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Article

Differing Responses of Three Scleractinian Corals from Phuket Coast in the Andaman Sea to Experimental Warming and Hypoxia

by
Tarun Jain
1,2,
Pimchanok Buapet
2,3,
Long Ying
1,2 and
Mathinee Yucharoen
1,2,*
1
Marine and Coastal Resources Institute, Faculty of Environmental Management, Prince of Songkla University, Songkhla 90110, Thailand
2
Coastal Oceanography and Climate Change Research Center, Prince of Songkla University, Songkhla 90110, Thailand
3
Division of Biological Science, Faculty of Science, Prince of Songkla University, Songkhla 90110, Thailand
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(2), 403; https://doi.org/10.3390/jmse11020403
Submission received: 13 December 2022 / Revised: 28 January 2023 / Accepted: 7 February 2023 / Published: 11 February 2023
(This article belongs to the Special Issue The 10th Anniversary of JMSE - Recent Advances in Section Marine Biology)
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Abstract

:
An unprecedented decline in the diversity and health of coral reefs is occurring around the world as they are threatened by multiple global and local stressors. Rising seawater temperature and low dissolved oxygen (DO) conditions are expected to intensify as a result of climate change. Understanding the responses of corals to these stressors is necessary for making predictions and devising mitigation strategies. The three coral species—Porites lutea, Montipora tuberculosa, and Pocillopora verrucosa—were sampled from Patong Bay, Phuket, Thailand, as representatives of different coral morphologies. Coral nubbins were subjected to experimental investigation under ambient conditions (29 °C, DO > 6 mgL−1), heat stress (32 °C), hypoxia (DO < 2 mgL−1), and heat stress + hypoxia treatments. Photosynthetic performance indicators Fv/Fm and Fv/F0 and physiological parameters Symbiodiniaceae density, pigment concentration, and growth rate were quantified. We found P. verrucosa (branching) to be the most sensitive and severely affected by heat stress or hypoxia, more so than P. lutea (massive) and M. tuberculosa (tabular). The combination of these stressors had less impact on these species, except for a decline in growth rate of M. tuberculosa. This study also suggests that the corals respond differently to high temperature and low oxygen, with their sensitivity depending on species. These responses, however, may differ according to the lighting, especially in hypoxic conditions. The results fill a research gap to help predict the vulnerability of these three coral species in shallow reef habitats under climate change scenarios.

Graphical Abstract

1. Introduction

The ocean absorbs over 90% of the total heat accumulation in the Earth’s climate system, which has increased rapidly over the past several decades due to greenhouse gas emissions, leading to ocean warming [1,2,3,4,5]. An estimated 1–3 °C increase in sea surface temperature (SST) by the year 2100 is now a likely scenario [6]. The occurrence and extent of marine heatwaves and temperature anomalies are also changing as a result of global warming [7,8,9,10]. This increase in ocean temperatures can affect the habitat, population, migration, and breeding patterns of marine plants, animals, and microbes as well as threaten the building blocks of ocean life such as corals [7,11]. Heat stress (as well as ocean warming and heat waves) has been correlated with the increase in frequency and scale of mass coral bleaching events since the late 1990s, when the first evidence of mass bleaching was recorded after a series of El Niño events [12]. At the mechanism level, heat stress raises the metabolic energy requirement of the coral host, altering the nutrition cycle, and this has been shown to be the key cause for functional breakdown of symbiotic algae in corals [1], leading to a decline in calcification processes [13,14]. The response of corals to heat stress also depends on their morphology, as small encrusting colonies are more likely than big branching colonies to continue mass transfer and hence to endure temperature stress. The volume of space between colony branches also predicts their reaction to temperature stress, and as the frequency and intensity of heat stress rise, huge branching coral colonies may give way to tiny colonies and flat-massive colonies with low aspect ratios [15]. There is growing evidence to also suggest that a recent increase in coral disease outbreaks can be attributed primarily to heat stress, among other local factors [16].
Corals reefs are facing an unprecedented threat from heat stress, hypoxia, acidification, and other scenarios as a result of anthropogenic activities and climate change, leading to stress and decline of several reef-building corals [2,17,18,19,20]. Some simulations and downsized climate models applied on eutrophic and seasonally hypoxic estuaries or coastal areas predict a reduction of dissolved oxygen (DO) by 1–2 mgL−1 and a 10–30% increase in hypoxic and anoxic volumes by the mid-21st century. These reductions are primarily attributed to the decreasing solubility as a result of ocean warming [21,22]. An overall decrease of 2–4% in oceanic oxygen reserves is also projected based on the range of different climate change scenarios [6,23]. In recent years, several coral bleaching-induced mass mortality events have been observed in large areas with low oxygen (hypoxia/anoxia) and indicate that oxygen level can also be a critical factor impacting the survival of coral reefs. Nevertheless, the exact effects of periodic or persistent hypoxia on coral reefs are currently unpredictable [24,25]. Tropical reefs in particular are estimated to be at higher risk from localized hypoxia [24], as reefs with inherently restricted water movement, such as atolls, tidal pools, semi-enclosed lagoons, and fringing reef flats, have regular occurrences of low DO concentration (2–3 mgL−1), and this condition is compounded by the increase in metabolic rates and episodic nutrient flushing due to tidal and seasonal warming [26,27,28,29,30].
These stressors can promote micro- and macroalgal blooms [31,32], further deteriorating the situation as the capacity to buffer deoxygenation through photosynthetic oxygen production by coral’s Symbiodiniaceae, macroalgae, and phytoplankton is also limited due to reduced light levels caused by turbidity [33]. Corals have been noted as being more susceptible to low oxygen than other marine organisms [6] as hypoxia can lead to reduced photosynthesis and calcification, inducing bleaching mortality in extreme cases [24,25]. It can also promote diseases such as black band disease (BBD), which creates a high concentration of sulfides that kill the underlying coral tissue [24,34,35,36].
Global warming and local eutrophication also lower the DO (by reducing the solubility and saturation) and increase the biological oxygen demand of most marine organisms, worsening the effect. This stress caused by low DO concentrations and relatively high temperatures is an energy challenge for most marine organisms’ metabolisms as they face frequent exposure to oxygen below their optimum functioning thresholds [32,37,38,39,40]. In isolation, hypoxia may be more dangerous to corals than other stressors, and there are also some studies showing that the combined effects of hypoxia and other stressors can be more damaging than their individual effects [41,42]. However, most of the research and studies on corals affected by hypoxia have reported field observations as a response to bleaching or mass mortality events [43], and the exact effects of multiple stressors in relation to hypoxia on coral physiology are currently unknown.
The coral reefs at our study site of Patong Bay, located on the west coast of Phuket, Thailand, have been subjected to excessive nutrient enrichment due to the rapid increase in tourism activities since the 1980s [44,45]. As a result, the reefs are not only vulnerable to heat stress, with a reported annual seawater temperature range of 29–32 °C [14,46], but may also be at risk from co-occurring episodes of hypoxia as algal blooms have been reported periodically in this area [44]. The aim of this study was to contribute to understanding the individual and combined (additive, synergistic, or antagonistic) effects of heat stress and hypoxia on three reef-building corals, Porites lutea, Montipora tuberculosa, and Pocillopora verrucosa. The results obtained in this study provide insights into the impacts of ocean warming and deoxygenation, to support projections of reef biodiversity under a changing climate.

2. Material and Methods

2.1. Sample Collection and Acclimation

In April 2021, three coral species representing different growth forms, namely P. lutea, M. tuberculosa and P. verrucosa, were selected for sampling based on their abundance in the reef edge at Patong Bay, Phuket, Thailand, 7°53′31.3″ N 98°15′56.8″ E (Figure 1A). The healthy coral colonies (no stress, bleaching, compromised tissues, or diseases) were investigated. Four source colonies of each coral species were selectively sampled using a hammer and chisel, from a depth of 5–6 m. All coral colony samples were transferred with natural seawater to the aquarium facility of the Coastal Oceanography and Climate Change Research Center (COCC), Prince of Songkla University, within 12 h of collection.
All the coral colonies were allowed to acclimate in a 600 L holding tank fitted with recirculating pumps (WP-300M, SOBO, Zhongshan, China and AT-107, Atman, Zhongshan, China), a heater chiller (CS-160CIRV1, Atman, Zhongshan, China), COB light (TS-A600, aquarium lamp, Shandong, China), and LED light (A601, Chihiros, Ningbo, China) for a week at 29 °C temperature, 32 ppt salinity, pH 8.2, 12:12 h light:dark cycle at 150 µmol photons m−2s−1, and 6.45 mgL−1> DO > 6.04 mgL−1, similar to the conditions recorded at the sampling site (Supplementary Table S1). After one week, the coral colonies were cut into nubbins of 3–5 cm diameter and transferred into 62 L treatment tanks (20 nubbins/species/tank) with the same conditions and equipment as that of the holding tank, except for the models of water pumps (AP-1200, SONIC, Zhongshan, China) and heater chiller (JMC-02, JBA, Zhongshan, China). Each replicate was allocated from each coral colony and assigned for a specific sampling (Figure 1B). The coral nubbins were then allowed to acclimate for an additional week in the experiment tanks. Temperature, DO, pH, and salinity of the seawater were monitored every day throughout the experiment. Partial seawater changes (20%) were conducted every 3 days. Prior to seawater replacement, nitrate and ammonia concentrations of the seawater in each tank were measured using an aquarium test kit (Salifert Profi-Test®, Duiven, The Netherlands).

2.2. Experimental Design

After acclimation in treatment tanks, temperature and DO concentration were modified as follows:
  • Treatment 1 (ambient conditions), 6.45 mgL−1> DO > 6.04 mgL−1 and temperature 29 °C.
  • Treatment 2 (heat stress), 6.45 mgL−1> DO > 6.04 mgL−1 and temperature 32 °C.
  • Treatment 3 (hypoxia), 2 mgL−1 > DO > 1.75 mgL−1 and temperature 29 °C.
  • Treatment 4 (heat stress + hypoxia), 2 mgL−1> DO > 1.75 mgL−1 and temperature 32 °C.
The 2 mgL−1 DO concentration is generally defined as hypoxia in marine ecosystems [6] and therefore was set to represent hypoxic condition. Similarly, the annual seawater temperature range of 29–32 °C has been reported in Phuket [14,46]. As a maximum of 32.45 °C sea surface temperature was recorded in the central part of the Bay of Bengal for over a month in 2010 [47], and a warmer scenario is predicted for the future [48,49], 32 °C was chosen for heat stress. The ambient DO and temperature were determined from field measurements (Supplementary Table S1) and the long-term sea surface temperature of Patong Bay, Phuket (Supplementary Figure S1).
Constant temperature was maintained by the heater chiller (JMC-02, JBA, Zhongshan, China) while DO concentration was maintained by carefully controlling the flow of air (from air pumps) and nitrogen gas (from N2 tanks) using multiple flow controllers. The high pressure from N2 tanks was reduced to a pressure slightly above ambient in 2 steps by connecting the nitrogen high-pressure regulator (IM-TECH, Zhejiang, China) to an air compressor pressure regulator and a switch control valve (Xcpc, Zhejiang, China). Aquarium flow control valves with air stones were also used to further control the amount of air and N2 being introduced into each treatment tank. A moderate water flow within the tank was generated with recirculating pumps (AP-1200, SONIC, Zhongshan, China). DO was measured at frequent intervals using the YSI ProDSS Multiparameter (Xylem Inc., Ohio, USA). The parameters were mostly stable except for a slightly elevated pH in hypoxia and heat stress + hypoxia treatment tanks as a result of N2 bubbling [50,51] (Supplementary Table S2).
The experiment was run for nine days, and the photosynthetic efficiency was measured every day at 08:45 and 21:30 for dark-adapted coral nubbins. The light was set on a schedule to switch on and off every day at 09:00 and 21:00, respectively. Destructive sampling was conducted on days 0, 3, 6, and 9 (refer to Figure 1B) at 10:00 in the morning. Each nubbin was snap-frozen using liquid nitrogen and stored at −80 °C for Symbiodiniaceae density and chlorophyll concentration analysis. Buoyant weight measurements were taken on days 0 and 9 to determine coral growth rate.

2.3. Measurement Protocols

2.3.1. Photosynthetic Efficiency

Coral–Symbiodiniaceae photosynthetic performance was assessed by measuring the maximum quantum yield (Fv/Fm) and the photochemical efficiency (Fv/F0) of Photosystem II (PSII), where F0 represents minimum fluorescence, Fm represents maximum fluorescence of dark-adapted sample after a saturating pulse is applied, and Fv (Fm − F0) is the variable fluorescence. The measurements were taken at three random points on the coral tissue surface for each replicate using a Diving-PAM fluorometer (Walz GmbH, Effeltrich, Germany) connected to a 6 mm diameter fiber-optic probe. The PAM intensity of measuring light (MEAS-INT) was set at 5, electronic signal gain (GAIN) at 2, saturation pulse intensity (SAT-INT) at 8, and width of saturating light pulse (SATWIDTH) at 0.6 s. The measurements were taken twice a day, before the light was turned on (08:45) and after the light was turned off (21:30).

2.3.2. Symbiodiniaceae and Chlorophyll Content

The coral nubbins (n = 4) were collected for destructive testing on days 0, 3, 6, and 9, for Symbiodiniaceae density and chlorophyll analysis. The frozen nubbins were blasted with 50 mL of artificial seawater (35% NaCl solution) to remove the coral tissue. The slurry was homogenized for 10 min at 1500 rpm and 4 °C temperature to obtain a well-mixed sample [52]. Then, 1 mL of each suspension was taken for counting Symbiodiniaceae cells with a hemocytometer, under a light microscope with 40× magnification. The remaining sample from Symbiodiniaceae counting was centrifuged at 4,000 rpm for 5 min to separate Symbiodiniaceae cells from the coral tissue. The supernatant containing coral tissue was discarded, and the Symbiodiniaceae pellet was collected, 3 mL of 90% acetone was added to it, and it was kept at 4 °C for 24 h. The algal pellet was centrifuged again, and the chlorophyll a and c2 concentrations were determined using the standard spectrophotometric method [53] with absorbance measured at 630, 664, and 750 nm [54].
Each coral skeleton was bleached in 10% sodium hypochlorite and washed several times before measuring the surface area using a modified paraffin wax dipping method [55,56]. The Symbiodiniaceae cell density and chlorophyll concentration were normalized as number of individual cells per cm2 and µg per cm2, respectively.

2.3.3. Growth Rate

The buoyant weight technique was used to determine coral growth rate [57,58] in a nondestructive manner. The same coral nubbin was weighed initially and at the end of experiment using a 4-digit precision balance (Ohaus, New Jersey, USA). During each measurement, both temperature and salinity were recorded for the calculation of seawater density, and a glass reference was weighed in both sea water and air [58]. The skeleton bulk densities used for P. lutea, M. tuberculosa, and P. verrucosa were 1.41, 1.58, and 2.93 g cm−3, respectively [59,60,61]. Coral growth rates were expressed as net increases in biomass (%) per day.

2.3.4. Statistical Analysis

The data for all parameters were tested for normality using Shapiro–Wilk test. Sphericity was tested for Fv/Fm and Fv/F0 data while homoscedasticity was tested for other parameters. Repeated measures ANOVA was used to determine significant differences between temperature, DO, and time of sampling for Fv/Fm and Fv/F0 of each coral species.
Three-way ANOVA was used to determine statistically significant differences between temperature, DO, and time for Symbiodiniaceae density and chlorophyll concentration of each species. Two-way ANOVA was used to test significant differences by temperature and DO in growth rate of each species. All tests used 95% confidence level threshold, and post hoc Tukey HSD test was performed to determine statistically significant differences among the distinct groups. All analyses were performed using R Studio version 1.4.1717.

3. Results

Exposure to high temperature and low DO were found to induce physiological changes in corals as well as in the symbiotic algae. The temperature and DO affect the photosynthetic performance, Symbiodiniaceae density, chlorophyll concentration, and coral growth (see Supplementary Tables S3–S5). Each coral species revealed a different response, and the combined stresses had a significantly worse effect only on the growth rate of M. tuberculosa.

3.1. Photosynthetic Efficiency

The Fv/Fm and Fv/F0 of P. lutea measured before the light period under ambient conditions on day 0 were 0.639 ± 0.023 and 1.781 ± 0.177, respectively. The treatment with heat stress + hypoxia showed a significant decrease compared to ambient on day 1 (p = 0.003 for Fv/Fm and p = 0.003 for Fv/F0), but the performance subsequently increased, and samples could maintain effective photosynthesis until day 9, with no significant differences between the treatments (Figure 2A,B). For the measurements taken after the light period, the Fv/Fm and Fv/F0 of P. lutea under heat stress significantly decreased starting on day 1 (p = 0.008 and 0.009, respectively).
In contrast, significant increases were recorded under hypoxia (p = 0.049 for Fv/Fm, p = 0.038 for Fv/F0) and heat stress + hypoxia (p = 0.004 for Fv/Fm, p = 0.002 for Fv/F0) on day 3 (Figure 3A,B). There was no significant interaction between the factors for measurements taken before the light period whereas the measurements taken after light period showed significance for all interactions (Supplementary Table S3).
M. tuberculosa had similar results to P. lutea and seemed to express a tolerance to stress conditions. During the experiment period, Fv/Fm and Fv/F0 showed no significant differences between the stress treatments when compared to ambient conditions in measurements taken before the light period (Figure 2C,D). For measurements taken after light period, coral nubbins under heat stress + hypoxia showed significant decrease only on day 5 for both Fv/Fm and Fv/F0 (p = 0.019 and 0.023, respectively) compared to ambient condition treatment (Figure 3C,D). Subsequently, there was no significant difference between the treatments. We found no significant interaction between the factors (in Fv/Fm and Fv/F0) in measurements taken before or after the light period; however, the temperature and DO factors individually affected the coral nubbins (Supplementary Table S4).
P. verrucosa measurements taken before the light period presented a significant decline on day 2 for heat stress (p = 0.003 for Fv/Fm, p = 0.003 for Fv/F0) and for heat stress + hypoxia (p = 0.045 for Fv/Fm, p = 0.038 for Fv/F0) compared to ambient condition (Figure 2E,F). Progressive decreases by 33.3% for Fv/Fm and by 22.6% for Fv/F0 were detected under heat stress by day 6. Coral nubbins experienced bleaching and death afterwards. In measurements taken after the light period, the photosynthetic performance of coral nubbins (Figure 3E,F) significantly declined after day 1 under heat stress (p = 0.031 for Fv/Fm, p = 0.029 for Fv/F0) and continued to decline, especially on day 6, with decreases by 30.2% and 15% from day 0 in Fv/Fm and Fv/F0, respectively. In hypoxia condition, the corals showed a slight decrease on day 6 (p < 0.001 for Fv/Fm, p < 0.001 for Fv/F0) while heat stress + hypoxia significantly differed from day 2 when compared to ambient condition (p < 0.001 for Fv/Fm, p < 0.001 for Fv/F0). The measurements taken before the light period showed significant differences by time (p = 0.004 for Fv/Fm, p < 0.001 for Fv/F0), by temperature (p < 0.001 for Fv/Fm, p < 0.001 for Fv/F0), and an interaction effect of time × DO (p < 0.001 for Fv/Fm, p < 0.001 for Fv/F0). Measurements taken after the light period were significant for the interaction time × DO (p < 0.001 for Fv/Fm, p < 0.002 for Fv/F0) and for the individual factors time (p = 0.012) and temperature (p < 0.001) in Fv/Fm and for temperature (p < 0.001) and DO (p = 0.006) in Fv/F0, as shown in Supplementary Table S5.

3.2. Symbiodiniaceae Density

On day 9, Symbiodiniaceae densities in P. lutea in all actual treatments were significantly lower than in the baseline ambient condition (heat stress p < 0.001, hypoxia p = 0.019, heat stress + hypoxia p = 0.001) (Figure 4A). There were significant effects of time (p = 0.036), temperature (p < 0.001), DO (p = 0.015), and their interaction time x temperature × DO (p = 0.024) (Supplementary Table S3). Interestingly, M. tuberculosa presented a significant increase in Symbiodiniaceae density (Figure 4B) during the experimental period (p = 0.012, <0.001, <0.001 for days 3, 6, and 9, respectively, compared to initial value). Otherwise, the factors had no significance except for time (p < 0.001) and interaction temperature × DO (p = 0.030), as shown in Supplementary Table S4. P. verrucosa revealed significant difference in Symbiodiniaceae density by treatment (Figure 4C), especially on day 9. We identified a drastic decline under heat stress (p = 0.003) and hypoxia (p = 0.028) compared to ambient condition. The temperature and DO factors were significant (p < 0.001 and p = 0.010, respectively), including influences in the interactions time × temperature (p = 0.049), temperature × DO (p < 0.001), and time x temperature × DO (p = 0.042) (Supplementary Table S5).

3.3. Chlorophyll Content

In P. lutea, we found consistent chlorophyll a and c2 concentrations throughout the experiment period in all treatments (Figure 5A and Figure 6A), and the interaction time × temperature × DO was the only significant factor for chlorophyll a (p = 0.047; Supplementary Table S3) whereas chlorophyll c2 was significantly influenced by the individual factor temperature (p = 0.014; Supplementary Table S3). On the other hand, M. tuberculosa revealed a significant increase on day 6 in chlorophyll a (p < 0.001) and on days 3, 6, and 9 in chlorophyll c2 (p < 0.001), although the coral nubbins were under stress (Figure 5B and Figure 6B). Time was a significant factor for both chlorophyll a and c2 in M. tuberculosa (p < 0.001; Supplementary Table S4). In P. verrucosa, we found an obvious significant difference between the treatments, as a reduction in chlorophyll a was recorded from day 3 for all stress exposures compared to ambient condition (p < 0.001), but a subsequent increase was found on day 9 under heat stress + hypoxia (Figure 5C). Chlorophyll c2 in P. verrucosa presented a similar trend (Figure 6C), with significant decreases under heat stress (p < 0.001) and hypoxia (p < 0.001) on day 3. The significant interactions of factors for both chlorophyll a and c2 were temperature × DO and time × temperature × DO (p < 0.001; Supplementary Table S5).

3.4. Growth Rate

There was no significant difference in growth rate of P. lutea between the treatments (Figure 7A), while a significant decrease in the growth of M. tuberculosa was recorded under heat stress + hypoxia (46.9% reduction, p = 0.041) compared to ambient condition (Figure 7B). The growth rate of M. tuberculosa under hypoxia showed a slight increase but had no significant difference from ambient condition. On the other hand, some tissue loss was detected in P. verrucosa under heat stress and hypoxia. The growth rates were significantly lower compared to ambient (Figure 7C) for both heat stress (p = 0.044) and hypoxia (p = 0.042). However, no significant difference was observed in the heat stress + hypoxia treatment compared to ambient condition.

4. Discussion

The 32 °C temperature had significant adverse effects on all three species. Nevertheless, the severity of effects and responses vary by coral species. P. verrucosa was the most sensitive and experienced complete bleaching by the end of our experiment, unlike P. lutea and M. tuberculosa (refer to Supplementary Figures S2–S4). Under heat stress, a significant decline in P. verrucosa’s growth rate, Symbiodiniaceae density, and chlorophyll concentration on day 9 were detected. The photochemical efficiency showed a gradual decline starting on day 1, but it decreased sharply on day 6. This suggests that 5–6 days might be the limit for P. verrucosa to handle direct heat stress of 32 °C. Previous experiments have found that tropical Pocillopora is sensitive to moderate heat (32–33 °C) whereas Porites can maintain the symbiont population and their performance to keep up with the metabolic energy requirements of the coral host [14,62]. P. lutea and M. tuberculosa in this study did not reveal drastic effects from heat stress. A slight increase in Symbiodiniaceae was observed in P. lutea after facing the elevated temperature, with a subsequent decline on day 9. This case can occur when a coral lacks in carbon translocation, and the nutrition is balanced by Symbiodiniaceae growth for a short period [1]. Our results also support previous findings that the response of corals to heat stress is related to coral morphology, with branched coral species being the most susceptible, i.e., the first to bleach and die in mass bleaching events [63,64,65,66,67,68]. The difference in bleaching vulnerability of branching corals has been attributed to several physiological and morphological properties: tissue thickness [69], skeletal fragility and within tissue light scattering [70,71], genetic constitution of symbiotic algae [72], Symbiodiniaceae density per coral cell [73], and mass transfer rate [15,74].
Symbiotic cnidarians are subjected to broad, fast, and daily changes in oxygen content because of the presence of intracellular dinoflagellates. The oxygen levels in coral tissue can be hyperoxic during daylight and hypoxic during darkness as they become net consumers of oxygen in light-limiting conditions [6,75,76]. The fast shift between hyperoxia and hypoxia sometimes induces microenvironment acclimation in coral tissues [77]. Our results indicate that light availability plays a role in the response of some coral species when hypoxia is involved. The Fv/Fm and Fv/F0 trends were different after light/dark in measurements for P. lutea and P. verrucosa, while M. tuberculosa only presented slight fluctuations. During the initial days, P. lutea occasionally presented significantly higher photosynthetic performance under hypoxia during light availability compared to ambient condition. This might be a cellular mechanism of photosynthetic translocation for energy saving and photo acclimation contributing to this species’ tolerance of stress [78,79]. Photosynthesis (CO2 consumption and O2 production) could partially reduce the stress of deoxygenation, but increased respiration by the same photosynthetic organisms during the night could have the opposite effect, particularly with rising temperatures [80]. Thermal stress and coral bleaching usually occur in conjunction with high summer temperatures and calm breezes when water-flow rates are low. Anoxia can occur when there is little or no water flow, resulting in limited diffusion in many branching coral colonies [15,66,81].
The respiration rate of corals is generally believed to be directly proportional to ambient DO concentration based on their anatomy. Some evidence has suggested that corals can moderately sustain respiration rates during declining oxygen concentration, for example, deep-sea corals (thriving in less than 1 mgL−1 DO concentration in the Red Sea [82]), and some corals appear to oxy-regulate using epidermal cilia movements during stagnant flow [83]. Furthermore, previous studies have revealed polyp expansion process of cold-water coral, Lophelia pertusa, and other cnidarians, such as sea anemones, to increase tissue surface area, thereby increasing the diffusive gas exchange [84,85,86], while some soft corals use tentacle pulsation to increase oxygen levels in their tissue [87]. The hypoxia (~2 mgL−1) in our case showed severe adverse effects on P. verrucosa in terms of physiological and visual expressions, bleaching, and tissue loss (refer to Supplementary Figure S4). The growth rate of Symbiodiniaceae and the chlorophyll concentration had significantly declined by the end of experiment, while a reduction in photosynthetic parameters was detected earlier. Further supported by experimental studies, the branching corals have been shown to be highly susceptible to low oxygen, with some species expressing rapid tissue loss even when subjected to a 4 mgL−1 oxygen concentration [32,88]. On the other hand, massive or submassive corals seem to be the survivors of severe hypoxic events [89,90], even when exposed to 0.5 mgL−1 oxygen levels [24]. However, hypoxia stress can also lead to changes in microbial populations, altering the nutrient cycle, for example, from nitrification towards nitrogen fixation and thereby increasing the host’s susceptibility to pathogens. It can also lead to the production of toxic compounds, such as H2S, NO, and H2O2, that further compromise the host’s immunity [6,91,92].
The growth rates of M. tuberculosa in the combined heat and hypoxia treatment were lower than in control and hypoxia treatments, suggesting that heat aggravated the hypoxic stress effects in this coral species. Energy deficit could be an explanation for such an effect on growth, as hypoxia limits ATP production [39] while heat stress increases metabolic energy demand [1]. Nevertheless, the photosynthetic performance and chlorophyll content of M. tuberculosa and P. lutea in the combined stress treatment were generally higher than in the only heat treatment, suggesting that hypoxia may alleviate heat stress at the physiological level. Heat stress is known to lead to an overproduction of reactive oxygen species (ROS) [93,94]. In contrast, reduced activity of mitochondrial electron transport chain as a result of hypoxia could decrease the formation of other ROS and relieve the oxidative stress. Lower ROS has been reported in Acropora species facing hypoxia [95]. Although more replicates and experiments are needed to confirm this speculation, our results suggest that responses at the physiological level may be decoupled from the more integrative response in growth rate, depending on the mechanisms of the stressors.
The ocean is warming at an alarming rate, with an estimated 1–3 °C increase in sea surface temperature (SST) being a likely scenario by the end of this century [96,97,98]. The frequency and scale of mass coral bleaching events associated with thermal stress have been increasing. An anomaly with high sea water temperature between 30 and 34 °C was reported in the Andaman Sea from April–June 2010 that led to a decline in Acropora and Pocillopora cover [99,100] and reduction in P. lutea growth [101]. Unfortunately, thermal stress does not occur in isolation, but is compounded by coastal runoff, nutrient enrichment-induced eutrophication, etc., contributing to progressive decrease in oceanic oxygen reserves over the last 50 years [17,26,102]. Almost 15% of tropical coral reefs are estimated to be at high risk from local hypoxia due to their exposure to anthropogenic activities and geomorphology [19,24,103]. Coral reefs at our study site of Phuket are also vulnerable to heat stress [14,46] and excessive nutrient enrichment, and co-occurring episodes of hypoxia with harmful algal blooms (HAB) are periodically reported in the area [44,45]. The frequency of extreme temperatures and hypoxic events in Thai waters is increasing at an alarming rate [9], and the stress conditions used in our experiment might soon become a likely scenario. Recent observational studies show that corals exposed to sublethal doses of thermal stress have potential to acclimatize, increasing the baseline of thermal limit for subsequent stress events [90,104,105]. Most species also have an inherent tolerance to naturally occurring hypoxia, but its coexistence with other stressors can lead to a breakdown of mutualisms and feedback systems pushing them beyond limits [106]. Ongoing global and local threats may cause a shift toward tolerant local species (for example, P. lutea and M. tuberculosa from our study). Other studies also point towards a lower physiological threshold with the concurrence of high temperatures and low dissolved oxygen leading to a loss and change in reef marine biodiversity [37,107,108].
While the baseline information from our results can be integrated into a guideline for evaluating coral sensitivity to future scenarios where warming and hypoxic events are expected to occur with greater intensity and increased frequency, extrapolation of the results obtained from experiments conducted in a closed system should be interpreted with caution. Limitations in the setup such as a lack of flow may result in a drift of certain physicochemical characteristics of the seawater. In addition, more replicates and a longer experimental period would improve future experiments. We also propose that warming and hypoxic episodes should be closely monitored in order to protect the coral ecosystem.

5. Conclusions

Heat stress was dominant as a stressor compared to hypoxia. Among the three coral species, P. verrucosa seems to be the most vulnerable to both heat stress and hypoxia when these are present individually. The short-term combined stress showed a stronger negative effect compared to individual stresses only on the growth rate of M. tuberculosa. Under hypoxic condition, coral responses varied according to light availability. The photosynthetic efficiency, especially Fv/F0, is a sensitive parameter for early detection, whereas growth-related attributes may serve well as indicators of the long-term effects under a future scenario. Further studies are needed to dissect the combined effects of heat stress and hypoxia and to improve mechanistic understanding of synergistic and antagonistic responses in these three scleractinian corals.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/jmse11020403/s1. Table S1: environmental parameters recorded at the study area, Patong Bay, Phuket, Thailand, during April–October 2021. Table S2: Water quality parameters in the treatment tanks measured during the experiment. Data are shown as mean ± SE. Table S3: Summary of different ANOVAs for photosynthesis, Symbiodiniaceae density, chlorophyll content, and growth rate of P. lutea. Significant values (p < 0.05) are shown in bold. Table S4: Summary of different ANOVAs for photosynthesis, Symbiodiniaceae density, chlorophyll content, and growth rate of M. tuberculosa. Significant values (p < 0.05) are shown in bold. Table S5: Summary of different ANOVAs for photosynthesis, Symbiodiniaceae density, chlorophyll content, and growth rate of P. verrucosa. Significant values (p < 0.05) are shown in bold. Figure S1: Sea surface temperature data for Patong Bay, Phuket, from 2016 to 2021. Data source—Multi-scale Ultra-high Resolution (MUR) SST Analysis fv04.1, Global, 0.01°, 2002–present, daily. These data were provided by JPL under support from NASA MEaSUREs program. Figure S2: P. lutea samples from day 0 to day 9 under ambient, heat stress, hypoxia, and heat stress + hypoxia treatments. The white lines represent 1 cm scale bar. Figure S3: M. tuberculosa samples from day 0 to day 9 under ambient, heat stress, hypoxia, and heat stress + hypoxia treatments. The white lines represent 1 cm scale bar. Figure S4: P. verrucosa samples from day 0 to day 9 under ambient, heat stress, hypoxia, and heat stress + hypoxia treatments. The white lines represent 1 cm scale bar.

Author Contributions

Conceptualization and methodology, T.J., L.Y., P.B. and M.Y.; sample and data analysis, T.J., L.Y. and M.Y.; writing—draft preparation and editing, T.J., P.B. and M.Y.; supervision, P.B. and M.Y.; project administration, P.B. and M.Y.; funding acquisition, M.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Science, Research and Innovation Fund (NSRF) and Prince of Songkla University (Grant number: SCI6505095M).

Institutional Review Board Statement

The study was conducted according to the Animals for Scientific Purposes Act, B.E. 2558 (A.D. 2015) and approved by the Institutional Animal Care and Use Committee, Prince of Songkla University. The coral collection was permitted under Wildlife Conservation and Protection Act, B.E. 2535 (A.D. 1992) and approved by the Department of Fisheries, Ministry of Agriculture and Cooperatives.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Acknowledgments

We thank the Coastal Oceanography and Climate Change Research Center (COCC) and the Marine and Coastal Resources Institute (MACORIN), Faculty of Environmental Management, Prince of Songkla University, for research facilities. The authors thank Butchanok Kongket for her help in map generation and Watchara Samsuvan and Wilawan Hwan-air for assistance in the field and laboratory.

Conflicts of Interest

The authors declare that this research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. (A) Sampling site at Patong Bay, Phuket, Thailand. (B) Design of experiments and placement of coral nubbins (20 nubbins/species/tank) in the four treatments. The nubbins in the first row (black dots) were used for photosynthetic and growth rate measurements, while the next rows were used for destructive sampling of Symbiodiniaceae and chlorophyll analysis on days 0, 3, 6, and 9.
Figure 1. (A) Sampling site at Patong Bay, Phuket, Thailand. (B) Design of experiments and placement of coral nubbins (20 nubbins/species/tank) in the four treatments. The nubbins in the first row (black dots) were used for photosynthetic and growth rate measurements, while the next rows were used for destructive sampling of Symbiodiniaceae and chlorophyll analysis on days 0, 3, 6, and 9.
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Figure 2. Maximum quantum yield of PSII (Fv/Fm; left) and photochemical efficiency of PSII (Fv/F0; right) in P. lutea (A,B), M. tuberculosa (C,D), and P. verrucosa (E,F) measured before the light period. Data are shown as mean ± SE (n = 4).
Figure 2. Maximum quantum yield of PSII (Fv/Fm; left) and photochemical efficiency of PSII (Fv/F0; right) in P. lutea (A,B), M. tuberculosa (C,D), and P. verrucosa (E,F) measured before the light period. Data are shown as mean ± SE (n = 4).
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Figure 3. Maximum quantum yield of PSII (Fv/Fm; left) and photochemical efficiency of PSII (Fv/F0; right) in P. lutea (A,B), M. tuberculosa (C,D), and P. verrucosa (E,F) measured after the light period. Data are shown as mean ± SE (n = 4).
Figure 3. Maximum quantum yield of PSII (Fv/Fm; left) and photochemical efficiency of PSII (Fv/F0; right) in P. lutea (A,B), M. tuberculosa (C,D), and P. verrucosa (E,F) measured after the light period. Data are shown as mean ± SE (n = 4).
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Figure 4. Symbiodiniaceae density (× 105 cells cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient baseline conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
Figure 4. Symbiodiniaceae density (× 105 cells cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient baseline conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
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Figure 5. Chlorophyll a and c2 concentration (µg cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
Figure 5. Chlorophyll a and c2 concentration (µg cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
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Figure 6. Chlorophyll c2 concentration (µg cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
Figure 6. Chlorophyll c2 concentration (µg cm−2) of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient conditions, heat stress, hypoxia, and heat stress + hypoxia on days 0, 3, 6, and 9. Data are shown as mean ± SE (n = 4).
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Figure 7. Growth rates of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient, heat stress, hypoxia, and heat stress + hypoxia. Data are shown as mean (+), median, and range (n = 4) in a boxplot, where an asterisk indicates statistical significance of treatment when compared to ambient.
Figure 7. Growth rates of P. lutea (A), M. tuberculosa (B), and P. verrucosa (C) under ambient, heat stress, hypoxia, and heat stress + hypoxia. Data are shown as mean (+), median, and range (n = 4) in a boxplot, where an asterisk indicates statistical significance of treatment when compared to ambient.
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MDPI and ACS Style

Jain, T.; Buapet, P.; Ying, L.; Yucharoen, M. Differing Responses of Three Scleractinian Corals from Phuket Coast in the Andaman Sea to Experimental Warming and Hypoxia. J. Mar. Sci. Eng. 2023, 11, 403. https://doi.org/10.3390/jmse11020403

AMA Style

Jain T, Buapet P, Ying L, Yucharoen M. Differing Responses of Three Scleractinian Corals from Phuket Coast in the Andaman Sea to Experimental Warming and Hypoxia. Journal of Marine Science and Engineering. 2023; 11(2):403. https://doi.org/10.3390/jmse11020403

Chicago/Turabian Style

Jain, Tarun, Pimchanok Buapet, Long Ying, and Mathinee Yucharoen. 2023. "Differing Responses of Three Scleractinian Corals from Phuket Coast in the Andaman Sea to Experimental Warming and Hypoxia" Journal of Marine Science and Engineering 11, no. 2: 403. https://doi.org/10.3390/jmse11020403

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