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Genesisofmicrobialitesascontemporaneousframeworkcomponentsofdeglacialreefs,Tahiti(IODP310)

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Facies (2010) 56:337–352

DOI 10.1007/s10347-009-0207-3

ORIGINAL ARTICLE

Genesis of microbialites as contemporaneous framework components of deglacial coral reefs, Tahiti (IODP 310)

H. Westphal · K. Heindel · M. Brandano · J. Peckmann

Received: 25 August 2009 / Accepted: 31 October 2009 / Published online: 11 December 2009© Springer-Verlag 2009

Abstract Deglacial reefs from Tahiti (IODP 310) featurea co-occurrence of zooxanthellate corals with microbialitesthat compose up to 80 vol% of the reef framework. Thenotion that microbialites tend to form in more nutrient-richenvironments has previously led to the concept that suchencrustations are considerably younger than the coralframework, and that they have formed in deeper storeys ofthe reef ediWce, or that they represent severe disturbances ofthe reef ecosystem. As indicated by their repetitive inter-bedding with coralline red algae, the microbialites of thisreef succession of Tahiti, however, formed immediatelyafter coral growth under photic conditions. Clearly, thedeglacial reef microbialites present in the IODP 310 coresdid not follow disturbances such as drowning or suVocationby terrestrial material, and are not “disaster forms”. Giventhat the corals and the microbialites developed in closespatial proximity, highly elevated nutrient levels caused byXuvial or groundwater transport from the volcanic hinter-land are an unlikely cause for the exceptionally voluminousdevelopment of microbialites. That voluminous deglacialreef microbialites generally are restricted to volcanicislands, however, implies that moderately, and possibly epi-sodically elevated nutrient levels favored this type ofmicrobialite formation.

Keywords Tahiti · IODP 310 · Microbialites · Reef development · Nutrients

Introduction

Whereas modern stromatolites have been studied fordecades (e.g., Black 1933; Logan 1961; Dravis 1983; Reidet al. 1995), only later did modern microbialites in coralreefs become the subject of scientiWc study (Land andMoore 1980; Montaggioni and Camoin 1993; Webb andJell 1997). Despite the increase in knowledge of the struc-ture and diversity of microbialites and the ecological condi-tions favoring their occurrence, the biological processesand the exact mechanisms of formation are still far frombeing fully understood (Arp et al. 2008).

Microbialites are organosedimentary deposits that arelayered, massive, domal or dendritic, and have precipitatedas a result of microbiological activity or trapping and bind-ing of detrital sediment; the term microbialite describes thelithiWed product. The role of microbes in the formation ofmicrobial crusts is still under debate and is certainly quitevariable for diVerent microbiological communities andprecipitates (e.g., Babel 2004; Jenkins et al. 2008; Sanz-Montero et al. 2008). In particular, the ecological conditionsleading to the formation of microbialites encrusting shallow-water tropical coral reefs is still enigmatic, given that suchcorals prosper under euphotic, oligotrophic conditions,whereas microbialite formation is thought to be favored byelevated trophic levels (Hallock and Schlager 1986; Brachertand Dullo 1991; Dupraz and Strasser 2002). One reason forthe slow progress in understanding reefal microbialites is thescarcity of modern analogs (cf. Camoin et al. 1999).

In Earth history, microbialites commonly overgrow orsucceed framework builders and thus have been interpreted

H. Westphal (&) · K. Heindel · J. PeckmannMARUM, Center for Marine Environmental Sciences, Universität Bremen, Leobener Straße, 28359 Bremen, Germanye-mail: hildegard.westphal@uni-bremen.de

M. BrandanoDipartimento di Scienze della Terra, Università di Roma “La Sapienza”, Ple Aldo Moro, 5, 00185 Rome, Italy

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to represent shifts in ecological conditions (e.g., Whalenet al. 2002; Adachi et al. 2007). The notion that elevatedtrophic conditions favor microbialite development wassuggested by several lines of evidence. For example, inDevonian strata, oligotrophic taxa (stromatoporoids) arereplaced by mesotrophic taxa (tabulate and rugose corals)that are accompanied by microbialites (Whalen et al. 2002).However, coeval growth of corals and microbialites hasalso been described, e.g., from Jurassic (Olivier et al. 2004;Dupraz and Strasser 2002) and Miocene coral reefs (up to80 vol% microbialites in the coral framework; Riding et al.1991).

Modern tropical shallow-water reefs usually feature onlyminor, mostly cryptic microbialite crusts (Reitner et al.1995; Webb and Jell 1997; Webb et al. 1998). In contrast,numerous Pleistocene to Early Holocene deglacial reefs areencrusted by large volumes of microbialites. In suchpostglacial reefs, microbialites were Wrst reported fromTahiti (<7 ka: Camoin and Montaggioni 1994) and sincehave been described in a variety of environmental andoceanographic settings (see references in Cabioch et al.2006). Nonetheless, voluminous microbialites in reefs seemto be restricted to settings with a volcanic hinterland(Cabioch et al. 1999).

In documenting the occurrence and nature of microbia-lites in one illustrative succession, the results of this studyprovide insights into the environmental signiWcance ofmicrobialites, the relative timing of coral framework devel-opment and microbialite encrustation, and how the ecologi-cal prerequisites of corals and microbialite growth can bereconciled. A better understanding of the environmental fac-tors leading to microbialite formation is required to utilizethe microbialites themselves as paleoenvironmental archives.

Study area and material: the deglacial reef sequence of Tahiti

Tahiti, located at 17°50�S and 149°20�W in the centralPaciWc Ocean (French Polynesia, Society Archipelago) wastargeted during IODP Expedition 310 to reconstruct thedeglacial sea-level rise back to the last glacial maximum(LGM; Camoin et al. 2007a). IODP 310 also aimed at iden-tiWcation of short-term paleoclimatic and paleoceano-graphic changes associated with the last deglacial sea-levelrise and corresponding changes in reef growth and geome-try. To recover the deglacial reef succession, drownedPleistocene to Early Holocene reef terraces seaward of themodern barrier reef were drilled (Fig. 1; Expedition 310Scientists 2006).

The deglacial (post-LGM) succession accumulated athickness of 25–45 m prior to the drowning (Camoin et al.2007a). Drowned reefs form distinctive submarine ridges in

two depth intervals, an inner ridge at around 60 m belowsea level (m b.s.l.) and an older, outer ridge at around90–100 m b.s.l. (Fig. 2; Camoin et al. 2007b). The deglacialcoral reef framework is heavily encrusted by microbialites,in many cases preceded by coralline algal crusts.The microbialites usually show a laminated Wrst stage orencrustation, in many cases succeeded by crusts of a

Fig. 1 Location of drilling sites oV Tahiti (slightly modiWed afterCamoin et al. 2003). The numbered black dots (e.g., 9B) represent theIODP 310 drill sites. The dashed line indicates the approximate posi-tion of the seismic line shown in Fig. 2

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dendritic growth habit (Camoin et al. 2007b). Most of thereef framework is preserved in growth position. This in situreef framework of two sites is studied here, site Tiarei inthe north, site Mara’a in the south of the island of Tahiti,that were drilled in water depth between 41.6 and 117.5 m(Figs. 1, 3).

The Pleistocene to Holocene deglacial reef successionon the slopes of Tahiti diVers from its modern counterpartby its unusual and outstanding quantity of microbial crusts(up to 80 vol%) largely that occlude the primary macropo-rosity of the coral reef (Camoin et al. 1999; Expedition 310Scientists 2006). It has been suggested that this abundance

of microbialites in the deglacial reefs oV Tahiti could be aresult of environmental change accompanying the rapid lastdeglacial sea-level rise (Camoin et al. 1999, 2006).

Methods

Within the IODP procedure during the onshore scienceparty, the microbialites were described in terms of colorand morphology (laminated, dendritic, domal) and abun-dance of encrusted material (Camoin et al. 2007b). Thoseinitial descriptions are reWned in this study.

Fig. 2 Seismic line crossing the Tiarei sites (approximate posi-tion of line is marked in Fig. 1). Two drowned reef tracts are visible, an inner ridge (drowned reef 1; water depth about 60 m b.s.l.) and an older outer ridge (drowned reefs 2 and 3; water depth 90–100 m b.s.l.). Volcano-clastic sediment bodies (marked by blue and green) cover large parts of the sea Xoor around the drowned reefs. (Seismic data is from the site survey (Camoin et al. 2003) as provided on the IODP Site Survey Data Base Web site: http://ssdb.iodp.org.). TWT two-way travel time

Fig. 3 Thickness of deglacial reef sequence for the sites Mara’a and Tiarei drilled during IODP expedition 310

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For petrographic analysis, in addition to 18 regular-sizedthin-sections, 20 16 £ 8 cm thin-sections provided impor-tant perspectives on the coral-to-encrusters succession.Thin-sections have been partially stained with Feigl’s solu-tion for the optical identiWcation of aragonitic components.Fluorescence microscopy was performed on a Zeiss Axio-skop 40 optical microscope (lamp: HBO 50; Wlters: BP 365/12 FT 395 LP 397 and BP 450–490 FT 510 LP 515).

For scanning electron microscopy (SEM) analysis, oneset of samples was mounted with the growth direction per-pendicular to the stub to examine the grown surface of themicrobialite. The other set was mounted with the growthdirection parallel to the stub for examination of the layer-ing. The samples of this second set were cut and polished,etched for 20 s with 0.1 N HCl, and subsequently cleanedin an ultrasonic bath. The gold-coated samples were studiedunder a Weld emission scanning electron microscope (ZeissSUPRA 40). An EDX device was used to determine ele-mental composition. Carbonate mineralogy was determinedby X-ray diVractometry (XRD) of ground microbialitepowder in a Bragg–Brentano diVractometer. The measuringrange was 25–40° with a Cu K� cathode.

For estimating growth rates of microbialites, two 14C agedates have been determined for a laminated microbialitefrom site Mara’a using the AMS 14C method (Czernik andGoslar 2001) at the Poznaj Radiocarbon Laboratory(Poland). The two samples were taken at the base and thetop of the 4-cm-thick crust (sampling distance 0.37 cm).The calibration of the AMS 14C ages to calendar years withthe software CALIB REV 5.0.1 (Stuiver and Reimer 1993)used the marine calibration dataset marine04.14c (Hughenet al. 2004) with adjustment to the regional reservoir age�R = 82 § 42 (�R = deviation from the average global res-ervoir age of »400 years; Stuiver and Braziunas 1993). Theregional reservoir age of Moorea, French Polynesia is409 years (CHRONO marine reservoir database).

Results

Macroscopic description

The deglacial succession consists of a coral reef frameworkin growth position without sedimentological breaks. Thecoral framework is heavily encrusted by various organisms.In many cases, coralline algal crusts form the Wrst stage ofencrustation (Fig. 4). Locally, vermetid gastropods are

Fig. 4 Core photographs of the deglacial reef sequence from Mara’aand Tiarei. Note that in the cores from the Tiarei, which is situatedclose to the river mouth of the Papenoo River, the microbialites aremuch darker and show more dendritic growth patterns than those fromMara’a (photographs are from the IODP database)

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present between the individual algal thallus layers. A greymicrobialite crust of 2 cm to up to 15 cm thickness is thelatest stage of encrustation. Microbialites compose up to 80vol% of the reef framework. In most cases, the initial partof the microbialite crusts is laminated (Fig. 5a–e), and maybe succeeded by dendritic structures (Fig. 5d, f). Themicrobialites developed on all sides of their substrate;upward growth, however, is dominant (Fig. 5a). Withinmicrobialites, carbonate grains such as Halimeda plates aretrapped and enclosed (Fig. 5b, c). The corals and red algaethat provide the substrate for the microbialite show markedmacrobioerosion (Fig. 4).

At Tiarei, close to the Papenoo River, dark grey den-dritic microbialites are dominant, reXecting the higher con-tent of incorporated volcanic detritus (Fig. 5d, f). AtMara’a, the microbialites are lighter colored and usuallyshow the laminated growth habit (Fig. 5a–c). These obser-vations are reXected by the lower average carbonate con-tents for microbialites from site Tiarei (average: 74%) thanfor those from site Mara’a (average: 94%; Heindel et al.2009a).

The corals in the reef framework are largely preserved ingrowth position as indicated by red algal crusts that arethickest on the upper surfaces of the corals. Reworkeddebris is rare. This rather uncommon appearance of shal-low-water coral reefs, which usually tend to be partlydestroyed by hurricanes, points to early stabilization byencrusting microbialites, preserving a “reef in aspic”.

Light microscopic observations

The microbialites show a micritic fabric, and in most cases,a clotted to peloidal texture (Fig. 6) and large amounts ofincorporated aragonite grains are common. Volcanoclasticgrains (crystals, glass, lithoclasts) are prevalent, and moreso at Tiarei than at Mara’a. Corals and red algae arestrongly bioeroded. The macroscopically conspicuous lami-nation of the microbialites is faint and vague under the lightmicroscope, but is reXected in varying abundance of vol-canoclastic grains. The light-colored laminae in the lami-nated microbialites are more strongly Xuorescent than thedark laminae, indicating a higher content of organic matter.Volcanoclastic and carbonate grains occur in microbialitesgrowing downwards.

The microbialites succeed the coral colonies directly orencrust intercalated coralline red algae. The coralline algalcrusts consist of a successive overgrowth of planar to wartycoralline algae thalli intercalated by vermetid gastropodsand encrusting homotrematid, acervulinid, and victoriellidforaminifera (Gypsina, Acervulina, Carpentaria). The coral-line algal crusts are up to 5 mm thick and are composed ofHydrolithon, Lithophyllum, Mesophyllum, Lithoporella, andLithothamnion. The associations from the lower to middle

part of the succession tend to be dominated by Lithoporellaand Mesophyllum. In samples from the base of the succes-sion, the corals are encrusted by thick layers (up to 5 mm) ofHydrolithon with a sharp contact with the microbialite.Here, the coralline algal crust thalli are thicker (up to 2 mm)at the base of the red algal crusts, and become thinner (to upto 50 �m) and more contorted towards the top of the crusts.Hydrolithon of the subfamily Mastophoroideae character-izes the euphotic zone with water depths <10 m and is abun-dant in reef crests and uppermost reef slopes exposed tostrong wave action; it also occurs on forereef slopes at morethan 30 m water depth (Adey 1986; Bosence 1983; Aguirreet al. 2000; Flamand et al. 2008). Here, however, the thickHydrolithon thalli indicate that the water depth at the base ofthe succession was very shallow. A deepening trend is indi-cated by the shift in associations to Lithoporella (co-occur-rence with corals in mesophotic environments) andLithothamnion and Mesophyllum (subfamily Melobesioi-deae, abundant in forereef environments indicating euphoticto oligophotic conditions; Adey 1986; Bosence 1983;Aguirre et al. 2000; Flamand et al. 2008; Fig. 7).

The petrographic series of encrustations is more com-plex than it appears macroscopically. At the base of indi-vidual microbialite crusts, red algal thalli (mainly contortedLithothamnion sp.) are repeatedly interlayered by microbialcrusts (Fig. 5). Interlayering of microbialite with the veryshallow, euphotic coralline alga Hydrolithon has not beenobserved. Interlayering of microbialites and red algae hasonly been observed in laminated microbialites, not indendritic ones.

SEM observations

Mara’a site

The ultrastructure of the microbialites is micritic and isdominated by peloidal aggregates uniformly composed ofirregular scalenohedral to dog-tooth-shaped crystals(Fig. 8a). The samples from the Mara’a site incorporateabundant grainy material. Whereas they incorporate onlylittle volcanoclastic detritus in the microbialites, abundantchips of coral skeletons produced by the boring spongeCliona make up as much as 50% of the surface of thesamples examined under the SEM (Fig. 8b).

Carbonate fabrics that can be recognized unequivocallyas of microbial origin are rare. Random to spherical aggre-gates made of Xaky crystals, representing authigenic clayminerals, are sparse (Fig. 8c; identiWcation of Al by EDXconWrms that the Xaky grains are composed of clay miner-als). They are reminiscent of microbially induced clay min-erals (cf. Konhauser 2009). Some of the samples fromMara’a contain abundant pyrite in pores of the microbia-lites (Fig. 8d). In laminated microbialites, thin layers of red

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algal thalli occur interlayered in the microbialites close totheir surface (Fig. 8e, f).

Tiarei site

In many cases where the microbialites directly encrust coralskeletons, the contact is a surface shaped by the activity of theboring sponge Cliona (Fig. 9a). Borings in corals usually areinWlled by microbialite. Abundant volcanoclastic and carbon-ate grains are encrusted in the microbialites, and Cliona chipsof coral skeletons are commonly incorporated (Fig. 9b).

The microbialites are composed of peloidal aggregatesmade of irregular scalenohedral to dog-tooth-type carbon-ate grains, commonly enclosing incorporated grains(Fig. 9b). Random and spherical aggregates composed ofXaky authigenic clay minerals reminiscent of microbiallyinduced clay minerals are more common in the Tiarei sam-ples than in the Mara’a samples. In some cases these aggre-gates apparently have formed subsequent to the growth ofthe microbial crusts (Fig. 9c, d). Other putative microbialfabrics include chains of calcium carbonate aggregatesresembling cells (Fig. 9e). Radial carbonate spherulites thattend to show syntaxial cements are possibly of a biologicalorigin; however, it is unclear what they represent (Fig. 9f).Pyrite framboids are rare in the samples from site Tiarei.

Whereas the uppermost millimeters of the microbialitesare highly porous, immediately below this zone the micro-structure gets much tighter. Here, original porosity isinWlled by micritic cements, leading to early lithiWcation.This addition of early cement potentially dilutes primarygeochemical signals.

Carbonate mineralogy

X-ray diVractometry measurements reveal that the micro-bialites are composed of high-Mg calcite (HMC) with anMgCO3 content of 15.6–16.6 mol%. The HMC of some

dendritic microbialites from the Mara’a site contain up to17.3 mol% MgCO3. This spread is much narrower than pre-viously reported ranges of MgCO3 contents (7–16 mol%;Camoin and Montaggioni 1994; Camoin et al. 2006). Themicrobialites show strongly variable aragonite contentsranging from 38 to 68 vol% of the total calcium carbonate.Low amounts (<2 vol%) of protodolomite are observed.

Radiocarbon ages

The calibrated and corrected 14C ages of the samples fromthe base and top of a laminated microbialite from siteMara’a give an age diVerence of about 540 years (base:12,848–12,935 cal. years BP, top: 13,331–13,506 cal yearsBP; Table 1).

Discussion

Age diVerence between corals and microbialites

For reconstructing the environmental conditions of themicrobialite formation, the relative timing between coralgrowth and microbial encrustation is of great interest, espe-cially for constraining the possible role of changing photic,trophic, and energetic conditions during the formation of thediVerent reef components, corals, and microbialites. Whereasage dating by radiometric methods appears to be the straight-forward method for determining the age diVerence betweencorals and microbialites, fundamental problems arise fromthe fact that microbialites include detrital grains and are earlycemented as demonstrated here petrographically and miner-alogically. The high aragonite content of up to 68% as deter-mined by means of XRD is thought to reXect the abundanceof Cliona chips from coral skeletons and other incorporatedskeletal debris. This incorporation of carbonate grains proba-bly results in a shift of the true age to greater 14C ages. At thesame time, the abundant cement inWlling the microporosityof the microbialite as seen under the SEM is expected to shiftthe 14C ages to younger ages. The eVect of these opposingfactors is diYcult to assess. This problem also applies for the14C ages presented in this study. Moreover, the radiometricdating method (230Th/238U) also faces diYculties because ofthe incorporated volcanoclastic material (Camoin et al. 2006;J. Collins, pers. comm.).

Both, 14C and 230Th/238U dating has been previouslyattempted on microbialites from Tahiti. For the top of thedeglacial succession, Heindel et al. (2009c) found that themicrobialites are <170 years younger than the corals theyencrust. The microbialites from the base of the deglacialsuccession show a larger age diVerence of up to 1,000 yearsto the corals they encrust. This is a considerably lowerage diVerence than the 1,600–8,400 years previously

Fig. 5 Various growth patterns of microbialites. a–c Mara’a, d–f Tiarei.a Laminated microbialite with dominant upward growth but also cleardownward growth around ramiform coral. Sample 5B 7R 1 W 0–29.b Laminated domal microbialite. Halimeda plates are trapped in adepression. Coral shows strong macrobioerosion. Sample 7A 29R 2 W4–10. c Laminated microbialite around ramiform coral. Some parts ofthe coral are Wrst encrusted by red algae. Halimeda plates are encrustedin the microbialites. Sample 5C 15R 2 W 26–44. d Laminated micro-bialite that passes to dendritic growth habit. Corals are Wrst encrustedby thick red algal crusts (white) and subsequently by microbialite.Corals and coralline algae are strongly bioeroded. Sample 21A 8R 1 W15–29. e Microbialite encrusts corals and passes from laminated todendritic growth habit. Sample 24A 5R 2 W 49–66. f Corals are Wrstencrusted by thin red algal crusts and subsequently by laminated anddendritic microbialite. Sample 24A 6R 1 W 64–74. C coral, CAencrusting red algae, H Halimeda, LMB laminated microbialite, DMBdendritic microbialite. Red arrows marked on the samples point inupward direction

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determined for dredge samples from the drowned reefs ofTahiti by means of 230Th/238U dating (Camoin et al. 2006).The reason for the diVerent estimates for the age gapbetween corals and microbial encrustations (Camoin et al.2006; Heindel et al. 2009c) is presumably the prolongedexposure of the dredged sampled studied by Camoin et al.(2006) to open marine seawater.

Growth succession of corals and encrusting microbialites

Red algal thalli occur at diVerent levels within the lami-nated microbialites, suggesting development of MB crusts

in the photic zone. We speculate that the transition fromlaminated to dendritic microbialites, on the other hand, pos-sibly reXects the decreasing water circulation as themacroporosity of the reef framework progressively becameless and less permeable. As such, both water circulationand light levels progressively would be reduced, leadingto a less regular microbialite growth, and Wnally to itstermination.

This model of formation of the laminated microbialitesin the photic zone is corroborated by an earlier study ofmicrobioerosion ichnotaxa in the deglacial microbialites(Heindel et al. 2009b, 2009c). Microbioerosion producedby phototrophic endolithic organisms (mainly the cyano-bacterium Plectonema terebrans and the green alga Ostreo-bium quekettii) was detected in both corals andmicrobialites. The fact that the corals were bored prior toencrustation by the same photic microbioeroders as boredthe encrusting microbialites supports the interpretation thatphotic conditions prevailed during microbial encrustation.

Fig. 6 Thin-section micrographs. a Cross section through coral,coralline algae, and microbialite. Encrusting foraminifers areintercalated. b Sketch of a. c Thalli of coralline algae alternating withmicrobialite. Lower right corner is epoxy. d Sketch of c. e Thin-layered intercalation of coralline algal thalli with microbialites.f Mesophyllum thallus coats microbialite. C coral, CA encrusting redalga, EF enrcrusting foraminifers, M microbialite, P porosity

Fig. 7 Fluorescence micrographs of thin-section of sample 5C 9R 17–27.a, b Transmissive light; c, d epiXuorescence. a Microbialite in porosity(dark areas) of the coral (light areas). b Microbialite shows stronger

Xuorescence than the coral skeleton. c Clotted to peloidal micrite.d Strong Xuorescence of the authigenic micrite

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The interpretation that the microbialites have formed inthe photic zone and are coeval with red algal encrustationdiVers from previous interpretations of earlier cores, cover-ing the time interval of 13.8–3 ka from the reef tract oVPapeete on Tahiti (Camoin et al. 1999). In those cores,microbialites are the last stage of encrustation, suggestingthat microbialites and red algae did not compete for space,

and that microbialites developed only after a non-deposi-tional hiatus. The dredge samples recovered from the mod-ern Xanks of the reef oV Tahiti showed a large time gapbetween coral and microbialite growth (based on U/Thdates; Camoin et al. 2006), suggesting a diVerent setting ofmicrobialite formation. Phosphate-iron-manganese crustson these samples indicate slow deposition and prolonged

Fig. 8 SEM micrographs of samples from the site Mara’a (polishedand etched). a Peloidal aggregates that compose the microbialites(sample 15B 25R 1 W 33–36). b Microbialite with abundant chips ofcoral skeletons produced by boring sponge Cliona (sample 15B 25R1 W 33–36). c Authigenic, platy clay minerals in a pore (sample 15B25R 1 W 33–36). d Pyrite framboid in a pore surrounded by

scalenohedral high-magnesian calcite cement (sample 7A 22R 1 W62–75). e, f Coralline red algal thalli intercalated with microbialiteclose to the top of a thick microbialite crust (sample 7A 32R 1 W 29-33).CC Cliona chip, MB microbialite, CA coralline red alga, white arrowspoint to top of microbialite crust

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exposure, implying that these microbialites formed or havebeen altered during long-term exposure at the sea Xoor.

Microbialites from the cores studied here apparently didnot grow in oligophotic or aphotic conditions after sea-levelrise and continued reef framework. The observation that themicrobialites developed in the photic zone at the time of

rapid sea-level rise (1–4 cm per year) corroborates thatencrustation by microbialites must have been early beforethe reef moved below the euphotic or mesophotic zone.Microbialite formation was not an event following a seriousdisturbance of the reef ecosystem, rather it was a continu-ous coeval process and an integral part of the ecosystem at

Fig. 9 SEM micrographs of samples from the site Tiarei (polished andetched: a, f; primary upper surfaces: b, c, d, e). a Contact between coraland encrusting microbialite; surface of coral has been shaped by theboring sponge Cliona, note Cliona chip within microbialite (sample9D 9R 1 W 108–114). b Encrusted Cliona chips on the surface of adendritic microbialite (sample 9D 9R 1 W 108–114). c Flakey randomto spherical aggregates of authigenic clay minerals that appear to have

been precipitated at a late stage of encrustation (sample 9D 9R 1 W108–114). d Flakey aggregate of authigenic clay minerals (sample 9D9R 1 W 108–114). e Chains of aggregates (sample 25B 10R 1 W 62–69). f Carbonate spherulite of unknown origin (spicule?) with syntaxialcement (sample 9D 9R 1 W 108–114). CC Cliona chip, C coral, MBmicrobialite, white arrows point to authigenic clay

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that time. Environmental conditions must have pushed theecosystem to the development of the widespread microbia-lites, but apparently have never been lethal for corals at thesame time.

Origin of the microbialites

The post-LGM microbialites from IODP 310 show the typ-ical micritic, clotted to peloidal fabric that has beendescribed before from the barrier reef oV Tahiti (Camoinand Montaggioni 1994; Camoin et al. 1999) and other sitesfrom the southwest PaciWc (Cabioch et al. 1999). Thestrong Xuorescence is typical for authigenic micrite(“automicrite” of Neuweiler and Reitner 1995; Fig. 7).SEM analyses also show some features consistent with amicrobial origin of the crusts such as peloids, cell-likechains, and authigenic clay minerals (Figs. 8c, 9c,e). Clot-ted fabrics have been linked to EPS calciWcation (Riding2000). However, most of the microbialites studied hereconsist of micrite not indicative of a speciWc origin. Suchmicrites are common in (but not restricted to) organominer-alization, i.e., precipitates mediated by organic compounds(cf. Trichet and Défarge 1995). As Riding (2000) pointedout, microbial carbonates with abundant agglutinated grainsare characterized by a micritic matrix that resemblestrapped Wnes or micritic cement, created by bacterialprecipitation. He added that linking particular products tospeciWc bacterial processes remains an elusive goal.

An involvement of sulfate-reducing bacteria in the pre-cipitation of the microbialites is supported by the presenceof pyrite framboids. This interpretation is corroborated bythe study of lipid biomarkers by Heindel et al. (2009a) whoshow that the Tahiti microbialites yield abundant molecularfossils of sulfate-reducing bacteria, whereas molecular fos-sils of cyanobacteria and anoxygenic phototrophs wereabsent. The spherulites observed under the SEM in thisstudy thus probably are not cyanobacterial products.Sulfate-reducing bacteria are known to initiate CaCO3

precipitation by degrading organic matter (von Knorre andKrumbein 2000) leading to the precipitation of micriticor slightly coarser calcite (Reitner et al. 1995). Sulfate

reducers produce large amounts of EPS, which promotecarbonate nucleation under laboratory conditions (Braissantet al. 2007). The former presence of microbial mats andthus abundant EPS is supported by the large amounts oftrapped grains in the microbialites; microbial mats withlarge EPS production tend to trap more and larger grainsthan those with little EPS production (Riding 2000). Thefact that encrusted volcanoclastic and carbonate grains arepresent in microbialites growing downwards, i.e., on lowersurfaces, additionally points to a microbial surface withbinding abilities.

Growth rates of microbial crusts

The 14C age dates from the base and top of the laminatedmicrobialite from site Mara’a yield an apparent growth rateof 6.8 mm/100 years. This growth rate is consistent withthe lower end of rates from other microbialites, valueswhich have ranged up to decimeters per 100 years(Holocene microbialites from the Great Barrier Reef:2.9 mm/100 years, Webb and Jell 2006; Jurassic reefmicrobialites: from 1 mm/year, e.g., Leinfelder 2001; to agrowth rate equivalent to that of the corals they encrusted,Dupraz and Strasser 2002).

In contrast to the 14C-derived growth rates, two lines ofevidence imply a growth rate of microbialites on the sameorder as that of the corals (cf. Dupraz and Strasser 2002).First, encrustation appears to be almost immediate as thereef is preserved largely in situ with very little stormdestruction (early encrustation is thought to have played arole for the high recovery during IODP Expedition 310, andfor the fact that the reef framework recovered in the cores islargely preserved in growth position). A similar protectiveeVect of voluminous microbialite encrustation has beenobserved for Miocene reefs of the western Mediterranean(Riding et al. 1991). Second, the spectrum of traces of thephotic endolithic boring organisms in the corals and thesurfaces of microbialites (Heindel et al. 2009b, 2009c)implies that the growth rate must have been rapid as photicconditions were similar for both even though sea-level risewas rapid.

Table 1 AMS 14C data of base and top of a microbialite from site Mara’a, base of the Tahitian deglacial reef succession

a AMS 14C ages in radiocarbon years BPb Radiocarbon ages were calibrated using calib rev 5.0.1 (Stuiver and Reimer 1993) and the marine04.14c dataset (Hughen et al. 2004) with afurther adjustment of a regional reservoir age �R = 82 § 42 (�R = deviation from the average global reservoir age of »400 years). The extremesof 1� cal. age ranges are givenc Intercept points of the calibrated age ranges (1�) with the calibration dataset marine04.14c

Mara’a site IODP 310 sample code Water depth Position in microbialite crust

14C age (year BP)a 1� cal. age ranges (cal. BP)b

Calendar years (BP)c

Base of post-LGM succession

M00018A 17R 1 W 3–9 110 m b.s.l. Top 11,430 § 60 12,848–12,935 12,890

Base 12,080 § 60 13,331–13,506 13,420

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Environmental conditions required for widespread microbialite growth

The intercalation of microbialite crusts with red algal thalli(contorted Lithothamnion sp.) indicates that the red algaeand the microbialites developed coevally in the same envi-ronment (Fig. 5). The fact that in laminated microbialites,thin layers of red algal thalli occur close to their uppersurface (Fig. 8e, f), demonstrates that photic conditionsprevailed during the entire formation of those microbialites.Interlayering of microbialite with the very shallow, eupho-tic coralline alga Hydrolithon has not been observed. Thisplaces the initiation of microbialite precipitation in a timerange shortly after the death of the coral while it was stillpositioned in the photic zone, but below the shallowest reefcrest. It also indicates that there is no large time gapbetween red algal growth and the microbial encrustation,but both crusts developed at least partly coeval. Interlayer-ing of microbialites and red algae has only been observed inlaminated microbialites, not in dendritic ones. The absenceof thick encrusting foraminifer crusts on the microbialcrusts also points to photic conditions, because withdecreasing light intensity, foraminiferal crusts tend to pro-gressively replace coralline algal crusts (Flamand et al.2008).

The absence of sedimentation breaks and the develop-ment of microbialites in the coralgal environment appearsenigmatic if meso- to eutrophic conditions are a prerequi-site of microbialite formation. However, proof that elevatedtrophic conditions are crucial for microbialite formation isfar from being unequivocal. Therefore it is not clearwhether there truly is a trophic paradox of oligotrophic cor-als co-occurring with meso- to eutrophic microbialites.Solving this problem is exacerbated by the paucity ofmicrobialites in other modern settings. One considerationfrequently put forward to reconcile the assumed diVerencesin trophic conditions is based on an inferred large time gapbetween the growth of corals and microbial encrusters (e.g.,Camoin et al. 2006). As argued above, this argument doesnot appear consistent with the observations or prevailingphotic conditions and, with all caution required, the 14C agedates. The coral communities in the cores from IODPExpedition 310 appear undisturbed (L. Abbey pers. comm.)and thus also argue against the notion that environmentalchange triggered the formation of voluminous microbia-lites. The absence of hardgrounds from the deglacial suc-cession of IODP 310 also renders unlikely the demise of thecoral reefs as a prerequisite for microbialite formation—instead microbialites developed continuously and coevalwith the coral reef framework.

As has been suggested earlier, elevated nutrient levelsseem to play a prominent role in the widespread develop-ment of deglacial reefal microbialites (Camoin et al. 1999;

Cabioch et al. 2006). The phosphate-iron-manganese crustsdescribed from dredge samples from Tahiti have been inter-preted to support the hypothesis that elevated trophic condi-tions are a prerequisite for voluminous microbialiteformation (Camoin et al. 2006). In the samples studiedhere, similar crusts were not found, arguing against a prom-inent role of increased upwelling or strong fertilization byerosive products from the volcanic hinterland. Similarly, nosuch crusts are present in microbialite-rich reef cores fromVanuatu (Cabioch et al. 2006).

InXux of volcanoclastic detritus is obvious from thelithology of the microbialites and from purely detrital inter-vals in the IODP 310 cores (Castillo 2009). This detritalinXux potentially introduced nutrients into the shallow-marine setting. Rare earth element and yttrium analyses ofthe microbialites from Vanuatu point in the same direction(Cabioch et al. 2006). The modern surface waters from theisland of Tahiti, however, carry only low concentrations ofdissolved nutrients as they run oV too fast for any consider-able enrichment (Hildenbrand et al. 2005). In addition, sta-ble oxygen isotopes show normal marine values between¡1.1 and 0.7‰ (Heindel et al. 2009a, cf. Camoin et al.1999, 2006) and thus rule out strong fresh water inXuence.Nevertheless, submarine weathering might have played arole in slightly increasing trophic levels. Heindel et al.(2009a) have proposed moderate fertilization to a pointwhere corals still Xourished, but also favoring phototrophicprimary producers and subsequent heterotrophic degrada-tion by sulfate reducers. The fact that bryozoans and otherWlter feeders are not excessively abundant also arguesagainst highly elevated trophic levels but for moderatelyelevated levels (cf. Hallock 1987).

The occurrence of microbialites in reefs around volcanicislands in the PaciWc realm is conWned to the last deglacialsea-level rise. Microbialite development ceased when sealevel stabilized between 7 and 4 ka B.P. (microbialiteoccurrences: Tahiti: 17 to some 5 ka B.P., Camoin et al.1999, 2006; Vanuatu: 24–6 ka B.P., Cabioch et al. 2006).Thus, the development of the voluminous microbialitesappears to be linked to a rapidly rising sea level. The reasonfor this dependence on rising sea level or any related envi-ronmental property of the deglacial period remains enig-matic. A general rise in nutriWcation in the equatorialPaciWc has not been observed, nor any constant trend butrather strong variability in pCO2 through the deglacialperiod (Montaggioni 2005).

Whether a change in trophic conditions occurred duringthe formation of the deglacial reef sequence is crucial forthe reconstruction of sea-level curves based on reef corals,which was one of the main goals of IODP 310 (Camoinet al. 2007a). For example, water transparency, which isalso a function of trophic conditions and sediment load,aVects the actual depth limit of the coral species used for

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sea-level reconstructions. In the case of the Tahitian degla-cial reef sequence, water transparency apparently was notstrongly reduced given that signiWcantly elevated trophicconditions can be ruled out—a moderate reduction by onlyslightly elevated trophic levels appears more likely.

Microbialites as disaster forms?

Microbialites have been suggested to represent disasterforms throughout the Phanerozoic (Schubert and Bottjer1992; cf. Riding 2005). Microbialites in this concept areseen as opportunists that brieXy proliferate in the aftermathof mass extinctions until they are suppressed again byspecialist taxa (Rodland and Bottjer 2001). However, Flügeland Kiessling (2002, p. 698) emphasized that for majorfaunal turnover events in Earth’s history, microbialites asdisaster forms appear to be rather the exception than therule—only four out of 11 major reef crises feature develop-ment of microbialites instead of metazoans. Contrarily,microbialites decline during most reef crises in concert withother reef-building organisms (Flügel and Kiessling 2002).

The apparently undisturbed coral fauna found in thedeglacial reefs from IODP 310 (E. Abbey pers. comm.) andthe immediate encrustation by microbialites demonstratesthat the hypothesis that microbialites represent disasterforms does not apply here. The microbialites apparentlygrew continuously in the reefal framework beneath theundisturbed corals under photic conditions. Similar obser-vations from the reefs oV Vanuatu, which are richer in coralspecies and thus even more sensitive than the Tahitianreefs, point in the same direction (Cabioch et al. 2006). Thecarbonate saturation state, which on large time scales isknown to have played a role in microbialite formation inthe geologic past (Riding 2005), is unlikely to have had aneVect on the formation of the reefal microbialites as satura-tion increased from the Pleistocene to the Holocene; micro-bialite formation, however, ceased when sea-levelstabilized in the Holocene (e.g., Camoin et al. 1999, 2006).

Conclusions

The deglacial microbialites from Tahiti (IODP 310) devel-oped coeval to the coral reefs they encrust. They are neitherdisaster forms, nor is there any signiWcant time gap betweencoral demise and microbialite precipitation. The microbia-lites developed while the reef framework was still situatedin the photic zone. Coral growth took place in the upper-most levels of the framework ediWce while microbialencrustation occurred coevally in lower levels, whereencrusting red algae and microbialites competed to somedegree. This scenario of microbialite formation as a coevalprocess in a moderately fertilized but still healthy coral reef

is in contrast to earlier models that proposed repeateddemise of the corals and later encrustation by microbialitesunder diVerent environmental conditions. InXux of volcan-oclastic sediment from the hinterland is a potential sourceof nutrients promoting microbialite formation in the degla-cial reefs of Tahiti and elsewhere in the tropical PaciWc.

Acknowledgments This research used samples and data provided bythe Integrated Ocean Drilling Program (IODP) as part of the IODPExpedition 310 Science Party research of HW (sample requestsMSP0070 and MSP21083B). Our thanks are extended to the co-chiefsGilbert Camoin and Yasufumi Iryu and to the IODP 310 Science Party,in particular Jody Webster, for discussions and collaboration. Eliza-beth Abbey and James Collins are thanked for information on theirongoing work on the Tahiti cores. Gilles Lericolais helped with thevisualization of the seismic data. Thanks are due to two anonymousreferees, Nora NoVke, and Gene Rankey, for their helpful andconstructive comments, and to FACIES editor André Freiwald. SEMwork was undertaken in the laboratory of Helmut Willems (UniversitätBremen) with the technical support of Petra Witte. The study was fund-ed by the Deutsche Forschungsgemeinschaft (DFG We2492/8 to HW).

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