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First published online March 14, 2008
Journal of Experimental Biology 211, 1050-1056 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013284
The effect of thermal history on the susceptibility of reef-building corals to thermal stress
Centre for Marine Studies and ARC Centre of Excellence for Coral Reef Studies, University of Queensland, St Lucia, QLD 4072, Australia
* Author for correspondence (e-mail: r.middlebrook{at}uq.edu.au)
Accepted 16 January 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: acclimation, thermal stress, Symbiodinium sp., photoprotective mechanisms, coral bleaching
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). This increase is
expected to have substantial impacts on coral reefs and the tens of thousands
of organisms that inhabit them
(Hoegh-Guldberg, 1999;
Hughes et al., 2003).
Comparisons of known thermal tolerance levels for corals with projections of
sea temperature changes strongly suggest that the frequency and intensity of
coral bleaching and mortality is set to increase sharply, leading to declines
in coral reefs worldwide (Hoegh-Guldberg,
1999; Hoegh-Guldberg,
2005; Donner et al.,
2005). These studies based their conclusions on the assumption
that the thermal threshold for a population of corals is relatively constant.
It is important, therefore, that we understand the dynamics associated with
the thermal threshold, especially when it comes to understanding how thermal
history can influence bleaching response.
Reef-building corals are highly dependent on their symbiotic relationship
with photosynthetic dinoflagellates (Symbiodinium sp.). As part of
this mutualistic endosymbiosis, corals receive the majority of their carbon
and energy requirements from Symbiodinium
(Muscatine et al., 1984;
Falkowski et al., 1993). The
transfer of photosynthetic products from the Symbiodinium to the host
enables corals to grow and calcify at high rates within the warm and sunlit
subtropical and tropical waters (Barnes and
Chalker, 1990). The loss of these symbiotic dinoflagellates due to
environmental stresses (coral bleaching) is likely to impact the energy and
carbon budget of corals, and may result in death if the stress is severe and
prolonged (Glynn, 1996).
Bleaching [disassociation of the endosymbiosis between coral and
Symbiodinium (Hoegh-Guldberg and
Smith, 1989)] results in reduced Symbiodinium cell
densities and/or their photosynthetic pigments. The loss of
Symbiodinium and/or pigments begins with the dysfunction of the
photosynthetic apparatus of Symbiodinium
(Iglesias-Prieto et al., 1992;
Fitt and Warner, 1995;
Warner et al., 1996;
Iglesias-Prieto and Trench,
1997; Brown et al.,
1999; Jones et al.,
1998; Downs et al.,
2000; Tchernov et al.,
2004).
Organisms tend to have thermal tolerances that reflect the environment in
which they are found. This can occur either through acclimation, where an
organism alters its phenotype, or through adaptation, where propagules are
better suited to altered conditions. Corals and their symbionts have adapted
to geographical differences in sea temperature through genetic shifts in
thermal tolerance over long periods of time
(Coles et al., 1976;
Hoegh-Guldberg, 1999), which
ultimately defines the response of the coral holobiont to stress within a
region (Donner et al., 2005).
However organisms are also able to shift their phenotypic responses to a
limited extent through acclimation to environmental extremes (Schmidt-Nielsen,
1996). In this respect, many organisms show the ability to acclimate to
stressors at both the physiological and molecular levels
(Feder and Hofmann, 1999;
Tomanek and Somero, 1999;
Sorte and Hoffman, 2005). The
coral holobiont is no exception, and several studies have demonstrated that
corals (Brown et al., 2002;
Coles and Brown, 2003;
Castillo and Helmuth, 2005;
Dove et al., 2006) and
Symbiodinium (Iglesias-Prieto and
Trench, 1997; Downs et al.,
2000) can acclimate to heat and light stress. In addition,
variations in the bleaching susceptibility of conspecifics across
environmental gradients, for instance latitude, suggest the further potential
for corals to acclimate to rising sea temperatures in the field
(Coles and Brown, 2003;
Donner et al., 2005;
Ulstrup et al., 2006). The
ability to acclimatize to different local conditions has the potential to play
an important role in explaining small- and large-scale patterns in bleaching
susceptibility.
The physiological behavior of reef-building corals is actively influenced
by their dinoflagellate symbionts (Little
et al., 2004; Berkelmans and
van Oppen, 2006). Acclimation to light stress in
Symbiodinium has been shown to occur through changes in peridinin
chlorophyll a–binding protein complexes (PCP) and chlorophyll
a–chlorophyll c2–peridinin protein
complexes (acpPCP), light harvesting pigments
(Iglesias-Prieto and Trench,
1997), the efficiency of photosystem II (PS II) and xanthophyll
turnover rates (Brown et al.,
1999). Symbiodinium may acclimate to stressful conditions
such as high light and temperature during periods of pre-exposure by the early
activation of photo-protective mechanisms. Such mechanisms include changes in
the efficiency of the xanthophyll cycle
(Brown et al., 1999;
Brown et al., 2000),
photosynthetic efficiency (Anthony and
Hoegh-Guldberg, 2003) and non-photochemical quenching.
The ability of the coral symbiosis to acclimate to stressors has been
ignored in much of the recent experimental work on coral bleaching that
consists of single thermal stress events, which often do not mirror actual
conditions. Corals located on reef crests are often exposed to thermal and
light conditions above their predicted thresholds for several hours on
consecutive days (R.A.M., personal observations). Few controlled experiments
have attempted to determine the effect of short-term elevated temperatures on
subsequent bleaching outcomes (Coles and
Jokiel, 1978).
The aim of the present study was to explore the influence of thermal history on the response of the coral symbiosis (Acropora aspera) to thermal stress. In particular, our study explores the changes in photosystem II efficiency, non-photochemical quenching, xanthophyll cycling and symbiont density in response to thermal stress in pre-exposed (31°C) and control coral populations. In particular, the study investigates the effect of three different prior thermal stress histories on the acquisition of thermal tolerance in order to explore whether the pattern of pre-exposure is important over and above the actual amount of exposure.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)] containing
Symbiodinium clade C3 (LaJeunesse
et al., 2004) were collected from three large colonies on the reef
flat adjacent to Heron Island Research Station (HIRS, 23°33'S,
151°54'E) in April 2006. Single upward-growing branch tips
(3–4 cm long) were removed using wire cutters and transported to the
seawater facility at HIRS and placed in racks immersed in running seawater.
Coral branches were acclimated in 4 large experimental aquarium tanks to the
mean local ambient temperature (27°C, drawn from the reef crest). Corals
were exposed to natural reef flat summer daily light levels (average daily
maximum 1271.28±40.07 µmol m–2
s–1, average daily light dosage 21.37±0.88 mol
m–2 day–1) throughout the experiment.
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Five coral branches per treatment were removed each day from the experiment at 18:00 h for measurement of photosynthetic efficiency. One branch per colony per tank for each corresponding treatment was snap-frozen using liquid nitrogen at 12:00 h on each day of treatment exposure and stored in a –70°C freezer. These branches were used to measure Symbiodinium cell densities, chlorophyll and xanthophyll pigment concentrations (Fig. 1B).
Measurements of photosynthetic efficiency
Effective dark-adapted quantum yield
(Fv/Fm) is a relative measure of the
rate at which PS II can use light to process electrons flowing during the
photosynthesis and the photosynthetic efficiency of the light reactions
(Hoegh-Guldberg and Jones,
1999). An imaging pulse amplitude modulation (PAM) chlorophyll
fluorometer (MAXI Imaging PAM, Walz, Effeltrich, Germany) was used to analyse
the photosynthetic efficiency of corals daily at 18:00 h. Five coral branches
were measured per treatment per tank (totalling ten branches per treatment) in
a glass Petri dish containing seawater from the flow-through system. Corals
were dark-adapted for 40 min prior to measuring effective quantum yield
(Fv/Fm) to assess whether PS II was
adversely affected by the treatments
(Warner et al., 1996).
Induction recovery curves were also performed to examine the ability of
Symbiodinium to acclimate to short-term light stress. Coral branches
were exposed to 461 µE m–2 s–1 for 6 min
followed by a dark recovery period of 14 min. Photo-kinetic parameters,
including non photochemical quenching and PS II quantum yield, were measured
during the light period using a saturation pulse every second. A saturating
pulse was used 16 times integrated over 13 min 58 s during the recovery phase.
Dynamic yield and non-photochemical quenching were determined using the
calculations of Warner et al. (Warner et
al., 1996).
The extraction of non water-soluble pigment
Coral tissue from frozen coral branches was removed using an air brush and
5 ml of filtered (0.45 µm) seawater solution. Symbiodinium were
separated from the coral tissue by centrifugation at 4500 g
(4°C) for 5 min. The supernatant was discarded and the pellet resuspended
in HPLC grade methanol (1 ml methanol for every 750 µl of sample).
Solutions were filtered through a 0.22 µm membrane filter (GSWP04700,
Millipore, North Ryde, NSW, Australia) and 50 µl sterilised milli-Q was
then added to a 250 µl aliquots prior to use in High Performance Liquid
Chromatography (HPLC). Samples were then separated and analysed using the
methods of Dove et al. (Dove et al.,
2006) and Zapata et al.
(Zapata et al., 2000) using a
SHIMADZU (Tokyo, Japan) SCL-10 HPLC attached to a SHIMADZU SPD-M10A photodiode
array detector.
Cell densities of Symbiodinium
One branch per colony from each corresponding treatment within each tank
was used to assess dinoflagellate density in A. aspera. Density was
determined using a SEDGEWICK rafter cell 550 (ProSciTech S8050, Kirwin,
Queensland, Australia). Fourteen 1 µl cells were counted within a 1 ml
slide, and averaged per sample. Coral surface area was determined using the
melted paraffin technique (Stimson and
Kinzie, 1991).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Induction recovery curves were performed to indicate the speed of recovery of the PS II reaction centre from PAR pressure (Fig. 3A) and thermal stress. Induction recovery curves performed on corals during the final evening (day 18) of the experiment revealed that the recovery potential of those preheated 1 and 2 weeks prior to the prolonged thermal stress was greater than those not preheated (Fig. 3B, P=0.02). After 6 min of light exposure (461 µmol quanta m–2 s–1, 400–700 nm), the PS II reaction centre in corals that did not undergo prior thermal stress became saturated almost immediately (Fig. 3C). This effect was significantly less in corals that were preheated 2 weeks prior and those preheated 1 week prior to the main experimental period of thermal stress (F54,216=13.44, P<0.001).
Non-photochemical quenching (NPQ) data obtained from the induction recovery curve from day 18 (Fig. 3D) provides a measure of how intact PS II is on the cessation of the simulated bleaching event. Dark-adapted NPQ measured over the duration of the prolonged thermal stress period is shown in Fig. 4A. An increase in rate of dark-adapted NPQ on Day 18 can be correlated with a pronounced decline in dark-adapted fluorescence yield in all samples that had been heated, due to its role in the dissipation of excess heat, in response to pressure on PS II. A higher rate of NPQ in treatment corals compared to the control can be seen in the light induction recovery curve recorded on day 18 (Fig. 3D) showing a significant effect of treatment (P=0.029). Corals preheated 2 weeks prior to the bleaching event had significantly higher NPQ values than those preheated 1 week prior and those not preheated during both actinic illumination (P=0.00075) and dark acclimation period (P=0.01). The induction recovery curve recorded 2 days prior (data not shown) saw corals preheated 1 week prior having a significantly lower rate of NPQ in comparison to the two other treatments at the end of the acclimation period (P=0.023). Therefore, it can be inferred that during the last 3 days of the simulated bleaching event (days 16–18), there is an increase in rate of NPQ in coral branches preheated 2 weeks prior, a decrease in rate of NPQ in corals not preheated, and no difference in rate of NPQ in corals preheated 1 week prior.
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;
Brown et al., 1999) and
performs a critical role in dissipating excess energy from the antenna of PS
II. Symbiodinium in the corals preheated 2 weeks prior and in those
not preheated had greater xanthophyll pool size than those preheated 1 week
prior and the control (Fig. 4C,
Table 1). A significant
increase in diatoxanthin was seen in corals that were not exposed to prior
thermal stress conditions (day 19, P=0.007), contributing
significantly to the increased pool size, which was twofold greater that in
corals preheated 1 week prior.
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A significant interaction was found between `TimexTreatment' in the xanthophyll cycling ratio (Dt)/(Dt+Dd) (F9,96=13.5, P<0.001), with the greatest difference between treatments occurring on day 19 (Fig. 4D). Day 19, the final day of the experiment where the decline in effective quantum yield of PS II was greatest the previous day, saw a significant increase in xanthophyll cycling in corals preheated 2 weeks prior and corals not preheated (P<0.0001 in both), whereas there was no significant difference in dinoflagellates from corals preheated 1 week prior to the bleaching stress event.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Hughes et al., 2003). A large
number of studies have demonstrated that corals and their symbionts are living
close to their current thermal maxima. Projections that combine the behaviour
of corals with projections of sea temperature from global climate change
models suggest that mass bleaching events will become a yearly phenomenon
within the next 30–50 years
(Hoegh-Guldberg, 1999). This
is expected to lead to a rapid decline in coral cover on tropical reef
systems, which may be the basis of the observed decline seen by a number of
recent studies (e.g. Bruno and Selig,
2007). Given that these models depend heavily on the behaviour of
the thermal threshold, it is important that variability stemming from
acclimation is understood. This study is one of a small number that has
focused on experimentally exploring the effect of issues such as thermal
history on the tendency of reef-building corals and their dinoflagellate
symbionts to undergo bleaching.
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). Hoegh-Guldberg
(Hoegh-Guldberg, 2000) and
Donner et al. (Donner et al.,
2005) estimated that the thermal tolerance of reef-building corals
will have to rise by approximately 0.2–1.0°C per decade to keep pace
with rising global temperatures. Thermal history has also been shown to lead
to acclimation in coral conspecifics at intra-colony (e.g.
Brown et al., 2002), colony,
reefal (Castillo and Helmuth,
2005) and latitudinal
(Hoegh-Guldberg, 1999;
Ulstrup et al., 2006) scales.
However, only a single study has examined thermal acclimation in corals
experimentally (Coles and Jokiel,
1978). Given that coral bleaching is predominantly associated with
short-term increases in temperature, ranging from a few hours to a few days,
and that these bleaching conditions may be preceded by warmer than average
temperatures (Fig. 5), we
examined if short-term prior thermal stress leads to increased thermal
tolerance through acclimation.
Corals that were subjected to warmer than average temperatures prior to
thermal stress beyond the bleaching threshold were found to be more thermally
tolerant, as indicated by reduced loss of Symbiodinium compared to
corals that had not been pre-stressed (Fig.
2B). While pre-stressed coral symbiont densities were unchanged at
the end of the bleaching, symbiont densities in non-prestressed corals
declined by approximately 40%. Given that the Symbiodinium
photosynthetic apparatus has been suggested as the point of thermal lesion in
a number of studies (Iglesias-Prieto et
al., 1993; Warner et al.,
1996; Jones and
Hoegh-Guldberg, 1999), we explored the responses by corals and
their symbionts with respect to photosynthetic efficiency and pigment
profiles, particularly the xanthophyll pool, which provides the majority of
NPQ.
The dark-adapted yield of photosystem II has been used extensively as a
measure of damage to photosystem II and has been shown to be a conventionally
good proxy for bleaching susceptibility
(Warner et al., 1999;
Jones et al., 2000;
Fitt et al., 2001). Those
corals that had not been stressed had significantly lower dark-adapted yields
than pre-stressed and control corals in the final 3 days of the bleaching
event (Fig. 2A), indicating
that pre-stress provided some level of thermal protection to photosystem II.
Significant differences between the yield of control and pre-stressed corals
were only seen on the final day of the experiment. In the case of corals that
were pre-stressed 2 weeks prior to bleaching (H2), tolerance was
correlated with higher levels of NPQ (Fig.
2D) and xanthophyll pool to Chl a ratio
(Fig. 4B) while the xanthophyll
cycling remained unchanged relative to non-prestressed controls
(Fig. 4C).
A very different pattern was observed in xanthophyll cycling for those
corals pre-stressed 1 week prior to bleaching. Despite bleaching less than
non-prestressed corals, these pre-stressed corals did not differ from control
corals with respect to xanthophyll pool size
(Table 1) and cycling rate
(Fig. 4C). The ratio of
diatoxanthin to dinoxanthin and diatoxanthin was significantly less than those
seen in coral that were pre-stressed 2 weeks prior and those not pre-stressed
(Fig. 4C). The rate of NPQ was
also found to be less in corals prestressed 1 week prior compare to other
prestressed corals (Fig. 3D).
These contrasting patterns of NPQ, xanthophyll levels and xanthophyll cycling
indicate that acclimation is a dynamic process, with distinct differences in
stress profiles that differed by 7 days. In addition it indicates that a
variety of other thermal protective pathways are occurring in the coral
holobiont in addition to those examined here. This is not surprising given
that acclimation in the holobiont can involve the coral host,
Symbiodinium, or a combination of both
(Dove, 2004). Both corals
(Kortschak et al., 2003) and
Symbiodinium (Leggat et al.,
2007) have been shown to possess a wide variety of genes that
encode for stress response proteins (e.g. heat shock proteins, superoxide
dismutase, ubiquitin etc.), which can impart protection, indicating that a
more comprehensive study is required to elucidate all of the underlying
mechanisms of thermal acclimation.
Although commonly interchanged, the terms acclimation and heat shock refer
to very different cellular responses
(Bowler, 2005). Acclimation
results from long-term exposure, in the order of days to weeks, to new
conditions that are within the normal limits of an organism's response.
Acclimation generally results in a variety of cellular and molecular responses
such as alteration of lipid composition, protein isozymes and protein
expression, which will provide protection from long-term gradual changes in
the environment. In contrast heat shock generally refers to a period of short
exposure to near lethal temperature that may or may not provide a very
distinct cellular and molecular response to those seen in acclimation. Which
cellular and biochemical mechanisms occur in the coral holobiont to different
conditions will be a future area of important research. An examination of the
literature on perhaps the most well-studied invertebrate model for
acclimation, Drosophila sp., demonstrates that the ability of an
organism to acclimate to various conditions, how it acclimates and, indeed,
the costs of acclimation, can vary significantly between con-specifics and
species and have profound effects on an organism (for a review, see
Hoffman et al., 2003). For
example, the induction of acclimatory responses has been shown to have effects
on a variety of other performance measures resulting in such disparate
responses as increased longevity, increased cold tolerance and decreased
fertility, to list a few (Hoffman et al.,
2003). A history of exposure to a range of stresses has also been
found to alter subsequent higher plant responses where a priming stress
activates genes that leave an epigenetic mark, facilitating a quicker response
to subsequent stresses (Bruce et al.,
2007). What costs and benefits accrue to the coral holobiont will
need to be determined.
This study conclusively demonstrates that thermal stress events 2 weeks and
1 week prior to a bleaching event provide significantly increased thermal
tolerance to the coral holobiont, suggesting that short time-scale thermal
adaptation can have profound effects on coral bleaching. The inclusion of
physiological and acclimatory properties into the modeling of climate change
on populations and ecosystems has already been advocated
(Helmuth et al., 2005); in the
case of the coral holobiont, a better understanding of thermal history on
bleaching susceptibility may provide insights into what reefs will look like
in the near future under altered climate regimes.
LIST OF ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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Present address: School of Pharmacy and Molecular Sciences, James Cook
University, Townsville, QLD 4811, Australia 
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