REVIEW ARTICLE - Northeastern University ARTICLE Effects of secular variation in seawater Mg⁄Ca...

REVIEW ARTICLE

Effects of secular variation in seawater Mg ⁄Ca ratio(calcite–aragonite seas) on CaCO3 sediment production by thecalcareous algae Halimeda, Penicillus and Udotea – evidence fromrecent experiments and the geological record

Justin Baker RiesMarine Sciences, University of North Carolina – Chapel Hill, CB#3300, 340 Chapman Hall, Chapel Hill, NC 27599, USA

Introduction

Calcareous bryopsidalean algae areamongst the most important contrib-utors of aragonite sediments to mod-ern carbonate environments (Hillis,1997; Rees et al., 2007). The arago-nite-secreting bryopsidalean algaeassumed their role as importantsediment producers in middle Palaeo-gene time (Hillis, 2001), around thetime of the most recent calcite-to-aragonite sea transition (Hardie,1996). They retained this rolethroughout the remainder of Cenozoictime, as seawater Mg ⁄Ca ascendedfurther into the aragonite domain(Hillis, 2001). There is mounting evi-dence that this protracted transitioninto the aragonite stability field played

an important role in the rise of cal-careous bryopsidalean algae as impor-tant carbonate sediment producers inearly Cenozoic time and enabled themto continue functioning as limestone-forming algae through to present time(Stanley and Hardie, 1998; Ries, 2005,2006; Stanley et al., 2009).Multiple independent lines of evi-

dence suggest that the Mg ⁄Ca ratio ofseawater fluctuated between 1.0 andthe modern value of 5.2 throughoutPhanerozoic time (Fig. 1), this evi-dence includes (1) secular variation inthe ionic composition of fluid inclu-sions in primary marine halite(Lowenstein et al., 2001), (2) secularvariation in the mineralogy of latestage marine evaporites (MgSO4 andKCl; Hardie, 1996), (3) secular varia-tion in concentrations of Br in marinehalite (Siemann, 2003) and (4) secularvariation in the skeletal Mg ⁄Ca ratioof fossil molluscs (Steuber and Rauch,2005) and echinoderms (Dickson,2002, 2004). Hardie (1996) and Dem-icco et al. (2005) suggest that thisvariation in seawater Mg ⁄Ca has been

primarily driven by variations in theglobal rate of ocean crust production,which caused fluctuations in the mix-ing rates of the primary sources ofseawater – Ca2+-rich hydrothermalbrines and river water.Variations in the Mg ⁄Ca ratio of

seawater is of particular interest topalaeobiologists and carbonate sedi-mentologists because experiments(Fuchtbauer and Hardie, 1976, 1980)have shown that seawaterMg ⁄Ca ratiocontrols which polymorph(s) of theskeleton-, sediment- and limestone-forming mineral CaCO3 will be kinet-ically favoured. Molar Mg ⁄Ca ratios(mMg ⁄Ca) greater than 2 support pre-cipitation of aragonite and high-Mgcalcite (aragonite seas), while ratios lessthan 2 support precipitation of low-Mgcalcite (calcite seas). Secular trends inthe original polymorph mineralogy ofooids and marine cements (Fig. 1,Sandberg, 1983) reveal that these fluc-tuations in seawater Mg ⁄Ca have hadsystematic effects on abiotic marinecalcification throughout Phanerozoictime (Hardie, 1996).

ABSTRACT

Independent lines of geological evidence suggest that fluc-tuations in the Mg ⁄ Ca ratio of seawater between 1.0 and 5.2have caused the oceans to alternate between favouring theprecipitation of the aragonite and high-Mg calcite polymor-phs of calcium carbonate (mMg ⁄ Ca > 2; aragonite seas) andthe low-Mg calcite polymorph (mMg ⁄ Ca < 2; calcite seas)throughout Phanerozoic time. The rise of aragonite-secretingbryopsidalean algae as major producers of carbonate sedi-ments in middle Palaeogene time, a role that they main-tained through to the present, has been attributed to atransition from calcite-to-aragonite seas in early Cenozoictime. Recent experiments on the modern, carbonate-sedi-ment-producing bryopsidales Halimeda, Penicillus and Udoteareveal that their rates of calcification, linear extension andprimary production decline when reared in experimental

calcite seawaters (mMg ⁄ Ca < 2). These normally aragonite-secreting algae also began producing at least one-quarter oftheir CaCO3 as calcite under calcite sea conditions, indicatingthat their biomineralogical control can be partially overriddenby ambient seawater chemistry. The observation thatprimary production and linear extension declined alongwith calcification in the mineralogically unfavourable seawa-ter suggests that photosynthesis within these algae isenhanced by calcification via liberation of CO2 and ⁄ or H+.Thus, the reduced fitness of these algae associated with theirlow rates of calcification in calcite seas may have beenexacerbated by concomitant reductions in tissue mass andalgal height.

Terra Nova, 21, 323–339, 2009

Correspondence: Prof. Justin Baker Ries,

Marine Sciences, University of North Car-

olina – Chapel Hill, CB#3300, 340 Chap-

man Hall, Chapel Hill, NC 27599, USA.

Tel.: 919 962 0269; fax: 919 962 1254;

e-mail: [email protected], riesjustin@hotmail.

com

� 2009 Blackwell Publishing Ltd 323

doi: 10.1111/j.1365-3121.2009.00899.x

There is mounting evidence thatthese fluctuations in seawater Mg ⁄Caalso played a role in determining whichgroups of hypercalcifying marineorganisms functioned as the dominantreef-builders and sediment-producersthroughout Phanerozoic time (Stanleyand Hardie, 1998; Porter, 2007; Kies-sling et al., 2008). One group of hy-percalcifying marine organisms whosecontribution to limestone formation isthought to have been particularlyinfluenced by fluctuations in seawaterMg ⁄Ca is the aragonite-secreting bry-opsidalean algae (known to geologistsas �codiacean algae� or �calcareousgreen algae�), which are major sedi-ment producers in modern carbonateplatform environments (Hillis, 1997;Rees et al., 2007).Although these calcifying algae have

been identified in Permian-age lime-stones (Poncet, 1989), they did not

become important producers of car-bonate sediments until middle Palaeo-gene time (Hillis, 2001), coincidentwiththe rise of seawater mMg ⁄Ca above 2into the aragonite stability field (Fig. 1;Hardie, 1996; Lowenstein et al., 2001;Demicco et al., 2005). Significantly,they persisted in their role as majorproducers of carbonate sedimentsthroughout Cenozoic time, as seawaterMg ⁄Cagradually ascended further intothe aragonite stability field (Fig. 1).Their modern rate of carbonate sedi-ment production is thought to repre-sent a Cenozoic maximum (Hillis,2001) and occurs in seawater condi-tions (mMg ⁄Ca = 5.2) that are morefavourable for the nucleation of arago-nite than at any other time in theirgeological past. The apparent suscep-tibility of the bryopsidalean algae tosecular variation in seawater chemistrymay be attributable to their relatively

rapid and uncontrolled mode of calci-fication, in which precipitation of ara-gonite needles proceeds mostlyextracellularly, within invaginationsof the algal cell wall.It is perhaps important to note here

that the Stanley-Hardie calcite–arago-nite sea hypothesis (1998, 1999) doesnot address macroevolutionary trendswithin the bryopsidalean order. In-deed, there is no compelling evidencepresented to date to suggest thatcompatibility between seawaterMg ⁄Ca and the polymorph mineral-ogy of these algae played any part intheir origination, diversification orextinction. Rather, the Stanley-Hardiehypothesis asserts that the ascendanceof calcareous bryopsidalean algae asimportant producers of carbonate sed-iments in early-middle Cenozoic timewas permitted by the coeval rise inseawater Mg ⁄Ca into the aragonitestability field. Critically, these algaeretained their role as importantmanufacturers of carbonate sedi-ments throughout the remainder ofCenozoic time, as seawater Mg ⁄Cacontinued to rise further into thearagonite domain.Here, I review the physiological,

geological and experimental evidencethat suggests that secular variation inseawater Mg ⁄Ca has influenced bry-opsidalean biomineralization andcarbonate sediment productionthroughout Phanerozoic time. Thisreview covers three general subjects:(1) anatomy, mechanisms of calcifica-tion, ecology and phylogeny of thecalcareous bryopsidalean algae; (2)sedimentary and geological evidencein support of secular variation inseawater Mg ⁄Ca and its effect on algalcarbonate sedimentation and (3)recent experiments on living bryops-idalean algae (Halimeda, Penicillusand Udotea) that were conducted toempirically constrain the relationshipbetween seawater Mg ⁄Ca and algalcalcification and growth.

Anatomy, mechanism of calcification,ecology and phylogeny

Anatomy

Halimeda, Penicillus and Udotea areupright-standing green algae withthalli that are anchored to the sedi-ment with fibrous holdfasts. TheHalimeda thallus is constructed from

0

1

2

3

4

5

6

1000 200 300 400 500 600

MgSO4 KCl MgSO4 KCl MgSO4

A ? AAC ? C ?

OSDMPPmTrJKPgNg Pre-CC0

5

4

3

2

1

6

Sea

wat

er M

g/C

a ra

tio (

mol

ar)

Time (Ma)

Aragonite + high-Mg calcite

Calcite

Fig. 1 Secular variation in seawater Mg ⁄Ca throughout Phanerozoic time supportedthree intervals of predominantly aragonite + high-Mg calcite precipitation alternat-ing with two intervals of predominantly calcite precipitation. Curve is Mg ⁄Ca ratio ofseawater (Demicco et al., 2005) calculated from a mid-ocean ridge hydrothermalbrine ⁄ river water mixing model. Closed squares (Brennan, 2002), closed triangles(Timofeeff et al., 2006), large closed circles (Lowenstein et al., 2005), circumscribedsmall closed circle (Brennan and Lowenstein, 2002), closed diamonds (Brennan et al.,2004) and open circles (Horita et al., 2002) are seawater mMg ⁄Ca ranges estimatedfrom fluid inclusions in primary marine halite. Crosses represent seawater Mg ⁄Cainferred from the Mg ⁄Ca and dolomite content of fossil echinoderms (Dickson, 2002,2004; Ries, 2004). Star represents modern seawater (mMg ⁄Ca = 5.2). Horizontalblack bar represents temporal range over which bryopsidalean algae have beenimportant contributors of carbonate sediments (Wray, 1977; Hillis, 2001). Horizontalline divides the calcite (mMg ⁄Ca < 2) and aragonite + high-Mg calcite(mMg ⁄Ca > 2) nucleation fields in seawater at 25 �C. Intervals of primarilyaragonitic (�A�) and calcitic (�C�) abiogenic (ooids, marine cements, seafloorprecipitates; Sandberg, 1983) and biogenic (hypercalcifying reef-building and sedi-ment-producing organisms; Stanley and Hardie, 1998) precipitates, as well as KCland MgSO4 marine evaporites (Hardie, 1996), are plotted along the top of the figure.

Seawater Mg ⁄ Ca and algal CaCO3 sediment production • J. B. Ries Terra Nova, Vol 21, No. 5, 323–339

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324 � 2009 Blackwell Publishing Ltd

sub-centimetre scale calcified segments(Fig. 2A). Growth of the Halimedaalga occurs through the addition ofnew segments, as well as through theaugmentation of previously formedsegments. Segments are joined byflexible, non-calcified filaments thatrun the length of the thallus. Branch-ing of the Halimeda thallus occurswhen multiple segments grow from asingle, pre-existing segment (Hillis,1957; Hillis-Colinvaux, 1980; Macin-tyre and Reid, 1995). Unlike Halime-da, the Penicillus (Fig. 2B) and Udotea(Fig. 2C) thalli are continuous, withthe Penicillus thallus terminating as acap and the Udotea thallus terminat-ing as a fan.TheHalimeda,Penicillus andUdotea

thalli comprise medullar filaments that

run the length of these algae. Themedullar filaments trifurcate laterallyto form cortical filaments that ramifyinto distally swollen structures termedutricles (Fig. 2). The appressed, swo-llen utricles coalesce to form the outersurface of these algae, effectively seal-ing off their interutricular regions fromambient seawater (Fig. 2). It is withinthese interutricular regions that mostcalcificationoccurs.Differences in thal-lusmorphology are used to divide thesegenera into different species.

Mechanisms of calcification

The Halimeda, Penicillus and Udoteaalgae each deposits CaCO3 crystalsprimarily as the aragonite polymorphextracellularly within the interutri-

cular space (IS, Fig. 2) of the algae�smedullar and cortical regions (Boro-witzka and Larkum, 1976a, 1977;Borowitzka et al., 1974). These algaealso deposit a small portion of theiraragonite intracellularly, between theinner and outer walls of their fila-ments. The precipitation of aragonitebegins shortly after the appearance ofchloroplasts (Wilbur et al., 1969). Theextent of calcification increases withthe age of the alga, with matureportions of tissue containing up to88 wt% CaCO3 (Multer, 1988). Hal-imeda, Penicillus and Udotea arethought to precipitate CaCO3 withintheir tissue for increased rigidity inturbulent hydraulic regimes, for main-taining an erect posture to maximizeexposure to sunlight and as a deter-

Thallus

Cap

Holdfast 1 cm

1 mm

Cortical filaments

Medular filaments

100 µm

1 cm

iii

ii

iiv

i

iii

ii

i iii

ii

iv

Thallus

(A)

(B) (C)

Holdfast

Ut ri cl e

100 µm

Cortical filament

CaCO3 deposits

SeawaterCaCO 3

Utricl e CO 2 + H 2 O H2CO3

H 2 CO 3 HCO3–+ H +

HCO CO3 – → 3

= + H +

HNO 3 H 2 PO 4

–

CO 2 + H 2 O → CH2 O + O 2

CO 2 + H 2 O HCO 3 – + H+

CO 3 = + Ca 2+ →

←

←

←

CaCO 3

Mg 2+ /C a 2+

Utricl e pH ↓

pH↑

↑

IS

IS

IS

10 µm

5 µm

1 cm Thallus

Cap

Holdfast

Fig. 2 Anatomy of the predominant CaCO3-producing bryopsidalean algae in modern carbonate platform environments. (A)Halimeda incrassata showing (i) the thallus, the calcified segments, and the uncalcified holdfast; (ii) an SEM image of a verticalsection through the cortical layer of the thallus, showing extracellular calcification in the interutricular space (�IS�), external to theouter algal wall; (iii) corticated surface of a calcified segment resulting from coalescence of utricles; (iv) diagram showing thechemical connectivity between the primary mass-forming reactions (calcification, photosynthesis), the primary carbonate systemequilibria, nutrient shuttling, localized Mg ⁄Ca ratios and pH within and between the coalescing utricles that form the calcifiedcortex of the Halimeda, Penicillus and Udotea algae. (B) Penicillus capitatus showing (i) a full grown plant revealing uncalcifiedholdfast, calcified thallus and calcified cap; (ii) an offspring alga sprouting from rhizoids and (iii) magnified diagram of thallusrevealing the constituent calcified medullar and cortical filaments. (C) Udotea flabellum showing (i) full-grown alga revealinguncalcified holdfast, calcified thallus and calcified fan; (ii) an offspring alga; (iii) vertical section through the cortical layer of thefan, showing coalescence of the utricles and (iv) corticated surface of the fan (after Fritsch, 1948; Bohm et al., 1978).

Terra Nova, Vol 21, No. 5, 323–339 J. B. Ries • Seawater Mg ⁄ Ca and algal CaCO3 sediment production

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rent of predatory grazing, especiallywhen combined with toxic, secondarymetabolites and nocturnal growth ofnew, non-calcified segments (Paul andFenical, 1984; Hay et al., 1988, 1994;Paul and Van Alstyne, 1992; Schuppand Paul, 1994).The primary substrate-forming

reactions in calcifying algae (Fig. 2A)are photosynthesis:

CO2 þH2O$ CH2OþO2 ð1Þ

and calcification:

Ca2þþ2HCO�3 $CaCO3þH2OþCO2

ð2Þ

and ⁄or

Ca2þ þHCO�3 $ CaCO3 þHþ ð3Þ

and ⁄or

Ca2þ þ CO2�3 $ CaCO3 ð4Þ

As inorganic C is integral to each ofthese reactions, it is not surprising thatexperiments have revealed an intimatecoupling between photosynthesisand calcification (Borowitzka andLarkum, 1976b; Borowitzka, 1977,1982a,b; Pentecost, 1978; Smith andRoth, 1979; Gattuso et al., 1999; DeBeer and Larkum, 2001; Marshall andClode, 2002). However, their relation-ship is complex and remains some-what ambiguously defined.An aqueous system�s affinity for

calcification can be quantified by itsCaCO3 saturation state (WCaCO3):

XCaCO3¼ ½Ca2þ�½CO2�

3 �=K�sp; ð5Þ

where [Ca2+] and [CO32)] are the

concentrations of Ca2+and CO32)

and K*sp is the stoichiometric solubil-ity product of the appropriate poly-morph of CaCO3. If WCaCO3

> 1,calcification should occur; ifWCaCO3

< 1, dissolution should occur.The equilibrium reactions that gov-

ern the aqueous carbonate system canbe summarized as follows:

CO2 þH2O$ H2CO3 ð6Þ

H2CO3 $ HCO�3 þHþ ð7Þ

and

HCO�3 $ Hþ þ CO2�3 ð8Þ

Photosynthesis is thought to en-hance calcification in the calcareous

bryopsidalean algae by removing CO2

from the algae�s interutricular fluid,which would shift the carbonate sys-tem equilibria of the algae�s calcifyingfluid towards increased [CO3

2)] andWCaCO3 (Fig. 2A). Alternatively, cal-cification may be enhanced by photo-synthesis within algae through theintracellular extraction of CO2 fromHCO3

) by the enzyme carbonic an-hydrase, which liberates OH- that isextruded into the algae�s interutricularfluid (Borowitzka and Larkum,1976b; Axelsson et al., 2000; Hellblomet al., 2001; Hellblom and Axelsson,2003; Uku et al., 2005). This OH)

complexes with H+ in the interutric-ular fluid, thereby increasing thefluid�s pH and therefore its [CO3

2)]and WCaCO3. The algae also utilize H+

ions from the interutricular fluid toshuttle HCO3

), PO43) and NO3

)

across the cell wall to fuel photo-synthesis (Fig. 2A; McConnaugheyand Whelan, 1997). Such photo-synthetically driven removal of H+

ions from the algae�s interutricularspace effectively increases WCaCO3 ofthe alga�s interutricular fluid, therebyenhancing calcification. Photosynthe-sis may also enhance calcification byproducing Ca2+-binding polysaccha-ride mucilage within cell walls that actas nucleation sites for CaCO3 crystals(Borowitzka and Larkum, 1976a,b). Ithas also been suggested that the cat-ion-binding properties of this polysac-charide influence the polymorphmineralogy of the nucleating CaCO3

(Borowitzka, 1977).Calcification may enhance photo-

synthesis in the calcareous bryopsida-lean algae by removing CO3

2) ionsfrom the algae�s interutricular fluid,thereby liberating CO2 and H+ as thecarbonate system re-equilibrates (seereactions 6, 7 and 8 above; Fig. 2A).CO2 liberated within the interutricularcalcifying fluid would diffuse acrossthe algal cell wall, where it would fuelphotosynthesis within chloroplasts(Borowitzka and Larkum, 1976b).Protons released to the interutricularfluid would complex with HCO3

) andform H2CO3, some of which would beconverted to CO2 via cellular de-hydration (see reactions 6 and 7above; Fig. 2A; McConnaughey andWhelan, 1997; Hellblom et al., 2001).Protons liberated by calcification inthe interutricular fluid may also assistin the active transport of HCO3

) and

nutrients such as NO3) and PO4

3)

across the algal cell wall by H+

symporters or co-transporters(Fig. 2A; Price and Badger, 1985;Price et al., 1985; Badger and Price,1994; Hellblom et al., 2001; Hellb-lom and Axelsson, 2003). This wouldincrease the alga�s rate of photosyn-thesis directly via nutrient enrich-ment or indirectly via increased CO2

liberation from the importedHCO3

) by the enzyme carbonic an-hydrase.There is also evidence that a light-

induced H+ pump controls pH withinthe Halimeda alga (Fig. 2A; De Beerand Larkum, 2001; Kangwe, 2006).This H+ pump is reported to regulatethe distribution of so-called acid andalkaline zones, which promote disso-lution and calcification of CaCO3

respectively within the alga (Boro-witzka, 1977; De Beer and Larkum,2001; Kangwe, 2006).

Ecology and biogeography

Halimeda, Penicillus and Udotea arerestricted to tropical and subtropicalmarine environments (>20 �C),where they grow either on unconsol-idated sediments or on the reef itself.They are pantropically distributed,with greatest densities occurring inthe Caribbean Sea, followed by theMediterranean Sea (Hillis-Colinvaux,1980), the Great Barrier Reef Province(Drew and Abel, 1988) and restrictedIndian (Kangwe, 2006), Pacific andAtlantic Ocean localities (Bach, 1979;Garrigue, 1985; Hillis, 1991). Penicil-lus and Udotea exist primarily inshallow, low-energy environments,while Halimeda algae tolerate a rangeof hydrodynamic regimes, flourishingfrom the back-reef lagoon to the fore-reef slope, at depths ranging from <1to 150 m (Moore et al., 1976; Hillis-Colinvaux, 1980).These algae grow rapidly, attain-

ing heights up to 15 cm over their 1–3 month lifespan. Population densi-ties of over 80 plants m)2 have beenobserved in embayments off thecoast of Antigua (Multer, 1988).Due to their high productivity,these calcareous algae are consid-ered important geological and bio-logical components of tropical andsubtropical carbonate platform envi-ronments (Blair and Norris, 1988;Hillis, 1997).


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Phylogeny

Halimeda, Penicillus and Udotea arethe most abundant representatives ofthe carbonate producing bryopsida-lean algae in modern tropical seas.These three algae are classified withinthe phylum Chlorophyta, class Bryop-sidophyceae and order Bryopsidales.Analysis of 18s DNA sequences fromthese algae (Verbruggen et al., 2009)reveals that Penicillus and Udotea arethe more closely related genera andare both assigned to the udoteaceanfamily. The more distant Halimedagenus is assigned to the halimedaceanfamily.

Geological evidence

Secular variation in seawater Mg ⁄Ca

Analysis of fluid inclusions (Lowen-stein et al., 2001, 2003, 2005; Horitaet al., 2002; Brennan et al., 2004; Tim-ofeeff et al., 2006) trapped in primarymarine halite crystals from the geolog-ical record indicates that the molarMg ⁄Ca ratio of seawater has variedbetween approximately 1.0 and 5.2through the Phanerozoic Eon (Fig. 1).These estimates of ancient seawaterMg ⁄Ca are consistent with multipleindependent proxies of seawaterMg ⁄Ca, including (1) secular variationin the polymorphmineralogy of abioticmarine carbonates (Sandberg, 1983)and the dominant reef-building ⁄ sedi-ment-producing marine organisms(Stanley and Hardie, 1998, 1999; Steu-ber, 2002; Porter, 2007;Kiessling et al.,2008); (2) the precipitation of MgSO4

evaporites during aragonite sea inter-vals (mMg ⁄Ca > 2) and KCl evapor-ites during calcite sea intervals(mMg ⁄Ca < 2; Sandberg, 1983; Har-die, 1996; Lasemi and Sandberg, 2000);(3) secular variation in concentrationsof Br in marine halite (Siemann, 2003)and (4) secular variation in the skeletalMg ⁄Ca ratio of fossilmolluscs (Steuberand Rauch, 2005) and echinoderms(Dickson, 2002, 2004).Hardie (1996) and Demicco et al.

(2005) suggested that this variation inseawater Mg ⁄Ca was caused by fluctu-ations in the rate of ocean crust pro-duction (Engel andEngel, 1970;Gaffin,1987;Vail et al., 1991) that alter the fluxof hydrothermal brine through mid-ocean-ridge and large-igneous-prov-ince zones of ocean crust production.

The fresh basalt in these systems isconverted to greenstone as it reactswith the circulating hydrothermalbrine, a reaction that effectivelyremoves Mg2+ from the brine andreleases Ca2+ to it. Ancientseawater Mg ⁄Ca ratios calculatedfrom this model are consistent withempirical estimates, suggesting that theprincipal tenants of the model arecorrect.Laboratory experiments conducted

at standard conditions (1 atmpressure,T = 25 �C, pCO2 = 380 p.p.m.) havedemonstrated that low-Mg calcite willprecipitate from seawater whenmMg ⁄Ca < 2 (±0.5), whereas arago-nite and high-Mg calcite will precipi-tate when mMg ⁄Ca >2 (±0.5;Leitmeier, 1910, 1915; Lippmann,1960; Muller et al., 1972; Berner,1975; Fuchtbauer and Hardie, 1976,1980; Given and Wilkinson, 1985;Morse et al., 1997). Therefore, thecalcareous bryopsidalean algae wouldhave experienced two transitionsbetween aragonite and calcite seassince Permian time, which is the ageof the oldest known fossils assigned tothis order (Poncet, 1989).

Role of atmospheric pCO2 andseawater temperature

Sandberg (1975) originally attributedhis single calcite-to-aragonite shift inocean state to a protracted increasein the Mg ⁄Ca ratio of seawaterthroughout Phanerozoic time, drivenby the selective removal of calciumions via planktonic calcification.Mackenzie and Pigott (1981) laterargued that Sandberg�s single shiftwas driven by tectonically inducedshifts in atmospheric pCO2. As moreancient oolite and early marine ce-ment data became available, Sand-berg abandoned his single-shifthypothesis in favour of the currentlyaccepted fourfold shift in carbonatemineralogy (Sandberg, 1983; Lasemiand Sandberg, 2000), which he attrib-uted to Mackenzie and Pigott�s(1981) pCO2 mechanism.Morse et al. (1997) and Stanley and

Hardie (1998) discounted the pCO2

mechanism on the ground that itcould only effect a shift to calcite seasif it caused seawater to become simul-taneously oversaturated with respectto calcite and undersaturated withrespect to aragonite. As the stoichio-

metric solubility coefficients (Ksp) ofaragonite (10)6.19) and calcite (10)6.37)are relatively close, the range ofCaCO3 saturation states thatyields simultaneous calcite oversatu-ration and aragonite undersatura-tion is correspondingly narrow (1 <Wcalcite <1.5; 0.7 < Waragonite < 1)and requires that seawater be nearundersaturation with respect to calciteover protracted intervals of geologicaltime. Given the ubiquity and abun-dance of both biogenic and abiogeniclimestone deposits throughout the cal-cite seas of Early Cambrian – LateMississippian time and Late Jurassic –Middle Palaeocene time, it is improb-able that the CaCO3 saturation stateof seawater during these intervals wasregularly constrained to such a lowand narrow range, teetering on theedge of total CaCO3 undersaturation(Wcalcite < 1). And unlike Hardie�s(1996) seawater Mg ⁄Ca model, atmo-spheric pCO2 does not explain thesimultaneous transitions in the miner-alogy of late stage marine evaporites(KCl-to-MgSO4) and abiotic marinecarbonates (calcite-to-aragonite)throughout Phanerozoic time.However, Morse et al. (1997)

showed experimentally that tempera-ture can strongly influence whichpolymorph of CaCO3 precipitates abi-otically from seawater. In modernseawater (mMg ⁄Ca = 5.2), the calciteand aragonite nucleation fields aredivided by a temperature of �6 �C –which is of little consequence heresince the carbonate forming environ-ments relevant to the calcite–aragonitesea hypothesis have probably beenconfined to tropical waters that areinherently more saturated with respectto CaCO3 throughout Phanerozoictime. However, for seawater withmMg ⁄Ca ratios between 3.0 and 1.0,Morse et al. (1997) showed that thecalcite and aragonite nucleation fieldsare divided by temperatures rangingfrom 15 to 25 �C respectively. Thus, aslight change in the temperature oftropical, carbonate-forming waterscould effect a threshold change inoceanic state. It is therefore likely thatpCO2-induced fluctuations in climatehave modulated the effect of seawaterMg ⁄Ca on oceanic state (calcite vs.aragonite seas) throughout Phanero-zoic time, particularly when seawatermMg ⁄Ca was in its lower range(1.0 < mMg ⁄Ca < 3.0).


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Along these lines, Zhuravlev andWood (2008) attributed an apparentlyshort-lived aragonite sea interval inmiddle Cambrian time (late Atbada-nian–Botoman), which occurredshortly after the commencement ofthe protracted Palaeozoic calcite sea,to the onset of global greenhouseconditions at a time when seawatermMg ⁄Ca was near the calcite–arago-nite boundary value of 2.

Modern carbonate sedimentproduction

The role of Halimeda, Penicillus andUdotea as important producers ofmodern carbonate sediments is welldocumented (David and Sweet, 1904;Finckh, 1904; Halligan, 1904; Chap-man and Mawson, 1906; Emery et al.,1954; Ginsburg, 1956; Milliman, 1977,1993; Hillis-Colinvaux, 1980; Drew,1983; Drew and Abel, 1988; Payri,1988, 1995; Hillis, 1991, 2001; Freileet al., 1995; Rees et al., 2007). Thesealgae are reported to contribute 25 to39% of carbonate sediments in theBahama Banks (Emery et al., 1954;Neumann and Land, 1975), 25% to80% in parts of the Great Barrier ReefProvince (Drew, 1983; Rees et al.,2007), 80% in carbonate platformsof the Timor Sea, NW Australia(Heyward et al., 1997), 28% off theIsland of Moorea, Tahiti (Payri, 1988)and 20–30% in the Florida Keys(Ginsburg, 1956). Rates of carbonatedeposition range from 0.18 to 5.9 m1000 yr)1 (Neumann and Land, 1975;Marshall and Davies, 1988; Orme andSalama, 1988; Roberts et al., 1988;Searle and Flood, 1988; Hillis, 1991;Freile et al., 1995). Sediment produc-tion by these algae occurs fromshallow back-reef environments(Ginsburg, 1956) to the deep fore-reef(Goreau and Goreau, 1973).Such rapid rates of sediment pro-

duction are attributable to the algae�srelatively large size (up to 20 cm),rapid turnover because of a short,1–2 month lifespan (Wefer, 1980),massive standing biomasses (up to1560 g-dw m)2; Kangwe, 2006) andhigh rates of growth (3–4 mm day)1).Detailed field studies of Halimedasedimentary production have yieldedCaCO3 sedimentation rates of 2227 gCaCO3 m

)2 yr)1 from a standingstock of 228.4 g-dw m)2 in parts andof the Great Barrier Reef Complex

(Drew, 1983); 1400 g CaCO3 m)2 yr)1

from a standing stock of111 g-dw m)2 off the Island of Moo-rea, Tahiti (Payri, 1988); 6205–20805 g m)2 yr)1 from a standingstock of 1560 g-dw m)2 in ChkawaBay of the Indian Ocean, off the coastof Tanzania (Kangwe, 2006), 2300 gCaCO3 m

)2 yr)1 in Moorea Islandlagoon in Tahiti (Freile et al., 1995),2400 g CaCO3 m

)2 yr)1 in WesternGreat Bahama Bank (Freile andHillis, 1997), 2300 g CaCO3 m

)2 yr)1

around the San Blas islands off thecoast of Panama (Freile and Hillis,1997) and 404.9 g CaCO3 m

)2 yr)1 offthe coast of Guam (Merten, 1971).Massive �Halimeda reefs� (Martin

et al., 1997), tens of metres thick, kilo-metres in width and consisting almostentirely of Halimeda segments that arecemented and bound by microbiallyprecipitated micrite and marine ce-ment, have been observed in the GreatBarrier Reef Province (Orme et al.,1978a,b; Marshall and Davies, 1988;Orme andSalama, 1988;Roberts et al.,1988), the Timor Sea off the northwestcoast of Australia (Heyward et al.,1997), the Fly River Delta in the Gulfof Papua New Guinea (Harris et al.,1996), Indonesia (Phipps and Roberts,1988; Roberts et al., 1988; Granieret al., 1997), the Caribbean Sea (Hineet al., 1988) and offshore western India(Rao and Veerya, 1994).Significantly, Neumann and Land

(1975) observed that although theCaCO3 within living Halimeda algaeconstitutes half of the total CaCO3

within all calcareous bryopsidaleanalgae in the Bight of Abaco (Baha-mas), only 25% of the underlyingCaCO3 sediments contain recogniz-able Halimeda grains. This suggeststhat half of the Halimeda grains areeither exported by currents and stormsfrom the basin or remain within thebasin and disaggregate into loose,unrecognizable aragonite needles.The tendency for calcareous bryo-psidalean algae – particularly Udoteaand Penicillus – to disaggregaterapidly into nondescript grains ofaragonite may cause their contribu-tion to carbonate sedimentation to beunderestimated. In fact, Lowenstamand Epstein (1957) showed that thecarbon and oxygen isotopic signaturesof aragonitic carbonate muds areconsistent with a predominantly algalorigin. However, microbial precipita-

tion in the water column has also beenshown to be capable of producingsubstantial quantities of carbonatemud in tropical marine environments(Yates and Robbins, 1998, 1999,2001).

Geological history of the calcareousbryopsidalean algae

The oldest fossil representative of thebryopsidalean order to which Halime-da, Penicillus and Udotea belong isHalimeda soltanensis (Poncet, 1989;Bucur, 1994), which has been identi-fied in Permian-age limestones. How-ever, calcareous bryopsidalean algaedid not exhibit extensive diversityuntil Late Cretaceous time (c. 80 Ma;Elliott, 1960, 1965, 1978, 1981, 1984;Conrad and Rioult, 1977; Bassoulletet al., 1983; Flugel, 1988, 1991; Hillis,1991, 2000, 2001). After a brief periodof stasis that followed the Creta-ceous ⁄Tertiary mass extinction event(Hillis, 2001), the algae�s contributionto sediment production increasedmarkedly throughout early-middleCenozoic time (Elliott, 1984; Flugel,1988, 1991; Hillis, 2000, 2001), aninterval marked by the ocean�s transi-tion into the aragonite nucleation field(seawater mMg ⁄Ca > 2). Their highlevel of diversity, abundance and sed-iment production persisted through-out the latter half of the Cenozoic Era(Elliott, 1960; Bassoullet et al., 1983;Flugel, 1988; Mankiewicz, 1988) asthe mMg ⁄Ca of seawater ascendedfurther into the aragonite nucleationfield (from �3 in Miocene time to 5.2in the modern ocean). Hillis (2001)showed that the abundance of calcar-eous bryopsidalean algae was punctu-ated by a burst of productivity inHolocene time, but he notes that thisis probably an artefact of the highquality of the sedimentary record overthis interval.The emergence of calcareous bry-

opsidalean algae as important produc-ers of carbonate sediments in earlyCenozoic time is based on numerousyet largely qualitative observations byElliott (1960, 1965, 1978, 1981, 1984),Wray (1977), Conrad and Rioult(1977), Bassoullet et al. (1983), Flugel(1988, 1991) and Hillis (1991, 2000,2001). This generally qualitative ap-proach to assessing these algae�s con-tribution to carbonate sedimentationand their evolution in general may be


.............................................................................................................................................................


partly attributable to their tendency todisaggregate rapidly into nondescriptgrains of aragonite shortly after depo-sition on the sea floor (Hillis, 2001),which may preclude a more rigorousand systematic examination of theirfossilized remains.

Experimental evidence

Multiple studies have been publishedover the past several years investigat-ing the effects of seawater Mg ⁄Ca andabsolute Ca2+ on the polymorphmineralogy, primary production andcalcification of calcareous bryopsida-lean algae (Ries, 2005, 2006; Stanleyet al., 2009). The Halimeda incrassata,Penicillus capitatus and Udotea flabel-lum species were investigated in thesestudies because of their pantropicaldistribution (Wray, 1977; Hillis-Colinvaux, 1980) and relatively densecoverage (Bach, 1979; Garrigue,1985), which makes them particularlyimportant producers of carbonatesediments in modern carbonateplatform environments. These stud-ies are reviewed in the followingsection.

Overview of experimental designs

Specimens of Halimeda incrassata(Stanley et al., 2009), Penicillus capit-atus (Ries, 2005) and Udotea flabellum(Ries, 2006) were grown for up to90 days in 10-gallon glass aquariafilled with 30 L of experimental sea-water (Bidwell and Spotte, 1985) for-mulated with Mg ⁄Ca ratios of 1.0–1.5,2.5 and 5.2, corresponding to calcitesea, boundary calcite–aragonite seaand aragonite sea conditions respec-tively. For the experiments onHalimeda, additional experimentalseawaters were employed to investi-gate the effects of absolute [Ca2+].These experimental seawaters wereformulated with identical Mg ⁄Ca ra-tios and differed only in absolute[Ca2+], which was fixed at 25.3, 18.1and 10.2 mM, as well as [Mg2+],which was adjusted to maintain theprescribed Mg ⁄Ca ratio and [Na2+],which was adjusted to offset the pre-scribed variations in [Mg2+] and[Ca2+] so that salinity remained atthe modern value of 35 PSU.The polymorph mineralogy of the

CaCO3 precipitated by the algae wasdetermined by scanning electron

microscopy (SEM) and powder x-raydiffraction (XRD). The proportion ofaragonite-to-calcite was calculatedfrom the ratio of the area under theprimary aragonite peak [d (111):3.39 A; 2h = 26.3�] to the area underthe primary calcite peak [d(104): 2.98–3.03 A; 2h = 29.5–30.0�], using stan-dardized mixtures to calibrate thisrelationship. The Mg ⁄Ca ratio ofcalcite was determined from thed-spacing of the calcite crystal lattice(calibrated with Mg-calcite standards)and confirmed with EDS microprobespot analysis in the SEM.Rates of calcification, linear exten-

sion and primary production werecalculated from the offspring algaethat were produced from the parentalgae via rhizoid extension. Linearextension was determined by directmeasurement. Calcification and pri-

mary production were determinedthrough a standard loss-on-combus-tion method (Heiri et al., 2001).

Mineralogical analysis

Powder X-ray diffraction (XRD) ofthe mineral precipitates (Fig. 4) de-rived from the Halimeda, Penicillusand Udotea offspring algae from thenormal seawater treatments(mMg ⁄Ca = 5.2) confirms that thesealgae produce the majority of theirCaCO3 as aragonite (Halimeda =92% aragonite, 8% Mg-calcite; Peni-cillus and Udotea = 100% aragonite)under these conditions. However,XRD analysis also revealed that allthree species of algae produced aportion of their CaCO3 as low-Mgcalcite (Halimeda = 46%; Penicillus= 22%; and Udotea = 25%) under

A-i A-ii

B-ii

AragoniteAragonite

Aragonite

Aragonite

Aragonite

Aragonite

Calcite Calcite

Calcite

Calcite

B-i

C-i C-ii

Fig. 3 Back-scatter electron images showing the distribution of the aragonite andcalcite precipitated within the interutricular space of segments comprising the thalli ofHalimeda grown in experimental seawaters with mMg ⁄Ca = 5.2 and [Ca2+] =10.2 mM (aragonite seawater; A-i, A-ii), mMg ⁄Ca = 2.5 and [Ca2+] = 18.1 mM

(aragonite-calcite boundary seawater; B-i, B-ii), and mMg ⁄Ca = 1.5 and [Ca2+] =25.3 mM (calcite seawater; C-i, C-ii). Scale bars are 1 lm (from Stanley et al., 2009).


.............................................................................................................................................................


the experimental calcite sea conditions(mMg ⁄Ca = 1.0–1.5; Figs. 3–5). AndHalimeda actually produced smallamounts of high-Mg calcite in theboundary and aragonite sea condi-

tions as well (Figs. 3–5). The propor-tion of calcite produced by theHalimeda alga increased significantly(P <<0.001) as the Mg ⁄Ca ratio ofthe experimental seawater treatmentdecreased into the calcite stability field(Figs 3–5). Furthermore, the mMg ⁄Caratio of the calcite produced by theHalimeda specimens increased propor-tionately (P << 0.001) with themMg ⁄Ca ratio of the experimentalseawater treatment (Fig. 6).Backscatter electron images of the

Halimeda offspring algae from each ofthe seawater treatments reveal thedistribution of aragonite and calciteprecipitates within the interutricularspace of the algae (Fig. 3). The ara-gonite crystals are acicular and euhe-dral, ranging in length from 1 to10 lm, and packed in apparently

random orientations. The calcite crys-tals are rhombic and subhedral, lessthan one micron in diameter andgenerally clustered between the arago-nite bundles. Both mineral phasesexhibit clumped distributions.

Reproduction under experimentalconditions

The total number of offspring algaeproduced by the parent algae variedamongst the different experimentalseawater treatments. In the calcite,boundaryandaragonite seawater treat-ments, Halimeda produced 18, 37 and45 offspring algae, Penicillus produced13, 29 and 16 offspring algae andUdotea produced 16, 17 and 23 off-springalgae respectively.That thealgaegenerally produced fewer offspring inthe experimental seawaters formulatedat lowerMg ⁄Ca ratios suggests that thealgaewere stressedbyproducinga largeportion of their CaCO3 as aragonite inseawater favouring the nucleation ofcalcite. If the precipitation of aragoniteunder such conditions requires extraenergy to manipulate the compositionof the algae�s calcifying fluid (e.g. toelevate Mg ⁄Ca back into the aragonitedomain) to produce aragonite under

25 2726 28 29 30 31

(B)

Calcite standard

mMg/Ca = 5. 2

Cou

nts

mMg/Ca = 2. 5

(D)

(C)

mMg/Ca = 1. 5

(E)

Aragonite standard(A)

Fig. 4 X-ray diffraction patterns for: (A)pure aragonite, revealing primary arago-nite peak [d(111)] at 2h = 26.3� (3.39 A);(B) a Halimeda alga that produced 92%aragonite and 8% calcite when grown inexperimental seawater that favours thenucleation of the aragonite polymorph(mMg ⁄Ca = 5.2; [Ca2+] = 10.2 mM);(C) a Halimeda alga that produced 84%aragonite and 16% calcite when grownin the boundary aragonite-calcite exper-imental seawater (mMg ⁄Ca = 2.5;[Ca2+] = 18.1 mM); (D) a Halimedaalga that produced 54% aragonite and46% calcite when grown in the experi-mental calcite seawater (mMg ⁄Ca= 1.5;[Ca2+] = 25.3 mM); (E) pure calcite,revealing primary calcite peak [d(104);3.01–3.02 A; 2h = 29.6–29.7�] (fromStanley et al., 2009).

Pol

ymor

ph m

iner

alog

y (w

t-%

)

(A)

(B)

(C)

Cal. SW Bound. SW Arag. SW

0 10 20 30 40 50 60 70 80 90

100

0 10 20 30 40 50 60 70 80 90

100

0 10 20 30 40 50 60 70 80 90

100

Arag

Arag Arag

Ca l

Ca l Ca l

Arag

Arag Arag

Ca l

Arag

Arag Arag

Ca l

Seawater composition

Fig. 5 Relative distribution (wt%) of thecalcite and aragonite polymorphs ofCaCO3 precipitated within Halimeda(A), Penicillus (B), and Udotea(C) reared in the experimentalseawaters (mMg ⁄Ca = 1.5, [Ca2+] =25.3 mM; mMg ⁄Ca = 2.5, [Ca2+]= 18.1 mM; mMg ⁄Ca = 5.2, [Ca2+] =10.2 mM), as determined by powderX-ray diffraction. Error bars representinstrument error and variation withinand amongst specimens (from Ries,2005, 2006; Stanley et al., 2009).

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0 1 2 3 4 5 6

mM

g/C

a in

cal

cite

Seawater Mg/Ca ratio (molar)

Fig. 6 Molar Mg ⁄Ca of calcite precipi-tated by Halimeda algae in theexperimental seawaters (mMg ⁄Ca =1.5, [Ca2+] = 25.3 mM;mMg ⁄Ca= 2.5,[Ca2+] = 18.1 mM; mMg ⁄Ca = 5.2,[Ca2+] = 10.2 mM), as determined bypowder X-Ray diffraction and energy-dispersive spectrometry.Mg-fractionationalgorithm (solid curve) is calculated usinga least squares regression and is defined asy = 0.0460x0.899 (R2 =0.996) at 25 �C.Dashed curve is Mg-fractionation curvefor calcite precipitated abiotically fromseawater at 25 �C (y = 0.0482x0.898,R2 = 0.930; Fuchtbauer and Hardie,1976). Error bars represent instrumenterror and variation within and amongstspecimens (from Stanley et al., 2009).


.............................................................................................................................................................


such conditions, this energy may bediverted away fromother physiologicalactivities, such as reproduction andtissue growth.

Rates of calcification, linear extensionand primary production

Rates of calcification (Fig. 7), linearextension (Fig. 8) and primaryproduction (Fig. 9) for the Halimeda,Penicillus and Udotea algae were thehighest (P < 0.05) in the seawatertreatments that favoured nucleationof their aragonitemineral (mMg ⁄Ca =5.2) and the lowest (P < 0.05) in thetreatments that favoured nucleation ofthe calcite mineral (mMg ⁄Ca = 1.0–1.5). These results are consistent withthe hypothesis that the calcite-to-ara-gonite sea transition in early Cenozoictime facilitated the rise of these algae asimportant producers of CaCO3 sedi-ments across that interval of geologicaltime.

Effect of absolute [Ca2+] on linearextension, calcification and primaryproduction in Halimeda

As variations in seawater Mg ⁄Cathroughout the geological past arethought to be partially driven byinverse changes in [Ca2+], it is possi-ble that the positive effects of elevatedseawater Mg ⁄Ca on bryopsidaleancalcification (i.e. favouring nucleationof the algae�s preferred aragonite min-eral) would have been offset by thenegative effects of reduced [Ca2+] [i.e.reducing the CaCO3 saturation state([Ca2+] · [CO3

2)]) of seawater]. Toisolate the effects of [Ca2+] andMg ⁄Ca, the Halimeda algae werereared in an array of experimentalseawaters specifically formulated totest for the effects of [Ca2+] whenMg ⁄Ca is held constant and vice versa(Fig. 10). When mMg ⁄Ca was heldconstant (at 1.5, 2.5 and 5.2), increasesin [Ca2+] from 10.2 to 18.1, to25.3 mM resulted in increased(P < 0.05) rates of linear extension,

calcification and primary production(Fig. 10). And when [Ca2+] was heldconstant (at 10.2, 18.1 and 25.3 mM),increases in mMg ⁄Ca from 1.5 to 2.5,to 5.2 resulted in increased (P < 0.05)rates of linear extension, calcificationand primary production (Fig. 10).However, over the range of valuesthat are thought to have occurredthroughout the geologic history of thebryopsidalean algae, the magnitude ofthe effects of seawater Mg ⁄Ca onlinear extension, calcification andprimary production of the Halimedaalgae was greater than that of [Ca2+].

Discussion

These experiments show that bryops-idalean algae exhibit higher rates ofcalcification, linear extension andprimary production when reared inexperimental seawaters that favournucleation of their preferred aragonitepolymorph of CaCO3 (mMg ⁄Ca >2).

Cal

cific

atio

n (m

g da

y–1)

(A)

(B)

(C)


0.0

0.2

0.4

0.6

0.8

1.0

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7


Fig. 7 Rates of linear extension for Hal-imeda (A), Penicillus (B) and Udotea (C)grown in the experimental calcite,boundary and aragonite seawaters.Rates of linear extension increase signif-icantly (P < 0.05) with increasing sea-water Mg ⁄Ca. Error bars representstandard error (from Ries, 2005, 2006;Stanley et al., 2009).

0.4

0.3

0.2

0.1

0.0

0.5

1.2

1.0

0.8

0.6

0.4

0.2

0.0 0.4

0.3

0.2

0.1

0.0

Line

ar e

xten

sion

(m

m d

ay–1

)

(A)

(B)

(C)

Cal. SW Bound. SW Crag. SW Seawater composition

Fig. 8 Rates of calcification for Hali-meda (A), Penicillus (B) and Udotea (C)grown in the experimental calcite,boundary and aragonite seawaters.Rates of calcification increase signifi-cantly (P < 0.05) with increasing sea-water Mg ⁄Ca. Error bars representstandard error (from Ries, 2005, 2006;Stanley et al., 2009).

Prim

ary

prod

uctio

n (m

g da

y–1)

(A)

(B)

(C)


0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 1.2

1.0

0.8

0.6

0.4

0.2

0.0 0.5

0.4

0.3

0.2

0.1

0.0


Fig. 9 Rates of primary production forHalimeda (A), Penicillus (B) and Udotea(C) grown in the experimental calcite,boundary and aragonite seawaters.Rates of primary production increasesignificantly (P < 0.05) with increasingseawater Mg ⁄Ca. Error bars representstandard error (from Ries, 2005, 2006;Stanley et al., 2009).


.............................................................................................................................................................


This observation is consistent with theassertion that the steady elevation ofseawater mMg ⁄Ca ratios (from 1.0 to5.2) throughout Cenozoic time hasfostered their role as major sedimentproducers in carbonate platform envi-ronments throughout this interval.

Relationship between calcification andprimary production

Although the observed relationshipbetween seawater Mg ⁄Ca and calcifi-

cation of the Halimeda, Penicillus andUdotea algae may be expected, it isless obvious why seawater Mg ⁄Cawould also affect primary productionand linear extension of these algae. Ithas been proposed that some calcare-ous bryopsidalean algae and cocco-lithophores utilize CO2 liberated viacalcification directly in their ownphotosynthesis (Fig. 2A; see equation2; Paasche, 1968; Borowitzka andLarkum, 1976b; Borowitzka, 1977;Sikes et al., 1980; Reiskind et al.,1988, 1989; Ries, 2005, 2006; Stanleyet al., 2005). Thus, elevated rates ofcalcification would increase CO2 with-in the interutricular calcification spaceof the Halimeda, Penicillus and Udo-tea algae (Fig. 2), thereby increasingthe rate of photosynthesis within adja-cent cells, resulting in increased ratesof primary production and linearextension for the algae. While calcifi-cation is certainly not the sole sourceof CO2 for photosynthesis within cal-careous bryopsidalean algae (as manynon-calcifying bryopsidalean algae ex-ist), its role in CO2 liberation may besufficient to explain the observed con-nection between calcification and pri-mary production ⁄ linear extension.The negative impact of low inter-

utricular CO2 on primary production,resulting from reduced calcification inlow Mg ⁄Ca seawater, could have beenpartially offset by the elevated atmo-spheric pCO2 (Berner and Kothavala,2001; Royer et al., 2001, 2004; Yatesand Robbins, 2001; Tyrrell and Zeebe,2004; Pagani et al., 2005) that mayhave accompanied the tectonicallyforced reductions in seawater Mg ⁄Ca.If this offset occurred, then the lowrates of primary production and linearextension observed in the experimen-tal calcite and boundary seawatertreatments of the present study, forwhich pCO2 was fixed at the relativelylow modern value of 385 p.p.m., maynot be applicable to calcareous bry-opsidalean algae inhabiting the poten-tially high-CO2 calcite seas of thegeological past. Under such elevatedpCO2 conditions, photosynthesis bythese algae would likely not have beenlimited by ambient CO2 and thuswould have been less affected byreductions in the amount of CO2

liberated within the algae�s interutric-ular space by calcification. Thus,although their role as carbonate sed-iment producers would have been

diminished under such low Mg ⁄Ca-high pCO2 conditions, they may stillhave been important constituents ofshallow tropical ecosystems if theywere able to resist predation in theirweakly calcified state.An alternative mechanism that

explains why algal linear extensionand primary production would trackcalcification is based on the release ofH+ ions during calcification (seeequation 3; Fig. 2A). In one model,the liberated H+ ions complex withHCO3

) ions within the algae�s interu-tricular space, thus facilitating CO2

extraction by dehydration of H2CO3

within the algal cell (Fig. 2A;McConn-aughey and Whelan, 1997; Hellblomet al., 2001; Hellblom and Axelsson,2003). In another model, H+ ionsliberated by calcification are utilizedby the alga as symporters or co-trans-porters of HCO3

) and nutrients, suchasNO3

) andPO4)3, across the algal cell

wall (Fig. 2A; Price and Badger, 1985;Price et al., 1985; McConnaughey andWhelan, 1997; Hellblom et al., 2001).Increased rates of assimilation of thesetypically limiting substrates couldeffectively increase the algae�s rates ofphotosynthesis and primary produc-tion as their rates of calcificationincrease.

Mg ⁄Ca ratio versus CaCO3 saturationstate

The results of the study on Halimedareveal that both elevated Mg ⁄Caratios and elevated [Ca2+] promotecalcification, primary production andlinear extension within this alga. Theelevated Mg ⁄Ca ratios evidentlytranslate into higher rates of calcifica-tion by creating ambient chemicalconditions favourable for the precip-itation of the alga�s preferred arago-nite biomineral. Elevated [Ca2+]probably fosters higher rates of calci-fication by increasing the CaCO3 sat-uration state of the alga�s ambientseawater.Over the range of mMg ⁄Ca ratios

(1.0–5.2) and absolute [Ca2+] (10.2–25.3 mM) that are believed to haveoccurred throughout Phanerozoictime, the favourable effects of elevatedMg ⁄Ca on bryopsidalean algal calcifi-cation are generally greater in magni-tude than the unfavourable effects ofreduced CaCO3 saturation statecaused by concomitant reductions in

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0.0 0

Ca2+ = 25.3 mM

Ca2+= 18.1 mM

Ca2+ = 10.2 mM

Ca2+ = 25.3 mM

Ca2+ = 18.1 mM

Ca2+ = 10.2 mM

Ca2+ = 25.3 mM

Ca2+ = 18.1 mM

Ca2+ = 10.2 mM

1.4

1.2

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(A)

(B)

(C)

Line

ar e

xten

sion

(m

m d

ay–1

)P

rimar

y pr

oduc

tion

(mg

day–1

) C

alci

ficat

ion

(mg

day–1

)

Seawater Mg/Ca ratio (molar)

1 2 3 4 5 6

0 1 2 3 4 5 6

0 1 2 3 4 5 6

Fig. 10 Rates of linear extension (A),calcification (B) and primary production(C) for Halimeda grown in the nineexperimental seawaters formulated toisolate the effects of seawater Mg ⁄Caand [Ca2+]. Rates of linear extension,calcification and primary productionincrease significantly (P < 0.05) withboth increasing seawater Mg ⁄Ca([Ca2+] fixed) and increasing seawater[Ca2+] (Mg ⁄Ca fixed). Rates of linearextension, calcification and primary pro-duction also increase significantly(P < 0.05) with elevations in seawaterMg ⁄Ca that are formulated withgeologically realistic (Hardie, 1996;Demicco et al., 2005) reductions in[Ca2+] (circumscribed data). Error barsrepresent standard error (from Stanleyet al., 2009).


.............................................................................................................................................................


[Ca2+]. Thus, Mg ⁄Ca ratio appears tobe the primary determinant of howcalcareous bryopsidalean algae willrespond to calcite–aragonite sea tran-sitions. However, it should be notedthat at least one scenario was identi-fied in which increasingly favourableMg ⁄Ca ratios were outweighed byincreasingly unfavourable CaCO3 sat-uration states (via decreasing [Ca2+]),in terms of their relative effects oncalcification rate. This was evident(Fig. 10) when experimental seawaterconditions shifted from mMg ⁄Ca =1.5, [Ca2+] = 25.2 mM to mMg ⁄Ca= 2.5, [Ca2+] = 10.2 mM.

Biomineralogical control

The observation that the Halimeda,Penicillus and Udotea algae each pre-cipitate the majority of their CaCO3 asthe aragonite polymorph in the exper-imental calcite seawater suggests thatthese algae exhibit some control overthe Mg ⁄Ca ratio of their interutricularcalcifying fluid. Yet because, as thesealgae commence producing a portionof their CaCO3 as the kineticallyfavoured calcite polymorph undersuch conditions, it is evident that theirbiomineralogical control can be par-tially overridden by ambient seawaterMg ⁄Ca.The distribution of aragonite and

calcite clusters precipitated withinHalimeda (Fig. 3), Penicillus and Udo-tea grown in the experimental calciteseawater occurs on a spatial scale thatis comparable to that of the purportedacid and alkaline zones within thesealgae (De Beer and Larkum, 2001).Both conditions may reflect the algae�sspatially limited control over thechemical milieu of their interutricularfluid.

It has been suggested that Halimedaalgae control calcification solelythrough pH regulation (Borowitzka,1987; De Beer and Larkum, 2001).If this assertion is correct, thenHalimeda algae grown in the experi-mental calcite seawater should precip-itate exclusively calcite which they didnot. De Beer and Larkum�s (2001)conclusion that Ca2+ is not activelytransported into the interutricularspace of Halimeda is based on theirobservation that the alga�s rate ofcalcification remains unaffected byinhibition of the Ca-ATPase enzyme.While their findings show that Hali-meda are not actively transportingCa2+ into the calcifying space, it isconceivable that Halimeda, as well asPenicillus and Udotea, pumps Ca2+

out of the interutricular space, therebymaintaining the Mg ⁄Ca ratio of cer-tain regions of the algae�s interutricu-lar space within the aragonitenucleation field (mMg ⁄Ca > 2).Alternatively, the drawdown of Ca2+

via calcification (Fig. 2A) may also besufficient to maintain the Mg ⁄Ca ofthe interutricular fluid at an elevatedsteady-state (favouring precipitationof aragonite), despite low ambientMg ⁄Ca. These scenarios, of course,require that the CaCO3 saturationstate of the interutricular fluid is main-tained at a level sufficient to promotecalcification, even after Ca2+ is re-duced via cation transport or calcifi-cation, perhaps by increasing [CO3

2)]by removing CO2 via photosynthesis(Fig. 2A; Borowitzka, 1982b, 1987) orby increasing pH through H+-pump-ing (Fig. 2A; De Beer and Larkum,2001). Alternatively, the same out-come could be achieved by activelytransporting Mg2+ ions into thealgae�s interutricular space, thereby

elevating the Mg ⁄Ca ratio into thearagonite nucleation field. However, amechanism capable of such rapidtransport of Mg2+ across the algalcell wall is yet to be identified in thebryopsidalean algae.

Comparison of biomineralogicalcontrol amongst Halimeda, Udoteaand Penicillus

The degree of biomineralogical con-trol appears to vary amongst the threegenera of calcareous bryopsidaleanalgae, with Halimeda exerting the leastcontrol and Penicillus and Udotea themost. This is evidenced by the obser-vation that the Halimeda algae (Stan-ley et al., 2009) produced 46 (±8)wt% calcite in the experimental calciteseawater treatment, whereas Penicillus(Ries, 2005) and Udotea (Ries, 2006)produced only 22 (±3) and 25 (±3)wt% of their CaCO3 as calcite in theexperimental calcite seawater. Morelimited biomineralogical control byHalimeda is also evidenced by thesurprising observation that it pro-duced a portion of its CaCO3 asmagnesian calcite even in the bound-ary [16.2 (±1.8) wt%] and experimen-tal aragonite [8.1 (±1.9) wt%]seawaters (Figs 3–5). Penicillus andUdotea, in contrast, precipitatedexclusively aragonite under these con-ditions (Table 1). Furthermore, theMg2+ fractionation pattern for calciteprecipitated by the Halimeda algae inthe various seawater treatments(Fig. 6) mimics Mg2+ incorporationin abiotically precipitated calcite(Fuchtbauer and Hardie, 1976,1980), supporting the assertion thatprecipitation of calcite by the Halime-da algae proceeds in an uncontrolled,nearly abiotic manner.

Table 1 Summary of mineralogy, linear growth, calcification and primary productivity for Halimeda incrassata, Penicillus

capitatus and Udotea flabellum grown in experimental seawater treatments formulated at differing Mg ⁄Ca ratios.

Alga SW mMg ⁄ Ca*

Mineralogy

(%cal:%arag)

Calcification ±SE

(mg day)1)

Linear extension ±SE

(mm day)1)

Primary production ±

SE (mg day)1) Study

Halimeda incrassata 5.2 8: 92 ± 2 0.83 ± 0.07 0.41 ± 0.04 0.73 ± 0.02 Stanley et al., 2009



Penicillus capitatus 5.2 0: 100 ± 3 0.70 ± 0.06 1.00 ± 0.11 0.87 ± 0.10 Ries, 2006



Udotea flabellum 5.2 0: 100 ± 3 0.55 ± 0.04 0.29 ± 0.05 0.38 ± 0.05 Ries, 2005



*mMg ⁄ Ca = 1.0, [Ca2+] = 31.6 mM; mMg ⁄ Ca = 1.5, [Ca2+] = 25.3 mM; mMg ⁄ Ca = 2.5, [Ca2+] = 18.1 mM; mMg ⁄ Ca = 5.2, [Ca2+] = 10.2 mM.


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Analysis of nuclear-encoded ribo-somal DNA reveals that the Penicillusand Udotea algae are more closelyrelated to each other than they are totheHalimeda algae (Verbruggen et al.,2009). The phylogenetic relationshipsamongst these algae are consistentwith their apparently varying degreesof biomineralogical control.Nonetheless, the observation that

three genera of bryopsidalean algae,belonging to two separate families(udoteacea and halimedacea), eachexhibited highly similar responses toreductions in seawater Mg ⁄Ca – interms of their rates of calcification,primary production and linear exten-sion and their control over polymorphmineralogy – suggests that these re-sponses are indeed representative ofmost aragonite-secreting algae as-signed to this order.

Palaeoecological implications

The results of the experimental studiessuggest that the predominant carbon-ate-producing bryopsidalean algae –Halimeda, Penicillus and Udotea –would have been slower growing,smaller and less calcified during calciteseas of the geological past. Suchgeochemically induced reductions inthe fitness of these algae would havehad important ecological implicationsfor these algae and for carbonateplatform environments, in general.Their slower growth rates and smallersize would have reduced their abilityto compete for space and sunlight onthe substrate-limited shallow tropicalseafloor; and their reduced calcifica-tion would have rendered them moresusceptible to predation by grazingfish, which, in modern aragonite seas,are largely deterred by the algae�s highCaCO3 content (Hay et al., 1994). Thealgae�s contribution of biogenicCaCO3 to shallow tropical carbonateplatforms would have been compara-bly diminished by such reductions incalcification, primary production andpopulation density during calcite seaintervals.Needless to say, such extrapolation

from the laboratory aquarium to thegeological past assumes that the mod-ern Halimeda, Penicillus and Udoteaspecies employed in these experimentsare sufficiently representative of theancient species and that these ancientspecies were not better adapted for

producing aragonite, or even calcite,in seawater favouring the precipita-tion of calcite.

Additional factors contributing toincreased carbonate sedimentation bybryopsidalean algae in early Cenozoictime

Resistance to herbivory is an impor-tant determinant of the distributionand abundance of calcareous bryop-sidalean algae. The two main defencesemployed by these algae to deterherbivory are calcification and pro-duction of secondary metabolic toxins(see Hay et al., 1994 for review).Although the timing of the evolutionof toxic compounds within calcareousbryopsidalean algae is not known, it ispossible that this contributed to theirincreased abundance and sedimentproduction in early Cenozoic time.Alternatively, increased predationpressure in early Cenozoic time (e.g.from the diversification of reef fish inEocene time; Bellwood, 1996) mayhave given algae that possessed de-fences such as calcification and toxicitya competitive advantage. Increasedcarbonate production by these algaein early Cenozoic time may have alsoresulted from the existence of warm,greenhouse conditions at that time(Pagani et al., 2005), which wouldhave favoured the nucleation of thearagonite mineral (Morse et al., 1997),and enhanced the primary productiv-ity of tropical marine algae, in general.However, none of these variablesshould have continuously fosteredelevated rates of carbonate sedimentproduction by the bryopsidalean algaethroughout the latter half of the Ceno-zoic Era. Only seawater Mg ⁄Ca, whichcontinued ascending further into thearagonite stability field throughoutCenozoic time, is consistent with thebryopsidalean algae�s late Neogeneapex in carbonate sediment produc-tion (Hillis, 2001).

Conclusions

1 The mMg ⁄Ca ratio of seawater hasvaried between approximately 1.0and 5.2 throughout Phanerozoictime. This is evidenced from thecomposition of fluid inclusions inprimary marine halite, the Mg con-tent of fossil echinoids and molluscs

and synchronized transitions in themineralogy of ooids and marinecements (aragonite and high-Mgcalcite vs. low Mg calcite) and latestage marine evaporites (MgSO4 vs.KCl).

2 A mid-ocean ridge hydrothermalbrine ⁄ river water mixing modeldriven by global rates of oceancrust production predicts fluctua-tions in seawater Mg ⁄Ca ratiosthroughout Phanerozoic time thatare consistent with the geologicalrecord of seawater Mg ⁄Ca (i.e. fluidinclusions, Mg-contents of echi-noids and molluscs and primarymineralogy of abiotic CaCO3 depos-its and marine evaporites). Thissuggests that the principal tenantsof the model are correct and thatseawater Mg ⁄Ca has generally var-ied inversely with the global rate ofocean crust production.

3 When seawater mMg ⁄Ca was great-er than 2, precipitation of the ara-gonite and high-Mg calcitepolymorphs was favoured. Whenseawater mMg ⁄Ca was less than 2,precipitation of low-Mg calcite wasfavoured. This relationship is re-flected in the primary polymorphmineralogy of ooids and marinecements and in the skeletal miner-alogy of the major reef-building andsediment-producing calcareousmarine organisms throughoutPhanerozoic time.

4 Today, calcifying bryopsidaleanalgae are among the most impor-tant contributors of aragonitesediments to carbonate platformenvironments. These aragonite-secreting algae assumed theirimportant sediment-producing rolesin early Cenozoic time, coincidentwith the most recent transition fromcalcite-to-aragonite seas. Signifi-cantly, they retained their sedi-ment-producing roles throughoutthe remainder of Cenozoic time, asseawater continued to rise furtherinto the aragonite stability field.However, this trend is based largelyon qualitative descriptions of thealgae�s contribution to Cenozoiclimestones. Evaluation of thesetrends in the context of thecalcite–aragonite sea hypothesiswould be substantially improvedby a more quantitative assessmentof the algae�s geological record ofsediment production. This repre-


.............................................................................................................................................................


sents an important area of futureresearch.

5 Experiments on modern Halimeda,Penicillus andUdotea algae revealedthat their rates of calcification,primary production and linearextension declined in experimentalseawaters formulated with reducedMg ⁄Ca ratios that favour nucle-ation of the calcite polymorph overthe algae�s preferred aragonite poly-morph. Assuming that these mod-ern algae mimic the response ofancient related taxa to modifiedseawater Mg ⁄Ca, these experimen-tal studies suggest that calcareousbryopsidalean algae would havebeen smaller, less abundant, lesscompetitive for space on the sea-floor and less resistant to grazingwhen seawater Mg ⁄Ca did notfavour their inherently aragoniticmineralogy. This is consistent withthe assertion that a shift from cal-cite-to-aragonite seas in early-to-middle Cenozoic time enabled thearagonite-secreting bryopsidaleanalgae to flourish and to becomethe important producers of CaCO3

sediments that they are today.6 Experiments on Halimeda revealed

that the elevation of Mg ⁄Ca and[Ca2+] both result in increasedrates of calcification, primary pro-duction and linear extension. Dur-ing calcite seas intervals, lowMg ⁄Ca would have been accompa-nied by relatively high [Ca2+].Thus, their effects on algal calcifi-cation, primary production andlinear extension would have par-tially offset each other. However,the experiments revealed that overthe range of coupled seawaterMg ⁄Ca ratios and [Ca2+] that arebelieved to have occurred through-out the geological history of thebryopsidalean algae, seawaterMg ⁄Ca was probably the control-ling variable. Simultaneous, inversevariations in [Ca2+] appear only tomoderate the effects of seawaterMg ⁄Ca.

7 The concomitant variations in cal-cification, primary production, andlinear extension of the Halimeda,Penicillus and Udotea algae suggestthat there are important connec-tions amongst these processes with-in the algae. Seawater Mg ⁄Caappears to directly influence calcifi-cation via CaCO3 polymorph com-

patibility. Calcification, in turn,may influence primary productionand linear extension by liberatingCO2 for photosynthesis and ⁄or sup-plying H+ ions for various cellularfunctions that support photosyn-thesis, such as the transcellular pro-ton-shuttling of nutrients or HCO3

)

and the formation of intracellularH2CO3, from which CO2 can beefficiently extracted via dehydra-tion.

8 Halimeda, Penicillus and Udoteaeach produced a portion (<50%)of their CaCO3 as the calcite poly-morph in the experimental calciteseawater. This indicates that thealgae�s biomineralogical controlcan be partially overridden byambient seawater chemistry andsuggests that these algae may haveproduced a mixture of aragoniteand calcite throughout Cretaceoustime, when ocean chemistry fa-voured nucleation of calcite ratherthan aragonite (mMg ⁄Ca < 2).Nonetheless, the observation thatthe algae precipitated the majorityof their CaCO3 as aragonite inexperimental seawater that favoursthe precipitation of calcite indicatesthat these algae must actively spec-ify nucleation of the aragonite poly-morph. This may be accomplishedby controlling Mg ⁄Ca of their in-terutricular fluid through cationpumping or with chemical and ⁄ormechanical templates that specifynucleation of the aragonite poly-morph (Borowitzka, 1987). Regard-less of the mechanism, theobservation that calcification, pri-mary production, linear extensionand reproduction each declined forthe algae reared under calcite seaconditions suggests that their activespecification of the aragonite poly-morph in mineralogically unfavour-able seawater comes at a substantialenergetic cost.

9 The similarity amongst the re-sponses of the three genera of bry-opsidalean algae (belonging to twoseparate families) to the experimen-tal calcite seawater – i.e. reducedrates of calcification, primaryproduction and linear extensionand partial precipitation of low-Mg calcite – suggests that theseresponses are representative of mostaragonite-secreting algae assignedto this order.

Ackowledgments

The author is grateful to Rachel Wood andBrian Pratt for critically reviewing thismanuscript.

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Received 18 March 2009; revised versionaccepted 12 June 2009


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