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Controls on microbial activity and tidal flat evolution in Shark Bay, Western Australia

Authors


Abstract

Microbial deposits at Shark Bay constitute a diverse living microbial carbonate system, developed in a semi-arid, highly evaporative marine setting. Three tidal flats located in different embayments within the World Heritage area were investigated in order to compare microbial deposits and their Holocene evolution. The stressing conditions in the intertidal–subtidal environment have produced a microbial ecosystem that is trapping, binding and biologically inducing CaCO3 precipitation, producing laminated stromatolites (tufted, smooth and colloform), non-laminated thrombolitic forms (pustular) and cryptomicrobial non-laminated forms (microbial pavement). A general shallowing-upwards sedimentary cycle was recognized and correlated with Holocene sea-level variations, where microbial deposits constitute the younger (2360 years bp) and shallower sedimentary veneer. In addition, sediments have been documented with evidence of exposure during the Holocene, from 1040 to 940 14C years bp, when sea-level was apparently lower than present. Filamentous bacteria constitute the dominant group in the blister, tufted and smooth mat types, and coccus bacteria dominate the pustular, colloform and microbial pavement deposit types. In the subtidal environment within colloform and pavement structures, microbial communities coexist with organisms such as bivalves, serpulids, diatoms, green algae (Acetabularia), crustaceans, foraminifera and micro-gastropods, which are responsible for exoskeleton supply and extensive bioturbation. The internal fabric of the microbial deposits is laminated, sub-laminar, scalloped, irregular or clotted, depending on the amount of fine-grained carbonate and the natural ability of microbial communities to trap and bind particles or induce carbonate precipitation. Nilemah tidal flat contains the thickest (1·3 m) and best-developed microbial sedimentary system; its deposition pre-dated the Rocky Point and Garden Point tidal flats, with the most positive isotope values for δ13C and δ18O, reflecting strong microbial activity in a highly evaporative environment. There is an evolutionary series preserved within the tidal flats reflecting relative ages and degree of salinity elevation.

Introduction

Shark Bay is a World Heritage area that is well-known for its microbial mats, stromatolites and coquinas developed under saline water conditions in a semi-arid and highly evaporative marine system. Hamelin Pool is the most notable embayment and is surrounded by extensive tidal flats: Gladstone, Hutchinson and Nilemah. Other nearby tidal flats located in L'Haridon Bight and Henri Freycinet embayment, at Rocky Point and Garden Point, respectively (Figs 1 and 2), were also colonized by microbial communities, but under slightly different environmental conditions and timing. Previous studies have focused on tidal flats inside Hamelin Pool (Davies, 1970; Logan et al., 1970, 1974; Playford & Cockbain, 1976), identifying microbial mat fabrics and fenestral fabrics that are useful when interpreting ancient rocks and environments. The present study is the first to compare microbial deposits from different embayments within Shark Bay, focusing on their ages, distributions, types, taxonomy and differential evolution.

Figure 1.

Shark Bay and its most notable inlets Hamelin Pool, L'Haridon Bight and Henri Freycinet.

Figure 2.

(A) Location of investigated tidal flats in Shark Bay; (B) detail of Rocky Point; (C) Garden Point and (D) Nilemah embayment with the respective littoral zones and microbial deposits. Rocky Point and Garden Point are re-entrances behind coquina barriers, whereas Nilemah tidal flat re-occupied an ancestral embayment.

Microbial mats from tidal flats in Shark Bay are composed of various microbial communities (Burns et al., 2004; Papineau et al., 2005) that reveal distinct colours, texture, growth morphologies and distributions. Despite the very gentle morphological gradient (20 to 150 cm−1 km−1) revealed by high-resolution Differential Global Positioning System (DGPS) surveys, the microbial communities live in very specific topographic positions, showing definite zonation relative to water depth and energy conditions in the tidal environment. Parameters such as salinity, calcium availability, alkalinity, water depth, turbulence, luminosity and accommodation, associated with shore morphology, waves, wind direction, sediment influx (Logan et al., 1974) and residence time, are responsible for the occurrence and distribution of microbial communities and their resultant organo-sedimentary deposits.

Distinct carbonate fabrics result from the interactions between microbial growth behaviour, the quantity of trapped carbonate particles, carbonate produced by organomineralization (Burne & Moore, 1987; Reid et al., 2003; Perry et al., 2007; Dupraz et al., 2009) and aragonite cement. This interaction is recorded in the sediment facies and is responsible for substantial variability in the internal fabrics; from well-laminated to irregular patterns. The organic matter that constitutes a considerable portion of the microbial carbonate fabrics is strongly affected when exposed to desiccation and oxidation, mainly by space creation, producing fenestral porosity (Logan et al., 1974). In many cases, this is still preserved in the geological record and is a distinctive characteristic of some rock sequences and a guide for environmental reconstruction (Riding, 1991; Walter, 1999; Grammer et al., 2004).

The Holocene microbial mats are composed of carbonate mud and grains representing the upper portion of a shallowing sedimentary depositional cycle as a thin carbonate layer (maximum 1·3 m) over a sandy quartz and shelly substrate. Microbial deposit mineralogy (X-ray diffraction analysis) obtained from 87 samples from the three tidal flats revealed the following average percentages: aragonite (51%), quartz (35%), halite (6%), magnesium-calcite (3·9%), calcite (2·8%) and gypsum (0·9%) as the principal constituents of the sediment.

The carbonate system developed in response to a progressive change in environmental conditions, transforming a more open marine system into a restricted tidal embayment with high salinity and high evaporation. Deposition of microbial sediments started after the Holocene maximum sea-level at about 6800 U/Th years bp (Collins et al., 2006), when the water level gradually dropped 2·5 m, to the present sea-level, within the Holocene stratigraphic highstand systems tract. The microbial deposits in this study are classified according to the terminology defined by Logan et al. (1974). Tidal zonation is related to sea water areal influence, where the subtidal zone corresponds to permanently submerged areas, the intertidal zone is between the high and low normal tides and the supratidal zone is reached only in abnormal tides or storm surges.

To investigate the evolution of Holocene morphology and to define and compare sedimentary microbial deposits, two tidal flats were fully and another partially sampled and mapped at L'Haridon Bight, Henri Freycinet and Hamelin Pool within Shark Bay (Fig. 1), using georeferenced orthophotographs, and aerial-photographs, DGPS surveys, ground truth, box-core and push-core analysis applied to the study of three ecosystems that differ in setting, timing of salinity onset and degree of hypersalinity.

Geology and Geomorphology

The prominent geographic features of Shark Bay are controlled tectonically by a regional normal fault system trending north–south that cuts a Palaeozoic NNW–SSE oriented fold system responsible for confining the bays to synclines, with peninsulas located over the anticlines (Butcher et al., 1984). Petroleum wells and seismic reflection images show that the Tamala Limestone (Pleistocene) and the Cenozoic/Mesozoic rocks beneath are located over an anticline with the axis parallel to Dirk Hartog Island (Playford, 1990). North-east/south-west oriented dextral faults have been recognized in seismic image mapping and on the basis of field work, because they affect the coastal morphology, producing minor indentations. The tidal flats at Garden Point and Rocky Point are partially controlled by this north-east/south-west trending fault system (Fig. 2B and C), which is responsible for creating headlands and protected minor re-entrances, where microbial environments flourish.

The tidal flats studied – Garden Point, Rocky Point and Nilemah – are located, respectively: in Henri Freycinet embayment at the west portion of Shark Bay; in L'Haridon Bight embayment in the central area; and in Hamelin Pool the easterly embayment of Shark Bay (Fig. 2). Normal marine water (salinities 35 to 40) and metahaline waters (salinities 40 to 56) occur most of time in Garden Point where hypersalinity (salinities 56 to 70) is seasonal and restricted to ponds and portions of the supratidal–intertidal zones. L'Haridon Bight is subjected to metahaline to hypersaline waters while Nilemah tidal flat is constantly influenced by hypersaline waters (cf. Logan et al., 1974).

Tidal flats are shallow and are characterized by low and smooth bottom gradients that vary from 20 to 80 cm km−1 at Garden Point and Rocky Point and from 20 to 150 cm km−1 at Nilemah. It is these features that are responsible for the restricted tidal influx and laterally well-defined tidal zonation.

The Rocky Point tidal flat (Fig. 2B), an area of about 8 km2, is located on the west flank of L'Haridon Bight in a prominent geomorphological element of the coastline. Microbial establishment and evolution is older than at the Garden Point embayment, because water circulation was restricted earlier in the Holocene by a barrier seagrass carbonate bank between the L'Haridon Bight embayment and the open sea (Fig. 1). Also a linear to arcuate barrier ridge complex flanking the embayment has inhibited free water connection with the sublittoral area, the most important factor for microbial activity.

Physical and chemical conditions (Table 1) established by the restricted water circulation and strong evaporation have been favourable for microbial growth. Despite the strong clastic influence at Rocky Point, microbial activity continues to improve and expand in the intertidal and subtidal zones. The supratidal zone is dominated by an extensive breccia pavement as a consequence of exposure of lithified microbial carbonate, which developed as a consequence of a late Holocene sea-level regression.

Table 1. Continuous measurements of water parameters (24 to 48 h record) recorded 5 cm above the microbial substrate during periods of 16 to 26 October 2008, 3 to 10 April 2008 and 22 to 29 October 2009. Note the lower salinity values and higher ranges at Garden Point and Rocky Point
Water parameters
LocationParameters/Mat typeT°CpHSalinityDissolved oxygen (mg l−g)
Rocky PointPustular20·6–31·57·4–8·042·8–73·6
NilemahPustular16·4–32·07·8–8·562·3–65·3
NilemahSmooth17·3–30·87·5–8·461·2–65·04·3–8·3
Garden PointSmooth17·6–33·17·8–8·740·1–68·15·5–8·5
NilemahPavement18·5–28·47·8–8·461·4–64·04·6–8·5

Garden Point (Figs 2C and 3) is a small re-entrant, of about 11 km2, located on the east coastline of the Henri Freycinet embayment. The region is regularly affected by southerly winds and longshore currents, responsible for the southerly sand supply (mainly Pleistocene quartz sand) deposited over a large sub-littoral and intertidal embayment area. The aeolian sand supply is considerable in the summer, when strong southerly winds rework part of the hinterland, where unconsolidated Pleistocene quartz sand is available. Cyclones and storms coming from the north and west are responsible for concentrating bivalve shells and producing washover deposits over the ridges on the offshore side of the tidal flat and also forcing a subtidal sand sheet to enter the embayment at the north.

Figure 3.

Scenic view of the north portion of the Garden Point tidal flat, with extensive shallow areas with dark microbial mats. Vegetated supratidal coquina ridge in foreground. View looking to north at falling tide.

Nilemah tidal flat, with an area of about 16 km2 (Fig. 2D), is the semi-enclosed portion of southernmost Hamelin Pool. It is a hypersaline environment well-protected by carbonate banks that restrict sea water influx. The Nilemah supratidal zone is extensive and notable due to its coquina deposits, which have accreted laterally, generating a shell ridge system with 20 principal convex-up crests, the oldest ones standing 7·5 m above sea-level, with some disrupted by younger storm events. Nilemah contains the best-developed microbial carbonate system; it has completely colonized subtidal zones to water depths greater than 2 m, with such deposits occupying larger areas than its intertidal deposits.

Materials and Methods

Maps were prepared using high resolution (50 cm per pixel) Shark Bay orthophotographs from the Department of Environment and Conservation (DEC) and from Landgate (Perth, WA, Australia). In addition, a set of Shark Bay aerial-photographs (1 : 25000) from Landgate was interpreted using stereoscopy equipment to support map construction. A DGPS using SOKKIA antenna and Allegro System (GSR2650 LB; SOKKIA Co Ltd., Japan), from the Department of Spatial Sciences, Curtin University allowed the recording of high-resolution elevation (±5 cm) and horizontal positioning (±50 cm) from transects across the tidal flats.

Sampling involved the following: push coring of sediments to a maximum depth of 1·8 m, using 50 cm diameter PVC and aluminum pipes; the use of small (20 cm) aluminum tubes to obtain shallow material, mainly living mats, taken at the same site as the drilling, with freezing to preserve organic matter for laboratory analysis; and box coring at selected sites to provide wedge-shaped samples 20 cm × 10 cm × 40 cm (the longest dimension is depth) of different types of microbial mats. Water samples were placed in glass vials (300 ml) for laboratory analysis. Water parameters were obtained with a WP-81 conductivity–salinity–pH–temperature instrument and using 90FLT equipment (TPS, Brisbane, Australia) to acquire continuous measurements of salinity, pH, conductivity, total dissolved solids (TDS), dissolved oxygen, turbidity and temperature. The water depth measurements are relative to the highest sea-level reached under high-tide and low-wind conditions, corresponding to the ‘Winter High-Water Level’ (WHWL) of Logan et al. (1974).

A taxonomic study of cyanobacteria was performed in the Microbiology Department at the University of Rio de Janeiro, Brazil, using permanent, semi-permanent and fresh ‘palynological slides’ described using optical microscopy (Axio-Zeiss; Carl Zeiss, Oberkochen, Germany) and microphotographs obtained with a Zeiss Axio MRc (Carl Zeiss, Jena, Germany), digital camera. Organo-sediment (microbial mat) was prepared and isolated using a liquid solvent consisting of three volumes of 0·5% chromic acid, four volumes of 10% nitric acid and three volumes of alcohol at 70° or 90º, depending on the presence of lithified carbonate. Preservation of cyanobacteria was ensured using an aqueous solution of formaldehyde at 4% with distilled water, buffered with borax and maintained in the absence of light. For each specimen, six measurements were performed: (i) the diameter of the bacteria filaments; (ii) the diameter of the colonies; (iii) the diameter of the trichomes; (iv) the thickness of the sheaths; (v) the length; and (vi) the width of the cells. Chemical analysis of microbial sediment and water samples including X-Ray Fluorescence Spectroscopy (XRF), Inductively Coupled Plasma Mass Spectometry (ICP-MS) and Optical Emission analyses were performed by Ultratrace Analytical Laboratories (Perth, WA, Australia) and the Research Center from Petrobras S.A (Rio de Janeiro, Brazil). The solutions have not been treated other than by dilution. Water composition (Ca, K, Mg, S and Na) has been determined by the ICP optical emission; Ba, Li, Mo, Rb and Sr have been determined by ICP-MS. To ensure a robust quality control, the samples analysed by mass spectrometry included two dilution blanks; two samples were analysed in duplicate and six spiked solutions containing various concentrations for various elements were run to give a measure of accuracy and precision. Both the obtained and expected concentrations were reported for most elements. Internal standardization was used. Accuracy and precision are typically within 5% of the absolute value once they are higher than 50 times the detection limit. Below this value, there is a 1 or 2 detection limit variation, thereby incurring a greater variation because reporting is in detection limit increments. The uncertainty at the detection limit is typically plus or minus the detection limit but is somewhat element specific. Fluoride (F) in solution has been determined using specific ion-selective electrodes, and differential electrode and fluoride electrode instruments, whereas chloride (Cl) in solution has been determined colourimetrically.

Carbon-14 ages were produced using analytical procedures from the Radiocarbon Dating Centre of the Australian National University. The ages in radiocarbon years were obtained using a Libby half-life of 5568 years and following Stuiver & Polach (1977). The dates have been calibrated (marine reservoir effect) against the Marine-09 calibration curve in OxCal version 4·1 assuming a delta R of 70 ± 50 (Table 3). Carbon and oxygen isotopes from sediment samples (precision of 0·05‰ and 0·07‰, respectively) were produced at the University of Sao Paulo (USP), Brazil. X-ray diffraction (XRD) techniques were used to characterize the crystallographic structure and identify the different mineralogical constituents of the sediment. These analyses were performed at the Mineralogy Laboratory of the Federal University of Parana, Brazil using PW1830-Philips and Panalytical Empyrean equipment (Ermelo, Netherlands) with the software X'Pert HighScore-Phillips. Diffractogram spikes were compared with the data bank of the Joint Committee on Powder Diffraction Standards (JCPDS). Thin sections were produced by Minerex Services, Esperance-Australia and by Petrobras Research Center, Brazil and analysed in a Leica (DC200) microscope (Leica Microsystems GmbH, Wetzlar, Germany) and imaged with Leica DC100/DC350F software at Curtin University, Australia. Scanning electron microscopy (SEM) was conducted at Curtin University on an EVO 40XVP (Carl Zeiss, Oberkochen, Germany) using secondary electrons (SE) as well as backscattered electrons (BSE). Polished sections (7.6 × 5.1 cm) were coated with platinum and crude samples of dried sediment (1 × 1 cm) were coated with gold. Elemental analysis was performed using Oxford Instruments energy-dispersive X-ray spectrometer (EDS). Analysis of X-ray spectra was performed using the Inca-Analyser software (Oxford Instruments, Abingdon, UK).

Results

Environmental Information

Water parameters

Continuous measurement of water parameters (Fig. 4) on the tidal flats allowed environmental conditions and microbial activity to be compared during the day and night. Data acquired 5 cm above the surface of subtidal deposits reveal that Nilemah is considerably more stable based on salinity, always remaining within the hypersaline field (Table 1).

Figure 4.

Continuous water parameter measurements recorded 5 cm above colloform structures at Nilemah. Salinity changes related to tides and other parameters are related to the presence or absence of light and microbial activity. The turbidity anomaly is probably an artifact due to disturbance.

The other two tidal flats experience strong salinity variations depending on the stage of the tidal cycle or yearly season with values ranging from 40 to nearly 75. Measurements of pH, temperature and dissolved oxygen reveal lower values during the night and higher values during daytime, attesting to the ability of bacteria to deal with strong water temperature variations in an alkaline environment with low turbidity.

Sea water samples were collected within the studied Shark Bay tidal flats, also in the shoreline of Denham (the administrative town for the Shire of Shark Bay) and in the shoreline of Perth (capital of Western Australia) for comparative purposes. The Shark Bay water samples reveal high concentrations of Mg, K, S, Na, Cl and Ca on tidal flats, characteristic of a highly evaporative marine environment, especially in samples collected above pustular mats. The high Mg/Ca ratio near 4 : 1 observed in the Shark Bay tidal flats strongly favours precipitation of aragonite instead of calcite (Jones & Renaut, 2010). Trace elements include Li, Mo, Sr and Rb in significant concentrations. These elements are attributed to microbial metabolic activity and are essential for producing pigments and biomineralization (Table 2).

Table 2. Chemical data from water samples collected 1 cm above the mat surface in tidal flats or sand in open sea at Denham and Fremantle (Perth). Note the significantly elevated values in all elements compared with sand substrate controls (Perth and Denham)
Water chemistry
LocationUnitsmg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mg l−1mcg l−1
Mats/substrateCaBaFKSMgNaCILiMoSrRb
Sea water - PerthSand4130·001·0412956128011100202500·200·018·15120
Sea water - DenhamSand4640·002·04701090147012600221500·200·018·75120
Rocky PointPustular6920·022·09482110293028000505000·450·0314·9280
NilemahPustular10800·033·011403130368035900640000·550·0323·1340
NilemahSmooth5770·012·06721660205017600321000·300·0212·0220
Garden PointSmooth5280·012·05461480165016300298000·250·0210·6160
CarblaColloform7160·022·07601710233020000356500·300·0214·2200
NilemahPavement5890·012·05981620186019000300500·300·0211·9160

Physiography, Sediment Fabric and Distribution

Tidal flat evolution

Cyclone and storm activities in Shark Bay have been recorded by the Bureau of Meteorology since 1906. Coming from the north and north-east, these events generate strong storm surges capable of reworking, transporting and depositing sediment, mainly bivalve shells that are available near the shore. As a consequence, a carbonate shell ridge (coquina) system has been left in the internal areas of all of the tidal embayments, with a variable amount of quartz sand. The coquina system corresponds to the most landward Holocene unit inside the bays (Hamelin Coquina of Logan et al., 1974). Sea-level fall over the last 6000 years has been responsible for a shallowing in water depth throughout the region, causing a seaward shift in the depositional system. As a consequence of this marine regression, new beach ridges have developed due to storms and longshore currents, also controlled by southerly winds and high tides in seaward zones. As a result, re-entrant coastal areas have been protected by north–south oriented ridges restricting water circulation, generating extensive tidal flats with different stages of evolution and microbial colonization.

A sequence of events affecting the Shark Bay proximal embayments can be described with four main phases of evolution (Fig. 5). Regional stratigraphy and sedimentary relations are provided in Fig. 6.

Figure 5.

Morphological evolution proposed for the Garden Point embayment. Storm wave activity was very important during the initial phase, while longshore currents, winds and tides were the morphological drivers during the late stages. Microbial activity started near 2300 years during the fall in sea-level.

Figure 6.

Cross-section of the three tidal flats showing sediment diversity and organo-facies distribution and regional stratigraphy for each tidal flat. Pre-Holocene stratigraphy inferred from data in Logan et al., 1974 (Fm = Formation).

  1. At the onset of the Holocene inter-glacial Flandrian transgression, Shark Bay was drowned by marine water across aeolian sand dunes and littoral sands, producing a Holocene basal transgressive layer composed mainly of carbonate breccia, bivalve shells, quartz and bioclastic sand from the reworked sublittoral and near-littoral Pleistocene platform. As the sea reached its maximum level, nearly 2·5 m (estimated from coquina ridge measured altitudes and based on Logan et al., 1974) above the current level, a thin sublittoral layer of fine-grained sand with mud, bioclasts and fragments was deposited over the basal transgressive layer. This sediment facies was described in core samples as skeletal wackestone by Logan et al. (1974) as part of the Basal Sheet Unit within Hamelin Pool and is interpreted here as representing the maximum flooding.
  2. After the maximum flooding near 6800 (U/Th) years bp (Collins et al., 2006), waves and reworking processes generated by storms transported a thick layer of quartz sand onto offshore areas, where sand pinches out. The erosional action of littoral waves was responsible for establishing a flat sandy sublittoral platform, colonized by seagrass in the outermost domains, producing carbonate mud and skeletal sand deposits. The sandy substrate is common to the three embayments, and is present in almost all 60 core samples recovered from those sites, underlying the microbial carbonate deposits, and is composed of quartz-rich and bioclastic sand as part of the sublittoral platform in these proximal areas.
  3. Following the onset of the Late Holocene regression (see Logan et al., 1974), after sea-level fell by presumably close to 1 m, changes in environmental conditions took place mainly at Nilemah and Rocky Point due to restriction in sea water influx. Hamelin Pool reached hypersalinity and L'Haridon Bight became a metahaline environment, where microbial activity took place in tidal flats, producing carbonate particles not only by inducing CaCO3 precipitation, but also by trapping and binding sediment in the shallow protected near-beach sites of the tidal systems. Targeting abundant microbial food sources, the bivalve mollusc Fragum erugatum developed a high tolerance to stressing environmental conditions and became the most important colonizer of the sublittoral habitat. At that same time, Garden Point was still receiving waves from the Henri Freycinet open area, as well as the influence of tidal currents on a very shallow sandy substrate. Internal areas of tidal flats were regularly reached by storms, producing an accretionary ridge system on the supratidal zone, composed mainly of quartz sand and shells, while prominent high relief morphologies in the subtidal zone became shallower, amplifying the potential retention of shells, bio-fragments and sand.
  4. Sea-level fell until it reached the current level. Small-size Fragum erugatum bivalves successfully adapted and became endemic in the Shark Bay area, inhabiting sublittoral zones and supplying shells to the deeper embayment plain and shore zones. New beach ridges oriented north–south were deposited by storm flooding and abnormal tides, semi-closing the north side of the Rocky Point embayment, while longshore currents and winds coming from the south created the south ridges of the embayment. The barrier ridge system displayed a strong influence on the tidal flats' hydrological system, once the water influx became limited to tidal channels, restricting coarse sediment influx and lowering the energy conditions. The shallow hypersaline environment promoted expanding microbial activity that has been producing extensive microbial mats since 2000 years bp. The sediment deposits registered in cores represent a shallowing-up sedimentary cycle, where carbonate intertidal–subtidal microbial fabrics overlie sublittoral quartz-bioclastic sand.

At Garden Point, longshore currents controlled by southerly winds were responsible for an increased coastal sediment supply, and barrier ridge evolution grew from south to north, promoting a partial disconnection between the coastal embayment and the open sublittoral and basinal areas. The barrier ridge system restricted the tidal influence to the north entrance of the embayment (Fig. 5) and a few tidal channels across the barriers. The environment became hypersaline mainly in the south and central parts. Rocky Point tidal flat experienced similar processes, with one principal difference in that the northerly external coquina ridge was constructed by events coming from north to south, driven by spring tides and storms entering the L'Haridon Bight embayment. Nilemah tidal flat has an evolutionary history linked to forced regression, shoaling and sediment seaward shift processes around Hamelin Pool embayment where hypersalinity was reached relatively earlier due to greater restriction by barrier seagrass banks across northern Hamelin Pool (see Fig. 1).

Sedimentary cycle, sea-level variation and stratigraphic sequences

Cross-sections based on high-resolution DGPS surveys show similarities between Rocky Point and Garden Point water depths (Fig. 6), where the maximum water depth is 0·87 m in the subtidal zones, and just above 1 m inside the tidal channels. The Nilemah embayment is a northward-facing tidal flat in southern Hamelin Pool with a relatively high sloping substrate gradient and well-developed microbial carbonate domain in the subtidal zone, able to accrete vertically and construct structures. Rocky Point and Garden Point are protected by a coquina barrier ridge system that is responsible for isolating the embayments, with such ridges reaching a maximum height of 1·83 m and a width of more than 200 m, depending on washover occurrence and intensity.

Based on sediment information from shallow cores (1·8 m maximum) recovered in the three study sites and using the data provided by Logan et al. (1974) for the Basal Sheet Unit, a shallowing upward sedimentary sequence has been recognized and correlated with sea-level variation (Fig. 8). The base of the sequence, which overlies calcrete deposits (Read, 1976) from the last interglacial phase, includes skeletal wackestone and skeletal packstone of the basal sheet, here considered representative of the sea-level transgressive and maximum flooding stages, using a sea-level maximum of about 2·5 m at around 6800 U/Th years bp (Logan et al., 1974; Nakata & Lambeck, 1990; Collins et al., 2006). The extensive amount of quartz sand that provides the substrate for the bivalve and microbial carbonate sediment is a layer of reworked Pleistocene aeolian deposits derived from the Peron Sandstone (Butcher et al., 1984). Box coring has provided further evidence and good visualization of the changing environment and the internal arrangement of sublittoral quartz-rich sediment passing upwards to a shoaling superficial microbial carbonate system as salinity increased (Fig. 7).

Figure 7.

Box core sediment slice with clastic sand at the base passing upwards to carbonate, representing a shallowing-up depositional cycle. The basal sediment is from a sublittoral sandy domain overlain by a subtidal–intertidal microbial carbonate system (vertical thickness of box core 30 cm).

The establishment of hypersaline conditions in Nilemah and development of specialized fauna are the result of a fall in sea-level by about 1 m nearly 4600 years ago (based on 14C dating of coquina ridges at nearby Telegraph Station and subsurface shell layers deposited at Nilemah tidal flat). Microbial carbonate deposits are younger than 2360 years (based on 14C dating of bivalve shells at the base of the microbial deposits at Nilemah) and were deposited over a sandy substrate composed of quartz, bioclastic and ooid grains. The uppermost layer of the sedimentary cycle is represented by an extensive exposed breccia system produced due to sea-level regression. The Holocene sedimentary deposits in the tidal flats represent a shallowing-up cycle with subtidal clastic deposits at the base and microbial carbonate on top, partially exposed on the supratidal zone. The depositional cycle (Moore, 2001) represents a fifth-order sequence and is applicable to understanding a microbial carbonate deposit constructed mainly in a highstand systems tract, after a minor sea-level fall.

The presence of a lithified carbonate pavement, with evidence of exposure, was recognized at Garden Point and Rocky Point close to the surface, usually at a 5 to 10 cm depth. This pavement is composed of carbonate micrite, bioclastic fragments, quartz sand, Fragum erugatum shells and aragonite cement, usually covered by a black veneer from a film mat. In some places near the coquina ridges and tidal channels, the exposed pavement is represented by a partially cemented black shell layer. The pavement is interpreted as an exposure of the overall area in the recent history of the embayment. Dating indicates ages of 1040, 960 and 940 14C years bp for this short regression with surface emergence and helps in reconstructing the sea-level variation (Fig. 8).

Figure 8.

Rocky Point and Garden Point idealized sedimentary cycle pattern correlated with sea-level variations based on an interpretation of sedimentary deposit characteristics and 14C dating. The maximum flooding is based on Logan et al. (1974); Nakata & Lambeck (1990) and Collins et al. (2006). The sedimentary system reflects regression, shoaling and salinity increase during the Late Holocene.

The Holocene coquina ridge system located at the internal part of Garden Point was dated as 2050 to 2150 (±35) conventional years; younger than in Rocky Point bivalve samples aged 2420, 2830 and 3160 (±35) years (Fig. 9). The dating information confirms that Garden Point is the younger tidal flat and that Nilemah is the oldest one, where coquina shells are 4600 years old (Table 3).

Table 3. Summary of 14C dating showing the conventional and calibrated data for marine reservoir effect using the Marine-09 calibration curve
Tidal flatConventional 14C age (years)Error ± (years)Calibrated ages (marine reservoir effect) 68% probability (years)Error ± (years)
Rocky Point24350902852954
9602548111
316025282019
12290351362925
283025241726
242025193219
Garden Point205025149920
10402554412
<50025Modern0
215025160819
9402546911
Nilemah236035186319
463035472221
Figure 9.

Rocky Point and Garden Point sedimentary ages from AMS 14C dating of bivalve exoskeletons and the respective sampling location. See Table 3 for details.

Microbial deposits: aspect and distribution

The tidal flat environment has been colonized by microbial communities specialized in surviving at specific water depths, where a delicate balance between tidal energy, waves, exposure time and water depth results in accretion or erosion (Logan et al., 1974). Low water energy associated with high evaporation rates, sediment pattern and space creation are the key elements for sediment accretion in Shark Bay. Microbial communities take advantage of daily waves and tidal currents that slowly cover the very flat area, supplying sediments and a habitat for microbes that are still adapting and expanding, producing carbonate by trapping and binding particles (agglutination), biologically inducing carbonate precipitation and being lithified by aragonite cement.

Hot summer temperatures (around 40°C) and strong south winds (40 km−1 h−1), however, force water out of the tidal flats, causing large areal exposure and desiccation of microbial deposits (predominantly pustular mats), which separate from the substrate forming globules of dead microbial mats. The dead organic material is washed to the shoreline, constructing ephemeral deposits. Considering the 7·5 km of internal shoreline at Garden Point, bordered by a zone of 2 m wide and 0·2 m thick dead pustular mat, the volume of material can reach 3000 m3 year−1 of mainly organic matter. The distribution of sediments and microbial types at Garden Point (Fig. 10) reveals a thin sediment veneer composed of carbonate, reflecting recent microbial activity within an environment that is adapting to new conditions (see Fig. 7). Six different microbial deposit types (Fig. 11) were recognized, mapped and sampled with principal development and occurrence as mats concentrated in the intertidal zone at Garden Point and Rocky Point and as additional microbial structures in the Nilemah subtidal.

Figure 10.

Cross-section of Garden Point and the principal organo-sedimentary facies. Plio-Pleistocene and Cretaceous unit boundaries are inferred. Storm deposits with bivalve and quartz sand (A), bioclastic and quartz sand (B), blister mat (C), breccia pavement (D), tufted mat (E), mini-pustular mat (F), pustular mat (G), subtidal sand and mud with smooth mat (H), shell ridges and washover deposits (I) and shoreface bivalve shells and quartz sand (J).

Figure 11.

Microbial deposit types recognized and mapped at the Shark Bay tidal flats, with details of the external–internal aspects and their relation with tidal zones.

The supratidal zone does not preserve or develop extensive mats because of the strong erosional processes, constant sediment movement and adverse conditions of temperature, where microbial communities survive in detached sites subject to a sporadic high-wind-driven water supply or abnormal tides. Microbial deposits in those sites are film and blister mats. Film mats are a black veneer normally covering lithified surfaces exposed to the sun for most of the time and belong to a novel type of halophilic archaeon, Halococcus hamelinensis sp. (Goh et al., 2006; Goh, 2007).

Tufted mats occur in the upper intertidal zone, growing in scallops due to long filaments made by Lingbya (Hoffman, 1976) that exploit the ability to avoid direct contact with the substrate, and may block water and sediment within the relief created. This mat normally develops over shallow muddy substrate where sediment maintains moisture landward of the pustular mat type. The presence of quartz sand and dead shells of Fragum erugatum is common over the mats and is transported by winds, tides and storms. A significant amount of dried sediment grains, mainly quartz sand, shells and shell fragments, were observed floating on water entering Garden Point and Rocky Point during flood tides coming from the barrier ridges that surround the tidal flats.

The intertidal zone is the growth domain of pustular mat spread as brown dark sheets of small ‘bushes’, inhabiting the upper intertidal to the upper subtidal zone. To construct a detailed map, the term mini-pustular was introduced to refer to small ‘bushes’ or pustules less than 1 cm in height and diameter. Pustular mats in the intertidal zone normally reach 3 cm high and more than 1 cm in ‘bush’ diameter. In the upper subtidal zone, the high rate of peloid deposition discourages pustular growth that is still small in size (less than 1 cm high) and sparse, such as mini-pustular mats.

In the upper subtidal zone, different bacteria such as Schizothrix friesii and Microcoleus produce a smooth mat composed of fine carbonate grains placed between vertical bacterial filaments that are able to permeate and trap sediments and produce laminar stromatolitic fabrics. Garden Point includes a proximal pond where very calm water rich in sediment particles has developed a set of coarse laminar smooth microbial mats. However, Garden Point, unlike the other tidal flats, is in the initial phases of establishing microbial communities, and only the proximal substrate portion of the subtidal zone is colonized. Nilemah tidal flat contains, in the subtidal zone, seaward of smooth mats, colloform microbial deposits (−0·5 to −1·5 m) displayed as elongate structures followed by a tabular microbial carbonate pavement extending to deep subtidal zones (−1·0 to −6·0 m).

The improved knowledge of the nature and distribution of the tidal flat microbial deposits is documented in georeferenced maps of the sediments and organo-deposits of Garden Point and Rocky Point (Fig. 12). These are characterized by relatively extensive and prolific microbial activity during the last 2000 years, producing microbialites that are exposed in the supratidal zone now under erosion and are progressively colonizing the subtidal zone as a consequence of sea-level fall, although evidence of recolonization observed in the intertidal zone points to a recent short marine transgression.

Figure 12.

Sediment and organo-facies map constructed for Garden Point and Rocky Point.

Organo-sedimentary Fabrics, Microfabrics And Phylogeny

Microbial deposit fabrics

The organo-sedimentary products documented in the tidal flats over the three studied areas have a specific distribution regarding topography and water depth. Each tidal zone displays substrate deposits with a distinct external aspect and characteristics (Fig. 13) that are associated with specific microbial communities, also responsible for different internal fabrics.

Figure 13.

Summary of the principal fabrics and external aspects of the microbial deposits for Nilemah, Rocky and Garden Point tidal flats. Coin for scale has a 20.5 mm diameter.

As a result of microbial processes of trapping/binding and organomineralization, organic matter content, amount of sediment input, microbial community, presence of voids, bioturbation and macropore orientation, different fabrics are recognized, referred to as laminar, scalloped, irregular and clotted (Fig. 13). The fabrics imprint important characteristics (Monty, 1976) in the sediments that form environmental markers useful as analogues for interpreting the ancient environment.

Blister mats are associated with exposed sediment in supratidal zones that produce, as a result of desiccation and reworking, an irregular muddy fabric rich in gypsum. Tufted mats produce laminar fabrics with a variable and asymmetrical millimetric thickness composed of carbonate and quartz grains with bivalve shells alternating with laminae of organic matter (Fig. 13). Due to the vertically oriented tufts of Lingbya aestuarii, a semi-regular interruption of the laminae produces a peculiar fabric called scalloped fabric (Logan et al., 1974).

Pustular mats (0 to −40 cm) produce a bushy brown surface composed of jelly-like pustules that display green, gold and purple thick mucilage inside. Pustular mats trap sediments composed of grains of peloids, ooids, quartz, shell fragments, bioclastic grains of gastropods, serpulids and foraminifera. In addition, white micrite is visible inside the mucilage (biomineralization), forming patches of mud that connect other particles or grains. As a consequence of their vertical growth pattern (Golubic, 1976a), after lithification, the ‘bushes’ generate a non-laminated, irregular, thrombolitic clotted fabric (sensu Aitken, 1967). Pustular mats dominate the intertidal zone and are not prevalent in the upper subtidal zone, where an excess of fine carbonate particles discourages their growth.

Smooth mats (−5 to −60 cm) reveal beige to light yellow-orange surface colour and internal fabric of flat sub-horizontal millimetre-scale laminae composed of fine-grained carbonate sediment trapped and bound into cyanobacteria filament mesh. Laminae of carbonate grains (peloids, ooids, shell fragments, foraminifera, serpulids and seagrass) alternate with laminae of microbial organic matter. Smooth mats occur in the upper subtidal zone, where a large amount of particles in suspension transported by high tides or storms deposit as sedimentary layers. The macro-fabric is easily recognizable, because it exhibits laminar parallel layers similar to those in ‘classic’ stromatolites. When exposed, smooth mats desiccate and shrink, and the oxidizing organic matter produces a characteristic laminoid fenestral fabric (Logan et al., 1974).

Colloform microbial deposits (−0·5 to −1·5 m) construct beige elongate prismatic structures (long axis oriented normal to tidal action and shoreline) in the subtidal environment of Nilemah (Fig. 14), by trapping fine carbonate particles and producing lithified layers of micrite. The laminae are sub-parallel with convex-up forms showing different curvature angles, displaying a wavy pattern with space between the laminae. The coarse undulating lamination is peculiar and distinctive for colloform subtidal deposits, designated as a laminar wavy fabric. Between lithified laminae, some sub-horizontal less-lithified and porous layers make it easy to distinguish and characterize the fabric. The subtidal colloform structures provide shelter for many living organisms, with bioturbation and disrupted laminae often visible in samples.

Figure 14.

Underwater photograph at Nilemah showing colloform structures growing over microbial pavement. Colloform microbialites construct elongate prismatic structures as ‘fingers’ oriented according to the tidal runoff.

Microbial pavement (−1·0 to −6 m) is a light brown deposit (Fig. 14) of bioclastic, oolitic and peloidal grains, also including Fragum erugatum shells, shell fragments, serpulids, foraminifera, gastropods, the green alga Acetabularia, brown alga Fucales, and red alga Gigartinales. Layers of lithified grains alternate with irregular layers of shells, with large voids remaining between sub-parallel laminae. Biologically induced white micrite, peloid fusion and aragonite cement produce lithification of the pavement, which colonizes extensive areas of the subtidal zone at Nilemah as a lithified layer with tabular or blocky surfaces. Layers of bivalve shells oriented convex-up define incipient laminations. The fabric is sub-laminar to irregular with coarse voids. Evidence of microbial activity generating the carbonate pavement is given by: (i) the presence of micritized and fused peloid grains; (ii) carbonate re-precipitation inside fused peloids; (iii) the presence of an organomineralized carbonate film (probably exopolymeric substances, EPS) that binds and envelopes grains and particles (Fig. 15); (iv) taxonomic study that recognized the presence of living cyanobacteria; (v) genomic DNA analysis that recognized genetic sequences from Archaea and Bacteria domains.

Figure 15.

Scanning electron microscopy and thin-section micrographs from sediment samples showing evidence of microbial activity constructing the subtidal ‘microbial pavement’. (A) Thin section (crossed nicols) revealing a pink micrite (light) from peloid fusion, surrounded by green micrite (dark) from a subsequent generation and aragonite crystal growth in some of the voids. (B) Recrystallized micrite observed inside the fused peloids. (C) Evidence of bioturbation, micritization and recrystallization in ooids and skeletal grains. (D) Skeletal grain (serpulid) coated by micrite. (E) Detail of a quartz grain with a coating of micrite followed by aragonite crystals. (F) Carbonate sediment with ooids presenting evidence of bioturbation, recrystallization and micrite connecting grains.

Microbial sediment microfabrics

Thin-section and SEM (Figs 15 and 16) have revealed details of the internal arrangement of the microbial sediments. Samples representing soft recent sediments were taken from microbial mats and sediments at the surface or just below, from the supratidal to the subtidal zone. Because of the soft organic rich substrate, thin sections were not always able to reproduce the fabric relations and preserve sedimentary characteristics; many sections contained only disconnected portions of the mats.

Figure 16.

Photographs and photomicrographs of microbial products in different tidal zones. Blister mats (‘1A’ to ‘1D’) represent the supratidal environment with micrite, peloids, skeletal grains and gypsum ‘g’ crystals (1A), orange microcrystalline micrite as patches and quartz ‘q’, (1B), detail showing micrite with aragonite fringe (1C), and detail showing peloids ‘p’ partially affected by micritization, skeletal grains ‘s’ and micrite (1D); pustular mat (‘2A’ to ‘2D’) from the intertidal zone with coarse dark mucilage ‘m’ over carbonate white peloids and micrite (2A), alternation of fine grainy layers and micrite-rich horizons (2B), detail of micrite patches with a golden ‘go’ and other dark green ‘gr’ micrite, presumably from biomineralized bacterial capsules (2C), detail of golden ‘go’ and dark green ‘gr’ micrite (2D); smooth mat (‘3A’ to ‘3D’) from the subtidal zone with grainy levels and red organic-rich laminae (3A), detail of skeletal grains with black sulphate and peloids and micrite layers (3B), partially micritized and fused peloids with orange organic matter films (3C), detail of peloid grains surrounded by microbial mucilage ‘om’ and bacterial filaments ‘f’ (3D); colloform structure (‘4A’ to ‘4D’) with coarse sub-parallel laminar lithified levels alternating with skeletal and carbonate grains with voids (4A), detail of the carbonate sand (4B), peloids and ooids surrounded by needles of aragonite cement ‘a’ (4C), detail of a lithified level and two generations of cream and dark green micrite (4D).

Microfabrics are composed of grains/fragments of quartz or carbonate, microcrystalline micrite, organic matter and aragonite. Carbonate grains of peloids and ooids (cf. Tucker, 2001; Scholle & Ulmer-Scholle, 2003) interact with the skeletal fragments of shells, calcified algae and exoskeletons of bivalves, serpulids, gastropods and foraminifera. Quartz grains occur in microbial mats, mainly in the supratidal or intertidal zones. Micrite appears golden or dark green to black, composed of microcrystalline aragonite. Aragonite cement occurs mainly in the subtidal zone as needles surrounding the peloids and ooids, filling interstitial space. As highlighted by the mineralogical XRD analysis, the sedimentary deposits forming on tidal flats in Shark Bay are composed almost entirely of aragonite and quartz, with only small amounts (less than 3%) of magnesium-calcite and calcite.

The supratidal blister mat (Fig. 16, ‘1A’ to ‘1D’) is composed of skeletal grains, peloids, quartz and golden yellow micrite as a product of bacterial precipitation (biomineralization), which produces calcarenitic (Reid et al., 2003) microfabric. The microcrystalline micrite resembles a primary organic deposit surrounding and connecting grains in the sediment matrix. Aragonite and small gypsum crystals are also present as secondary infilling. No lamination or any kind of organization can be recognized in these sediments, which are always disturbed by high evaporation rates and exposure. Peloid aggregates and micritized grains are observed and may produce patches of irregular micrite when lithified (cf. Spadafora et al., 2010).

Tufted mats are recognizable as an important sediment trapper because they are rich in carbonate grains, bioclasts and quartz. Microbial activity in tufts promotes a differential fabric of grains and patches of micrite with non-laminar characteristics in thin section.

Pustular mats (Fig. 16, ‘2A’ to ‘2D’) in thin section reveal a microfabric of skeletal grains, shell fragments, fine quartz grains and distinct golden yellow and dark green to black microcrystalline micrite with a granular texture of 1 to 3 µs.

The amount of micrite in irregular patches is an important characteristic of pustular mats. It has been attributed to the process of biologically induced carbonate mineralization (see Dupraz et al., 2009) in microbial polysaccharides surrounding the cells of coccus bacteria, Gloeocapsa, Chroococcus and Entophysalis (sensu Golubic, 1976a), and is also extensively produced by sulphate-reducing bacteria (Decho, 2000; Riding, 2000; Reid et al., 2003; Dupraz & Visscher, 2005; Visscher & Stolz, 2005; Baumgartner et al., 2006; Vasconcelos et al., 2006).

Smooth mats (Fig. 16, ‘3A’ to ‘3D’) dominate the upper subtidal zone, trapping and binding carbonate peloids and ooids, and produce a microfabric of carbonate grains interbedded with films of orange microbial organic gel with bacterial filaments (Fig. 16, ‘3D’), organized as a fine parallel laminar microfabric. Fresh uncemented peloid grains are trapped, surrounded by films of microbial gel and bacterial filaments in millimetric horizontal laminae. A film of orange gel with filaments limits the layer above to another layer of micritized peloidal grains, some fused and others truncated. The mechanism of microbial structure lithification by endololithic bacteria reworking carbonate by fusing grains and inducing carbonate recrystallization is important for early lithification (Golubic et al., 1984; Macintyre et al., 2000; Reid et al., 2003). The filamentous bacteria Schizothrix sp., the dominant genus in the smooth deposits, inhibit syndepositional aragonite precipitation in interstitial spaces (Reid et al., 2000, 2003; Kawaguchi & Decho, 2002).

Colloform internal fabrics and microfabrics show a succession of lithified and non-lithified laminae of carbonate grains, dark brown micrite and aragonite cement (Fig. 16,  ‘4B’ to ‘4C’). One important characteristic of the fabric is the presence of elongate sub-horizontal voids between the sub-parallel laminae that normally have convex-up morphology. The lithified laminae are vertically connected by lithified columns as a growth pattern in the subtidal environment. Sub-horizontal laminae of fused peloids, which vary in thickness from 0·5 to 2 mm and have lateral continuity over several centimetres, are surrounded by a last generation dark brown micrite (Fig. 16, ‘4C’).

Microbial pavement displays a microfabric composed of carbonate sand and bivalve shells interbedded with layers of micrite and aragonite. However, some samples do not show any kind of lamination, and the sediment contains abundant exoskeletons of bivalves and serpulids. Bioturbation and the presence of large voids with growing aragonite needles seem responsible for this irregular macrofabric and microfabric, designated as cryptomicrobial non-laminated (sensu Kennard & James, 1986). Carbonate grains with a sulphate coating and pyrite infilling internal skeletal voids are also recognizable.

Taxonomic studies

Gebelein (in Logan et al., 1974) established a basic framework of common microbial species in sediments at Hamelin Pool. The present study provides a more detailed account of the microbial communities within the three tidal flats analysed.

A taxonomic grouping was established based on microscopic characteristics of the dominant cyanobacteria on the surface of microbial mats or structures (Fig. 17). Sixteen species of cyanobacteria were identified using a bibliography from the classic work of Prescott (1975), Anagnostidis & Komarek (1988), Komarek & Anagnostidis (1999), and others.

Figure 17.

Principal microbial deposits and dominant microbial species. Filamentous bacteria dominate the blister, tufted and smooth mat environment and Coccus bacteria dominate the pustular, colloform and microbial pavement.

Ten species that belong to the Class Cyanophyceae, Order Chroococcales, live in coccus colonies and have small spherical to oval forms arranged in envelopes of jelly-like mucilage, normally yellow to dark orange in colour. Another six species belong to the Class Hormogonae, Order Oscillatoriales; these filamentous bacteria with elongate formats are often surrounded by a sheath that contains many individual cells with colours ranging from dark green to light green and blue. Filamentous bacteria are the dominant group, producing blister mats (Microcoleus chthonoplastes), tufted mats (Lyngbya aestuarii, Lyngbya fragilis and Phormidium willei) and smooth mats (Schizothrix friesii and Microcoleus chthonoplastes).

Coccus bacteria dominate the pustular mats (Gloeocapsa punctata, Chroococcus minimus and Entophysalis granulosa), colloform deposits (Entophysalis granulosa, Chroococcus turgidus and Gloeothece vibrio) and microbial pavement (Cyanosarcina thalassia, Chroococcus microscopicus and Entophysalis conferta). Diatoms from the genus Navicula bory and others were identified in samples from smooth, colloform and microbial pavement, but despite the thick mucilage around the diatom cells, colonies of bacteria have been seen inside the extracellular polymeric secretions (EPS), and the process of organomineralization appears to be driven by bacteria even in diatom domains.

Discussion

The exceptional variety of microbial communities and their distribution pattern according to the topography and tidal zones with their specific internal fabrics identifies Shark Bay as a unique environmental setting. The modern microbial system is producing internal fabrics with stromatolitic, thrombolitic and cryptomicrobial characteristics arranged laterally within the same environment. Thrombolitic fabrics also occur in shallow intertidal environments preceding stromatolitic fabrics in contrast to statements by other authors (Aitken, 1967; Kennard & James, 1986; Feldman & McKenzie, 1998). The widespread nature and distribution of microbialites emphasizes the applicability of Shark Bay as an analogue for ancient systems and increases scientific understanding of microbial deposits, which have significance as peritidal environmental markers and reservoir analogues. Table 4 is a summary of the contrasting properties of microbial mats and sediments within the littoral zones of the three tidal flats studied in Shark Bay.

Table 4. Comparison between tidal flats, water salinity and the contrasting properties of microbial mats and sediments within the littoral zones
Tidal flatWater salinityContrasting properties
Garden PointMetahaline to hypersalineMicrobial mats: Pustular mat dominates. Smooth mat only in restricted pond. Microbial sediments: Carbonate veneer (30 cm max.) with significant influx of quartz sand. Subtidal zone: Bioclastic-quartz sand sheets (proximal) and bioclastic seagrass banks (distal). Bioturbation: Disturbs and reworks microbial mats. Sediment isotopes: Concentrate in less positive values of δ13C (+3·4 to +5·2) and δ18O (+2·0 to +3·6). Onset of hypersalinity: Coquina storm deposits dated 14C 2050–2150 (±35 years)
Rocky PointMetahaline to hypersalineMicrobial mats: Pustular mat dominates intertidal zone and smooth mat incipient in the subtidal zone. Microbial sediments: Carbonate veneer (50 cm max.) with influx of quartz sand. Subtidal zone: Smooth mat (proximal) and bioclastic seagrass banks (distal). Bioturbation: Disturbs and reworks microbial mats. Sediment isotopes: Concentrate in intermediate values of δ13C (+3·6 to +5·3) and δ18O (+2·5 to +3·8). Onset of hypersalinity: Coquina storm deposits dated 14C 2420, 2830 and 3160 (±35 years)
NilemahHypersalineMicrobial mats: Pustular mat dominates intertidal and smooth, colloform and pavement in subtidal zone. Microbial sediments: Carbonate layer (1·30 m max.) and low influx of quartz sand. Subtidal zone: Smooth, colloform structures and microbial pavement widespread. Bioturbation: Limited by hypersalinity.Sediment isotopes: Concentrate in more positive values of δ13C (+4·0 to +5·9) and δ18O (+3·0 to +3·9). Onset of hypersalinity: Coquina storm deposits dated 14C 4630 (±35 years)

The main shallow intertidal microbial mat within the tidal flats is the pustular mat characterized by a superficial vertical growth style (cf. Golubic, 1976a,b) of small mucilaginous pustules that also trap peloidal carbonate particles. After desiccation, this mat produces a mesoclotted fabric that may be designated thrombolitic (Logan et al., 1974). In SEM images, pustular fabric exhibits two types of micrite: (i) a light pink to gold micrite that is apparently a product from the pustules’ mucilage mineralization from communities of coccus bacteria (Gloeocapsa, Chroococcus and Entophysalis), peloid fusion and EPS mineralization; and (ii) a dark green to black micrite that surrounds grains and is pervasive, occurring as the last generation product of extensive microbial EPS biomineralization, which is preferentially conducted below the sediment surface, mainly by communities such as sulphate-reducing bacteria and anoxygenic phototrophs (Decho, 2000; Reid et al., 2000; Dupraz & Visscher, 2005; Visscher & Stolz, 2005; Vasconcelos et al., 2006; Dupraz et al., 2009). Microbial sulphide oxidation to elemental sulphur has a positive effect on alkalinity because the pH shifts to alkaline, favouring carbonate precipitation (Vasconcelos et al., 2006).

The microbial pavement is a permanently subtidal microbial deposit that occurs in Nilemah embayment as flat substrate which is being lithified to form a bioclastic grainstone composed of Fragum bivalves, serpulids, micro-gastropods, foraminifera and algae. The meso-fabric is non-laminated cryptomicrobial (sensu Kennard & James, 1986) with open voids and shelter porosity. The microfabric is particularly related to the presence of bivalve shell bioclastic fragments and ooids that are being lithified by a spongy pervasive micrite (seen in SEM) presumably from sulphate-reducing coccoid bacteria and methanogenic activity.

Communities of dominant cyanobacteria living on the surface of microbial mats and structures indicates correlation of predominantly laminated fabrics (tufted and smooth mats) with filamentous bacterial activity (Lyngbya, Phormidium, Schizothrix and Microcoleus) while non-laminated fabrics relate to the presence of coccus bacteria. Within the intertidal zone in the pustular domain the coccus bacteria (families Entophysalidaceae Geitler, Microcystaceae Nageli and Chroococcaceae Nageli) occur as gelatinous colonies of spherical to sub-spherical cells exhibiting mainly light green-blue colours, cell diameters varying from 2 to 20 µm with predominance of sizes of less than 5 µm. Subtidal colloform structures, despite their weakly laminated fabric, reveal the dominance of coccus bacteria (families Chroococcaceae Nageli, Entophysalidaceae Geitler and Synechococcaceae Komarek & Anagnostids) which are usually in gelatinous spherical colonies with Chroococcus turgidus showing the larger diameters (15 to 25 µm). Microbial pavement is represented by non-laminated cryptomicrobial fabric with superficial coccus communities (families Chroococcaceae Nageli and Entophysalidaceae Geitler).

A lithified pavement that is commonly reached centimetres below the modern surface was described in the tidal flats of Shark Bay corresponding to an old Holocene surface. This surface was dated as 568, 503 and 490 ± 43 14C years (calibrated ages) and is presumably related to a regional small sea regression. The ages obtained correspond to a period between 1444 and 1521 ad that is referred to in the literature as dry in the Southern Hemisphere. Lake Malawi water level (from 1570 to 1850 years ad) was about 120 m lower than during the previous three centuries (Johnson et al., 2001) and ice core studies showed that atmospheric circulation intensity increased in the Polar South Pacific and North Atlantic at the beginning (ca 1400 ad) of the most recent Holocene rapid climate change known as the Little Ice Age (LIA; Kreutz et al., 1997).

Evidence of a modern sea-level rise has been recognized in several sites characterized by a minor landward shift of microbial activity. Exposed surfaces that were severely destroyed forming breccia are nowadays becoming covered by shallow film mats (Halococcus hamelinensis sp.; Goh et al., 2006; Goh, 2007) and other sites show clear recolonization of pustular mats over lithified pavements and over microbial build-ups (cf. Jahnert & Collins, 2012).

Microbial tidal flats in the Shark Bay World Heritage region occupy a ‘niche area’ of hypersalinity and alkalinity in the Holocene. Whilst they have apparently thrived during the relative climate stability of the last 6000 years of slowly falling sea-level, their future is more uncertain under the predicted climatic change scenario. Shark Bay tidal flats are reaching a critical moment in their evolutionary history; microbial deposits are highly susceptible to salinity and/or sea-level changes. If sea-level conditions remain at still stand or rise slowly, the microbial community will still produce aggrading carbonate layers, and the embayments will become more and more dominated by carbonate. Rapid sea-level rise could lead to environmental instability, increased sediment mobility, salinity fall and microbial decline. On the other hand, if sea-level falls significantly, microbial survival will also be threatened. A total detachment from the open embayment will generate a shallow evaporitic peritidal environment, and evaporites will progressively restrict microbial and mollusc life, creating a ‘sabkha’ environment.

In contrast, ancient microbial system analogues of the Phanerozoic and earlier often persisted for long (more than tens of millions of years) periods in stable tectono-eustatic and climatic settings allowing thick (many tens of stacked tidal flat cycles) sequences to accumulate over large areas of entire sedimentary basins recorded as microbial rocks. Examples from the Middle Ordovician of Canning Basin, Nita and Goldwyer Formations, Western Australia (Karajas & Kernick, 1984); Ordovician of the central Appalachian Basin, United States (Pope & Read, 1998); Permo-Triassic of central European Basins, Zechstein-Buntsandstein Group (Paul & Peryt, 2000) and Cretaceous of South America, Santos Basin pre-salt sequence (Formigli et al., 2009) reinforce the significant past distribution of these microbial deposits which frequently serve as hydrocarbon reservoirs and sometimes as source rocks.

Conclusions

This study has produced advances in the understanding of the Holocene microbial system and its establishment and development within three distinct tidal flats in Shark Bay. It provides a new detailed characterization of the taxonomic grouping of the dominant cyanobacterial consortium whilst describing previously undocumented tidal flat evolution, their microbial colonization and carbonate deposition.

A tentative chronological reconstruction of sea-level events emphasizes the late Holocene microbial activity that produces carbonate deposits with distinct macrofabrics and microfabrics. These fabrics are related to the different microbial communities inhabiting very specific topographic tidal zones, and their products can be defined as stromatolitic to thrombolitic and cryptomicrobial sediments. Also recognized was the importance of the ‘distal’ subtidal zone microbial deposits at Nilemah (designated ‘microbial pavement’) extending to as deep as 6 m. These deposits provide an essential element to the system by consolidating the soft sandy or shelly substrate and thereby providing a hardground as a solid base for microbial head growth.

Environmental differences were recorded between tidal flat waters of different salinity and also in microbial sediments that possess, in permanent hypersaline waters (Nilemah), more positive δ13C and δ18O isotopic values and have an older 14C age. In the Nilemah permanently hypersaline domain, extensive subtidal microbial activity and colonization generated structures (Colloform) or spread as cryptomicrobial pavement. In the Garden Point and Rocky Point, tidal flats where salinity values vary from metahaline to hypersaline there is incipient colonization of the subtidal substrate. Smooth mat is present but the subtidal zone does not display any microbial construction and is still receiving offshore sandy influx (Garden Point) during storm events. In addition, these younger tidal flats are distinguished by seagrass growth at their sublittoral margins. There is also a large amount of quartz sand within the microbial fabrics because of the relatively late onset of microbial activity (Table 4).

The following processes and findings are fundamental in explaining microbial prosperity in Shark Bay:

  1. Falling sea-levels over the last 6000 years have been responsible for a shallowing in water depth in the embayments and tidal flats, causing a seaward shift of the depositional system. Because of the marine regression, new beach ridges have developed, mainly by longshore currents controlled by southerly winds and high tides in seaward zones. As a result, coastal re-entrances have become protected by north–south oriented barrier ridges, which restricted water circulation, generating extensive tidal flats exhibiting different stages of evolution and with different stages of microbial colonization.
  2. A shallowing-up sedimentary cycle was established for the Holocene deposits and correlated with sea-level variations, where microbial sediments aged younger than 2360 (1901 calibrated age) 14C years occupy the upper levels of the sedimentary column.
  3. A lithified layer was described and interpreted as an exposure of the tidal flats, indicating a brief late Holocene event of sea-level below the current level at Shark Bay. Carbon-14 dating from shells associated with the exposure surface showed ages between 940 and 1040 years (490 to 568 years, calibrated age).
  4. The stressing conditions in the tidal environment were responsible for microbial establishment, trapping and binding or biologically inducing CaCO3 precipitation, and producing laminated stromatolites (tufted, smooth and colloform), non-laminated clotted thrombolites (pustular) and cryptomicrobial non-laminated deposits (blister and pavement).
  5. Tidal flats have low and smooth bottom gradients, varying from 20 to 80 cm km−1 at Garden Point and Rocky Point and from 20 to 150 cm km−1 in Nilemah. This low relief is responsible for the restricted tidal influx and well-defined tidal zonation. The intertidal zone occupies 70% of the environment with pustular mat dominance at Garden Point and Rocky Point. At Nilemah, the subtidal environment has significantly more widespread microbial deposits than the intertidal zone. Subtidal microbial deposits at Nilemah grow as mats (smooth) or microbial structures (colloform and microbial pavement) colonizing submerged areas (0·5 to 6·0 m water depth) in the subtidal zone of Hamelin Pool.
  6. Microbial mats living in the supratidal and intertidal zones trap coarse carbonate and quartz grains and bioclastic fragments, in contrast to subtidal systems, which accumulate, after storms, a large amount of very fine/fine grains of carbonate peloids/ooids temporarily suspended by the high water energy. Subtidal deposits have light colours because they lack dark pigment, unlike those living in shallower areas, which apparently require pigments in more exposed settings.
  7. Filamentous bacteria are the dominant group in the blister, tufted and smooth mats, and coccus bacteria dominate the pustular, colloform and pavement structures. In the subtidal zone, colloform and microbial pavement structures coexist with other living organisms, such as serpulids, bivalves, diatoms, Acetabularia, crustaceans, algae, foraminifera and micro-gastropods, which are responsible for both exoskeleton supply and extensive bioturbation.
  8. Microbial deposits are composed of carbonate grains and quartz, bioclasts, microcrystalline micrite, organic matter and aragonite needles. Carbonate peloids and ooids occur with shells and algal bioclasts, exoskeletons of bivalves, serpulids, gastropods and foraminifera. Fabrics include laminated, sub-laminar, scalloped, irregular, cryptomicrobial and clotted, depending on the amount of fine-grained carbonate and bioclasts available, bioturbation intensity, the microbial growth capacity and propensity to trap and bind or induce precipitation of CaCO3.
  9. Relative age and degree of salinity elevation control the contrasting characteristics of the Garden Point–Rocky Point–Nilemah tidal flat evolutionary sequence. Nilemah tidal flat exhibits the thickest and best-developed microbial system and was established before the other tidal flats, from 2360 years ago, with carbonate sediment composed mineralogically of aragonite with only traces of magnesium-calcite, calcite and gypsum, and revealing more positive values of δ13C and δ18O.

Acknowledgements

The authors are grateful to the Brazilian Oil Company Petrobras, who sponsored this project and Curtin University for overall support. They appreciate the suggestions and collaboration of Pieter T. Visscher during some of the field work activities. They also appreciate the support of the Department of Environment and Conservation (DEC) scientists, particularly David Holley (Denham), Alan Kendrick (Kensington), for digital orthophotos, sampling permission and field support, as well as Landgate, Western Australia, for providing aerial-photos and orthophotos. The authors thank Fabio de Paula for field assistance. Cavalcanti and Damazio of the University of Rio de Janeiro are thanked for providing taxonomic identifications. The authors are grateful for the support of Brian and Mary Wake (Hamelin Station), Bob Morris and Shane Shulze (Hamelin Pool Caravan Park) and Samuel Fenny (Carbla Station). Analytical support was provided by several collaborating agencies (acknowledged in Materials and Methods) who are also gratefully thanked. Ms Alexandra Stevens assisted and is thanked for her contributions to refining the manuscript. Two anonymous referees are thanked for their suggestions that resulted in improvements to the manuscript.

Ancillary