Biogeosciences 8 3331ndash3340 2011wwwbiogeosciencesnet833312011doi105194bg-8-3331-2011copy Author(s) 2011 CC Attribution 30 License

Biogeosciences

First discovery of dolomite and magnesite in living coralline algaeand its geobiological implications

M C Nash1 U Troitzsch1 B N Opdyke1 J M Trafford 2 B D Russell3 and D I Kline4

1Research School of Earth Sciences The Australian National University Acton ACT 0200 Australia2Geoscience Australia GPO Box 378 Canberra ACT 2601 Australia3Southern Seas Ecology Laboratories School of Earth amp Environmental Sciences University of Adelaide AdelaideSouth Australia 5005 Australia4Scripps Institution of Oceanography University of California San Diego La Jolla California 92093 USA andCoral Reef Ecosystems Laboratory School of Biological Sciences University of Queensland Brisbane QLD 4072 Australia

Received 24 May 2011 ndash Published in Biogeosciences Discuss 27 June 2011Revised 7 November 2011 ndash Accepted 7 November 2011 ndash Published 15 November 2011

Abstract Dolomite is a magnesium-rich carbonate min-eral abundant in fossil carbonate reef platforms but surpris-ingly rare in modern sedimentary environments a conun-drum known as the ldquoDolomite Problemrdquo Marine sedimen-tary dolomite has been interpreted to form by an uncon-firmed post-depositional diagenetic process despite mini-mal experimental success at replicating this Here we showthat dolomite accompanied by magnesite forms within liv-ing crustose coralline algaHydrolithon onkodes a prolificglobal tropical reef species Chemical micro-analysis of thecoralline skeleton reveals that not only are the cell walls cal-citised but that cell spaces are typically filled with magne-site rimmed by dolomite or both Mineralogy was con-firmed by X-ray Diffraction Thus there are at least threemineral phases present (magnesium calcite dolomite andmagnesite) rather than one or two (magnesium calcite andbrucite) as previously thought Our results are consistentwith dolomite occurrences in coralline algae rich environ-ments in fossil reefs of the last 60 million years We re-veal that the standard method of removing organic materialprior to Xray Diffraction analysis can result in a decrease inthe most obvious dolomite and magnesite diffraction patternsand this may explain why the abundant protodolomite andmagnesite discovered in this study has not previously beenrecognized This discovery of dolomite in living corallinealgae extends the range of palaeo-environments for whichbiologically initiated dolomite can be considered a possiblesource of primary dolomite

Correspondence toM C Nash(merindanashanueduau)

1 Introduction

11 Background on the ldquoDolomite Problemrdquo

The ldquoDolomite Problemrdquo has been of interest to geologistsand carbonate chemists for more than a century and relatesto the mystery surrounding the abundant presence of the min-eral dolomite [Ca05Mg05CO3] in fossil reefs (eg Daito-jima) and carbonate platform sediments (eg the Dolomites)and its apparent absence from equivalent modern reef envi-ronments (eg Ohde and Kitano 1981 McKenzie and Vas-concelos 2009 Budd 1997) Many geochemical modelsand environmental reconstructions (eg Griffith et al 2008Bao et al 2009) incorporate dolomitisation as a parametereven though the exact process has not been identified

12 Background on coralline algae

Coralline algae are calcifying red algae and are major reefbuilders occurring globally (Adey and Macintyre 1973)While modern corallines have only been confirmed back tothe Cretaceous (Aguirre et al 2000) calcifying red algaehave a long history in the geologic record back through thePaleozoic (Brooke and Riding 1998 Aguirre et al 2000)and red algae possibly existed as far back as the Neoprotero-zoic (Xiao et al 2004) and Mesoproterozoic (Butterfield2000) Modern corallines have a high magnesium calcite(Mg-calcite) skeleton typically ranging from 10ndash20 mol MgCO3 (Moberly 1970 Chave 1952 1954 Milliman etal 1971) (mol MgCO3 is of magnesium substitutingfor calcium) although there is some degree of uncertaintyaround these measurements as results vary depending on themethod used (Milliman et al 1971 Chave 1954) This highmagnesium calcite is meta-stable and prone to dissolution as

Published by Copernicus Publications on behalf of the European Geosciences Union

3332 M C Nash et al First discovery of dolomite and magnesite in coralline algae

pH declines (Morse et al 2006) While modern coralline al-gae are composed of Mg-calcite it has been shown that theincorporation of magnesium as measured in the cell walldecreases with declining magnesiumcalcium (MgCa) ratioof the ambient seawater (Ries 2006 Stanley et al 2002)and in low MgCa ratios equalling the Cretaceous calciteseas (11) coralline algae are able to continue growing albeitwith a low Mg-calcite skeleton Hogbom (1894) carried outsimple leaching experiments and found that by acid treatingsome coralline samples the mol of Mg actually increasedHe hypothesised the corallines had a crucial role in the for-mation of dolomite Researchers in the late 19th and early20th century proposed coralline algae contained dolomite aspart of the magnesium enriched calcite skeleton but were un-able to prove this hypothesis (Chave 1954) Later researchidentified magnesium enriched skeletal portions approachingdolomite composition however the presence of dolomite wasnot confirmed (Moberly 1970)

The importance of reef building coralline algae was firstrecorded in 1904 (Howe 1912) from cores taken down to360 m at Funafuti The organisms were grouped in or-der of their reef-building importance and coralline algaewas first followed byHalimeda foraminifera and coralslast Hydrolithon onkodes(Heydrich) Penrose and Woelk-ering (1992) has a key role in building and maintaining thereef edge places and this makes it among the most eco-logically important of the tropical crustose coralline algae(Littler and Doty 1975) H onkodescan dominate shal-low reef frontcrest coralline assemblages (Littler and Doty1975 Rasser and Piller 1997 Matsuda 1989) and some-times comprises 100 of species coverage (Littler and Doty1975)H onkodescan grow prolifically in the right environ-mental conditions and out-compete other calcifying algaeWhile Honkodesis prolific in tropical environments it hasalso been found in warm and cold temperate environmentsand distribution does not seem limited by temperature (Har-vey et al 2006) however the formation of thick crusts hasonly been recorded on tropical reefs (Littler and Doty 1975)The Atlantic-CaribbeanH pachydermum(then PorolithonPachydermum) is very similar to and considered perhapsonly a variety ofH onkodes(Adey and Macintyre 1973)H onkodeswas previously classified asPorolithon onkodesand has recently been reclassified asPorolithon (Kato etal 2011) however we useHydrolithon onkodesas it is thenomenclature that is presently in widespread use

Here we present evidence that dolomite and magnesite(MgCO3) form inside crusts of living coralline algae and thusmust be influenced if not caused by biological processesThe intimate association between dolomite and coralline al-gae suggested by our findings is consistent with the predom-inant occurrence of sedimentary dolomite in fossil carbonatereef environments (McKenzie and Vasconcelos 2009 Budd1997 Ohde and Kitano 1981) typically in calcifying redalgae facies (Saller 1984 Schlanger 1957 Budd 1997McKenzie and Vasconcelos 2009 Ohde and Kitano 1981)

2 Materials and methods

21 Sample collection and preparation

Samples of living crustose coralline algae were collected un-der permit G09299961 from between 3ndash5 m depth belowmean low tide along a 150 m transect on the north reef frontof Heron Island (transect headed east from 23433285 S151929648 E) southern Great Barrier Reef in December2009 Temperature was 261C and salinity 345 measuredusing an Orion hand held meter Photosynthetic activity wasconfirmed using a pulse amplitude modulated (PAM) fluo-rometer (Russell et al 2009) Samples were 2 mmndash10 mmthick not subjected to any chemical cleaning process andwere sun-driedH onkodeswere identified in SEM-EDS byanatomy of reproductive conceptacles and thallus contain-ing horizontal rows of trichocytes (Ringeltaube and Harvey2000)

22 Xray diffraction

Powder X-ray diffraction was carried out with a SIEMENSD501 Bragg-Brentano diffractometer equipped with agraphite monochromator and scintillation detector usingCuKα radiation Samples were milled by hand in acetonein an agate mortar some with fluorite added as an internalstandard and suspended on quartz-low background holdersScan range was 2 to 70 2theta step size 002 2theta andscan speeds varied from 1min to 7min The results wereinterpreted using the SIEMENS software package Diffrac-plus Eva 10 with ICDD database PDF-2 for identificationand RIETICA (Hunter 1998) for modelling Parameters re-fined in the Rietveld modelling using a Pseudo-Voigt func-tion included six background parameters zero correctionscale parameters of all phases (calcite dolomite magnesitearagonite) up to three peak shape parameters per phase apreferred orientation parameter for calcite and unit cell pa-rameters of calcite and magnesite Two different calcite com-positions were refined (175 mol and 24 mol ) as theybest account for peak asymmetry The Mg-content of cal-cite was calculated from the (104) peak position (Goldsmithet al 1955) Precision of measurements wasplusmn 025 mol Fifteen samples were analysed and 4 sub-samples All sam-ples were taken as a bulk slice down the sample

221 Scanning electron microscopy-energy dispersivespectroscopy (SEM-EDS) and inductively coupledplasma ndash atomic emission spectroscopy(ICP-AES)

The SEM-EDS was carried out using a Hitachi 4300 SEequipped with an integrated Oxford X-Max element detec-tor operated at 150 kV 25 mm working distance current06 nano ampere beam width and penetration approximately3 microm Measurement precision wasplusmn 005 mol Sampleswere cut with a rock saw and embedded in resin polished

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3333

and carbon coated and held in with carbon tape one sam-ple was coated with Platinum for one session When con-ducting the SEM-EDS a measurement was taken of the resinsurrounding the sample This enabled us to identify when asample measurement included resin and these measurementswere discarded The extent to which the resin infiltrated thethallus was impossible to be quantified however measure-ments returning a resin signature were infrequent and resininfill was not considered problematic ICP-AES was car-ried out using a Varian Vista Pro Axial CCD simultaneousICP-AES power 130 kW plasma flow 150 L minminus1 auxil-iary flow 150 L minminus1 nebulizer flow 070 L minminus1 repli-cate read time 500 s instrument stabilisation delay 15 s and5 replicates AccuTrace reference standards were used 3 mgof sample was digested in 10 ml of 10 nitric acid A checkstandard was run every third analysis Relative standard devi-ation of mol MgCO3 is less than 02 Thirteen sampleswere analysed

3 Results

For our results we use the term ldquoprotodolomiterdquo a descrip-tion commonly used for sedimentary dolomite that does notexhibit the XRD reflections associated with ordered dolomite(eg Ohde and Kitano 1981)

31 SEM-EDS

We found substantial amounts of protodolomite and mag-nesite within the Mg-calcite skeleton of the coralline al-gaeH onkodes(Fig 1) A detailed analysis using SEM-EDS reveals that protodolomite is pervasively present withinthe honeycomb-like cell wall structure as rims surroundingcell spaces that are in-filled to various degrees by magne-site SEM spot analyses (Supplement Table 1) show that theprotodolomite rims (2ndash4 microm thickness) range in compositionfrom 38ndash62 mol MgCO3 (n = 37) thus exceeding previ-ously reported protodolomite ranges of 38ndash50 mol MgCO3(Budd 1997) Cell walls have 8ndash25 mol MgCO3 (n = 57)Cells (5ndash15 microm) are partially filled by magnesite with 95ndash995 mol MgCO3 (n = 18) Concentric zonations are ap-parent around some cells extending into the cell wall andcould reflect organic material or varying magnesium con-tents however as the SEM-EDS weight results were gen-erally higher than the organic rich cell spaces and there wereno voids associated with these bands we consider it unlikelythese zonations are organic matter and therefore a varyingmagnesium content is the probable explanation An SEMcross section of a reproductive conceptacle (Fig 2) showslarger scale dolomite and magnesite in-fill It seems the dis-tribution of magnesite within the conceptacle is constrainedby the precursor organic fabric While mostly it is magne-site that in-fills the cell spaces dolomite also in-fills somecell spaces There are some small areas that do not conform

Fig 1 SEM backscattered electron (BSE) image of coralline alga(sample 302) showing detail of magnesite cell infill(a) (b) andprotodolomite rims(e) within Mg-calcite cell wall structure(d)Black lines and textures within the cells are most likely voidsor remnant organic structures Above(d) micron scale bands ofslightly darker grey within the cell walls indicate varying magne-sium within the cell wall Concentric zonation is seen around cells(top left) SEM-EDS spot analyses of labeled sites(a) = 9922(b) = 9919(c) = 239 (d) = 1517(e) = 4575 mol MgCO3Scale bar = 5 microm Cell wall structure (Mg-calcite 8ndash25 mol MgCO3) protodolomite (38ndash62 mol MgCO3) magnesite(95ndash9955 mol MgCO3) void

to the typical structure and may represent a second uniden-tified species (Fig 1 and 2 Supplement I) Most strikingabout these textural features (and Figs 3 4) is the similar-ity to those observed in Cenozoic island dolomites (Budd1997 Land 1973 Ward and Halley 1985) which showpronounced dolomite rims concentric zonation inclusionswithin cells and vuggy textures (Ward and Halley 1985)

Although the time frame over which dolomitisation of sed-imentary carbonates takes place has not been precisely iden-tified it is generally thought to form over time scales of up tomillions of years (Saller 1984) We note that while the cellsin the top photosynthetically active layers of the coralline al-gae are mostly void of mineral in-fill (Fig 5) small amounts

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3334 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 2 SEM BSE image of coralline alga (sample 302) showinginfilled cells within cell wall structure (top) and a large concep-tacle (bottom) that is filled with magnesite(a) and protodolomite(b) (c) SEM-EDS spot analyses of conceptacle mineralisation(a) = 9955(b) = 5975(c) = 6167 mol MgCO3 Original con-ceptacle fabric is ingrown by cells now dolomitised cell shapes arevisible in dolomitic areas Magnesite in-fill may be correlated withprecursor organic content Cells are either completely filled withprotodolomite(d) rimmed by protodolomite and filled to variousdegrees by magnesite(e) or filled by only magnesite(f) From theseimages it appears that dolomitisation spreads out from the cells intothe cell wall(g) Cell void of mineral in-fill(h) Increased dolomi-tisation can be seen at the top of the figure compared to the baseThese areas of dominance of one mineral phase over another ap-pear in patches throughout the section Scale bar = 40 micro Legendsee Fig 1

of magnesite in-fill were observed (Fig 3 Supplement I)Protodolomite rims occur within 1 mm of these top layersThere is a noticeable though not always consistent increasein the amount of magnesite and protodolomite down sampletowards the base of the crust (Fig 6) Thus in contrast toexisting theories protodolomite and magnesite precipitationare contemporaneous with organism growth

32 XRD

The presence of protodolomite and magnesite was confirmedwith XRD analyses (Fig 7) The XRD pattern is dominatedby peaks of the Mg-calcite of the cell walls These peaksare unusually asymmetrical and have high shoulders towardshigher 2-theta angles (towards smaller unit cell sizes) over-lapping with the wide peaks of protodolomite and magnesitesee for example peak C (104) In order to resolve these peaksprofile fitting with the Rietveld method was carried out Ri-etveld refinement using Mg-calcite as the only phase resultedin significant misfits in the areas of protodolomite and mag-nesite (Rp = 1253 Rwp = 1850) (Fig 7b) In contrast tothis Rietveld refinement including dolomite and magnesitein addition to Mg-calcite results in a good fit (Rp = 596

Fig 3 SEM BSE (SE) image of aragonite-bearing coralline al-gae (Sample 302) showing the typical fabric of protodolomite rimsaround cells that are partially to completely filled with magnesiteWhite rims at the top(f) are aragonite Textures within cells mayrepresent organic material or mineralisation that was constrainedby the organic fabric Concentric zonations are seen within the cellwall material SEM-EDS spot analyses of labeled sites(a) = 1132(b) = 1388(c) = 9844(d) = 9916 mol MgCO3 (e) = hole(f) = 067 (Strontium = 169 wt indicative of aragonite) Scalebar = 20 microm Legend see Fig 1

Rwp = 811) demonstrating that dolomite and magnesite arepresent in the sample (Fig 7c) The significant width of thedolomite XRD maxima suggests that the dolomite is veryfinely grained and not well crystallized probably disordered(Zhang 2010) and possibly bordering on an amorphouscrystal structure thus not diffracting X-rays well Moreoverfrom the SEM analyses we know that this protodolomite hasa range of compositions and thus unit cell dimensions alsocontributing to peak width This made refinement of the unitcell impossible and it was fixed to stoichiometric dolomiteThe refined magnesite unit cell dimensions area = 4678(1)A and c = 15192(1) and thus about 1 larger than idealmagnesite which is typical for sedimentary magnesite (Grafet al 1961)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3335

Fig 4 SEM BSE image of coralline alga section (sample 47) takenwith increased contrast to visualize the concentric zonations causedby different compositions of Mg-calcite in the cell wall Black rep-resents magnesite or void grey is protodolomite and white to light-grey is Mg-calcite (a) protodolomite rim 5065 mol MgCO3(b) protodolomite rim 5529 mol MgCO3 Black rims around aand b are not void and assumed to be magnesite but are too narrowfor accurate spot analysis Scale bar = 10 microm

Fig 5 SEM Secondary Electron image of coralline alga (sample47) showing varying amounts of mineralisation in the top pho-tosynthetically active layer and underlying crust White indicatesspace void of mineral in-fill grey is mineralised cell walls and in-filled cells black is epoxy resin Whilst the top layer clearly has lessin-fill it does contain some magnesite cell in-fill close to surfaceProtodolomite is noticeably least present in the top layer comparedto basal layers Scale bar = 200 microm

The typically very broad protodolomite (Zhang 2010)and magnesite (Graf et al 1961) reflections were observedin 10 out of 19 samples as a continuous shoulder on the

Fig 6 SEM (SE) images showing the difference in cell in-fill be-tween the top layers and the lower layers of a coralline alga (sam-ple 47) White indicates void of mineral in-fill (caused by chargebuild-up in sample) and shades of dark grey are in-fill Top imagetaken at base of photosynthetically active layer 05 mm from top ofsample showing that most cells are empty of mineral in-fill Scalebar = 25 microm Bottom image taken at 4 mm depth showing abundantcell mineral in-fill There was a general although patchy trend forincreasing cell in-fill towards the base

(104) calcite peak sometimes ending in a distinct magne-site maximum The remaining 9 samples displayed a strongasymmetry of the calcite peak towards higher 2-theta angles(Fig 8) While such an asymmetry is generally interpreted torepresent Mg-calcite that is more Mg-rich than the average(Milliman et al 1971) we note that it could also representprotodolomite Ca-Mg disorder in the dolomite structure in-creases the unit cell size (Zhang 2010) thus shifting the XRDpeaks of Mg-calcite and protodolomite even closer togetherso that the peak range for protodolomite with compositionsof 38ndash50 mol MgCO3 (Zhang 2010) actually sits in thesame peak range as 30ndash37 mol MgCO3 calcite calculatedusing a standard Mg-calcite correlation curve (Goldsmith etal 1955) Indeed when investigating one of the samplesH56 with such asymmetry using SEM-EDS similarly to themagnesite rich samples no clear compositions in the range28ndash36 mol MgCO3 were found however protodolomite

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3336 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 7 (a) Powder X-ray diffraction pattern of coralline algaeshowing the main peaks of protodolomite (D) magnesite (M) andMg-calcite (C)(b) Rietveld refinement using Mg-calcite as the onlyphase To account for peak asymmetry two calcite compositionswere refined (175 and 24 mol MgCO3) (c) Rietveld refinementincluding dolomite and magnesite in addition to calcite

composition of 38ndash40 mol MgCO3 was measured (Sup-plement Table 2) suggesting that its presence contributes tothe calcite peak asymmetry in this case Most of the cell in-fill in H56 was by Mg-calcite 16ndash27 mol MgCO3 H56appeared to contain multiple genera and identification tothe species level was not possible However it seemed thatbothHydrolithonsp andLithophyllumsp were likely to bepresent This opens up the possibility that previous stud-

Fig 8 Powder X-ray diffraction patterns of coralline algae demon-strating how the presence of protodolomite and magnesite manifestsitself in XRD analyses In examples(a) (b) and(c) the calcite 104reflection has a broad shoulder towards higher angles 2-theta in-dicative of the presence of significant amounts of protodolomite andmagnesite This is consistent with the high Mg-contents of thesesamples (2617ndash3333 mol Mg by ICP-AES) In(d) (e) and(f)the calcite 104 reflection has no significant shoulder but displays astrong asymmetry that is typical for biogenic Mg-rich calcite (Mil-liman et al 1971) This could mask the presence of protodolomiteFor easier viewing reflections are labelled in selected scans onlyMg-rich calcite (C) dolomite (D) magnesite (M) fluorite (F) arag-onite (A) halite (H)

ies noting similar peak asymmetry for other tropical species(Milliman et al 1971) may have overlooked the presence ofprotodolomite when basing their findings solely on XRD re-sults without the advantage of recent research on disordereddolomite cell size (Zhang 2010) Aragonite was identifiedby XRD in 12 of the 19 samples (Supplement Table 3) andis seen as rims in Fig 3 As SEM was not done on all thesamples it is not known whether all aragonite is present asrims or may be remnants of coral overgrown by the corallinealgae

Applying the standard method of calculating the aver-age Mg-calcite composition based on peak position (Gold-smith et al 1955) the samples with dolomite and magnesitepeaks returned a composition of 1745 mol MgCO3 (Sup-plement Table 3) and the remaining samples an average of1678 mol MgCO3

Using ICP-AES to measure bulk magnesium concentra-tion results ranged from 2260 to 3370 mol MgCO3 (Sup-plement Table 3) significantly higher than those returned byXRD reflecting the presence of the protodolomite and mag-nesium phases This discrepancy has been well recognized inprevious research (Chave 1954) where it was attributed to ei-ther Mg-calcite with up to 30 mol MgCO3 problems withthe peak modeling curve (Chave 1954) or to the presence ofamorphous brucite [Mg(OH)2] (Milliman et al 1971)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3333

and carbon coated and held in with carbon tape one sam-ple was coated with Platinum for one session When con-ducting the SEM-EDS a measurement was taken of the resinsurrounding the sample This enabled us to identify when asample measurement included resin and these measurementswere discarded The extent to which the resin infiltrated thethallus was impossible to be quantified however measure-ments returning a resin signature were infrequent and resininfill was not considered problematic ICP-AES was car-ried out using a Varian Vista Pro Axial CCD simultaneousICP-AES power 130 kW plasma flow 150 L minminus1 auxil-iary flow 150 L minminus1 nebulizer flow 070 L minminus1 repli-cate read time 500 s instrument stabilisation delay 15 s and5 replicates AccuTrace reference standards were used 3 mgof sample was digested in 10 ml of 10 nitric acid A checkstandard was run every third analysis Relative standard devi-ation of mol MgCO3 is less than 02 Thirteen sampleswere analysed

3 Results

For our results we use the term ldquoprotodolomiterdquo a descrip-tion commonly used for sedimentary dolomite that does notexhibit the XRD reflections associated with ordered dolomite(eg Ohde and Kitano 1981)

31 SEM-EDS

We found substantial amounts of protodolomite and mag-nesite within the Mg-calcite skeleton of the coralline al-gaeH onkodes(Fig 1) A detailed analysis using SEM-EDS reveals that protodolomite is pervasively present withinthe honeycomb-like cell wall structure as rims surroundingcell spaces that are in-filled to various degrees by magne-site SEM spot analyses (Supplement Table 1) show that theprotodolomite rims (2ndash4 microm thickness) range in compositionfrom 38ndash62 mol MgCO3 (n = 37) thus exceeding previ-ously reported protodolomite ranges of 38ndash50 mol MgCO3(Budd 1997) Cell walls have 8ndash25 mol MgCO3 (n = 57)Cells (5ndash15 microm) are partially filled by magnesite with 95ndash995 mol MgCO3 (n = 18) Concentric zonations are ap-parent around some cells extending into the cell wall andcould reflect organic material or varying magnesium con-tents however as the SEM-EDS weight results were gen-erally higher than the organic rich cell spaces and there wereno voids associated with these bands we consider it unlikelythese zonations are organic matter and therefore a varyingmagnesium content is the probable explanation An SEMcross section of a reproductive conceptacle (Fig 2) showslarger scale dolomite and magnesite in-fill It seems the dis-tribution of magnesite within the conceptacle is constrainedby the precursor organic fabric While mostly it is magne-site that in-fills the cell spaces dolomite also in-fills somecell spaces There are some small areas that do not conform

Fig 1 SEM backscattered electron (BSE) image of coralline alga(sample 302) showing detail of magnesite cell infill(a) (b) andprotodolomite rims(e) within Mg-calcite cell wall structure(d)Black lines and textures within the cells are most likely voidsor remnant organic structures Above(d) micron scale bands ofslightly darker grey within the cell walls indicate varying magne-sium within the cell wall Concentric zonation is seen around cells(top left) SEM-EDS spot analyses of labeled sites(a) = 9922(b) = 9919(c) = 239 (d) = 1517(e) = 4575 mol MgCO3Scale bar = 5 microm Cell wall structure (Mg-calcite 8ndash25 mol MgCO3) protodolomite (38ndash62 mol MgCO3) magnesite(95ndash9955 mol MgCO3) void

to the typical structure and may represent a second uniden-tified species (Fig 1 and 2 Supplement I) Most strikingabout these textural features (and Figs 3 4) is the similar-ity to those observed in Cenozoic island dolomites (Budd1997 Land 1973 Ward and Halley 1985) which showpronounced dolomite rims concentric zonation inclusionswithin cells and vuggy textures (Ward and Halley 1985)

Although the time frame over which dolomitisation of sed-imentary carbonates takes place has not been precisely iden-tified it is generally thought to form over time scales of up tomillions of years (Saller 1984) We note that while the cellsin the top photosynthetically active layers of the coralline al-gae are mostly void of mineral in-fill (Fig 5) small amounts

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3334 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 2 SEM BSE image of coralline alga (sample 302) showinginfilled cells within cell wall structure (top) and a large concep-tacle (bottom) that is filled with magnesite(a) and protodolomite(b) (c) SEM-EDS spot analyses of conceptacle mineralisation(a) = 9955(b) = 5975(c) = 6167 mol MgCO3 Original con-ceptacle fabric is ingrown by cells now dolomitised cell shapes arevisible in dolomitic areas Magnesite in-fill may be correlated withprecursor organic content Cells are either completely filled withprotodolomite(d) rimmed by protodolomite and filled to variousdegrees by magnesite(e) or filled by only magnesite(f) From theseimages it appears that dolomitisation spreads out from the cells intothe cell wall(g) Cell void of mineral in-fill(h) Increased dolomi-tisation can be seen at the top of the figure compared to the baseThese areas of dominance of one mineral phase over another ap-pear in patches throughout the section Scale bar = 40 micro Legendsee Fig 1

of magnesite in-fill were observed (Fig 3 Supplement I)Protodolomite rims occur within 1 mm of these top layersThere is a noticeable though not always consistent increasein the amount of magnesite and protodolomite down sampletowards the base of the crust (Fig 6) Thus in contrast toexisting theories protodolomite and magnesite precipitationare contemporaneous with organism growth

32 XRD

The presence of protodolomite and magnesite was confirmedwith XRD analyses (Fig 7) The XRD pattern is dominatedby peaks of the Mg-calcite of the cell walls These peaksare unusually asymmetrical and have high shoulders towardshigher 2-theta angles (towards smaller unit cell sizes) over-lapping with the wide peaks of protodolomite and magnesitesee for example peak C (104) In order to resolve these peaksprofile fitting with the Rietveld method was carried out Ri-etveld refinement using Mg-calcite as the only phase resultedin significant misfits in the areas of protodolomite and mag-nesite (Rp = 1253 Rwp = 1850) (Fig 7b) In contrast tothis Rietveld refinement including dolomite and magnesitein addition to Mg-calcite results in a good fit (Rp = 596

Fig 3 SEM BSE (SE) image of aragonite-bearing coralline al-gae (Sample 302) showing the typical fabric of protodolomite rimsaround cells that are partially to completely filled with magnesiteWhite rims at the top(f) are aragonite Textures within cells mayrepresent organic material or mineralisation that was constrainedby the organic fabric Concentric zonations are seen within the cellwall material SEM-EDS spot analyses of labeled sites(a) = 1132(b) = 1388(c) = 9844(d) = 9916 mol MgCO3 (e) = hole(f) = 067 (Strontium = 169 wt indicative of aragonite) Scalebar = 20 microm Legend see Fig 1

Rwp = 811) demonstrating that dolomite and magnesite arepresent in the sample (Fig 7c) The significant width of thedolomite XRD maxima suggests that the dolomite is veryfinely grained and not well crystallized probably disordered(Zhang 2010) and possibly bordering on an amorphouscrystal structure thus not diffracting X-rays well Moreoverfrom the SEM analyses we know that this protodolomite hasa range of compositions and thus unit cell dimensions alsocontributing to peak width This made refinement of the unitcell impossible and it was fixed to stoichiometric dolomiteThe refined magnesite unit cell dimensions area = 4678(1)A and c = 15192(1) and thus about 1 larger than idealmagnesite which is typical for sedimentary magnesite (Grafet al 1961)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3335

Fig 4 SEM BSE image of coralline alga section (sample 47) takenwith increased contrast to visualize the concentric zonations causedby different compositions of Mg-calcite in the cell wall Black rep-resents magnesite or void grey is protodolomite and white to light-grey is Mg-calcite (a) protodolomite rim 5065 mol MgCO3(b) protodolomite rim 5529 mol MgCO3 Black rims around aand b are not void and assumed to be magnesite but are too narrowfor accurate spot analysis Scale bar = 10 microm

Fig 5 SEM Secondary Electron image of coralline alga (sample47) showing varying amounts of mineralisation in the top pho-tosynthetically active layer and underlying crust White indicatesspace void of mineral in-fill grey is mineralised cell walls and in-filled cells black is epoxy resin Whilst the top layer clearly has lessin-fill it does contain some magnesite cell in-fill close to surfaceProtodolomite is noticeably least present in the top layer comparedto basal layers Scale bar = 200 microm

The typically very broad protodolomite (Zhang 2010)and magnesite (Graf et al 1961) reflections were observedin 10 out of 19 samples as a continuous shoulder on the

Fig 6 SEM (SE) images showing the difference in cell in-fill be-tween the top layers and the lower layers of a coralline alga (sam-ple 47) White indicates void of mineral in-fill (caused by chargebuild-up in sample) and shades of dark grey are in-fill Top imagetaken at base of photosynthetically active layer 05 mm from top ofsample showing that most cells are empty of mineral in-fill Scalebar = 25 microm Bottom image taken at 4 mm depth showing abundantcell mineral in-fill There was a general although patchy trend forincreasing cell in-fill towards the base

(104) calcite peak sometimes ending in a distinct magne-site maximum The remaining 9 samples displayed a strongasymmetry of the calcite peak towards higher 2-theta angles(Fig 8) While such an asymmetry is generally interpreted torepresent Mg-calcite that is more Mg-rich than the average(Milliman et al 1971) we note that it could also representprotodolomite Ca-Mg disorder in the dolomite structure in-creases the unit cell size (Zhang 2010) thus shifting the XRDpeaks of Mg-calcite and protodolomite even closer togetherso that the peak range for protodolomite with compositionsof 38ndash50 mol MgCO3 (Zhang 2010) actually sits in thesame peak range as 30ndash37 mol MgCO3 calcite calculatedusing a standard Mg-calcite correlation curve (Goldsmith etal 1955) Indeed when investigating one of the samplesH56 with such asymmetry using SEM-EDS similarly to themagnesite rich samples no clear compositions in the range28ndash36 mol MgCO3 were found however protodolomite

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3336 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 7 (a) Powder X-ray diffraction pattern of coralline algaeshowing the main peaks of protodolomite (D) magnesite (M) andMg-calcite (C)(b) Rietveld refinement using Mg-calcite as the onlyphase To account for peak asymmetry two calcite compositionswere refined (175 and 24 mol MgCO3) (c) Rietveld refinementincluding dolomite and magnesite in addition to calcite

composition of 38ndash40 mol MgCO3 was measured (Sup-plement Table 2) suggesting that its presence contributes tothe calcite peak asymmetry in this case Most of the cell in-fill in H56 was by Mg-calcite 16ndash27 mol MgCO3 H56appeared to contain multiple genera and identification tothe species level was not possible However it seemed thatbothHydrolithonsp andLithophyllumsp were likely to bepresent This opens up the possibility that previous stud-

Fig 8 Powder X-ray diffraction patterns of coralline algae demon-strating how the presence of protodolomite and magnesite manifestsitself in XRD analyses In examples(a) (b) and(c) the calcite 104reflection has a broad shoulder towards higher angles 2-theta in-dicative of the presence of significant amounts of protodolomite andmagnesite This is consistent with the high Mg-contents of thesesamples (2617ndash3333 mol Mg by ICP-AES) In(d) (e) and(f)the calcite 104 reflection has no significant shoulder but displays astrong asymmetry that is typical for biogenic Mg-rich calcite (Mil-liman et al 1971) This could mask the presence of protodolomiteFor easier viewing reflections are labelled in selected scans onlyMg-rich calcite (C) dolomite (D) magnesite (M) fluorite (F) arag-onite (A) halite (H)

ies noting similar peak asymmetry for other tropical species(Milliman et al 1971) may have overlooked the presence ofprotodolomite when basing their findings solely on XRD re-sults without the advantage of recent research on disordereddolomite cell size (Zhang 2010) Aragonite was identifiedby XRD in 12 of the 19 samples (Supplement Table 3) andis seen as rims in Fig 3 As SEM was not done on all thesamples it is not known whether all aragonite is present asrims or may be remnants of coral overgrown by the corallinealgae

Applying the standard method of calculating the aver-age Mg-calcite composition based on peak position (Gold-smith et al 1955) the samples with dolomite and magnesitepeaks returned a composition of 1745 mol MgCO3 (Sup-plement Table 3) and the remaining samples an average of1678 mol MgCO3

Using ICP-AES to measure bulk magnesium concentra-tion results ranged from 2260 to 3370 mol MgCO3 (Sup-plement Table 3) significantly higher than those returned byXRD reflecting the presence of the protodolomite and mag-nesium phases This discrepancy has been well recognized inprevious research (Chave 1954) where it was attributed to ei-ther Mg-calcite with up to 30 mol MgCO3 problems withthe peak modeling curve (Chave 1954) or to the presence ofamorphous brucite [Mg(OH)2] (Milliman et al 1971)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3334 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 2 SEM BSE image of coralline alga (sample 302) showinginfilled cells within cell wall structure (top) and a large concep-tacle (bottom) that is filled with magnesite(a) and protodolomite(b) (c) SEM-EDS spot analyses of conceptacle mineralisation(a) = 9955(b) = 5975(c) = 6167 mol MgCO3 Original con-ceptacle fabric is ingrown by cells now dolomitised cell shapes arevisible in dolomitic areas Magnesite in-fill may be correlated withprecursor organic content Cells are either completely filled withprotodolomite(d) rimmed by protodolomite and filled to variousdegrees by magnesite(e) or filled by only magnesite(f) From theseimages it appears that dolomitisation spreads out from the cells intothe cell wall(g) Cell void of mineral in-fill(h) Increased dolomi-tisation can be seen at the top of the figure compared to the baseThese areas of dominance of one mineral phase over another ap-pear in patches throughout the section Scale bar = 40 micro Legendsee Fig 1

of magnesite in-fill were observed (Fig 3 Supplement I)Protodolomite rims occur within 1 mm of these top layersThere is a noticeable though not always consistent increasein the amount of magnesite and protodolomite down sampletowards the base of the crust (Fig 6) Thus in contrast toexisting theories protodolomite and magnesite precipitationare contemporaneous with organism growth

32 XRD

The presence of protodolomite and magnesite was confirmedwith XRD analyses (Fig 7) The XRD pattern is dominatedby peaks of the Mg-calcite of the cell walls These peaksare unusually asymmetrical and have high shoulders towardshigher 2-theta angles (towards smaller unit cell sizes) over-lapping with the wide peaks of protodolomite and magnesitesee for example peak C (104) In order to resolve these peaksprofile fitting with the Rietveld method was carried out Ri-etveld refinement using Mg-calcite as the only phase resultedin significant misfits in the areas of protodolomite and mag-nesite (Rp = 1253 Rwp = 1850) (Fig 7b) In contrast tothis Rietveld refinement including dolomite and magnesitein addition to Mg-calcite results in a good fit (Rp = 596

Fig 3 SEM BSE (SE) image of aragonite-bearing coralline al-gae (Sample 302) showing the typical fabric of protodolomite rimsaround cells that are partially to completely filled with magnesiteWhite rims at the top(f) are aragonite Textures within cells mayrepresent organic material or mineralisation that was constrainedby the organic fabric Concentric zonations are seen within the cellwall material SEM-EDS spot analyses of labeled sites(a) = 1132(b) = 1388(c) = 9844(d) = 9916 mol MgCO3 (e) = hole(f) = 067 (Strontium = 169 wt indicative of aragonite) Scalebar = 20 microm Legend see Fig 1

Rwp = 811) demonstrating that dolomite and magnesite arepresent in the sample (Fig 7c) The significant width of thedolomite XRD maxima suggests that the dolomite is veryfinely grained and not well crystallized probably disordered(Zhang 2010) and possibly bordering on an amorphouscrystal structure thus not diffracting X-rays well Moreoverfrom the SEM analyses we know that this protodolomite hasa range of compositions and thus unit cell dimensions alsocontributing to peak width This made refinement of the unitcell impossible and it was fixed to stoichiometric dolomiteThe refined magnesite unit cell dimensions area = 4678(1)A and c = 15192(1) and thus about 1 larger than idealmagnesite which is typical for sedimentary magnesite (Grafet al 1961)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3335

Fig 4 SEM BSE image of coralline alga section (sample 47) takenwith increased contrast to visualize the concentric zonations causedby different compositions of Mg-calcite in the cell wall Black rep-resents magnesite or void grey is protodolomite and white to light-grey is Mg-calcite (a) protodolomite rim 5065 mol MgCO3(b) protodolomite rim 5529 mol MgCO3 Black rims around aand b are not void and assumed to be magnesite but are too narrowfor accurate spot analysis Scale bar = 10 microm

Fig 5 SEM Secondary Electron image of coralline alga (sample47) showing varying amounts of mineralisation in the top pho-tosynthetically active layer and underlying crust White indicatesspace void of mineral in-fill grey is mineralised cell walls and in-filled cells black is epoxy resin Whilst the top layer clearly has lessin-fill it does contain some magnesite cell in-fill close to surfaceProtodolomite is noticeably least present in the top layer comparedto basal layers Scale bar = 200 microm

The typically very broad protodolomite (Zhang 2010)and magnesite (Graf et al 1961) reflections were observedin 10 out of 19 samples as a continuous shoulder on the

Fig 6 SEM (SE) images showing the difference in cell in-fill be-tween the top layers and the lower layers of a coralline alga (sam-ple 47) White indicates void of mineral in-fill (caused by chargebuild-up in sample) and shades of dark grey are in-fill Top imagetaken at base of photosynthetically active layer 05 mm from top ofsample showing that most cells are empty of mineral in-fill Scalebar = 25 microm Bottom image taken at 4 mm depth showing abundantcell mineral in-fill There was a general although patchy trend forincreasing cell in-fill towards the base

(104) calcite peak sometimes ending in a distinct magne-site maximum The remaining 9 samples displayed a strongasymmetry of the calcite peak towards higher 2-theta angles(Fig 8) While such an asymmetry is generally interpreted torepresent Mg-calcite that is more Mg-rich than the average(Milliman et al 1971) we note that it could also representprotodolomite Ca-Mg disorder in the dolomite structure in-creases the unit cell size (Zhang 2010) thus shifting the XRDpeaks of Mg-calcite and protodolomite even closer togetherso that the peak range for protodolomite with compositionsof 38ndash50 mol MgCO3 (Zhang 2010) actually sits in thesame peak range as 30ndash37 mol MgCO3 calcite calculatedusing a standard Mg-calcite correlation curve (Goldsmith etal 1955) Indeed when investigating one of the samplesH56 with such asymmetry using SEM-EDS similarly to themagnesite rich samples no clear compositions in the range28ndash36 mol MgCO3 were found however protodolomite

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3336 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 7 (a) Powder X-ray diffraction pattern of coralline algaeshowing the main peaks of protodolomite (D) magnesite (M) andMg-calcite (C)(b) Rietveld refinement using Mg-calcite as the onlyphase To account for peak asymmetry two calcite compositionswere refined (175 and 24 mol MgCO3) (c) Rietveld refinementincluding dolomite and magnesite in addition to calcite

composition of 38ndash40 mol MgCO3 was measured (Sup-plement Table 2) suggesting that its presence contributes tothe calcite peak asymmetry in this case Most of the cell in-fill in H56 was by Mg-calcite 16ndash27 mol MgCO3 H56appeared to contain multiple genera and identification tothe species level was not possible However it seemed thatbothHydrolithonsp andLithophyllumsp were likely to bepresent This opens up the possibility that previous stud-

Fig 8 Powder X-ray diffraction patterns of coralline algae demon-strating how the presence of protodolomite and magnesite manifestsitself in XRD analyses In examples(a) (b) and(c) the calcite 104reflection has a broad shoulder towards higher angles 2-theta in-dicative of the presence of significant amounts of protodolomite andmagnesite This is consistent with the high Mg-contents of thesesamples (2617ndash3333 mol Mg by ICP-AES) In(d) (e) and(f)the calcite 104 reflection has no significant shoulder but displays astrong asymmetry that is typical for biogenic Mg-rich calcite (Mil-liman et al 1971) This could mask the presence of protodolomiteFor easier viewing reflections are labelled in selected scans onlyMg-rich calcite (C) dolomite (D) magnesite (M) fluorite (F) arag-onite (A) halite (H)

ies noting similar peak asymmetry for other tropical species(Milliman et al 1971) may have overlooked the presence ofprotodolomite when basing their findings solely on XRD re-sults without the advantage of recent research on disordereddolomite cell size (Zhang 2010) Aragonite was identifiedby XRD in 12 of the 19 samples (Supplement Table 3) andis seen as rims in Fig 3 As SEM was not done on all thesamples it is not known whether all aragonite is present asrims or may be remnants of coral overgrown by the corallinealgae

Applying the standard method of calculating the aver-age Mg-calcite composition based on peak position (Gold-smith et al 1955) the samples with dolomite and magnesitepeaks returned a composition of 1745 mol MgCO3 (Sup-plement Table 3) and the remaining samples an average of1678 mol MgCO3

Using ICP-AES to measure bulk magnesium concentra-tion results ranged from 2260 to 3370 mol MgCO3 (Sup-plement Table 3) significantly higher than those returned byXRD reflecting the presence of the protodolomite and mag-nesium phases This discrepancy has been well recognized inprevious research (Chave 1954) where it was attributed to ei-ther Mg-calcite with up to 30 mol MgCO3 problems withthe peak modeling curve (Chave 1954) or to the presence ofamorphous brucite [Mg(OH)2] (Milliman et al 1971)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3335

Fig 4 SEM BSE image of coralline alga section (sample 47) takenwith increased contrast to visualize the concentric zonations causedby different compositions of Mg-calcite in the cell wall Black rep-resents magnesite or void grey is protodolomite and white to light-grey is Mg-calcite (a) protodolomite rim 5065 mol MgCO3(b) protodolomite rim 5529 mol MgCO3 Black rims around aand b are not void and assumed to be magnesite but are too narrowfor accurate spot analysis Scale bar = 10 microm

Fig 5 SEM Secondary Electron image of coralline alga (sample47) showing varying amounts of mineralisation in the top pho-tosynthetically active layer and underlying crust White indicatesspace void of mineral in-fill grey is mineralised cell walls and in-filled cells black is epoxy resin Whilst the top layer clearly has lessin-fill it does contain some magnesite cell in-fill close to surfaceProtodolomite is noticeably least present in the top layer comparedto basal layers Scale bar = 200 microm

The typically very broad protodolomite (Zhang 2010)and magnesite (Graf et al 1961) reflections were observedin 10 out of 19 samples as a continuous shoulder on the

Fig 6 SEM (SE) images showing the difference in cell in-fill be-tween the top layers and the lower layers of a coralline alga (sam-ple 47) White indicates void of mineral in-fill (caused by chargebuild-up in sample) and shades of dark grey are in-fill Top imagetaken at base of photosynthetically active layer 05 mm from top ofsample showing that most cells are empty of mineral in-fill Scalebar = 25 microm Bottom image taken at 4 mm depth showing abundantcell mineral in-fill There was a general although patchy trend forincreasing cell in-fill towards the base

(104) calcite peak sometimes ending in a distinct magne-site maximum The remaining 9 samples displayed a strongasymmetry of the calcite peak towards higher 2-theta angles(Fig 8) While such an asymmetry is generally interpreted torepresent Mg-calcite that is more Mg-rich than the average(Milliman et al 1971) we note that it could also representprotodolomite Ca-Mg disorder in the dolomite structure in-creases the unit cell size (Zhang 2010) thus shifting the XRDpeaks of Mg-calcite and protodolomite even closer togetherso that the peak range for protodolomite with compositionsof 38ndash50 mol MgCO3 (Zhang 2010) actually sits in thesame peak range as 30ndash37 mol MgCO3 calcite calculatedusing a standard Mg-calcite correlation curve (Goldsmith etal 1955) Indeed when investigating one of the samplesH56 with such asymmetry using SEM-EDS similarly to themagnesite rich samples no clear compositions in the range28ndash36 mol MgCO3 were found however protodolomite

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3336 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 7 (a) Powder X-ray diffraction pattern of coralline algaeshowing the main peaks of protodolomite (D) magnesite (M) andMg-calcite (C)(b) Rietveld refinement using Mg-calcite as the onlyphase To account for peak asymmetry two calcite compositionswere refined (175 and 24 mol MgCO3) (c) Rietveld refinementincluding dolomite and magnesite in addition to calcite

composition of 38ndash40 mol MgCO3 was measured (Sup-plement Table 2) suggesting that its presence contributes tothe calcite peak asymmetry in this case Most of the cell in-fill in H56 was by Mg-calcite 16ndash27 mol MgCO3 H56appeared to contain multiple genera and identification tothe species level was not possible However it seemed thatbothHydrolithonsp andLithophyllumsp were likely to bepresent This opens up the possibility that previous stud-

Fig 8 Powder X-ray diffraction patterns of coralline algae demon-strating how the presence of protodolomite and magnesite manifestsitself in XRD analyses In examples(a) (b) and(c) the calcite 104reflection has a broad shoulder towards higher angles 2-theta in-dicative of the presence of significant amounts of protodolomite andmagnesite This is consistent with the high Mg-contents of thesesamples (2617ndash3333 mol Mg by ICP-AES) In(d) (e) and(f)the calcite 104 reflection has no significant shoulder but displays astrong asymmetry that is typical for biogenic Mg-rich calcite (Mil-liman et al 1971) This could mask the presence of protodolomiteFor easier viewing reflections are labelled in selected scans onlyMg-rich calcite (C) dolomite (D) magnesite (M) fluorite (F) arag-onite (A) halite (H)

ies noting similar peak asymmetry for other tropical species(Milliman et al 1971) may have overlooked the presence ofprotodolomite when basing their findings solely on XRD re-sults without the advantage of recent research on disordereddolomite cell size (Zhang 2010) Aragonite was identifiedby XRD in 12 of the 19 samples (Supplement Table 3) andis seen as rims in Fig 3 As SEM was not done on all thesamples it is not known whether all aragonite is present asrims or may be remnants of coral overgrown by the corallinealgae

Applying the standard method of calculating the aver-age Mg-calcite composition based on peak position (Gold-smith et al 1955) the samples with dolomite and magnesitepeaks returned a composition of 1745 mol MgCO3 (Sup-plement Table 3) and the remaining samples an average of1678 mol MgCO3

Using ICP-AES to measure bulk magnesium concentra-tion results ranged from 2260 to 3370 mol MgCO3 (Sup-plement Table 3) significantly higher than those returned byXRD reflecting the presence of the protodolomite and mag-nesium phases This discrepancy has been well recognized inprevious research (Chave 1954) where it was attributed to ei-ther Mg-calcite with up to 30 mol MgCO3 problems withthe peak modeling curve (Chave 1954) or to the presence ofamorphous brucite [Mg(OH)2] (Milliman et al 1971)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3336 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Fig 7 (a) Powder X-ray diffraction pattern of coralline algaeshowing the main peaks of protodolomite (D) magnesite (M) andMg-calcite (C)(b) Rietveld refinement using Mg-calcite as the onlyphase To account for peak asymmetry two calcite compositionswere refined (175 and 24 mol MgCO3) (c) Rietveld refinementincluding dolomite and magnesite in addition to calcite

composition of 38ndash40 mol MgCO3 was measured (Sup-plement Table 2) suggesting that its presence contributes tothe calcite peak asymmetry in this case Most of the cell in-fill in H56 was by Mg-calcite 16ndash27 mol MgCO3 H56appeared to contain multiple genera and identification tothe species level was not possible However it seemed thatbothHydrolithonsp andLithophyllumsp were likely to bepresent This opens up the possibility that previous stud-

Fig 8 Powder X-ray diffraction patterns of coralline algae demon-strating how the presence of protodolomite and magnesite manifestsitself in XRD analyses In examples(a) (b) and(c) the calcite 104reflection has a broad shoulder towards higher angles 2-theta in-dicative of the presence of significant amounts of protodolomite andmagnesite This is consistent with the high Mg-contents of thesesamples (2617ndash3333 mol Mg by ICP-AES) In(d) (e) and(f)the calcite 104 reflection has no significant shoulder but displays astrong asymmetry that is typical for biogenic Mg-rich calcite (Mil-liman et al 1971) This could mask the presence of protodolomiteFor easier viewing reflections are labelled in selected scans onlyMg-rich calcite (C) dolomite (D) magnesite (M) fluorite (F) arag-onite (A) halite (H)

ies noting similar peak asymmetry for other tropical species(Milliman et al 1971) may have overlooked the presence ofprotodolomite when basing their findings solely on XRD re-sults without the advantage of recent research on disordereddolomite cell size (Zhang 2010) Aragonite was identifiedby XRD in 12 of the 19 samples (Supplement Table 3) andis seen as rims in Fig 3 As SEM was not done on all thesamples it is not known whether all aragonite is present asrims or may be remnants of coral overgrown by the corallinealgae

Applying the standard method of calculating the aver-age Mg-calcite composition based on peak position (Gold-smith et al 1955) the samples with dolomite and magnesitepeaks returned a composition of 1745 mol MgCO3 (Sup-plement Table 3) and the remaining samples an average of1678 mol MgCO3

Using ICP-AES to measure bulk magnesium concentra-tion results ranged from 2260 to 3370 mol MgCO3 (Sup-plement Table 3) significantly higher than those returned byXRD reflecting the presence of the protodolomite and mag-nesium phases This discrepancy has been well recognized inprevious research (Chave 1954) where it was attributed to ei-ther Mg-calcite with up to 30 mol MgCO3 problems withthe peak modeling curve (Chave 1954) or to the presence ofamorphous brucite [Mg(OH)2] (Milliman et al 1971)

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3337

4 Discussion

41 Results compared to previous work on corallinealgae

While the composition of the cell wall structure measuredby SEM-EDS is in agreement with previous studies of trop-ical coralline algae (Stanley et al 2002 Moberly 1970) thepresence of protodolomite has not previously been confirmed(Moberly 1970) Other than a miniscule amount of magne-site composition (mineralogy not confirmed by XRD) in onecell of a fresh coralline algaHydrolithon gardineri from theMarshall Islands (Moberly 1970) we could find no previousrecord of magnesite in coralline algae Moberly (1970) iden-tified magnesium enriched cell rims (2 microm wide) and mea-sured compositions approaching dolomite yet rejected thepresence of dolomite We note however that the analyticalbeam was 6 microm wide and therefore measuring an average ofthe rim and surrounding cell walls which have 12ndash17 mol MgCO3 indicating that the rims themselves were likely tohave dolomite andor magnesite composition Moberly alsonoted the presence of cell in-fill by calcite and Mg-calcite intropical corallines

We propose that the standard method of bleaching us-ing either household bleach or peroxide prior to analysis(Bischoff 1983) may not only remove the cell organic ma-terial but also Mg-rich carbonates such as dolomite andmagnesite from within the cell space which could explainwhy their presence in coralline algae has not been discov-ered earlier This proposition is supported by two argu-ments Firstly bleaching has been noted in the past to re-duce the bulk magnesium content of samples (Milliman etal 1971) A decrease in magnesium equivalent to a fallfrom 29 mol MgCO3 to 25 mol MgCO3 was measuredfor a Hydrolithonsp Secondly we conducted bleaching ex-periments on eight samples comparing their XRD traces be-fore and after treatment whereby four samples displayedsignificant changes in the main carbonate peak (104) shape(Fig 9) two showed no change and two were inconclusiveWhile the calcite peak position used to calculate the mol MgCO3 is not affected the peak shape especially the asym-metry towards dolomite composition can be altered signif-icantly by bleaching with a noticeable reduction of the ob-vious dolomite signal in some samples The alteration ofthe magnesite peak was less conclusive ranging from re-duction in peak height to no change at all This showsthat bleach treatment has the potential to alter the carbonatecontent of such algae specimens and that XRD data takenfrom bleached samples may not be representative of the liv-ing organism Note that major studies on coralline miner-alogy in the 1950rsquosndash1980rsquos (Chave 1954a Schmalz 1969Moberly 1970 Milliman et al 1971 Bischoff et al 1983)treated their samples with bleach peroxide or otherwise toremove organic matter and it is possible that mineralisation

Fig 9 Comparison of XRD data of anHonkodessample before(grey) and after treatment with bleach (black) focusing on the (104)carbonate peak C D and M indicate peak positions of calcite idealdolomite and magnesite The decreased intensity between dolomiteand magnesite suggests removal of such compositions by bleachingSample from Bise Okinawajima Island Japan collected in May2007 from approximately 5 m depth at the reef front (Kato et al2011)

closely associated with such organic matter could have beenremoved at the same time

Possibly also contributing to the failure to recognizedolomite previously is the inconsistency in coralline iden-tification complicating reliable comparisons on mineralogyOriginally shallow water corallines were referred to collec-tively as lsquoNulliporesrsquo (Howe 1912) and this first major studyof coral reef cores incorrectly identified the corallines asLithothamnionndash a deep or cold water genus These wereprobably Hydrolithon (then Porolithon) and another com-mon tropical genusNeogoniolithon(Adey and Macintyre1973) When our study began theonkodeswasH Onkodessince completion theH onkodeshas been reclassified backto Porolithon (Kato et al 2011) Corallines have differentnames for what can be the same species egH pachyder-mumfrom the Atlantic is probably the same asH onkodes(Adey and Macintyre 1973) Identification to the specieslevel can challenging indeed even in this study sample H56was identified in the field asHonkodeshowever under SEM

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3338 M C Nash et al First discovery of dolomite and magnesite in coralline algae

was seen instead to be multiple species or even genera whichwere not able to be reliably identified

We could find no published or unpublished mineralogicalanalyses ofH onkodesand this may also explain why thisprotodolomite and magnesite has not previously been discov-ered The first studies on coralline mineralogy using XRDreferred only to algae (Chave 1952) or the genus (noHy-drolithon) (Chave 1954) Milliman (1971) identified mostcorallines to the species level however theHydrolithon(thenPorolithon) were only to genusHonkodesspecimens usedfor species identification studies are de-calcified in nitric acidas standard procedure before analysis is undertaken (Harveyet al 2006) Given the difficulty in identifying protodolomiteby XRD without the benefit of detailed SEM-EDS or the re-cent work identifying the shift in protodolomite peak posi-tion (Zhang 2010) to that of higher Mg-calcite from thecommon reporting of XRD curve asymmetry and discrep-ancies with bulk magnesium (Milliman et al 1971 Chave1952 Moberly 1970) it seems probable that protodolomitein coralline algae has been measured many times in past stud-ies but was not able to be identified or confirmed Moreoverthese reports have included various genera and species col-lected from diverse locations outside of the tropical environ-ment indicating the occurrence of protodolomite is not re-stricted to our sample locations and may be widespread

42 Applying results to interpret fossil dolomiteformation

Sedimentary dolomite in the geological record is commonlyfound in formerly warm shallow high energy platformor atoll margin environments (McKenzie and Vasconcelos2009 Ohde and Kitano 1981 Budd 1997 Schlanger 1957)and is typically associated with coralline algae (Ohde andKitano 1981 Budd 1997 Schlanger 1957) In recentcoral-algal reefs the primary marine carbonate minerals arelow magnesium calcite [rhombohedral CaCO3 with smallamounts (lt5 ) of magnesium substituting for calcium] andaragonite [orthorhombic CaCO3] Yet in a Pleistocene fossilreef around the reef crest the dolomite content was foundto be more than 70 (Ohde and Kitano 1981) It hasbeen considered that the inclusion of dolomite into sedimen-tary systems must be a post-depositional diagenetic processwhere magnesium replaces calcium in the existing carbon-ate crystal structures (ldquodolomitisationrdquo) (eg Budd 1997)This paradigm has been adhered to for at least half a centurydespite experimental studies failing to replicate the process(McKenzie and Vasconcelos 2009) While the discovery ofmicrobially associated dolomite forming in anoxic environ-ments (Vasconcelos and McKenzie 1997) and freshwater en-vironments (Roberts et al 2004) points towards a microbialmediation there has not yet been identified a microbial rolein dolomite formation in living coral reefs and thus it is un-clear whether microbially mediated dolomite could explainthe abundant dolomite found in relict coral-algal reefs

Table 1 Summary of XRD results full details in the Supplement

Summary of XRD results

Samples analysed n = 15Subsamples n = 4

average mol MgCO3 1745for magnesite samples

average mol MgCO3 1678for asymmetrical

replicate std dev (n = 4) 008 mol MgCO3subsample std dev (n = 7) 026 mol MgCO3

Assuming that the processes taking place to create the ob-served mineral phases have persisted through time we ap-ply our findings to interpret protodolomite formations in anemerged Pleistocene reef (Ohde and Kitano 1981) To es-tablish whether there is sufficient magnesium present withinthe coralline algae to form the quantity of dolomite ob-served in fossil coral reefs we assumed a closed systemand used a mass balance approach (Lohmann and Meyers1977) to calculate potential yield of dolomite We calcu-lated that 66 mol of the magnesite bearing algal carbon-ate of this study can potentially form protodolomite assum-ing an average composition for sedimentary protodolomite of44 mol MgCO3 (Ohde and Kitano 1981) and 1745 mol MgCO3 for Mg- calcite Carbonate rock from reef crestzones of the emerged Pleistocene reef contains approxi-mately 73 wt protodolomite and 27 wt low Mg-calcite(4 mol MgCO3) If all the magnesium in our dolomite andmagnesite- rich coralline algae samples were to convert tothis low Mg-calcite and protodolomite then the final equi-librium phase would comprise 72 wt protodolomite and28 wt low Mg-calcite showing there is sufficient magne-sium within the living phase to provide the final mineral pro-portions as measured in this Pleistocene reef The sampleswithout the magnesite shoulder return 47 ndash57 potentialprotodolomite however based on the visible high porositypresence of prolific borings and high degree of friability ofthese samples we consider it unlikely that they remain a partof the reef structure and instead break apart perhaps provid-ing micron scale dolomite crystals to proximal sediment

The total magnesium contained in our most magnesium-rich samples can provide an elegant mass balance for thefinal dolomite proportions in the fossil reef The loca-tions of protodolomite in the Pleistocene reef (Ohde and Ki-tano 1981) are consistently restricted to the same areas thatcoralline algal crusts particularly ofHonkodes form prolifi-cally in modern reefs ie shallow high energy zones of trop-ical coral-algal reefs (Rasser and Piller 1997 Ringeltaubeand Harvey 2000) With this in mind we can extend this inti-mate association of coralline algae and dolomite to examples

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

M C Nash et al First discovery of dolomite and magnesite in coralline algae 3339

of other occurrences of dolomite in the geological recordDolomitised coralline algae are ubiquitous in Cenozoic is-land dolomites and is in fact the fabric most likely to bedolomitised (Budd 1997) The mid Miocene saw a shift incoral reef formation with extensive development of corallinealgal facies replacing corals as the dominant carbonate pro-ducer (Halfar and Mutti 2005) and this may well explain theformation of massive dolomite occurrences during that time(Budd 1997) In Eocene sections of a core from Enewetakatoll dolomite appeared only in association with coralline al-gae and displayed crystal growth which appeared to be con-strained by the shape of the coralline algae (Schlanger 1957)Extending our comparison beyond the confirmed identifica-tion of corallines in the Cretaceous must remain speculative

Dolomite has been recorded forming in multiple biotic set-tings in echinoderms (Schroede 1969) by or in associationwith microbial activity (Vasconcelos and McKenzie 1997Bontognali et al 2010) and in association with algal mats(Davies et al 1975) Coralline algae is widespread and canbe volumetrically significant This discovery extends therange of palaeo-environments for which biologically initi-ated dolomite can be considered a possible source of primarydolomite

43 Possible processes taking place

Future studies should aim at identifying the exact forma-tion processes of the observed magnesite and protodolomitewhether they are biologically induced or biologically con-trolled by the coralline algae At this stage we can onlyspeculate as to the processes taking place As the magnesitein-fill within cells is pervasive but not consistent this sug-gests a biologically induced rather than controlled reactionThis may be mineralisation resulting from a supersaturationof magnesium relative to calcium in the cell space as cellwall calcification takes place Noting that there is an appar-ent increase in protodolomite towards the base layers of thecoralline algae (sample 47) and that protodolomite appearsalmost exclusively as cell rims this implies that over timea reaction takes place between the magnesite and cell wallto form the protodolomite dolomite The actual mechanismsthat induce this reaction may include internal changes of pHfrom photosynthesis and respiration (Chisholm et al 1990de Vrind-de Jong and de Vrind 1997) and metabolic activity(Pueschel et al 2005) that lead to localised dissolution andre-precipitation of the carbonate minerals

5 Conclusions

This study presents empirical evidence that formation ofprotodolomite can be biologically mediated in modern coralreef environments and occurs in an organism that has attimes in geological history dominated global carbonate reefdevelopment (Aguirre et al 2000 Adey and Macintyre

1973) While it is true that diagenesis has an important roleto play in the reorganization of magnesium in carbonates(Lohmann and Meyers 1977) the biologically associatedmechanism taking place in living calcifying algae could bethe key to understanding how the magnesium arrives in suchhigh concentrations in the first place Biological vital effectsmay play an important role in the fractionation of stable iso-topes in dolomite meaning that models and studies that relyon these isotopic data and assume that dolomite formationis diagenetic may have to be revisited (eg Bao et al 2009Budd 1997 Saller 1984) Further reconstruction of past en-vironments of dolomite deposition will be aided by consid-ering the conditions needed for the development of corallinealgal dominated reefs

Supplementary material related to thisarticle is available online athttpwwwbiogeosciencesnet833312011bg-8-3331-2011-supplementpdf

AcknowledgementsThank you to the FOCE team on HeronIsland Bianca Das for undertaking the ICP-AES Timothy FawcettThomas Blanton (ICDD) and Daniel Chateigner (IUT-Caen)for discussions and suggestions regarding XRD methods NicDarrenougue for access to his PhD data Sarah Tynan for herinformative thesis Frank Brink for SEM assistance Jacquelinede Chazal Patrick DeDekker Damian Gore and Hilary Stuart-Williams for reviewing the manuscript Daniel Nash JeremyCaves Tracey Lofthouse and Jacqueline de Chazal for assistancewith XRD sample preparation Matthew Valetich for criticaldiscussion Australian National University for analytical facilitiesGeoscience Australia for support with XRD methods Thanks to thereviewers J Ries an anonymous reviewer and editor W Kiesslingfor suggestions to develop the manuscript

Edited by W Kiessling

References

Adey W H and Macintyre I G Crustose Coralline Algae A Re-evaluation in the Geological Sciences Geol Soc Am Bull 84883ndash904 1973

Aguirre J Riding R and Braga J C Diversity of coralline redalgae origination and extinction patterns from the Early Creta-ceous to the Pleistocene Paleobiology 26 651ndash667 2000

Bao H Fairchild I J Wynn P M and Spotl C Stretching theEnvelope of past Surface Environments Neoproterozoic GlacialLakes from Svalbard Science 323 119ndash122 2009

Bischoff W D Bishop F C and Mackenzie F T Biogenicallyproduced magnesian calcite in homogeneities in chemical andphysical propertiescomparison with synthetic phases Am Min-eral 68 1183ndash1188 1983

Brooke C and Riding R Ordovician and Silurian coralline redalgae Lethaia 31 185ndash195 1998

Budd D A Cenozoic dolomites of carbonate islands their at-tributes and origin Earth-Science Reviews 42 1ndash47 1997

wwwbiogeosciencesnet833312011 Biogeosciences 8 3331ndash3340 2011

3340 M C Nash et al First discovery of dolomite and magnesite in coralline algae

Butterfield N J Bangiomorpha pubescens n gen nsp implications for the evolution of sex multicellu-larity and the MesoproterozoicNeoproterozoic radiationof eukaryotes Paleobiology 26 386ndash404 1016660094-8373(2000)026lt0386bpngnsgt20co2 2000

Chave K E A Solid Solution between Calcite and Dolomite JGeol 60 190ndash192 1952

Chave K E Aspects of the Biogeochemistry of Magnesium 1Calcareous Marine Organisms J Geol 62 266ndash283 1954

Chisholm J R M Collingwood J-C and Gill E F A novelin situ respirometer for investigating photosynthesis and calcifi-cation in crustose coralline algae J Exp Mar Biol Ecol 14115ndash29 1990

de Vrind-de Jong E W and de Vrind J P M Algal depositionof carbonates and silicates in Geomicrobiology interactionsbetween microbes and minerals edited by Banfield J F andNealson K H Mineralogical Society of America Washington267ndash302 1997

Goldsmith J R Graf D L and Joensuu O I The occurrenceof magnesian calcites in nature Geochim Cosmochim Ac 7212ndash228 IN211 229ndash230 1955

Graf D L Eardley A J and Shimp N F A Preliminary Reporton Magnesium Carbonate Formation in Glacial Lake BonnevilleJ Geol 69 219ndash223 1961

Griffith E M Paytan A Caldeira K Bullen T D and ThomasE A Dynamic Marine Calcium Cycle during the past 28 MillionYears Science 322 1671ndash1674 2008

Halfar J and Mutti M Global dominance of coralline red-algalfacies A response to Miocene oceanographic events Geology33 481ndash484 2005

Harvey A S Phillips L E Woelkerling W J and Millar AJ K The Corallinaceae subfamily Mastophoroideae (Coralli-nales Rhodophyta) in south-eastern Australia Australian Sys-tematic Botany 19 387ndash429doi101071SB05029 2006

Hogbom A G Ueber Dolomitbildung und dolomitische Kalk-organismen Neues Jahrbuch fur Mineralogie 262ndash274 1894

Hunter B A Rietica ndash A Visual Rietveld program Commissionon Powder Diffraction Newsletter 20 21 1998

Land L S Contemporaneous dolomitization of middle Pleis-tocene reefs by meteoric water North Jamaica B Mar Sci 2364ndash92 1973

Lohmann K C and Meyers W J Microdolomite inclusionsin cloudy prismatic calcites a proposed criterion for formerhigh-magnesium calcites J Sediment Res 47 1078ndash1088doi101306212f72e3-2b24-11d7-8648000102c1865d 1977

McKenzie J A and Vasconcelos C Dolomite Mountains and theorigin of the dolomite rock of which they mainly consist his-torical developments and new perspectives Sedimentology 56205ndash219 2009

Milliman J D Gastner M and Muller J Utilization of Mag-nesium in Coralline Algae Geol Soc Am Bull 82 573ndash580doi1011300016-7606(1971)82[573uomica]20co2 1971

Moberly R Microprobe study of diagenesis in calcareous algaeSedimentology 14 113ndash123 1970

Morse J W Andersson A J and Mackenzie F T Initial re-sponses of carbonate-rich sediments to rising atmosphericpCO2and ldquoocean acidificationrdquo Role of high Mg-calcites GeochimCosmochim Ac 70 5814ndash5830 2006

Ohde S and Kitano Y Protodolomite in Daito-jima OkinawaGeochem J 15 199ndash207 1981

Penrose D and Woelkering W J A reappraisal of Hydrolithonand its relationship to Spongites (Corallinaceae Rhodophyta)Phycologia 31 81ndash88 1992

Pueschel C M Judson B L and Wegeberg S Decalcificationduring epithallial cell turnover in Jania adhaerens (CorallinalesRhodophyta) Phycologia 44 156 2005

Rasser M and Piller W E Depth Distributions of Calcareousencrusting associations in the northern Red Sea (Safaga Egypt)and their geological implications 8th International Coral ReefSymposium 743ndash748 1997

Roberts J A Bennett P C Gonzalez L A Macpherson GL and Milliken K L Microbial precipitation of dolomite inmethanogenic groundwater Geology 32 277ndash280 2004

Ries J B Mg fractionation in crustose coralline algae Geochem-ical biological and sedimentological implications of secularvariation in the MgCa ratio of seawater Geochim CosmochimAc 70 891ndash900 2006

Ringeltaube P and Harvey A Non-Geniculate Coralline Algae(Corallinales Rhodophyta) on Heron Reef Great Barrier Reef(Australia) Bot Mar 43 431 2000

Russell B D Thompson J I Falkenberg L J and ConnellS D Synergistic effects of climate change and local stres-sors CO2 and nutrient-driven change in subtidal rocky habitatsGlobal Change Biol 15 2153ndash2162 2009

Saller A H Petrologic and geochemical constraints on theorigin of subsurface dolomite Enewetak Atoll An exampleof dolomitization by normal seawater Geology 12 217ndash220doi1011300091-7613(1984)12lt217PAGCOTgt20CO21984

Schlanger S O Dolomite growth in coralline algae J Sed-iment Res 27 181ndash186doi10130674d70696-2b21-11d7-8648000102c1865d 1957

Stanley S M Ries J B and Hardie L A Low-magnesium cal-cite produced by coralline algae in seawater of Late Cretaceouscomposition PNAS 15323ndash15326 2002

Vasconcelos C and McKenzie J A Microbial mediation ofmodern dolomite precipitation and diagenesis under anoxicconditions (Lagoa Vermelha Rio de Janeiro Brazil) J Sed-iment Res 67 378ndash390doi101306d4268577-2b26-11d7-8648000102c1865d 1997

Ward W C and Halley R B Dolomitization in a mixingzone of near-seawater composition late Pleistocene north-eastern Yucatan Peninsula J Sediment Res 55 407ndash420doi101306212f86e8-2b24-11d7-8648000102c1865d 1985

Xiao S Knoll A H Yuan X and Pueschel C M PhosphatizedMulticellular Algae in the Neoproterozoic Doushantuo Forma-tion China and the Early Evolution of Florideophyte Red AlgaeAmerican Journal of Botany 91 214ndash227 2004

Zhang F Xu H Hironi K and Roden E E A relationshipbetween d104 value and composition in the calcite-disordereddolomite solid-solution series Am Mineral 95 1650 2010

Biogeosciences 8 3331ndash3340 2011 wwwbiogeosciencesnet833312011