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Building biogenic beachrock: Visualizing microbially-mediatedcarbonate cement precipitation using XFM and a strontium tracer
Jenine McCutcheon, Luke D. Nothdurft, Gregory E. Webb,Jeremiah Shuster, Linda Nothdurft, David Paterson, GordonSoutham
PII: S0009-2541(17)30306-6DOI: doi: 10.1016/j.chemgeo.2017.05.019Reference: CHEMGE 18350
To appear in: Chemical Geology
Received date: 9 February 2017Revised date: 15 May 2017Accepted date: 17 May 2017
Please cite this article as: Jenine McCutcheon, Luke D. Nothdurft, Gregory E. Webb,Jeremiah Shuster, Linda Nothdurft, David Paterson, Gordon Southam , Building biogenicbeachrock: Visualizing microbially-mediated carbonate cement precipitation using XFMand a strontium tracer, Chemical Geology (2016), doi: 10.1016/j.chemgeo.2017.05.019
This is a PDF file of an unedited manuscript that has been accepted for publication. Asa service to our customers we are providing this early version of the manuscript. Themanuscript will undergo copyediting, typesetting, and review of the resulting proof beforeit is published in its final form. Please note that during the production process errors maybe discovered which could affect the content, and all legal disclaimers that apply to thejournal pertain.
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Building biogenic beachrock: Visualizing microbially-mediated carbonate cement
precipitation using XFM and a strontium tracer
Jenine McCutcheon a*
1, Luke D. Nothdurft
b, Gregory E. Webb
a, Jeremiah Shuster
c,d, Linda
Nothdurfta,b
, David Patersone, and Gordon Southam
a
aSchool of Earth & Environmental Sciences, The University of Queensland, St Lucia, QLD
4072, Australia bSchool of
Earth, Environmental and Biological Sciences, Queensland University of
Technology, Brisbane, QLD 4000, Australia cSchool of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia
dCSIRO Land and Water, Glen Osmond, SA 5064, Australia
eAustralian Synchrotron, Clayton, Melbourne, VIC 3168, Australia
*Corresponding author email: j.mccutcheon@leeds.ac.uk
1Present contact information for corresponding author: School of Earth and Environment,
University of Leeds, Leeds, LS2 9JT, United Kingdom; phone: +44 113 343 2846
A manuscript prepared for submission to: Chemical Geology
Keywords: beachrock; carbonate cement; cyanobacteria; sand cays; microbialite; X-ray
fluorescence microscopy; strontium
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Abstract
The fate of reef islands is a topic of ongoing debate in the face of climate change-induced
sea-level rise and increased cyclone intensity. Increased erosion and changes to the supply of
reef-derived sediment may put sand reef cays at risk of dramatic morphological changes.
These changes may have negative implications for the existence of reef cay environments,
which host vital sea turtle and bird rookery habitats. Beachrock, consolidated carbonate beach
sediment in the intertidal zone, forms naturally on many tropical beaches and reduces the
erosion rates of these beaches when compared to unconsolidated sand. In spite of the critical
role beachrock plays in stabilizing some reef cay shores, the method of beachrock formation
is still incompletely understood. In this investigation, beachrock was synthesized using beach
sand and beachrock samples from Heron Island (Great Barrier Reef, Australia) in aquarium
experiments in which natural beachrock formation conditions were simulated. Beachrock was
produced in two aquaria wherein the water chemistry was influenced by microorganisms
derived from the natural beachrock ‘inoculum’, whereas no cementation occurred in an
aquarium that lacked a microbial inoculum and was controlled only by physicochemical
evapoconcentration. The new cements in the synthesized beachrock were analyzed using
synchrotron-based X-ray fluorescence microscopy and were identified using a Sr-tracer
added to the experimental seawater. The resulting precipitates cement sand grains together
and contain abundant microfossils of the microorganisms on whose exopolymer they
nucleated, demonstrating the fundamental role microbes play in beachrock formation. These
results are of interest because beachrock could be utilized as a natural coastline stabilization
strategy on sand reef cays, and in turn, protect the unique habitats reef islands support.
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1. Introduction
Of all coastal environments that will be influenced by sea-level rise and increased
cyclone intensity, sandy beaches on low elevation coral reef cays are among the most
vulnerable due to their susceptibility to erosion. The complex geomorphological changes to
coral reef sand cay size, shape, and structure resulting from sea-level rise have been the focus of
several recent investigations (Cowell and Kench, 2001; Gibbons and Nicholls, 2006; Perry et
al., 2011; Webb and Kench, 2010; Woodroffe, 2008; Zhang et al., 2004). Additionally, damage
to coral reefs caused by an anticipated increase in cyclone intensity will likely outpace the
recovery rate of corals, which in turn negatively affects other species dependent on the reef
(Cheal et al., 2017). These changes, along with island inundation, have the potential to
negatively influence sand cays populated by humans (Ford, 2012) and those that provide
valuable wildlife habitats such as turtle and bird rookeries (Fuentes et al., 2009; Fuentes et al.,
2011; Pike et al., 2015; Poloczanska et al., 2009). Understanding, and potentially counteracting,
these alterations to island morphology may be a necessity for the future of life on reef islands.
An important factor in understanding how sand cays will respond to sea-level rise is the
role ecosystems play in maintaining coastal stability (Perry et al., 2011; Spalding et al., 2014).
Saltwater marshes and mangroves are known to reduce wave energy, wave height, water
velocity and turbulence, and thus reduce erosion and/or increase sedimentation (Christiansen et
al., 2000; Gedan et al., 2010; Möller et al., 1999; Spalding et al., 2014). Reefs generate the
carbonate sediment that make up reef islands, while also providing protection for the islands by
reducing wave energy and thus, erosion rates (Kench and Brander, 2006b; Sheppard et al.,
2005).
A coastal ecosystem that has received little attention for its potential to aid in
maintaining sand cay stability is beachrock. Beachrock forms on many subtropical beaches
through the lithification of sediment by cement composed of one or both, aragonite and calcite
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(Gischler, 2008; Hanor, 1978; Neumeier, 1999; Scoffin and Stoddart, 1983; Vousdoukas et al.,
2007; Webb et al., 1999). Beachrock formation has previously been attributed to strictly abiotic
physicochemical processes (Alexandersson, 1969; Alexandersson, 1972; Davies and Kinsey,
1973; Dickinson, 1999; El-Sayed, 1988; Ginsburg, 1953; Gischler and Lomando, 1997; Meyers,
1987; Moore, 1973; Russell and McIntire, 1965). Biological processes also have been suggested
(Davies and Kinsey, 1973; Krumbein, 1979; Maxwell, 1962) with recent studies highlighting
the potential importance of microorganisms in beachrock cementation processes (Danjo and
Kawasaki, 2013; Khan et al., 2016; Krumbein, 1979; Neumeier, 1999; Novitsky, 1981; Webb
and Jell, 1997; Webb et al., 1999). Our recent work (McCutcheon et al., 2016) examining
beachrock from Heron Island (Capricorn Group, Great Barrier Reef, Australia) demonstrated
that microbes are actively contributing to carbonate dissolution and precipitation in beachrock.
Beachrock hosts a unique shoreline ecosystem of lithophytic microorganisms that aid in
generating these lithified deposits by enabling carbonate cement precipitation (Díez et al., 2007;
McCutcheon et al., 2016; Webb and Jell, 1997; Webb et al., 1999). Beachrock forms only in the
intertidal zone, and is known to form relatively quickly on timescales as short as a few years
(Chivas et al., 1986; Easton, 1974; Frankel, 1968; Vousdoukas et al., 2007). These spatial and
temporal constraints on beachrock cementation have allowed relict beachrock to be utilized as
Quaternary sea-level and shore-line indicators (Mauz et al., 2015; Ramsay and Cooper, 2002;
Tatumi et al., 2003; Vousdoukas et al., 2007). Although beachrock has long been known to
reduce erosion of unconsolidated beach sediments by protecting them from wave action (Calvet
et al., 2003; Chowdhury et al., 1997; Dickinson, 1999; Kindler and Bain, 1993), there has been
little investigation into the potential use of beachrock as a means of stabilizing beaches that are
susceptible to erosion. In addition, as the health of many coral reefs decline (Pandolfi et al.,
2011) the extent of the protection they provide to their associated islands decreases, making it
critical to seek alternative strategies for protecting reef islands (Sheppard et al., 2005).
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Although there is a growing body of research suggesting that microorganisms play an
important role in beachrock formation, there has been little experimental work linking microbial
activity to beachrock cement precipitation. In this investigation, natural beachrock formation
conditions were simulated in the laboratory to test the role of microbial activity in beachrock
cementation. Synchrotron-based X-ray fluorescence microscopy (XFM) was used to
characterize the newly formed carbonate cements. These results provide a better understanding
of the role of microorganisms in beachrock generation, and could be used to guide future studies
examining in situ beachrock formation with the aim of stabilizing reef islands as sea-level rises.
2. Materials and Methods
2.1 Field site description and sample collection. Heron Island (750 m × 240 m) is a sand cay
on Heron Reef, a lagoonal platform reef (4.5 km × 10 km) in the Capricorn Group in the
southern Great Barrier Reef (Fig. 1a) (Jell and Webb, 2012; Webb et al., 1999). The northern
and southern shores of Heron Island host beachrock outcrops as much as 20 m in width,
which dip seaward at slopes of 4-16°. The beachrock is lithified primarily by isopachous,
acicular aragonite as well as micritic cements (Gischler, 2008; Webb et al., 1999). The
presence of cemented microbialites in the Heron Island beachrock has been one of the
primary pieces of evidence suggesting a microbial influence in the lithification of these
deposits (McCutcheon et al., 2016; Webb and Jell, 1997; Webb et al., 1999). The microbial
beachrock ecosystem is composed of a consortium of microbial endoliths living on, within,
and between the carbonate grains that make up these deposits (McCutcheon et al., 2016).
Several generations of beachrock occur on Heron Island, with blocks of older beachrock
cemented in place by younger beachrock. Examination of the different beachrock generations
suggests that cementation is an ongoing process; boring of carbonate grains by euendolithic
cyanobacteria releases ions into solution which are precipitated as new cement (McCutcheon
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et al., 2016). Over time, this process results in a transition from high porosity and low cement
content, to low porosity and high cement content. The ‘self-healing’ property of beachrock to
re-cement blocks into place after they have been ripped up by storm activity is examined in
this study. Samples of carbonate beach sand, the apparent youngest generation of beachrock
and associated microbial endoliths were collected from the southern beachrock outcrop of
Heron Island. The carbonate beach sand was collected from the supratidal portion of the
beach and consisted of carbonate sediment 0.5-3 mm in diameter. The apparent youngest
generation of beachrock was selected as a starting material for this study because it contains
less cement than its older counterpart, a characteristic of beachrock that results in the younger
generations being more porous and hosting more microbial biomass relative to older
beachrock (McCutcheon et al., 2016). Furthermore, younger beachrock was chosen for
experimental use as it contains less cement than the older beachrock, making it easier to
discern the precipitation of new cements during the experiment.
2.2 Experimental aquaria design. The samples described above were used in three
experimental aquaria to reconstruct the biogeochemical conditions of the Heron Island beach.
The aquaria were housed in a Conviron Adaptis A1000 growth chamber operating at 25°C,
and 12 h of light (06:00 - 18:00; light intensity: 700 mol) and 12 h of dark (18:00 - 06:00).
Each aquarium was 25 × 17 × 19 cm (l × w × h) in size and contained 8 cm of sediment in the
bottom (Fig. 2). Two of the aquaria acted as experimental systems while the third was used as
a control. The beachrock samples were fragmented so that the ~1 cm-thick surface layer
containing macroscopically visible endoliths was separated from the underlying ‘inner’
beachrock. The ‘fragmented beachrock’ (henceforth referred to as FBR) aquarium contained
7 cm of fragmented inner beachrock covered with 1 cm of the fragmented surface layer
beachrock (Fig. 2). The ‘sand’ aquarium (henceforth referred to as Sand) contained 7 cm of
90% (by weight) beach sand seeded with 10% inner beachrock fragments. This layer was
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topped with 1 cm of 90% beach sand seeded with 10% surface beachrock fragments (Fig. 2).
The control aquarium (Control) contained 8 cm of beach sand from Heron Island with no
beachrock ‘inoculum’. The base of each aquarium was wrapped with aluminium foil up to the
surface of the sediment to prevent light from stimulating cyanobacteria growth through the
sides of the glass.
One end of each aquarium was partitioned off with a plastic mesh screen creating a
sediment-free reservoir for the addition and removal of seawater. The seawater was able to
passively flow through the screen to infiltrate the sediment as a means of mimicking tidal
activity. In each aquarium, the alternating addition (06:00 – 06:30 and 18:00 – 18:30), and
removal of seawater (00:00 - 00:30 and 12:00 - 12:30) occurred at 6 hour intervals using
Masterflex L/S® Precision Variable-Speed Console Drive (07528 series) peristaltic pumps
and Norprene® tubing (internal diameter of 2.4 mm). A volume of 1 L of seawater remained
in each aquarium at all times saturating the bottom 2 cm of the sediment and acted as ‘low
tide’. A volume of 3 L was added to each aquarium as an incoming ‘high tide’, resulting in a
water depth of 13 cm (5 cm above the surface of the sediment). It is important to note that
‘fresh’ seawater (Tropic Marin™ Sea Salt, salinity of 35.0) was prepared for each incoming
tide and the ‘old’ seawater discarded after each outgoing tide. Nitrogen and phosphorous
were added to the seawater in concentrations equal to 10% of those in standard BG-11
cyanobacteria growth medium (109 mg/L NO3- added as NaNO3; 2.2 mg/L PO4
3- added as
K2HPO4) (Vonshak, 1986). These concentrations are comparable to those measured in
groundwater on Heron Island (Chen, 2000). Strontium (40 mg/L Sr2+
added as SrCl2·6H2O)
was used as a tracer to distinguish new carbonate cement from that already present in the
natural material (Banner, 1995; Capo et al., 1998). The concentration of Sr was chosen such
that new cement could be identified by a higher than normal Sr content, but would not be so
high as to interfere with mineral precipitation or cause the aquaria to be supersaturated with
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respect to strontium carbonate minerals. This latter point was confirmed by checking mineral
saturation indices using PHREEQC Interactive Version 3.1.1 (Parkhurst and Appelo, 1999).
The experimental aquaria were run for eight weeks.
2.3 Water chemistry analysis. Water samples were collected every 7 days. On each sampling
day, waters were collected at 07:00, 09:00, 11:00, 19:00, 21:00, and 23:00; providing a means
of documenting aqueous geochemistry conditions in the aquaria at the beginning, middle, and
end of high tide under both light and dark conditions. The pH, conductivity (mS/cm, then
converted to salinity) and dissolved oxygen (DO) (mg/L) of the bulk water were measured in
each aquarium at each sampling time point. Dissolved inorganic carbon was determined by
analyzing water samples using a Shimadzu TOC-L CSH Total Organic Carbon Analyzer by
measuring total inorganic carbon (TIC). Water samples were collected, filtered (0.45 µm
pore-size), and analyzed for cations (Ca2+
, K+, Mg
2+, S
6+, Sr
2+) using inductively coupled
plasma-atomic emission spectroscopy (ICP-AES) using a Perkin Elmer Optima 3300 DV
(measurement uncertainty: 12%). Phosphorous (P as PO43-
) and nitrogen (N as NOx)
concentrations were measured using a Lachat QuikChem8500 Flow Injection Analyzer
(FIA).
2.4 Cement characterization. The surface of the sediment in each aquarium was visually
checked weekly for signs of lithification, with samples of what appeared to be newly lithified
beachrock being collected each week after the first two weeks. Polished thin sections of the
original beach sand, fragmented inner beachrock, fragmented surface beachrock, and weekly
samples of synthetic beachrock collected from the Sand and FBR aquaria were analyzed on
the X-ray fluorescence microscopy (XFM) beamline at the Australian Synchrotron (Paterson
et al., 2011). The petrographic thin sections were affixed to a Perspex sample holder using
Mylar tape and mounted on the sample translation stages of the X-ray microprobe. A
monochromatic X-ray beam (18.5 keV) was focused to ~2.0 µm using Kirkpatrick-Baez
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mirrors (Paterson et al., 2011). The Maia detection system used on the XFM beamline
enables fast, high definition elemental mapping of complex natural materials (Paterson et al.,
2011; Ryan et al., 2010; Ryan et al., 2014). Regions of interest on each thin section were
raster-scanned on-the-fly through the focused beam to accumulate X-ray fluorescence spectra
at each scan pixel. The pixel size was 1×1 µm, 2×2 µm or 10×10 µm and the dwell time per
pixel was between 0.33 and 1.0 msec. GeoPIXE software was used to produce elemental
concentration maps from the raw data (CSIRO, 2011). Elemental concentrations were
quantified by calibrating to thin foil standards of Pt, Fe, and Mn of known areal density. A
large number of elements were simultaneously mapped and analyzed (P, S, Cl, Ar, K, Ca, Cr,
Mn, Fe, Co, Ni, Cu, Zn, Br, Sr) and the information from maps of Ca and Sr were the main
focus of this investigation.
The polished thin sections of synthesized beachrock and whole mount samples of the
associated microbial mats collected from the aquaria were characterized using scanning
electron microscopy and energy dispersive X-ray spectroscopy (SEM-EDS) using a JEOL
JSM-7100F Field Emission SEM (FE-SEM). The whole mount samples of microbial mat and
associated grains were fixed using 2.5% glutaraldehyde and dehydrated through an ethanol
dehydration series (25%, 50%, 75%, 100%, 100%, 100%) using a Pelco Biowave microwave
(each step: 250 W, 40 s, no vacuum) prior to being critical point dried (Tousimis Samdri-
PVT-3B critical point dryer). The dried samples were mounted on stainless steel slug stubs
using adhesive carbon tabs. All thin sections and whole mount samples were coated with 5
nm of iridium using a Quarum Q150T S sputter coater. The thin sections were examined
using back-scattered electron (BSE-SEM) mode at 15 kV and a working distance of 12 mm.
Whole mount samples were examined using secondary electron (SE-SEM) mode at 1, 2, or 5
kV at a working distance of 9 mm. Polished thin-sections of beachrock were observed using a
Leica DM6000M microscope equipped with a Leica DFC310 FX camera. The starting
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materials used to construct the aquaria were characterized using light microscopy and XFM
as described above (Fig. 3).
3. Results
3.1 Water chemistry. The average pH, and DO of the initial seawater were 8.30 and 9.1 mg/L,
respectively (Fig. 4a-b). The pH of the FBR and Sand aquaria increased during the day to
average values of 8.77 and 8.79 at 11:00, respectively; and decreased during the night to
average values of 8.15 and 8.18 at 23:00, respectively (Fig. 4a). The pH of the Control
aquarium remained steady at ~8.30 during both light and dark conditions (Fig. 4a). The DO of
the FBR and Sand aquaria increased to average values of 16.8 and 15.5 mg/L at 11:00 and
decreased to average values of 4.1 and 4.9 at 23:00, respectively (Fig. 4b). The 11:00 averages
are underestimates of the oxygen content of the FBR and Sand aquaria, as they reached the
saturation limit of the DO meter of 20 mg/L by week 5 and 4 of the experiment, respectively.
The DO of the seawater decreased upon addition to the Control aquarium, followed by a slight
increase during the day to a 11:00 time point average of 8.6 mg/L, and a small decrease at night
to a 23:00 time point average of 7.4 mg/L (Fig. 4b). The salinity of the initial seawater was
35.0, and the average salinity in the FBR, Sand, and Control aquaria over the course of the
experiment were 38.4, 38.3, and 37.9, respectively.
The concentration of DIC in the Control aquarium increased from 30.4 mg/L in the
initial seawater during the day to 33.4 mg/L at 11:00, and at night to 33.6 mg/L h at 23:00 (Fig.
4c). DIC in the FBR and Sand aquaria followed the same trend, increasing by 9:00 to 32.5 mg/L
and 33.2 mg/L, and then respectively declining to 26.9 mg/L and 28.0 mg/L by 11:00. At night,
the DIC increased to 38.2 mg/L in both aquaria by 23:00 (Fig. 4c).
The concentrations of Ca2+
and Mg2+
increased during both light and dark conditions in
all three aquaria (Fig. 4d,e). The concentration of Sr2+
measured in the initial seawater was 39.1
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ppm (vs. target of 40 ppm) and exhibited minor fluctuations between 38.4 and 40.9 ppm in all
three aquaria during light and dark conditions (Fig. 4f). Nutrient (N and P) concentrations
decreased during both light and dark conditions in the FBR and Sand aquaria (Fig. 4g,h). From
an initial seawater concentration of 24.7 ppm, nitrogen (as N in NOx) decreased in the FBR and
Sand aquaria to 11:00 average values of 22.9 and 21.5 ppm, and 23:00 average values of 23.9
and 22.2 ppm, respectively (Fig. 4g). Phosphorous (as P in PO43-
) decreased from 0.79 ppm in
the initial seawater to 0.56 and 0.49 ppm by 11:00 and to 0.72 and 0.61 ppm by 23:00 in the
FBR and Sand aquaria, respectively (Fig. 4h).
3.2 Cement formation and characterization. Over the eight week experiment, microbial
growth in the FBR and Sand aquaria resulted in the formation of microbial mats on the
surface of the sediment, reminiscent of those found on the beachrock on Heron Island.
Secondary electron SEM of whole-mount samples of the microbial mats revealed extensive
growth of filamentous cyanobacteria in association with cocci and bacilli bacteria (Fig. 5).
Small, millimeter- to centimeter-sized pieces of beachrock were synthesized in the top
5 cm of sediment in the FBR and Sand aquaria. Beachrock synthesis was first observed three
weeks into the experiment. The relative size of the new beachrock grains increased over time
to a maximum grain diameter of 2 cm. No cemented grains were found in the Control
aquarium at any point during the experiment.
X-ray florescence microscopy of thin sections of the synthesized beachrock from the
FBR and Sand aquaria revealed that the new cement precipitates could be easily identified
due to being enrichment in Sr (Fig. 6-9,11) compared to the original carbonate sediment and
cements (Fig. 3). The original aragonite sand grains and cements contained 0.13 atomic % Sr
while the new cements precipitated during the experiment contained an average of 0.85
atomic % Sr based on EDS analysis. Figure 6 shows cement precipitation in a large region of
a sample collected from the surface of the FBR aquarium after eight weeks, in which the
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plane of the thin section is parallel to the surface of the sediment in the aquarium, while
Figures 7-9a-d highlight smaller structures within this region. The new precipitates can be
seen cementing sand grains together and coating grain surfaces (Fig. 7a,d,e). Viewing the
new cements using SEM revealed abundant microfossils exhibiting a diverse range of cell
morphologies (Fig. 7b) that are commonly preserved as fossilized microcolonies (Fig. 7f-h).
Many of the cement coatings on grain surfaces form dendritic microbialites; they contain
mineralized cells as well as new microbial borings (Fig. 8). Structurally, these newly formed
microbialites are very similar to those pre-existing in the fragmented beachrock added to the
aquaria but can be differentiated from those due to the difference in Sr content (Fig. 9).
Some of the precipitates exhibit a ‘wheat-sheaf’ morphology, interpreted as aragonite
(Fig. 10a,b), while others are present as nanoscale granules (c,d). When viewed in a whole-
mount sample, these precipitates are found in association with extracellular polymeric
substances (EPS) (Fig. 10a,c). EDS of the cement (Fig. 10 e-g) showed a range of Mg-
content, from 0.01 to 12 atomic %, suggesting that co-precipitation of aragonite and calcite
may be occurring within microenvironments in the beachrock system (Berner, 1975; Ries et
al., 2008). The biofilm observed growing on the top surface of the sediment and in the
interstices between sediment grains contains both trapped-and-bound material and newly
precipitated carbonate (Fig. 11).
4. Discussion
4.1 Diurnal microbial activity as a trigger for beachrock cementation through carbonate
dissolution and precipitation. The data presented in Figure 4 is intended to demonstrate the
overall trends in the water chemistry as a function of the diurnal changes in microbial activity
in the FBR and Sand aquaria. During the day, cyanobacterial and algal oxygenic
photosynthesis resulted in the measured increase in dissolved oxygen, coincidentally
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increasing the pH through hydroxyl anion production. At night, heterotrophy would have
been the dominant form of microbial metabolism, resulting in oxygen consumption and a
decline in pH after dark. Note, the changes in water chemistry only reflect the bulk water
overlying the sediment and do not represent the pore water in the biofilm or underlying sand.
As a result, the changes that were measured are a diluted product of what is taking place in
the sediment and it is expected that changes in water chemistry between the grains are far
greater in magnitude. There is also potential that the bulk water chemistry does not reflect
other forms of microbial metabolism known to contribute to carbonate mineral precipitation,
such as that of sulfate reducing bacteria (SRB) (Braissant et al., 2007; Gallagher et al., 2012)
and ureolytic bacteria (Ferris et al., 2004; Mitchell and Ferris, 2006). Although natural
beachrock forms in the intertidal zone, and is thus well oxygenated overall, these organisms
could be found in protected anaerobic microenvironments below the surface of the
beachrock.
The increase in the concentrations of Ca2+
and Mg2+
in the Control aquarium are
likely a result of evaporation (Fig. 4d,e). Interpreting the changes in cation concentrations in
the FBR and Sand aquaria is more difficult because they represent the combined effects of:
evaporation, microbial processes, mineral dissolution, and mineral precipitation. The
summation of these processes makes it difficult to discern which processes took place in the
aquaria at any given time. However, the overall changes in Ca2+
and Mg2+
concentrations are
expected to be largely representative of the net balance between mineral dissolution and
precipitation. For instance, the concentration of Ca2+
measured at 07:00 in all three aquaria
was greater than that measured in the ‘fresh’ seawater added at 06:00. The increase in Ca2+
concentration measured in the Control aquaria was likely a result of evaporation, however,
the greater magnitude increases measured in the FBR and Sand aquaria were likely the
product of two microbial processes taking place contemporaneously: 1) mineral dissolution
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resulting from cyanobacteria boring into the grains; and 2) heterotrophic consumption of
EPS. First, endolithic cyanobacteria in the FBR and Sand aquaria were dissolving carbonate
in detrital grains, producing cations in solution. Some cyanobacteria are known to induce
spontaneous carbonate dissolution at the cell-borehole interface by causing a reduction in the
ion activity product of carbonate (Garcia-Pichel et al., 2010). Once in solution, the Ca2+
ions
are internalized by the apical cell of the cyanobacterium filament, transported down the
length of the filament through intercellular Ca2+
-ATPase pumps, and finally expelled away
from the borehole into the surrounding solution (Garcia-Pichel et al., 2010). Antiparallel
transport of two protons along the filament towards the boring front is necessary to balance
each Ca2+
ion moving away from the excavation site via this intercellular pathway (Garcia-
Pichel et al., 2010). These protons can then contribute to carbonate dissolution, after which
the resultant HCO3- can be utilized by the cyanobacterium for photosynthesis (Garcia-Pichel
et al., 2010). Previous studies on the occurrence of phototrophic boring in coastal
environments suggest that it can dissolve up to 0.6 kg of CaCO3/m2/year (Chazottes et al.,
1995). In natural beachrock formation in the intertidal zone, possible explanations for
cyanobacterial boring include: nutrient or space acquisition; and protection from grazing, UV
radiation, wave activity, and desiccation during low tide (Cockell and Herrera, 2008;
McCutcheon et al., 2016). Some of the borings were likely present in the grains prior to
sample collection; however, those found in the newly precipitated cements indicate that
active microbial boring was taking place during the experiment (Fig. 8b). In the aquaria, the
microbes lacked stressors such as wave activity, macroscopic grazers, nutrient limitation, and
solar UV radiation, suggesting that space acquisition or protection from desiccation during
low tide may be the incentive for microbial boring in beachrock. Some of the pre-existing and
new borings have been filled with new cement made visible by its high Sr-content (Fig. 6,7),
which is consistent with reports of carbonate re-precipitation as a result of localized
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microenvironments of carbonate supersaturation where Ca2+
ions are being excreted by
boring phototrophs (Bathurst, 1966; Garcia-Pichel et al., 2010; Margolis and Rex, 1971). The
presence of cement-filled borings across grain boundaries has been known to provide strength
to carbonate structures, such as stromatolites (Macintyre et al., 2000).
The second possible cause for the increase in Ca2+
concentration is heterotrophic
consumption of EPS. This substance is rich in carboxyl groups that give it a net negative
charge, enabling it to bind cations such as Ca2+
that, in turn, attract low molecular weight
organic compounds (Braissant et al., 2009; Flemming and Wingender, 2010; Körstgens et al.,
2001). Decho et al. (2005) demonstrated that the EPS production rate in cyanobacterial mats
coincides closely with photosynthesis, with the greatest EPS production occurring during
midday. In the present study, as cyanobacterial photosynthesis began to produce oxygen in
the morning, heterotrophic metabolism in the aquarium would have increased and
destabilized the EPS structure by oxidizing the organic compounds to bicarbonate (Braissant
et al., 2009; Decho et al., 2005). The bicarbonate would have then been able to react with the
‘reservoir’ of cations available in the EPS microenvironment. Decho et al. (2005) also
demonstrated that heterotrophic consumption of EPS has a diurnal cycle that peaks with
maximum photosynthesis during the day, as well as just after dark. Consumption of the EPS
releases the adsorbed cations back into solution, causing the concentration of Ca2+
in solution
to increase and making carbonate precipitation favorable. Carbonate mineral precipitation by
this process has resulted in mat lithification in many past and modern environments (Aloisi,
2008; Altermann et al., 2006; Braissant et al., 2007; Dupraz et al., 2009; Dupraz and
Visscher, 2005). Note, the intricate relationships between the dissolved cations and mineral
dissolution and precipitation, biofilm adsorption, and evaporation make it difficult to interpret
the cation concentration data beyond the described overarching trends.
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The beginning of the cementation process, which resulted in the formation of the
mineralized microbialites observed in the aquaria (Fig. 7-10), is captured in the nucleation of
new Sr-enriched carbonate grains within the biofilms (Fig. 11). The production of biofilm on
near surface grains in the FBR and Sand aquaria was extensive enough to provide nucleation
sites for carbonate precipitation such that the resultant cements were able to connect grains in
the span of only eight weeks, demonstrating the rapid nature of this process. This
characteristic is also highlighted by the presence of borings in the new cements (Fig. 8b) and
new cements filling borings, illustrating that beachrock is exceptionally dynamic. It is likely
that the initial stabilization and cementation of sand by microbes allows the longer-term,
more pervasive isopachous cement, common in the older beachrock, to form in the
underlying sand. As consolidation progresses, it appears that the interstitial spaces in the
beachrock become increasingly filled with cement, causing a reduction in the volume of pore
space available for habitation by endolithic cyanobacteria (McCutcheon et al., 2016). The
reduced porosity has a two-fold effect on microbial growth: while decreasing the space
available for biofilm growth it also reduces the amount of water than can be retained in the
beachrock interstices during low tide, thus increasing the likelihood of biofilm desiccation.
Although the older beachrock still hosts an endolithic microbial community, a decline in
microbial biomass over time would likely cause a corresponding decrease in the microbial
contribution to cementation. A subsequent increase in porosity of the beachrock, such as
would occur through damage to the outcrop by storm activity, could instigate a resurgence of
microbial activity and cementation.
4.2 Sea-level rise, beachrock, and island stability. The response of reef islands to sea-level
rise is one of ongoing discussion. Several studies have suggested that these islands will be
vulnerable to sea-level rise through increased erosion, inundation, and salinization of the
water table (Church et al., 2006; Gibbons and Nicholls, 2006; Khan et al., 2002; McLean and
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Tsyban, 2001; Mimura, 1999; Nicholls et al., 2007; Roy and Connell, 1991; Woodroffe,
2008; Yamano et al., 2007). The prevailing hypothesis, that reef islands will be subjected to
extensive erosion in the event of sea-level rise, is largely due to application of the Bruun Rule
to these shorelines (Bruun, 1962; Schwartz, 1967). Such predictions, however, have been
criticized because island shores cannot be treated in the same manner as linear continental
coastlines (Cooper and Pilkey, 2004; Cowell and Kench, 2001; Webb and Kench, 2010).
Reef islands, and particularly sand cays, are dynamic structures that change in morphology as
a result of changes in: wave regimes, longshore currents, ocean dynamics, sea-level, and
weather, particularly storm events (Cheal et al., 2017; Church et al., 2006; Kench and
Brander, 2006a; Mimura et al., 2007). High energy events such as cyclones and tsunamis can
result in either net island erosion (Harmelin-Vivien, 1994; Stoddart, 1963) or accretion
(Kench et al., 2006; Maragos et al., 1973). Cyclone intensity is predicted to increase in the
coming years and result in degradation of coral reefs, a trend already being observed in the
central-south part of the GBR (Cheal et al., 2017). The frequency at which a particular reef
island experiences storms affects the size of the sediment of which the island is comprised.
Sand-sized grains dominate islands that experience low storm frequencies, while islands that
experience frequent storms tend to be composed of rubble (Chivas et al., 1986; Gourlay,
1988; Stoddart, 1963). Some models suggest that reef islands are less delicate than previously
thought and will remain stable in the event of the projected sea-level rise of ~0.5 m by 2100
(Kench et al., 2005). That is not to say, however, that island morphology and location will not
change with increasing sea-level. Predicting these changes requires a better understanding of
the many factors that influence reef island morphodynamics, which necessitates better
monitoring of current changes to reef island morphology (Kench and Harvey, 2003; Webb
and Kench, 2010).
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A major factor in reef island sedimentological processes is the type and health of the
reef from which the islands’ sediments are derived (Woodroffe et al., 2007). The reef acts as a
sediment factory by producing carbonate grains from the skeletal remains of invertebrates living
in and on the reef, as well as through erosion of the reef framework by physical and biological
processes (Perry et al., 2011). Once sediment is generated by the reef, the grains are susceptible
to physical abrasion, microbial boring, and chemical dissolution; the summation of these
processes alter size, shape, and density of the sediment that reaches the island (Perry, 2000).
The sediment is deposited on the beach, where it becomes the starting material for potential
beachrock formation. The species richness and relative abundances of the organisms (corals,
coralline algae, foraminifera, molluscs) from which reef sediment is generated will alter the
type, quantity, hydrodynamic properties, and rate of deposition of the sediment available for
island building (Perry et al., 2011; Yamano et al., 2000). Predicting how ecological problems
such as overfishing, pollution, coral disease and bleaching, changes in storm intensity, sea-
level- rise, and ocean acidification will alter reef health is not a small task (Hoegh-Guldberg et
al., 2007; Jackson et al., 2001; Kuroyanagi et al., 2009; Pandolfi et al., 2003; Perry et al., 2011;
Ries et al., 2009), however, understanding how reefs will respond to these changes is necessary
for predicting their ability to supply sediment for reef island building as sea-level rises.
The dynamic nature of reef islands means that it will not be possible to avoid all changes
to island shape, size, and position on the reef flat. In cases where island erosion is likely to
increase in undesirable locations, such as those inhabited by humans or that provide unique
habitats for organisms, implementing strategies to minimize erosion may be necessary. Beaches
dominated by sand-sized grains are more susceptible to erosion than those composed of rubble
(Perry et al., 2011), and the prevalence of beaches composed of rubble grade sediment may
increase in the event of mass coral bleaching (Baker et al., 2008). The combination of these
factors means that sand beaches may be particularly vulnerable, and erosion or inundation of
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these shorelines may negatively impact sea turtles that rely on supratidal sandy beaches for
nesting (Fuentes et al., 2009; Fuentes et al., 2011; Pike et al., 2015; Van Houtan and Bass,
2007). Beachrock formation may provide a natural means of reducing erosion of sand beaches
on reef islands. The intrinsic process by which beachrock forms, demonstrated in this study,
restricts it to the intertidal zone where it will absorb a large portion of the wave energy that
reaches the shore and protect the supratidal part of the beach from storm activity and erosion.
Since lithification is limited to the intertidal zone, the supratidal sand remains unconsolidated
and suitable for nesting. Beachrock is found naturally on islands that host turtle rookeries,
which is a critical point in the potential to employ beachrock as a means of stabilizing beaches
because it maintains the shore as a ‘beach’, unlike other coastline habitats such as saltwater
marshes or mangroves (Christiansen et al., 2000; Gedan et al., 2010; Spalding et al., 2014). The
dynamic nature of beachrock means that it may continue to form in the intertidal zone even in
the event the island migrates on the reef flat, continuing to protect the unconsolidated sand
further up the shore.
The beachrock on Heron Island shows evidence of multiple generations of
cementation through the presence of older beachrock blocks, presumably ripped up during
storms, being cemented in place by younger beachrock. We have previously proposed an
explanation for how beachrock blocks are re-cemented by microbially generated precipitates
(McCutcheon et al., 2016). This ‘self-healing’ characteristic of beachrock is useful for
stabilizing shorelines because these outcrops can regenerate on decadal or shorter time scales.
The FBR aquarium was, in part, designed as a means of investigating this self-healing
property of beachrock and successfully recreated a small-scale version of a beachrock
outcrop damaged by a storm. This system also provides a natural analogue to the recent
advances in self-healing bioconcrete (Jonkers et al., 2010; Wiktor and Jonkers, 2011).
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It is currently unknown how widespread formation of beachrock could alter large-scale
beach morphodynamics through changes in sediment erosion and deposition (Cooper, 1991;
Larson and Kraus, 2000; Sumer et al., 2005; Vousdoukas et al., 2007). The presence of
beachrock on cay shores should be considered when predicting the morphological behavior of
reef cays, making it necessary to understand the processes driving beachrock formation. Further
investigations are required to understand how beachrock will factor into the already complex
conversation surrounding reef island responses to sea-level rise and reef health, especially if
there is potential to purposefully enhance these dynamic shoreline structures as a strategy for
maintaining reef cay stability.
5. Conclusions
The beachrock synthesis experiment conducted in this study demonstrated the
fundamental role microorganisms play in beachrock cementation processes, and suggested that
physicochemical controls such as evaporation and tidal wetting and drying are not sufficient to
instigate cement precipitation. The use of strontium enriched seawater enabled identification of
the new cements using XFM. Cementation appears to be driven by cation generation through
cyanobacteria dissolution of carbonate grains and subsequent precipitation of new cements in
association with EPS. High-resolution SEM of these precipitates, composed primarily of
aragonite, revealed abundant microfossils. The diversity of observed microfossils indicates that
entire microbial biofilms were becoming mineralized during the beachrock formation process.
These results provide a valuable contribution to the current understanding of the
biogeochemical controls on beachrock formation. These findings may be applied to designing in
situ beachrock cementation experiments, which, in turn, may aid in developing strategies to
utilize beachrock as a natural means of stabilizing vulnerable reef islands against sea-level rise.
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Acknowledgements
Part of this research was undertaken on the X-ray Fluorescence Microscopy beamline at the
Australian Synchrotron, Victoria, Australia. This work was supported by the Multi-modal
Australian ScienceS Imaging and Visualisation Environment (MASSIVE)
(www.massive.org.au). For their technical assistance, we thank Marietjie Mostert and Tracey
Crossingham of the Environmental Analytical and Geochemistry Unit at The University of
Queensland (ICP-OES), Dr. Beatrice Keller-Lehmann and Nathan Clayton of the Advanced
Water Management Centre at The University of Queensland (FIA and DIC), Dr. Ron Rasch
and the staff of the UQ Centre for Microscopy and Microanalysis (SEM-EDS). Beachrock
and sand samples were collected with permission from the Great Barrier Reef Marine Parks
Authority (permit no.: G14/37249.1). J. McCutcheon was supported by a National Sciences
and Engineering Research Council of Canada PhD Postgraduate Scholarship. Funding to G.
Southam was provided in part by Carbon Management Canada (C390).
Figure Captions
Figure 1. (a) Location of Heron Island on Heron Reef in the Capricorn Group of the Great
Barrier Reef off the east coast of Queensland, Australia (Google Earth, 2014). (b) Beachrock
in the intertidal zone along the southern shore of Heron Island. (c) The natural beachrock was
used as a starting material in the beachrock synthesis experiments. (d) Visible growth of
endolithic cyanobacteria near the surface of the beachrock.
Figure 2. The aquarium design used in the beachrock formation experiments. Adding and
removing seawater to and from each of the three aquaria using peristaltic pumps simulated
tidal activity. The three aquaria differed in their sediment content: 1) the fragmented
beachrock (FBR) aquarium contained 100% broken beachrock; 2) the Sand aquarium
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contained 10 wt% fragmented beachrock and 90 wt% beach sand; and 3) the Control
aquarium contained 100% beach sand.
Figure 3. Characterization of the fragmented beachrock and beach sand used in the beachrock
formation experiments. These materials are characterized using: 1) photography of whole
samples, 2) plane-polarized light (PPL), 3) cross-polarized light (XPL), 4) XFM of Ca
content, and 5) XFM of Sr content of polished thin sections. XFM scan conditions: pixel size:
10×10 µm, dwell time: 0.56 msec.
Figure 4. Water chemistry plots showing the change over time of mean (a) pH, and
concentrations of (b) dissolved oxygen, (c) DIC, (d) Ca2+
, (e) Mg2+
, (f) Sr2+
, (g) NOx-N, and
(h) PO43-
-P. Each data point is a time point average for the eight week experiment to reflect
overall trends in the water chemistry.
Figure 5. Secondary electron micrographs showing the biofilms that formed on the surfaces
of the (a-b) FBR and (c-f) Sand aquaria after the eight week experiment. The biofilms are
composed of filamentous cyanobacteria producing abundant EPS, and associated
heterotrophs.
Figure 6. XFM showing the (a) Sr and (b) Sr-Ca content in a sample collected from the
surface of the FBR aquarium after eight weeks of the experiment. In (a) the color scale
indicates Sr concentration, with bright yellow regions having the highest Sr content. In (b)
bright yellow regions indicate higher Sr content, while bright blue indicates higher Ca
content. Note, Sr-rich regions (bright yellow in (a) and (b)) indicate new cement
precipitation. The plane of the sample is parallel to the surface of the sediment in the
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aquarium. Boxes in (b) indicate regions depicted in Fig. 7-9. XFM scan conditions: pixel
size: 2×2 µm, dwell time: 0.33 msec.
Figure 7. (a) XFM showing the Sr-Ca content of a portion of the week 8 Sand aquarium
sample shown in Fig. 6. Note, bright yellow regions indicate higher strontium content, while
bright blue indicates higher calcium content. (b-c) These new cements (yellow in (a)) show a
diverse assortment of microfossil morphologies. (d-e) The newly precipitated carbonate can
be seen cementing sand grains together. (f-h) In many cases the new cements contain
fossilized microcolonies. XFM scan conditions: pixel size: 2×2 µm, dwell time: 0.33 msec.
Figure 8. (a) XFM and BSE-SEM showing the Sr-Ca content and structure of a small region
of the sample depicted in Fig. 6. Note, bright yellow regions indicate higher strontium
content, while bright blue indicates higher calcium content. (b) In-filled microfossils of
filamentous cyanobacteria seen in longitudinal section along with new borings visible among
the microfossils. Most of the new carbonate contains microfossils (c-f) enclosed in EPS and
infilled with micritic cement (f). XFM scan conditions: pixel size: 2×2 µm, dwell time: 0.33
msec.
Figure 9. (a) XFM highlighting the Sr-Ca content and (b) BSE-SEM micrograph of a Sr-
enriched microbialite that formed in the FBR aquarium. Compared to (c) XFM and (d) BSE-
SEM of a natural Heron Island beachrock microbialite, cementing detrital grains together.
Note, in (a) and (c), bright yellow regions indicate higher strontium content, while bright blue
indicates higher calcium content. XFM scan conditions: (a) pixel size: 2×2 µm, dwell time:
0.33 msec; (c) pixel size: 2×2 µm, dwell time: 1.0 msec.
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Figure 10. BSE-SEM micrographs with EDS demonstrating the structural and chemical
heterogeneity of carbonate precipitates: a wheat-sheaf morphology as (a) a whole mount and
(b) a thin section, interpreted as aragonite, and as nanometer-scale granules of carbonate
precipitated on EPS in (c) a whole mount and (d) thin section. EDS spectra (e-g) demonstrate
varying Mg-content.
Figure 11. A cross-section of an embedded biofilm collected from the surface of the Sand
aquarium after eight weeks viewed using (a) optical microscopy and (b) XFM. The bright
yellow grains in (b) show the occurrence of new mineral nucleation, while the blue grains
indicate trapping-and-binding. Bright yellow regions indicate higher strontium content, while
bright blue indicates higher calcium content. XFM scan conditions: pixel size: 1×1 µm, dwell
time: 1.0 msec.
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Graphical Abstract
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