic molecules synthesized outside their bodyas a source of energy and carbon.

Holomixis indicates the entire mixing of the watercolumn.Meromixis indicatespartial or incompletemixing.

Hopanoids are group of compounds (triterpenoids)produced by prokaryotic organisms, and the diage-netic alterationproducts of these compounds (foundin oils, rock extracts and sediment extracts). Just assteroids (steranes) are a useful group of biomarkersfor identifying input from various eukaryotic organ-isms (e.g. plants andanimals), an analogous groupofcompounds, hopanoids, are a useful group of bio-markers for identifying input from various bacteria.Hopanoids serve the same function in bacteria assterols do in eukaryotes: they act as cell wall rigidi-fiers. In petroleum and their source rocks, hopanoidbiomarkers exist asa subset of a groupof compoundscalled triterpanes (isoprenoids).

Hypersaline encompasses all waters more salinethan seawater (mesohaline, penesaline andsupersaline).

Hypertrophicationdescribes thepresence of exces-sive nutrients in a water body.

Isoprenoids are a major class of nonsaponifiablelipids that occur in plants, animals, and bacteriaand are characterized by chains of modular groupsof five carbon atoms in which the typical patternhas four of the carbon atoms in a linear chain and asingle carbon attached at the carbon one positionremoved from the end of the chain. The termisoprenoid is derived from the name of the five-carbon, doubly unsaturated branched hydrocar-bon isoprene, which could in principle be thesimplest monomeric chemical precursor for thisclass of compounds. Isoprenoids are also known asterpenes. Terpenes are usually grouped accordingto the number of isoprene (C5H8) units in themolecule: monoterpenes (C10H16) contain twosuch units; sesquiterpenes (C15H24), three; diter-penes (C20H32), four; triterpenes (C30H48), six; andtetraterpenes (C40H64), eight. The carotenoid pig-ments are the best known tetraterpenes.

Lithotrophs are organisms that use an inorganicsubstrate (usually of mineral origin) to obtainreducing equivalents for use in biosynthesis (e.g.carbon dioxide fixation) or energy conservation viaaerobic or anaerobic respiration.

Meromixis indicates partial or incomplete mixing.The term meromictic is used to describe a perma-nently stratified water mass where surface layersmay mix, but the bottom layer does not. Manymodern brine lakes are meromictic, the upperwater mass comes and goes.


Mesophiles are organisms that grow best in mod-erate temperatures, neither too hot nor too cold,typically between 15 and 40 �C.

Mixolimnion. An upper water mass that periodi-cally mixes is the mixolimnion, it sits atop themonolimnion.

Monolimnion. A lower, permanent unmixedwatermass.

Neutrophilic organisms are not stained strongly ordefinitely by either acid or basic dyes, but arestained readily by neutral dyes.

Oligomictic or oligotrophic is used to describestratified water masses that mix or homogenize forshort irregular periods every few years.

Photoautotrophsuse light as a source of energy andCO2 as a source of carbon. Term comes from auto-trophs (literally “self-feeders”), which describesorganisms capable of producing organic com-pounds from simple inorganic compounds.

Photophosphorylation is the production of ATPusing the energy of sunlight.

Platform evaporites are the other major type ofancientmarine-fed evaporite. They formed on con-tinentalmargins throughoutmuchmore of Phaner-ozoic time than basinwides. Salt fills are 10–50mthick, mostly CaSO4 and typically interbeddedwith normal-restrictedmarine carbonates. Stackedplatform sections characterised by this style ofaccumulation encompass time frames of �1–10Myr and are largely tied to times in earth historywhen climate was in greenhouse mode and theassociated eustacy favoured widespread epiconti-nental seaways subject to periodic restriction(Warren, 2006, 2010).

Red waters and brines. The pink to purple coloursthat typify many hypersaline water bodies comemostly from concentrations of carotenoid pig-ments present in the cytoplasm of various haloto-lerant and halophilic microorganisms. Mosthaloarchaea are red due to a high content of C-50carotenoids of the bacterioruberin series. Photo-synthetic cyanobacteria and eukaryotes (e.g.unicellular green algae of the genus Dunaliella)contribute to the pigmentation of the hypersalinewaters thanks to the presence of chlorophyllsand C-40 carotenoids (mostly all-trans- and 9-cis-b-carotene). Chlorophylls absorb red and bluewavelengths much more strongly than they absorb

green wavelengths, which is why chlorophyll-bearing cyanobacteria appear green (Fig. 2B). Thecarotenoids and phycobiliproteins, on the otherhand, strongly absorb green wavelengths. Algaeand microbes with large amounts of carotenoidappear yellow to brown (such as carotene-richforms of Dunaliella sp.), those microbes with largeamounts of phycocyanin appear blue, and thosewith large amounts of phycoerythrin appear red.Pigment levels can indicate the stratification ofthe microbial community in any photoresponsivebiomass in a brine column. Red wavelengths (longwavelengths) are absorbed in the first few metresof a brine column or the uppermost millimetre ortwo of amicrobialmat (where chlorophyll utilizersflourish). Blue and green wavelengths (shorter)reach deeper into the brine column or into thesediment.

Saprophytes obtain nourishment by absorbing dis-solved organic material; especially from the pro-ducts of organic breakdown and decay.

Schizohaline describes waters subject to substan-tial ongoing salinity changes and periodically passfrom brackish to hypersaline.

Third domain of life. In the late 1970s, ProfessorCarl Woese proposed, on the basis of ribosomalRNA affiliations (gene mapping), that life bedivided into three domains instead of two,namely; Eukaryota, Eubacteria, and Archaebac-teria (Woese, 1993). He later decided that the termArchaebacteria was a misnomer, and shortened itto Archaea and Eubacteria to Bacteria. Since the1970s, DNA base-pair studies (aka genomic stu-dies or gene sequencing) have shown thatArchaeaare as different from Bacteria as from Homosapiens. This new approach to taxonomy is stillworking its way through the scientific communityand some books and articles still ocassionallyrefer to archaea as types of bacteria. Prior to geno-mic studies, and based on their morphology andstaining response, the archaeal Halobacteriaceaewere grouped with the bacterial Gram-negativerods (a gram positive or gram negative descriptionindicates whether or not the bacterial cell wallreacts with Gram’s stain).

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