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Marine Pollution Bulletin 62 (2011) 246–250
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
The most temperature-adapted corals have an Achilles’ Heel
S.J. Purkis ⇑, D.A. Renegar, B.M. Riegl
National Coral Reef Institute, Nova Southeastern University Oceanographic Centre, 8000 N. Ocean Drive, Dania Beach, FL 33004, USA
a r t i c l e
i n f o
Keywords:
Persian/Arabian Gulf
Marine hardground
Coral habitat
Global change
a b s t r a c t
The corals of the Persian/Arabian Gulf are better adapted to temperature fluctuations than elsewhere in
the Indo-Pacific. The Gulf is an extreme marine environment displaying the highest known summer
water temperatures for any reef area. The small and shallow sea can be considered a good analogue to
future conditions for the rest of the world’s oceans under global warming. The fact that corals can persist
in such a demanding environment indicates that they have been able to acclimatize and selectively adapt
to elevated temperature. The implication being that colonies elsewhere may be able to follow suit. This in
turn provides hope that corals may, given sufficient time, similarly adapt to survive even in an impoverished form, under conditions of acidification-driven lowering of CaCO3 saturation state, a further consequence of raised atmospheric CO2. This paper demonstrates, however, that the uniquely adapted corals of
the Gulf may, within the next three centuries, be threatened by a chronic habitat shortage brought about
by the dissolution of the lithified seabed on which they rely for colonisation. This will occur due to modifications in the chemical composition of the Gulf waters due to climate change.
Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction
The corals of the Persian/Arabian Gulf display unusual resilience
to temperature stress (bleaching). Summer daily-mean temperatures routinely top 32 °C while winter winds can chill the water
to 12 °C (Sheppard et al., 2010; Sheppard, 2003). Catastrophic
bleaching only occurred in the summers of 1996, 1998, and 2002
when water temperature exceeded 35 °C (Purkis and Riegl, 2005;
Sheppard et al., 2010), well above the 25–29 °C range of thermal
tolerance for corals elsewhere in the world (Buddemeier and Wilkinson, 1994). While these radical temperature excursions in the
Gulf impart mortality on coral species such as Acropora, dominant
frame-builders persist with death-rates much lower than would be
predicted elsewhere in the Indo-Pacific (Baker et al., 2004). Indeed,
such is the ability of the Gulf system to rebound from severe temperature events, that the coral community can regenerate to a fully
healthy state in only a handful of years (Purkis and Riegl, 2005;
Riegl and Purkis, 2009). At the time of writing and even withstanding the again anomalously hot summer temperatures of 2010,
many coral-rich areas in the region boast dense, interlocking,
frameworks of Acropora surrounded by and indeed overtopping,
vigorous growth by faviids and Porites (personal obs.).
This resilience implies that the corals of the Gulf and their algal
symbionts have been capable of acclimatization and selectively
adapt to elevated temperatures (Baker et al., 2004; Obura, 2009;
Rowan, 2004). Such genetic plasticity is in line with recent
⇑ Corresponding author. Tel.: +1 954 262 3647; fax: +1 954 262 4098.
E-mail address: [email protected] (S.J. Purkis).
0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2010.11.005
observations that regions of maximal evolutionary potential exist
on the geographic periphery of reef growth, such as the isolated
high-latitude regime of the Gulf (Budd and Pandolfi, 2010). The
existence of bleaching-resistant populations is pertinent considering the dire predictions for reefs under projected increases in temperature due to global warming (Hughes et al., 2003; Veron et al.,
2009). Since many corals can distribute their larvae widely, their
dispersal is mediated by oceanic currents and the heat-adapted
trait can be imparted to reefs further afield through genetic connectivity. The Gulf therefore represents a potential source of temperature-capable corals that could spread through the adjacent
Indian Ocean, a region that has heretofore shown very little adaption to high water temperatures (Sheppard, 2003). If such a prophecy is to be fulfilled, the corals of the Gulf must maintain a large
and healthy population into the far-future to provide an effective
battery of larvae to nourish the migration.
In this paper we present evidence that the corals of the Gulf
have an Achilles’ Heel. Their weakness lies in a strong reliance on
the availability of lithified seafloor as a firm habitat. Under raised
atmospheric CO2, seawater in the Gulf will shift to become less
conducive to the precipitation of the carbonate cements that presently bind unconsolidated sand to modern rock. This process relies
on an intricate balance of the chemical conditions in the Gulf and
the tendency for cementation is dependent on the ambient pCO2
of seawater. Given that atmospheric pCO2 may rise from its current
value of ca. 380 ppm to 730–1020 ppm by the year 2100 (Caldeira
and Wickett, 2003), the future chemistry of the Gulf will no longer
support seafloor lithification. The formation of this hardground is
critical to the survival of the Gulf’s coral ecosystem as it provides
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S.J. Purkis et al. / Marine Pollution Bulletin 62 (2011) 246–250
substrate for the settlement of juvenile colonies which, with time,
grow into dense thickets (Purkis and Riegl, 2005; Riegl and Purkis,
2009). When production of cement ceases, areas previously offering suitable habitat will revert to the mobile unconsolidated sand
sheets from which the hardgrounds lithify. While corals can reject
sediments, the process is energetically expensive and they cannot
survive, even less settle, in such areas. With the exception of the
Iranian coastline, the Gulf lacks any significant rocky outcrops that
could replace the vast area of lithified substrate (Fig. 1). The ramifications are severe – a vibrant and functional coral ecosystem in
the region will not exist and accompanying its loss will be the
world’s most selectively-adapted heat-tolerant coral population.
The aims of this study are; (1) to investigate the influence of
pCO2 on hardground formation, and (2) to predict the approximate
point in the future where the saturation state for Gulf seawater will
switch to become corrosive to the lithifying carbonate cements
that create hardground.
2. Methods
The Gulf is located in a subtropical, hyper-arid region. It is shallow, and high salinity and summer temperatures lead to the supersaturation of seawater with calcium carbonate (CaCO3). The
carbonate system of the Gulf is hence rich in meta-stable minerals
and seafloor lithification through abiotic precipitation is widespread and rapid (Sheppard et al., 2010; Shinn, 1969). Though it
is typical that reefs contain some proportion of CaCO3 cement that
stiffens the seabed (Manzello et al., 2008), the southern Gulf is unique in that the precipitation of cement directly from the water
column is by far the dominant mechanism creating hard seafloor.
Hardgrounds in the Gulf form exceptionally smooth bedding
planes as sand sheets moving across them plane off topographic
247
irregularities (Shinn, 1969) (Fig. 1B and C). The carbonate cements
responsible for binding the seafloor are typically isopachous fibrous aragonite fringes around grains. With these fibres growing
at rates in the range of 30 lm per year, unconsolidated sand can
be converted to modern rock in a matter of a few years (Grammer
et al., 1993). Cementation starts near-instantaneously, requiring
only a brief cessation of grain movement for a few hours between
tides for the grains to become bound. Observations by diving show
the only difference between hardground and overlying loose sediment is the addition of cement (Shinn, 1969).
The regional extent of Gulf hardgrounds are reasonably well
constrained (Shinn, 1969; Uchupi et al., 1996) and with the exception of the deeper waters along the Iranian coast, it is clear that the
majority of the basin floor is lithified. Samples for this study were
collected using SCUBA from an expansive hardground sheet offshore Abu Dhabi at a water depth of 10 m (Fig. 1). The samples
were sliced into cubes with a mass of 20 g and each subjected to
1 of 5 pCO2 treatment regimes. Each cube was suspended in a bath
of filtered and sterilized seawater, in which 1 of 5 mean levels of
pCO2 were maintained (840, 1200, 1900, 3000, and 28,000) for
70 days. The water was vigorously circulated using a pump to simulate wave action, with temperature and salinity maintained at
25 °C and 35 ppt, respectively. As the seawater used in this experiment has a known and stable alkalinity, elevated pCO2 concentrations were achieved using a CO2 injection system, where a
controller opened a valve when pH rose above a specific level, thus
briefly injecting pure CO2 into the seawater until the target pH was
obtained. Total alkalinity and pH measurements were used to confirm the pCO2 (Lewis and Wallace, 1998). The buoyant weight of
each sample was measured weekly, and the mass loss/gain of each
sample was then calculated in relation to the initial saturated
buoyant weight. In addition, dye-impregnated thin sections and
electron micrograph images were obtained from the treated
Fig. 1. The extent of the lithified hardground province in the Gulf. (A) The province consists of 90,000 sq. km of diagenetically cemented seafloor and has been defined
through field sampling (Shinn, 1969) and as preventing penetration of a 3.5 kHz echosounder (Uchupi et al., 1996). Triangle marks the position of the sample site for this
study. (B) Shows the smooth surface of a lithified Gulf hardground. The circular pits are bored by lithophagous bivalves. This hardground crust is only several centimetres
thick, growths rapidly, and is the primary settlement substrate for corals in the Gulf. (C) Depicts juvenile faviid corals that have recruited onto a hardground sheet.
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samples in order to quantify changes in the character of the interstitial cements caused by the elevated pCO2 regimes.
3. Results and discussion
The experiments conducted were successful in simulating the
chemical conditions of the Gulf under lab-conditions, supporting
the precipitation of fibrous aragonite cement. This production
caused the mass of the sample to increase linearly with the duration that it was held in the chemical regime. Cement production
occurred for pCO2 values ranging from the present day ambient level of 380 ppm, to pCO2 = 1200 ppm (regression lines are inflected
upwards in Fig. 2 indicating a gain in mass). The switch-point at
which seawater is no longer conducive for lithification occurs with
a pCO2 of approximately 1900 ppm. This CO2 concentration will be
reached around the year 2300 according to the IPCC IS92a emission
scenarios coupled with a logistic function for burning of fossil fuels
beyond 2100 (Caldeira and Wickett, 2003). Further decreasing the
saturation state of the seawater by raising pCO2 to 3000 and
28,000 ppm causes the dissolution of cement and mass loss of
the sample (regression lines are inflected downwards in Fig. 2).
However, these high values could not realistically be achieved
prior to Earth’s hydrocarbon reserves becoming exhausted and
were simply used to demonstrate that further decreasing ocean
pH serves to increase the rate of dissolution. After the experiment,
the sample cubes treated with high pCO2 regimes were noticeably
more friable, indicating dissolution of the binding cements.
As has previously been reported (Shinn, 1969), thin section
petrography and scanning electron microscopy reveal the hardground samples to be composed of sand grains, foraminifera, as
well as mollusc and red algae fragments, bound to a rock-matrix
by fibrous aragonite cement (Fig. 3A). These grains and fragments
display a dark micritic envelope, likely resultant from microbial
boring by endolithic algae (Kobluk and Risk, 1977). The cement is
composed of densely packed aragonite needles with sharp chiselshaped ends (Fig. 3B). After the sample has been exposed to elevated pCO2 of 1900 ppm for 70 days, the aragonite cement is
clearly impacted by dissolution. The previously well-defined fringe
appears disorganised and the electron micrograph reveals individual crystals to have become blunt and rounded (Fig. 3C and D). This
level of decreased carbonate saturation is sufficient for the sample
to reduce in mass (Fig. 2). The photo- and micro-graphs suggest
this loss can be attributed to a reduction in the quantity and
Fig. 2. Percentage change in mass of hardground samples exposed for 70 days to
varying regimes of pCO2. The tipping point between cementation and dissolution
occurs at a pCO2 of 1900 which is predicted to be reached with 300 years (Caldeira
and Wickett, 2003).
quality of fibrous aragonite cement and hence an associated loss
of grains from the lithified matrix (Fig. 3). The effect of prolonged
exposure to lowered pH (elevated pCO2) is dissolution of the aragonite cements that bind the hardground together.
In the case of both cement dissolution and precipitation during
pCO2 treatment, the rate of mass loss or gain under each regime
was linear with respect to duration of exposure (Fig. 2). This indicates that the length of the experiment was sufficient to allow the
sample to equilibrate to a representative rate of cement production/dissolution which, within a closed system, could reasonably
be assumed to be maintained over longer periods. We are cognisant however that our experiments are simplified by ignoring
how the kinetics of the dissolution process potentially cascade in
an ocean circulation model. In nature, substrate dissolution reactions can be expected to occur on timescales of decades to centuries – perhaps allowing carbonates from distant regions to
somewhat buffer the effects of the loss of local carbonates. Also absent from our simple model is consideration of the chemical action
of other minerals, such as silicate, which can serve to buffer seawater pH (Sillen, 1967). Though not prevalent in the shallow nearshore, silicate is a relatively common mineral in the windblown
quartz sands that dominate the central axis of the Gulf basin (Wagner and van der Togt, 1973). It is in the form of reactive clays that
this mineral will offer the greatest buffering capacity and frequent
dust storms provide a plentiful supply. The extent to which the
Gulf’s complement of lithotopes and ongoing import of terrestrial
sediment will serve to buffer any change in pH over time, is unknown and difficult to quantify. Incorporation of a circulation
model to audit far-field effects is beyond the scope of this study
and we extrapolate the linear trends of Fig. 2 to highlight plausible
scenarios for the fate of Gulf hardgrounds under altered levels of
pCO2 into the future. It is relevant to note that, while not closed,
the Gulf is somewhat restricted in its exchange of waters with
the northern Indian Ocean by virtue of the narrow (55 km), but
reasonably deep (90 m), Strait of Hormuz. Oceanic inflow through
the Strait is hampered by partitioning density stratifications between the shallow and deep Gulf waters (Sadrinasab and Kämpf,
2004). This restriction will reduce the imported potential for buffering of carbonate dissolution in the Gulf.
We are also aware that changes in ocean climate are not the
most imminent threat to the coral ecosystems of the Gulf. The
massive rate of coastal development in the region over the last decade, which, along the shoreline of the western Gulf is nothing short
of extreme, has served to remove many important reef areas and
depress those that remain (Sheppard et al., 2010). More recently
though, a renewed vision of environmental stewardship has
emerged in the region – a network of marine protected areas has
been installed (Abuzinada et al., 2008) and security for several
large coastal infrastructure projects has turned other areas, which
lack formal protection, into de facto MPA’s as public access is prohibited. The fate of the Gulf’s coral ecosystem thus seems less jeopardized than would have been perceived just 5 years ago and it can
be tentatively hoped that some vibrant reef areas will exist into the
future, albeit alongside a greatly modified coastline.
The most well-understood biological impact of high seawater
CO2 is the reduction in calcification rate in calcifying organisms
due to acidification-driven lowering of the CaCO3 saturation state
(Kleypas et al., 1999; Manzello et al., 2008; Veron et al., 2009).
The mechanisms of stress are however difficult to quantify since,
in scleractinian corals for example, the locus of deposition of the
carbonate skeleton is separated from ambient seawater by multiple membranes which serve to buffer the intracellular pH from
that of bulk seawater (Venn et al., 2009). Since the precipitation
of fibrous aragonite cement in the Gulf hardgrounds is solely abiotic, the situation is simpler, linear (Fig. 2), and cannot be biologically buffered. As soon as pH drops to a level where carbonate
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249
Fig. 3. The impact of elevated pCO2 on the petrography of lithified hardground. (A) Is a photograph of a thin-section (crossed nicols, 10) cut from a sample after 70 days
treatment under ambient pCO2 conditions. The fibrous aragonite cement that fringes the grain fragments is dyed blue and pore spaces are black. (B) Is an electron micrograph
image obtained from (A). The 3000 magnification reveals the chisel-shaped needle structure of the individual fibrous aragonite crystals that compose the cement. (C) After
70 days of treatment under a regime where pCO2 is elevated to 1900 ppm, the aragonite fringe appears disorganised in thin section, and the effect of dissolution has served to
blunt the previously sharp crystal structure (D).
precipitation is no longer possible, hardground formation will
abruptly cease. The most informative experimental run is that with
pCO2 = 1900 ppm as this demarks the lowest pCO2 under which a
sample lost mass. This represents the conditions in the real world
at which previously formed hardgrounds will begin to revert back
to unconsolidated sands as their binding cements dissolve. It also is
the point at which new hardgrounds will be prevented from forming. Further drops in pH caused by raising pCO2 would accelerate
this reversion of lithified seabed to sand. While coral frameworks
have occasionally been observed to develop in areas dominated
by soft sediments (Johnson and Risk, 1987), mobile sand sheets
have long been recognised in the Gulf as one of the major impediments to more widespread coral settlement and growth (Purkis
and Riegl, 2005; Riegl, 1999; Riegl and Purkis, 2009). As such, we
perceive sediment-stress to be a physiological limitation that these
corals are unlikely to be able to adapt to and handle.
Though the ability has yet to be observed (Veron et al., 2009),
there exists the possibility that corals will gradually adapt to a persistent high CO2 environment. For high temperature, this certainly
seems to have already been the case in the Gulf (Sheppard, 2003).
This thermal acclimatization however should not be assumed to
have been rapid. It likely evolved over the last 6 kyr, by which time
sealevel had approximated its present position and the climate of
the Gulf region had shifted from monsoonal to the hot hyper-arid
conditions observed today (Purkis et al., 2010).
If it is assumed therefore that the unique temperature tolerance
for the Gulf corals was acquired over a period of several centuries
to millennia, it is also reasonable to assume that pH tolerance
would also take a similar timeframe to evolve. Having already
adapted for temperature, the Gulf ecosystem is already better
poised than corals elsewhere, certainly as compared to the IndoPacific, to confront the dual threat of ocean warming and acidification that is predicted to accompany the raised CO2 environment
that we now face (Hughes et al., 2003; Kleypas et al., 1999;
Manzello et al., 2008; Veron et al., 2009). However, given the present rate of atmospheric CO2 rise, this study evidences that within
only three centuries the chemical composition of the Gulf seawater
may shift to become corrosive to marine hardgrounds with the
accompanied decimation of its precious temperature-adapted corals. Even if this highly climate-change-adapted ecosystem evolves
to bolster its ability to cope with temperature extremes with added
tolerance to a low CaCO3 saturation state, this unique coral population may terminate from lack of suitable substrate.
Acknowledgements
We are indebted to K. Verwer, T. Correa, and R. Ginsburg for
assistance with the petrographic interpretation of the samples. H.
Ala Al-Sayegh kindly shot the electron micrograph images. We
remain ever-grateful to Ashraf Al-Cibahy for facilitating and supporting our research. This is NCRI publication 118.
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