Physiological responses of intertidal and subtidal corals Anomastraea irregularis and Pocillopora verrucosa exposed to experimental thermal stress

Abstract

Introduction:

Thermal stress experiments on corals from habitats with contrasting environmental regimes in understudied regions, such as South Africa, are essential to elucidate the mechanisms underlying coral resilience/susceptibility to thermal stress. This study examined the thermal resilience/susceptibility of Anomastraea irregularis (massive morphology) and Pocillopora verrucosa (branching morphology) collected from environmentally variable intertidal and more stable subtidal habitats from the east coast of South Africa.

Methods:

Corals were maintained in closed recirculating aquaria and exposed to two thermal stress conditions (28°C and 30°C) for three months, followed by recovery at control conditions (26°C) for two months. Rates of respiration, photosynthesis, and growth were measured monthly. The Symbiodiniaceae density, chlorophyll-a concentration, and lipid concentration were analysed at the start and end of the thermal stress and at the end of the recovery period.

Results:

The treatments induced bleaching in both species from both habitats with an associated decrease in photosynthetic and growth rates. Inherent differences across all measured physiological parameters, including variation in survival, were observed between the species and habitat throughout the experiment, highlighting that environmental origin and possibly morphology can influence thermal tolerance. The intertidal corals were more tolerant than their subtidal conspecifics, and A. irregularis appeared more tolerant than P. verrucosa in both treatments. The intertidal corals decreased their respiration rates to control levels by the end of thermal stress and, both initially and throughout the study, maintained higher Symbiodiniaceae densities, chlorophyll-a, and lipid concentrations than their subtidal conspecifics.

Discussion:

The tolerance of A. irregularis may stem from thicker tissue which allowed higher Symbiodiniaceae density and lipid concentrations and lower P:R ratios consistent with a more heterotrophic nature. The photosynthetic and growth rates, Symbiodiniaceae density, chlorophyll-a concentration, and lipid concentration of both species from both habitats did not recover two months after thermal stress indicating that restoration of physiological homeostasis following prolonged thermal stress likely requires substantially longer periods. Therefore, the results in this study should be interpreted as evidence of differential tolerance and early recovery responses rather than complete resilience. These findings provide insight into the physiological mechanisms underpinning thermal tolerance in high-latitude corals, highlighting that corals persisting in environmentally variable environments can exhibit traits critical for understanding resilience to climate change. An important caveat to consider, despite regular water changes, the closed recirculating systems may accumulate metabolic waste products over time, which can independently affect coral physiology and confound thermal stress responses.

1 Introduction

Coral symbiosis with photosynthetic algae, Symbiodiniaceae, is vital to the productivity of the corals and, by extension, the reef ecosystems (Brown, 1997; Stat et al., 2012; Muller-Parker et al., 2015). However, this symbiosis can disintegrate when the corals encounter biological or environmental stressors (Baker et al., 2008; Wooldridge, 2017). Coral bleaching is the resulting phenomenon when the corals eject the Symbiodiniaceae from their tissue, or there is a loss in the photosynthetic pigments of the Symbiodiniaceae in response to stress (Baird et al., 2009). In healthy corals, up to 90% or more of the daily metabolic requirements are met by the photosynthetically fixed carbon from the Symbiodiniaceae (Muscatine et al., 1981). However, this percentage is not universal across all corals, the relative contributions of symbiont photosynthesis and coral heterotrophy to energetic demands vary substantially among species and with environmental conditions. Nevertheless, an energy deficit follows bleaching due to the loss of photosynthates from Symbiodiniaceae coupled with usually increased metabolic costs (Rädecker et al., 2021) and altered energy metabolism (Pupier et al., 2024) in response to stress. The energy deficit may be lethal to the coral if the stress does not decrease or if the coral is not recolonised by Symbiodiniaceae (Muller-Parker et al., 2015). Many corals are mixotrophic, and some species, particularly those with massive morphologies, exhibit comparatively higher heterotrophic capacity under baseline conditions and may enhance heterotrophy to compensate for the energy deficit during bleaching (Grottoli et al., 2006; Anthony et al., 2009; Houlbrèque and Ferrier-Pagès, 2009). Therefore, the inherent heterotrophic/autotrophic dependence of a coral to meet their metabolic requirements may be important to their resilience when stressed.

Corals face multiple stressors, however, thermal stress driven by global climate change remains the primary threat (Ainsworth et al., 2016; Kim et al., 2023). The frequency, intensity, and duration of marine thermal stress events have increased over the last 35 years (Hughes et al., 2018). Consecutive global mass coral bleaching events were recorded for the first time during 2014-2017 (Skirving et al., 2019). Increased global mass coral bleaching events are predicted for the near future even with conservative global warming predictions (Skirving et al., 2019). Since corals are fundamental in reef functioning, the significant loss of corals has a domino effect detrimentally affecting all coral community by reducing reef habitat complexity which leads to a reduction in productivity in both an ecological and socio-economic sense (Moberg and Folke, 1999; Alvarez-Filip et al., 2011, 2013; Dietzel et al., 2021).

Nonetheless, there is large variability in the degree of coral bleaching severity and mortality when corals are faced with thermal stress events. Innate characteristics related to coral morphology, like greater tissue thickness and lipid reserves, as well as lower metabolic rates, are known to contribute to more thermal resilience in massive species compared to branching species (Coles and Jokiel, 1977; Loya et al., 2001; Guest et al., 2012; Levas et al., 2013; Schoepf et al., 2015; Jacobson et al., 2016). However, these morphological differences are often confounded with species identity, as comparisons typically involve different species with distinct physiological traits, making it difficult to fully understand the relative contributions of morphology and species-specific responses. In addition to intrinsic traits, environmental history also plays a key role in shaping coral thermal resilience. Corals that encounter highly variable thermal regimes, such as in intertidal rock pools, are more resilient to thermal stress than conspecifics that encounter moderate thermal regimes (Smit, 2014; Camp et al., 2018; Safaie et al., 2018; Schoepf et al., 2021; McRae et al., 2022; Huang et al., 2024). Importantly, resilience does not necessarily imply complete resistance to bleaching. Resilience to bleaching reflects a coral’s ability to withstand and recover from thermal stress, encompassing resistance to the onset of bleaching, tolerance during the bleached state, and recovery through regaining health and symbiont populations after stress (Obura, 2005; Osborne et al., 2017).

However, the underlying physiological mechanisms that drive the variability in coral resilience/susceptibility to thermal stress are still unclear and warrant investigation. Moreover, McLachlan et al. (2020) indicated that two-thirds of heat-stress experiments on corals over three decades (1990-2020) were conducted in only three countries and that three species were more heavily studied than others. Thus, the geographic and taxonomic bias necessitates investigating coral physiological performance of diverse coral species experiencing different levels of thermal stress to attain fundamental information that will aid in the conservation of corals. Such knowledge can help identify stress-tolerant species and populations that are more likely to persist under future climate scenarios and can therefore inform targeted management, restoration, and conservation strategies (Morikawa and Palumbi, 2019; Schoepf et al., 2023).

Therefore, investigating corals from the extreme and marginal habitats in understudied locations such as South Africa provides a valuable framework to examine how contrasting thermal histories shape physiological responses to thermal anomalies and ocean warming. Key physiological processes, including respiration, photosynthesis, and growth, are fundamental determinants of coral performance under thermal stress (Lesser, 2013). The Symbiodiniaceae density, Symbiodiniaceae chlorophyll-a concentration, and lipid concentration of corals influence their energy budget, thereby influencing their resilience/susceptibility to stress and are therefore also measured during experiments (Muscatine, 1990; Nystrom et al., 2001; Houlbrèque et al., 2003; Rodrigues and Grottoli, 2007). The resilience of corals combines their resistance to and recovery from thermal stress, so it is important to also investigate coral performance when thermal stress ceases (Visram and Douglas, 2007; Osborne et al., 2017). South African corals are close to the southern limits of coral distribution and corals in the iSimangaliso Wetland Park in the northern limits of the province of KwaZulu-Natal exhibited minimal bleaching from climate change (Schleyer et al., 2018; Porter et al., 2021). However, the underlying physiological mechanisms that drive this bleaching trend have yet to be thoroughly investigated in these corals or corals in non-reef habitats found further south of the province of KwaZulu-Natal. Several coral species of varying growth forms inhabit the environmentally variable intertidal and moderate subtidal zones of the rocky shores of Treasure Beach, east coast KwaZulu-Natal province, South Africa (Smit, 2014). Anomastraea irregularis (massive morphology) and Pocillopora verrucosa (branching morphology) are common species found thriving in both zones (Smit, 2014). Smit (2014) found differential physiological responses in Symbiodiniaceae density, chlorophyll-a and lipid content between the species in response to seasonal change in the intertidal pools. Pocillopora verrucosa exhibited more changes in Symbiodiniaceae density, chlorophyll-a and lipid content throughout the year than A. irregularis (Smit, 2014). Anomastraea irregularis from both habitats were found to be more thermotolerant, exhibiting less genetic change than P. verrucosa from both habitats when exposed to short-term experimental thermal stress (Onyango, 2020). Furthermore, upregulation in genes associated with protein synthesis in both species from the intertidal habitat were found to confer higher thermotolerance than the subtidal conspecifics (Onyango, 2020). These findings highlighted the possibility of species and habitat-specific physiological acclimatisation and/or adaptations in these corals to mediate thermal stress.

Therefore, this study aimed to determine the resilience or susceptibility of Anomastraea irregularis, and Pocillopora verrucosa, from environmentally variable intertidal pools and environmentally stable subtidal habitat at Treasure Beach, South Africa, under experimental thermal stress conditions. This was accomplished by measuring the corals’ physiological responses i.e., respiration, photosynthetic, and growth rates, as well as change in tissue composition (Symbiodiniaceae density, Symbiodiniaceae chlorophyll-a, and lipid concentrations) over three months of thermal stress and then two months of recovery. This study hypothesised that corals from the environmentally variable intertidal habitat would exhibit greater thermal resilience under the prolonged thermal stress treatments than their subtidal conspecifics. This would be reflected in smaller declines in photosynthetic and growth rates, higher Symbiodiniaceae densities, chlorophyll-a concentrations, and lipid reserves, as well as a more rapid recovery of these parameters following the cessation of thermal stress, consistent with greater physiological plasticity. Furthermore, it was hypothesised that A. irregularis would exhibit greater thermal resilience than P. verrucosa. This would be reflected in the maintenance of higher lipid reserves and Symbiodiniaceae densities, lower reductions in photosynthetic performance and growth rates, and improved recovery following thermal stress, consistent with traits usually associated with massive morphologies. Since thermal variability is thought to mechanistically drive pre-conditioning through heat shock protein induction, antioxidant upregulation, and Symbiodiniaceae shuffling, that can drive thermal resilience in corals. By removing thermal variability, this study examined whether corals originating from habitats that differ in presumed thermal variability exhibit differential physiological responses when exposed to prolonged constant thermal stress under laboratory conditions.

2 Materials and methods

2.1 Study site description

Anomastraea irregularis, a massive species, and Pocillopora verrucosa, a branching species, were collected during low tide from the highly variable intertidal and more stable subtidal habitats at Treasure Beach (29°57’32.8”S 30°59’19.0”E), on the east coast of South Africa. The South African east coastline is relatively high energy and experiences a semi-diurnal tidal cycle with a tidal range of 1.5-2.23 m (Smit and Glassom, 2017). Thus, approximately 4 h twice a day during spring low tides the rock pools at Treasure Beach are isolated and aerially exposed and then completely inundated during hightides (Smit and Glassom, 2017). The rock pools from which the corals were sampled were ~0.27 m² and ~0.39 m deep at low tide, and occurred at near-horizontal surfaces between the high- and low-tide marks. The average temperature in the intertidal rock pools in this region is stable however there are large daily fluctuations of up to 10 °C over as little as 2 h in summer and during daytime spring low tides (Smit and Glassom, 2017). The subtidal zone a few meters beyond the low tide mark was ~3 m deep and considered to be a relatively more moderate thermal habitat since there is no aerial exposure or isolation with tidal changes. However, no published in situ temperature records were available for the subtidal habitat during the study period, and therefore the magnitude of thermal differences between habitats could not be directly quantified. There was no published literature specifically on differences in the levels of turbidity, light, pH, wave action, oxygen, nutrients, etc. experienced in these two habitats. However, based studies from other regions it is highly likely that the light, pH, salinity stress are intensified in the rock pools during low tide isolation (Le Tissier and Brown, 1996; Helmuth et al., 2006).

2.2 Collection of corals

The two species were chosen as focal species because they are representatives of the dominant coral assemblages in the study area (Smit and Glassom, 2017) and have differing morphology. A hammer and chisel were used to remove ten healthy (colour 6 on Coral Health Chart (Coral Watch, Australia) and with no visual signs of disease or parasites) colonies (~8-12cm in diameter) of each species from the substrata of each habitat. The number of parent colonies was chosen to sustain more than 80% of allelic variability in the coral populations (Baums et al., 2019). Corals were sampled under the South African Department of Environmental Affairs and the Department of Agriculture, Forestry and Fisheries research permit number RES2022-50. No further permission or ethical approval was required (University of KwaZulu-Natal’s Animal Research Ethics Committee Standard Operating Procedures). The colonies were transported to the Marine Science Unit (MSU) at the University of KwaZulu-Natal in plastic buckets filled with seawater from the site. The colonies were left to acclimate for a week in four 160-L recirculating indoor aquaria (the aquaria setup can be seen in Supplementary Appendix 2) filled with sand-filtered natural seawater attained from uShaka Marine World (permit number WSWJ210028). Each tank was equipped with a submersible glass heater (300W, Enjoy Royal, China) to maintain the tank seawater temperature at 26 ± 0.5 °C (mean ± standard deviation). This is the long-term annual average temperature at Treasure Beach and was used as the control temperature during this study to reflect typical ambient conditions experienced by corals throughout the year.

2.3 Experimental design and maintenance of corals

Each colony was then fragmented into nine pieces (3.1 ± 0.45 cm long for P. verrucosa and 3.1 ± 0.41 cm wide for A. irregularis) using wire cutters to attain 90 fragments per species from each habitat (Supplementary Appendix 1B). Each coral fragment was stuck onto pre-labelled plastic tiles using epoxy (Pratley^® Quickset Putty, South Africa). The coral fragments were then randomly separated into nine 160-L recirculating aquaria (n=10 of each species from each habitat). Therefore, the stocking density for each tank was 40 coral fragments (Supplementary Appendix 2). The coral fragments were left to heal and further acclimate to the indoor aquarium conditions for one month before temperatures in the treatment tanks were increased (Supplementary Appendix 1A shows the full study timeline). The maximum monthly mean (MMM) for the study region is 27 °C (NOAA Coral Reef Watch). The two elevated temperatures chosen for this study were 28 °C and 30 °C. They represented the presumed local bleaching threshold of MMM for the region +1 °C and potential worst-case scenario where the local bleaching threshold would be exceeded with an increase of 3 °C from the MMM (IPCC, 2023). The experimental Degree Heating Weeks (DHW) based on the temperature loggers in each treatment tank were calculated as per Leggat et al. (2022).

Following acclimation, three replicate tanks were allocated per treatment (Supplementary Appendix 2C). The three control tanks remained at 26 °C while the temperature in the treatment tanks was ramped up at a rate of 0.5 °C per day. Tanks assigned to the 30 °C treatment reached the target temperature in eight days, while tanks assigned to the 28 °C treatment started heating on day four and reached the target temperature on the same day as the 30 °C treatment. The elevated temperature conditions in the treatment tanks were maintained for approximately three months after which the temperatures were ramped down to the control temperature at 0.5 °C per day by reducing the temperature on the submersible glass heaters. Since the fragments in the treatments were subjected to prolonged and constant thermal stress rather than fluctuating thermal regimes, the experimental design specifically tested the influence of prior environmental history or preconditioning effects, rather than the direct physiological effects of fluctuating temperature regimes during the experiment itself. All nine tanks were then maintained at an average temperature of 26 °C for approximately two months. The experiment was conducted in an air-conditioned room maintained at approximately 16–18 °C to cool ambient conditions to minimise external heat influence. Tank temperatures were independently controlled using the submersible heaters with adjustable thermostats. Temperature ramping up and down (0.5 °C per day) and maintenance at the target temperatures were all achieved by actively adjusting the heater setpoints in each tank.

A submersible pump with an output of 4000 L h^-1 in each sump maintained constant water flow in each tank throughout the acclimation and experimental study period. Each tank was illuminated daily for 12 hours with an artificial LED (light emitting diode) aquarium light (Zetlight 6600 qmavenII, China) throughout the acclimation and experimental study period. To prevent sudden overexposure to LED light during the initial acclimation of the colonies, the preprogrammed manufacturer acclimation setting was used. The programme gradually ramped up PAR (photosynthetically active radiation) intensities daily over the course of a week. Afterwards, throughout the study, the light over each tank was programmed to gradually increase from 06:00, reaching a peak midday average of ~245 μmol m^-2 s^-1 and then gradually decrease in intensity towards darkness at 18:00. Each tank’s average PAR levels were measured using an Apogee PAR meter (MQ-650 ePAR meter, United States of America) and found to range from 100 to 250 μmol m^-2 s^-1. The PAR range represents the spatial variability within each tank at peak midday light levels. The highest intensity was measured at the centre of the tank, while the edges of the tank received lower intensities due to the positioning of the light bulbs because of the design of the light. The physico-chemical seawater parameters were measured regularly in each tank from the start until the end of the study. A temperature logger (iButtons Maxim^®, United States of America) was placed in each tank and set to record temperature in 30-minute intervals (Supplementary Appendix 3A; overall the control tanks remained stable at approximately 26 ± 0.5 °C throughout the study). The salinity and pH were measured in each tank daily with a multiprobe water quality meter (P613 Portable combo meter, China) (Appendices 3B, C). Distilled water was added to the sumps when needed to maintain salinity at approximately 35 g kg^-1. The alkalinity, calcium, and magnesium levels in each tank were measured weekly using commercial kits (Red Sea, Reef Foundation Pro Multi Test Kit, Israel). Alkalinity was maintained at approximately 2870.8 µmol kg^-1, calcium was maintained at approximately 420 mg kg^-1, and magnesium was maintained at approximately 1280 mg kg^-1 by dosing with commercial liquid supplements when necessary, following the manufacturer’s instructions (Red Sea, Reef Foundation A, B, C+ Complete Pack, Israel). The accuracy of the test kits was: ± 25 µmol kg^-1 for alkalinity, ± 5 mg kg^-1 for calcium and ± 20 mg kg^-1 for magnesium (Red Sea, Reef Foundation A, B, C+ Complete Pack, Israel). Every week, seawater changes of approximately 50% fresh sand-filtered natural seawater, cotton filter changes were performed, and the tanks were cleaned of debris and algae. The coral fragments were also rotated within the tanks weekly to minimise potential positional effects of light and/or water circulation. Four mL of coral nutrition (Red Sea, Reef Energy Plus (AB+), Israel) was also added to each tank weekly.

2.4 Determination of physiological rates

The health of each coral fragment was monitored visually using the Coral Health Chart (Siebeck et al., 2006) approximately every week (23 sampling occasions in total see Supplementary Appendix 1C for exact sampling points) from the beginning of ramping up temperatures in the treatment tanks, start of the heat stress (when the treatment tanks reached the desired 28 °C and 30°) exposure until the end of the study. The number of fragments that died was noted for each tank, and the cumulative percentage mortality was calculated for each treatment on each occasion. Coral death was noted visually using a magnifying glass. Complete tissue loss, absence of live polyps, skeletal discoloration, and subsequent algal overgrowth were used as indicators of coral death.

The photosynthetic and respiration rates were measured on seven different occasions (see Supplementary Appendix 1C for exact sampling points) from before the start of thermal stress (23 July 2022) and then approximately monthly until the end of the study (20 December 2022). Three fragments of each species and from each habitat were randomly selected from each tank, and each fragment was placed in individual sealable 2-L glass jars filled with natural seawater and equipped with a submersible pump (385 L h^-1, Dophin, China) to ensure constant water movement during the three-hour incubations (Boodraj and Glassom, 2022), first under LED light and then under dark conditions. The incubation jars were kept in water baths maintained at the tank temperatures from which the fragments originated. Three experimental blank control chambers filled with natural seawater and a submersible pump but with no coral fragment were used as blank controls for each temperature treatment to correct for any non-coral metabolic activity within the seawater. The respiration and photosynthetic rates were calculated based on changes in measured dissolve oxygen concentrations (using a portable dissolved oxygen meter (T-Heng M1500K, China)) during the incubations (Boodraj et al., 2024). The surface area of each fragment was used to normalise the respiration and photosynthetic rates and was attained using the aluminium foil wrap method (Marsh, 1970) at the end of the experiment.

The buoyant weight method (Davies, 1989) was used to measure the skeletal growth rate of each coral fragment. Each fragment was weighed on seven different occasions (see Supplementary Appendix 1C for exact sampling points) from before the start of thermal stress (23 July 2022) and then approximately monthly until the end of the study (20 December 2022). An analytical mass balance (Radwag AS 220.R2 PLUS, Germany, accuracy ± 0.1 mg) with an under-weighing capability was used with a monofilament line with a fishing hook attached to the end. The fragments were weighed in a jar of seawater from their respective tanks to reduce the stress of environmental changes. For the density calculations, a metal 50-g calibration weight was weighed to determine the seawater density and the density of aragonite (2.94 g cm^-3) was used for the coral fragments (Davies, 1989). The change in mass (mg) between times for each fragment was normalised to surface area and number of days between measurements to attain the growth rate in mg cm^-2 day^-1.

2.5 Determination of tissue composition

At the start (31 July 2022) and end (23 October 2022) of the thermal stress and at the end of the recovery period (20 December 2022) three fragments of each species from each habitat from the control and treatment groups were removed. The fragments were flash-frozen in liquid nitrogen and kept in a -80 °C ultra-freezer (Snijders Labs, VF475-86, Germany) until further processing. The coral tissue from the fragments was then removed using an Aquaflosser filled with autoclaved seawater (Johannes and Wiebe, 1970). The coral tissue was diluted to a standard volume with autoclaved seawater and homogenized in a beaker using a homogeniser (Ultra-Turrax^®IKA^® T25 digital, Germany). Each sample homogenate was divided into three parts to determine Symbiodiniaceae cell densities, Symbiodiniaceae chlorophyll-a concentration, and lastly, total lipid content (Boodraj and Glassom, 2022).

The Symbiodiniaceae cell density was measured and normalised as described by Boodraj and Glassom (2022) but there were amendments to the chlorophyll-a concentration and lipid content analyses. The 15 mL of coral holobiont tissue homogenate was centrifuged at 1200 x g for ten minutes at 4 °C to separate the Symbiodiniaceae cells from the coral tissue (Gamba et al., 2022). Two mL of the supernatant containing the coral tissue was pipetted into Eppendorf tubes and immediately stored in a -80 °C-ultra-freezer to be used later for biochemical biomarker analyses not included in the present study. The pellet containing the algal cells were then treated and analysed as described by Boodraj and Glassom (2022). The Symbiodiniaceae efficiency of the fragments was determined by dividing the normalised chlorophyll-a concentration by the normalised Symbiodiniaceae densities to yield the chlorophyll-a concentration per Symbiodiniaceae cell metric (Boodraj and Glassom, 2022). The amendments to Boodraj and Glassom (2022) method to determine the lipid content were that the tissue homogenate was centrifuged at 1200 x g for ten minutes at 4 °C and that the supernatant (containing the coral host fraction) was resuspended in six mL of 2:1 (v/v) chloroform:methanol (Miktek, South Africa). These modifications were implemented to improve consistency of fractionation and ensure that lipid measurements reflect host-derived energy reserves following Symbiodiniaceae separation. Thereafter the lipid content determination and normalisation followed Boodraj and Glassom (2022).

2.6 Statistical analysis

All the statistical analyses were performed with the statistical programme IBM SPSS version 28. To determine if there were significant differences in coral health score, respiration rates, photosynthetic rates, P:R ratios, and growth rates between habitats (intertidal and subtidal) and temperature treatments (control (26 °C), 28 °C, and 30 °C) at the different times (see Supplementary Appendix 1C for exact times for each variable) for each species five Generalised Estimating Equations (GEE) were performed. The residuals of the dependent variables were found to be nonparametric (one sample Kolmogorov-Smirnov p < 0.05) therefore GEEs were performed with a gamma distribution with log link functions. The colony effect and tank replicate were added as covariates to account for random effects but were removed from the models if they were non-significant.

To determine if there were significant differences in Symbiodiniaceae cell density, Symbiodiniaceae chlorophyll-a concentration, chlorophyll-a per Symbiodiniaceae cell, and lipid concentration between habitats (intertidal and subtidal) and temperature treatments (control (26 °C), 28 °C, and 30 °C) at the different times (see Supplementary Appendix 1C for exact times for each variable) four Generalised Linear Models (GLM) were performed for each species. GLMs were performed with a gamma distribution with log link functions as the residuals were nonparametric (one sample Kolmogorov-Smirnov on residuals of the dependent variables p < 0.05). The colony effect and tank replicate were added as covariates to account for random effects but were removed from the models if they were non-significant (p > 0.05). To determine statistical differences (p < 0.05) within tested groups Bonferroni pairwise comparisons using estimated marginal means were also performed and all tables can be seen in the Supplementary Appendix. Statistical significance was assessed at α = 0.05. Exact p-values were reported where available, while values below the reporting precision of SPSS were presented as p < 0.001.

3 Results

3.1 Bleaching and mortality

Final cumulative experimental Degree Heating Weeks (eDHW) averaged 25.4 ± 1.5 SD in the 28 °C treatment and 48.5 ± 1.4 SD in the 30 °C treatment across replicate tanks (Figure 1). Coral fragments of both species from both habitats in the control tanks remained healthy, with no colour loss or mortality recorded throughout the study (Figure 2). The coral score of both species in the two elevated temperature treatments significantly differed from their conspecifics in the control throughout the study (Figure 1B; Supplementary Appendix 4). Bonferroni pairwise analysis shows exactly when the coral scores significantly differed with the mean differences between pairs for each species (Supplementary Appendix 4). Overall, subtidal and intertidal P. verrucosa fragments, and subtidal A. irregularis fragments in both temperature treatments began to lose colour after approximately a week of thermal stress (Figure 2). In contrast, colour loss in intertidal A. irregularis in both temperature treatments was only seen after approximately a month of thermal stress (Figure 2). Overall, after three months of thermal stress, the fragments of both species from both habitats experienced significant bleaching, with those in the 30 °C treatment experiencing more bleaching than those in the 28 °C (Figure 2; Supplementary Appendix 4). In general, the subtidal fragments of both species experienced more colour loss than their intertidal counterparts (Figure 2; Supplementary Appendix 4). At the end of two months of recovery, there was improvement in colour in the fragments of both species from both habitats, although the scores remained lower than the initial values (Figure 2; Supplementary Appendix 4).

Figure 1

Figure 2

Mortality mostly coincided with the bleaching trend (Figure 2). Overall, P. verrucosa experienced higher mortality than A. irregularis in the 30°C treatment and in the 28 °C treatment (Figure 3). Furthermore, no A. irregularis intertidal fragments died during the study, while P. verrucosa subtidal fragments in the 30 °C treatment experienced higher mortality than their intertidal fragments in the same treatments (Figure 3). After approximately two months of thermal stress, no intertidal fragments died but subtidal fragments experienced mortalities, with higher deaths recorded for P. verrucosa in the 30 °C treatment than in the 28 °C treatment and only mortality recorded for A. irregularis in the 30 °C treatment and no deaths in A. irregularis in the 28 °C (Figure 3). Pocillopora verrucosa fragments from the intertidal habitat only experienced mortalities after three months of thermal stress, and higher deaths were recorded in the 28 °C treatment than in the 30 °C treatment (Figure 3). After the first month of recovery, one subtidal A. irregularis fragment and two subtidal P. verrucosa fragments from the 30 °C treatment, as well as a one subtidal P. verrucosa from the 28 °C treatment died (Figure 3). No other mortalities were recorded at the end of the second month of recovery (Figure 3).

Figure 3

3.2 Respiration and photosynthetic rates

The respiration, photosynthetic rates, and P:R ratios of corals in the control conditions did not significantly differ during the study (Figure 4). Overall, the respiration rates of both species from both habitats in the thermal stress treatments were significantly higher than those in the control (Figure 4A; Supplementary Appendix 5). Furthermore, post-hoc comparisons revealed that respiration rates of the fragments in the 30 °C treatment were higher than the 28 °C treatment (Figure 4A; Supplementary Appendix 5). The subtidal fragments of both species had much higher respiration rates than the intertidal fragments overall (Figure 4A; Supplementary Appendix 5). The respiration rates of the subtidal fragments of both species had a more pronounced difference to controls than the intertidal fragments in both thermal stress treatments (Figure 4A; Supplementary Appendix 5). The respiration rates of both species in the thermal stress treatments began to decrease towards the end of the thermal stress and recovery period (Figure 4A; Supplementary Appendix 5). However, at the end of the recovery period, the respiration rates of the subtidal fragments of both species in the thermal stress treatments were still significantly higher than the controls (Figure 4A; Supplementary Appendix 5). At the end of the recovery period, the respiration rates of the intertidal fragments of both species in the thermal stress treatments were similar to their conspecifics in the control (Figure 4A; Supplementary Appendix 5). Throughout the study A. irregularis fragments from both habitats and in all treatments appeared to have higher respiration rates than P. verrucosa fragments (Figure 4A). Overall A. irregularis had higher respiration rates than P. verrucosa.

Figure 4

In general, the intertidal fragments of both species had higher gross photosynthetic rates than the subtidal fragments (Figure 4B; Supplementary Appendix 5). Overall, the gross photosynthetic rates of both species of both habitats in the thermal stress treatments were significantly lower than those in the control, with those in the 30 °C treatment being lower than the 28 °C treatment (Figure 4B; Supplementary Appendix 5). During the recovery period, there was a slight increase in the gross photosynthetic rates of the fragments in both thermal stress treatments, more especially in the subtidal fragments although not to rates of the control fragments (Figure 4B; Supplementary Appendix 5). The decrease in gross photosynthetic rates was more pronounced in thermally stressed intertidal A. irregularis fragments as compared to their thermally stressed subtidal conspecifics while the decrease was more pronounced in the thermally stressed subtidal P. verrucosa fragments as compared to their thermally stressed intertidal conspecifics (Figure 4B; Supplementary Appendix 5). Throughout the study, A. irregularis fragments from both habitats and all treatments had lower gross photosynthetic rates than P. verrucosa fragments from both habitats (Figure 4B).

Overall, the fragments of both species from both habitats in the thermal stress treatments had significantly lower P:R ratios than those in the control (Figure 4C; Supplementary Appendix 5). Despite some recovery of the respiration rates, the lower photosynthetic rates resulted in lower P:R ratios for the thermally stressed corals even after the recovery period (Figure 4C; Supplementary Appendix 5). Although the P. verrucosa fragments from both habitats were significantly lower when thermally stressed, the ratios were still above 1, while the ratios of A. irregularis fragments from both habitats were below 1 even in the controls (Figure 4C; Supplementary Appendix 5).

3.3 Growth rates

There was no significant change in the growth rate of the corals in the control throughout the experiment (Figure 5). The growth of both species from both habitats exposed to the two thermal stress treatments did not completely cease during the duration of the study (Figure 5). However, the two thermal stress treatments caused significantly lower growth rates in both species from both habitats than the control fragments, with those in the 30 °C treatment having lower growth rates than those in the 28 °C treatment (Figure 5; Supplementary Appendix 6). Overall, the growth rates of the subtidal fragments of both species were significantly lower than their intertidal conspecifics, especially when exposed to thermal stress (Figure 5; Supplementary Appendix 6). At the start of the heat-stress phase, Pocillopora verrucosa (both habitats) and intertidal Anomastraea irregularis in the 30 °C treatment had already experienced eight days of gradual warming (0.5 °C per day) and showed markedly reduced growth compared to conspecifics in the control and 28 °C treatments (Figure 5; Supplementary Appendix 6). During the recovery period, there were no signs of recovery (i.e., a subsequent increase) in the growth rates of any of the thermally treated fragments (Figure 5; Supplementary Appendix 6).

Figure 5

3.4 Symbiodiniaceae cell density

Symbiodiniaceae density of the control fragments did not significantly differ throughout the study (Figure 6A). The two thermal stress treatments caused significantly lower Symbiodiniaceae density in both species from both habitats than the control fragments throughout the study (Figure 6A; Supplementary Appendix 7). For both species from both habitats, the Symbiodiniaceae density did not significantly differ between the two treatments at the start of the thermal stress, but at the end of the thermal stress and at the end of the recovery period, the Symbiodiniaceae density was significantly lower in the 30 °C than those in the 28 °C treatment (Figure 6A; Supplementary Appendix 7). At the end of the recovery period there was an increase in the Symbiodiniaceae density of both species from both habitats, but still not to the control levels (Figure 6A; Supplementary Appendix 7). The intertidal fragments of both species had higher Symbiodiniaceae densities than their subtidal conspecifics (Figure 6A; Supplementary Appendix 7).

Figure 6

3.5 Chlorophyll-a concentration

Chlorophyll-a concentration of the control fragments did not change throughout the study (Figure 6B). The two thermal stress treatments caused significantly lower chlorophyll-a concentration in both species from both habitats compared to their conspecifics in the control conditions (Figure 6B; Supplementary Appendix 7). For both species from both habitats, the chlorophyll-a concentration did not significantly differ between the two treatments at the start of the thermal stress but at the end of the thermal stress and at the end of the recovery period the chlorophyll-a concentration was significantly lower in the 30 °C than those in the 28 °C treatment (Figure 6B; Supplementary Appendix 7). At the end of the recovery period there was an increase in the chlorophyll-a concentration of both species from both habitats, but still not to the control levels (Figure 6B; Supplementary Appendix 7). The intertidal fragments of both species had higher chlorophyll-a concentration than their subtidal conspecifics (Figure 6B; Supplementary Appendix 7).

3.6 Chlorophyll-a concentration per Symbiodiniaceae cell

Chlorophyll-a concentration per Symbiodiniaceae cell of the control fragments did not significantly change throughout the study (Figure 6C). The average chlorophyll-a concentration per Symbiodiniaceae cell in subtidal A. irregularis initially exposed to thermal stress were significantly lower than their conspecifics in the control, with those in the 30 °C treatments also having significantly lower chlorophyll-a concentration per cell than those in the 28 °C treatment (Figure 6C; Supplementary Appendix 7). However, at the end of the thermal stress and recovery period, the average chlorophyll-a concentration per Symbiodiniaceae cell in subtidal A. irregularis exposed to the two thermal stress treatments were not significantly different to their conspecifics in the control, nor were there significant differences between the two treatments (Figure 6C; Supplementary Appendix 7). The average chlorophyll-a concentration per Symbiodiniaceae cell in intertidal A. irregularis at the start and end of thermal stress did not significantly differ between the two elevated temperature treatments, nor were they significantly different to their conspecifics in the control (Figure 6C; Supplementary Appendix 7). Furthermore, at the end of the recovery period the average chlorophyll-a concentration per Symbiodiniaceae cell in intertidal A. irregularis in the two thermal treatments was significantly higher than their conspecifics in the control conditions (Figure 6C; Supplementary Appendix 7). The average chlorophyll-a concentration per Symbiodiniaceae cell in subtidal and intertidal P. verrucosa at the start and end of thermal stress as well as at the end of recovery were not significantly different to their conspecifics in the control, nor between the two thermal treatments (Figure 6C; Supplementary Appendix 7). Overall, throughout the study, intertidal P. verrucosa fragments had higher chlorophyll-a concentration per Symbiodiniaceae cell than their subtidal conspecifics (Figure 6C; Supplementary Appendix 7). Conversely, throughout the study, the subtidal A. irregularis fragments had higher chlorophyll-a concentration per Symbiodiniaceae cell than their intertidal conspecifics (Figure 6C; Supplementary Appendix 7).

3.7 Lipid concentration

Lipid concentration of the control fragments did not significantly change throughout the study (Figure 6D). At the start of thermal stress, the lipid concentrations of both species from both habitats did not significantly differ between treatments and the control (Figure 6D; Supplementary Appendix 7). At the end of the thermal stress both species from both habitats had significantly lower lipid concentration when compared to their conspecifics in the control conditions (Figure 6D; Supplementary Appendix 7). At the end of the recovery period, the lipid concentration of both species from both habitats in the two thermal stress treatments did not change from their concentrations at the end of thermal stress (Figure 6D; Supplementary Appendix 7). For both species from both habitats, the lipid concentration was significantly lower in the 30 °C than those in the 28 °C treatment at the end of the thermal stress and at the end of the recovery period (Figure 6D; Supplementary Appendix 7). Overall, the intertidal fragments of both species had higher lipid concentrations than their subtidal conspecifics (Figure 6D; Supplementary Appendix 7). However, the lipid concentrations of the intertidal and subtidal P. verrucosa in the 30 °C treatment did not significantly differ at the end of thermal stress and end of recovery (Figure 6D; Supplementary Appendix 7).

4 Discussion

4.1 Overview of thermal stress responses

This study measured the physiological responses and recovery of Anomastraea irregularis and Pocillopora verrucosa from an environmentally variable intertidal habitat and an environmentally stable subtidal habitat in response to long-term experimental thermal stress. The health scores, physiological rates, and tissue content of the control fragments of both species from both habitats remained fairly unchanged throughout the study (Figures 2, 4–6) and there were no recorded deaths (Figure 3) indicating that handling had negligible effect on the corals and that the changes seen in the fragments in the two experimental treatments were in fact due to the thermal stress experienced. This study found that prolonged higher than average temperatures (Figure 1) indeed significantly impacted coral physiology and caused bleaching and mortalities. Overall, the results of this study highlighted inherent physiological differences between the species and habitat that were maintained throughout the experiment. Anomastraea irregularis appeared more tolerant than P. verrucosa in both thermal stress treatments. The respective morphologies may in part have contributed to the differing thermal tolerance, literature has shown that branching species can be more susceptible to thermal stress than massive species (Stimson et al., 2002; Bay et al., 2016; Pisapia et al., 2016). After two months of the recovery period, only respiration rates showed some improvement, but all other studied parameters did not show any signs of improvement. This is an indication that restoration of physiological homeostasis following prolonged thermal stress likely requires substantially longer periods in the studied specimens. Therefore, the patterns observed in this study should be interpreted as evidence of differential thermal tolerance and early recovery responses rather than complete resilience. In both species, the intertidal corals appeared more tolerant than the subtidal corals in both thermal stress treatments. Overall, the results of this study indicate that highly variable habitats and species traits may influence coral resilience to thermal stress.

4.2 Influence of habitat thermal variability on coral resilience

Adaptive differences can exist between coral populations that experience differential thermal regimes causing thermal resilience in populations that experience highly variable thermal histories (Oliver and Palumbi, 2011; Kenkel and Matz, 2016; Tkachenko and Soong, 2017; Safaie et al., 2018; Tisthammer et al., 2021; Jacquemont et al., 2022; McRae et al., 2022; Speelman et al., 2023). High environmental variability may act as a natural selection pressure, favouring corals with greater thermal tolerance (Oliver and Palumbi, 2011; Barshis et al., 2018). Thermally variable habitats can also induce acclimatisation or non-genetic increases in fitness through mechanisms like phenotypic plasticity, symbiosis with stress-tolerant Symbiodiniaceae, maintaining higher levels of heat shock proteins and antioxidants, and epigenetic modifications (Palumbi et al., 2014; Bay and Palumbi, 2017; Howells et al., 2020; Thummasan et al., 2021; Lachs et al., 2023). For example, in the Kimberly region of Australia Acropora aspera corals exposed to daily temperature variability of up to 7 °C developed enhanced bleaching resilience compared to conspecifics from the subtidal habitat where daily temperature variability was moderate (Schoepf et al., 2020; Jung et al., 2021; Schoepf et al., 2021). Although direct in situ thermal comparisons between the intertidal and subtidal habitats were not available during the present study, previous work from this region has demonstrated that intertidal rock pools can experience substantial short-term temperature fluctuations especially during summer low tides (Smit and Glassom, 2017). The comparatively greater thermal tolerance observed in the intertidal corals in the present study may therefore reflect some degree of thermal preconditioning or acclimatisation to naturally variable thermal regimes. However, because concurrent habitat temperature records were unavailable during the experimental period, this interpretation should be considered cautiously. The high level of temperature variability may be a key forcing factor influencing the physiological and molecular differences observed between habitats, ultimately influencing their tolerance to bleaching. However, it is also noteworthy that intertidal corals are also exposed to a suite of cooccurring stressors like greater irradiance, desiccation risk, oxygen supersaturation and depletion cycles, and fluctuating pH and salinity during tidal cycles (Le Tissier and Brown, 1996; Helmuth et al., 2006). These environmental stressors may act synergistically with temperature fluctuations, further shaping the physiological and molecular responses of intertidal corals. Thus, the high degree of environmental variability characteristic of the intertidal zone may collectively drive the development of enhanced stress tolerance and influence the patterns observed between habitats.

4.3 Species and habitat specific physiological strategies

In both thermal stress treatments, intertidal A. irregularis took longer to bleach and experienced less bleaching, and no deaths compared to their subtidal counterparts and subtidal and intertidal P. verrucosa (Figures 2, 3; Supplementary Appendix 4). Intertidal P. verrucosa also experienced less bleaching and less deaths than their subtidal counterparts (Figures 2, 3; Supplementary Appendix 4). This variable thermal tolerance/susceptibility may have resulted from the different physiological strategies employed by the two species from the two different habitats. Environmental conditions have important influences on the respiration and photosynthetic performance of scleractinian corals (Ulstrup et al., 2011). Coral respiration rates generally increase or decrease in response to environmental perturbations while no change is indicative of acclimatisation or no stress response (Guppy and Withers, 1999; Sawall et al., 2011; Osinga et al., 2012; Al-Sofyani and Floos, 2013). Higher respiration rates in response to elevated seawater temperature has been reported for some coral species and is believed to reflect an increase in the metabolic activity that is associated with the production of heat-shock proteins, cellular repair, maintenance of cellular homeostasis, antioxidant production, and other stress-response mechanisms (Wooldridge, 2014; Sawall et al., 2015; Anderson et al., 2019). The subtidal corals of both species seemed more sensitive to the thermal stress since they maintained higher respiration rates throughout the thermal stress and recovery period when compared to their conspecifics in the control (Figure 4A; Supplementary Appendix 5). Conversely, the intertidal fragments of both species only had higher respiration rates at the start and a month into thermal stress, but by the third month of thermal stress and recovery period their respiration rates were not different to their counterparts in the control (Figure 4A; Supplementary Appendix 5) indicating that they may have acclimatised to the increased temperatures. For both species, there also seemed to be an inherent difference in the respiration rates between habitats. Throughout the study the subtidal corals of both species in both the control and thermal stress treatments had higher respiration rates compared to the intertidal conspecifics (Figure 4A; Supplementary Appendix 5). It is possible that the subtidal corals are not physiologically plastic enough to regulate their respiration rates when faced with above-average temperatures as compared to the intertidal corals that were able to acclimatise to the increased temperatures. This lower physiological plasticity in subtidal corals may be because of the absence of a selective pressure since their more stable habitats do not require large variations in their physiology to survive. Conversely, corals that experience large environmental variability would experience stronger selective pressures that favour corals with greater physiological plasticity to survive the variable conditions (Ziegler et al., 2014; Schoepf et al., 2015; Huang et al., 2024). Maintaining high respiration rates is energy-consuming and since bleaching deprives corals of symbiont-derived photosynthates, maintaining the higher respiration rates may have led to more bleaching and higher mortalities of the subtidal corals in the thermal stress treatments (Wooldridge, 2014; Anderson et al., 2019; Jacquemont et al., 2022).

Overall, the fragments of both species from both habitats in the thermal stress treatments had significantly lower photosynthetic rates and resultant P:R ratios than those in the control (Figures 4B, C; Supplementary Appendix 5). Despite the recovery of respiration rates of the intertidal corals and some recovery of the respiration rates of the subtidal corals, the lower photosynthetic rates resulted in significantly lower P:R ratios for the thermally stressed corals even after the recovery period (Figures 4B, C; Supplementary Appendix 5). Lower P:R ratios can be due to either increased respiration or lower photosynthesis or both (Coles and Jokiel, 1977). Reduced P:R ratios are typical in thermally stressed corals due to the significant loss of Symbiodiniaceae cells that follows thermal stress (Coles and Jokiel, 1977; Lesser, 2013; Muller-Parker et al., 2015). The proportion of energy the coral host receives from its Symbiodiniaceae can be assessed from the P:R ratio, with a ratio greater than one indicating sufficient energy from the Symbiodiniaceae while a ratio less than one indicates insufficient energy from their Symbiodiniaceae (Muscatine et al., 1981; Baker et al., 2015). Although the thermally stressed P. verrucosa fragments from both habitats had significantly lower photosynthetic rates, Symbiodiniaceae density, and chlorophyll-a concentration, the P:R ratios were still above one (Figures 4B, C). This would imply that despite the thermal stress the Symbiodiniaceae in these fragments were still producing enough energy for the coral hosts. The chlorophyll-a concentration per Symbiodiniaceae cell of these fragments was not significantly different to the controls at the start and end of the thermal stress (Figure 6C), which could explain why the P:R ratios remained above one despite the thermal stress. The maintenance or increase in chlorophyll-a per Symbiodiniaceae cell usually occurs with thermally induced bleaching to maintain light-harvesting rates, since there are lower Symbiodiniaceae densities (Jones, 1997). It may also be more energetically favourable for the coral host and/or the Symbiodiniaceae to increase the chlorophyll-a content per Symbiodiniaceae cell than to recruit Symbiodiniaceae cells (Rodrigues and Grottoli, 2007).

Throughout the study A. irregularis fragments from both habitats in the control and thermal stress treatments had higher respiration rates and lower photosynthetic rates compared to P. verrucosa (Figures 4A, B), and the resulting P:R ratios of A. irregularis fragments from both habitats were below one even in the controls (Figure 4C). The more porous skeleton and comparatively thinner tissue of P. verrucosa fragments may allow greater light penetration through the coral tissue and skeleton thereby permitting higher photosynthetic rates in these endosymbionts than in those housed in the thicker tissue A. irregularis fragments (Edmunds and Gates, 2002; Osinga et al., 2012; Conley and Hollander, 2021). The heterotrophic activity and energy acquisition pathways were not directly measured in the present study. However, through differences in the δ¹³C and δ¹⁵N isotopes between coral host tissue and Symbiodiniaceae cells Smit (2014) indicated that heterotrophy contributes more to the metabolism of A. irregularis than P. verrucosa. Therefore, the difference in P:R ratios between the species may be explained by their heterotrophic/autotrophic dependence to meet their metabolic requirements.

Pocillopora verrucosa from both habitats, and intertidal Anomastraea irregularis in the 30 °C treatment at the start of heat stress already had markedly lower growth (Figure 5; Supplementary Appendix 6). The gradual ramping up of temperatures by 0.5°C per day can elicit early differential responses in some physiological parameters (McLachlan et al., 2020). The early drop in growth likely reflects the energetic costs associated with the increased metabolic activity observed in these fragments. The elevated respiration rates at the start of heat stress may have represented attempts to maintain cellular homeostasis and repair heat-induced damage (e.g., through enhanced enzymatic or antioxidant processes), thereby deviating energy away from calcification and tissue growth (Rodrigues and Grottoli, 2006; Wooldridge, 2014). Interestingly, the subtidal Anomastraea irregularis fragments did not exhibit a significant reduction in growth at the start of heat stress, despite experiencing increased respiration rates during this time. This may indicate a delayed physiological response to thermal stress, whereby growth was temporarily maintained despite increasing metabolic demands. However, growth rates declined during prolonged heat exposure, suggesting that this response was not sustainable over time. Although the precise mechanism underlying this transient pattern remains unclear, it may reflect short-term physiological buffering or stress-response dynamics during the early stages of thermal exposure. The reduced growth rates of both species from both habitats during long-term thermal stress and recovery from the stress (Figure 5; Supplementary Appendix 6) is common since growth is an energy consuming process therefore the increase in energy demands following thermal stress prevents the coral hosts from investing energy in growth (Suzuki et al., 2003; Carilli et al., 2009; Colombo-Palotta et al., 2010; Levas et al., 2013; Foster et al., 2014; Razak et al., 2020; Kramer et al., 2022). Although the P:R ratios of P. verrucosa indicated enough energy from the Symbiodiniaceae, the quality of the photosynthates may have not been good enough to allow recovery of growth rates (Tremblay et al., 2016). The lower P:R ratios of the subtidal corals of both species may have caused their lower growth rates as compared to the growth rates of the intertidal corals of both species (Figures 4C, 5). The reduced growth rates of both species from both habitats in response to both thermal stress treatments could be a trade-off for surviving prolonged above-average temperature stress. However, this may not be a universal consequence as there have been other studies where corals survived thermal stress without detrimentally impacting their growth rates (Dandan et al., 2015; Wright et al., 2019; Kavousi et al., 2020; Brown et al., 2023).

4.4 Symbiodiniaceae dynamics and lipid reserves

In general, both species from both habitats had significantly lower Symbiodiniaceae density, chlorophyll-a concentrations, and lipid concentrations at the end of both thermal stress treatments compared to conspecifics in the control (Figures 6A, B, D). Thermal stress usually leads to the coral hosts losing Symbiodiniaceae cells via different pathways (Helgoe et al., 2024). One theory suggests that corals reduce their symbiont densities as a strategy to mitigate oxidative stress leaking from algal cells into host tissues during stress conditions (Weis, 2008; Fujise et al., 2014). The reduction in lipid concentrations could be because the corals were using the lipids as a source of energy (Rodrigues and Grottoli, 2007), or there was a decrease because of damage through lipid peroxidation from the production of reactive oxygen species due to the thermal stress (Lesser, 1997; Downs et al., 2002; Onyango, 2020). In all thermally stressed fragments, two months were not enough to recover initial levels of symbiont density, chlorophyll-a, and lipid concentrations. The time it takes for these properties to completely recover to pre-bleaching values is variable and can take more than eight months in some corals (Rodrigues and Grottoli, 2007). This can have implications for coral reefs in the near future because more frequent thermal anomalies may prevent bleached corals in situ from recovering from thermal stress events before another event occurs (Hoegh-Guldberg et al., 2023). However, recent studies show that some corals can improve their energetic balance after several years of thermal stress, providing some hope for the recovery of bleached corals (Brown et al., 2023; Roik et al., 2023). Overall, the intertidal fragments of both species in the control and thermal stress treatments had higher Symbiodiniaceae densities, chlorophyll-a, and lipid concentrations than their subtidal conspecifics (Figures 6A, B, D). Usually, corals that have higher Symbiodiniaceae density, chlorophyll-a concentrations, and lipid concentrations are considered to be more resilient to thermal stress (Gates and Edmunds, 1999; Stimson et al., 2002; Grottoli et al., 2004; Levas et al., 2013; Grottoli et al., 2017). The intertidal corals may, therefore, be more resilient to thermal stress than their subtidal conspecifics, they showed higher Symbiodiniaceae densities, chlorophyll-a, and lipid concentrations than their subtidal conspecifics even when thermally stressed. The higher chlorophyll-a per Symbiodiniaceae cell observed in the subtidal A. irregularis may reflect photoacclimation to lower light conditions in the subtidal habitat. Increased pigment concentrations per cell are often associated with Symbiodiniaceae adapted to lower-light environments as a way to enhance light-harvesting efficiency under low irradiance conditions (Titlyanov and Titlyanova, 2002). However, such photoacclimatory strategies may also increase susceptibility to photoinhibition and oxidative stress during elevated temperature exposure, potentially contributing to the comparatively lower thermal tolerance observed in the subtidal corals (Scheufen et al., 2017).

However, there is also evidence from Palau that heat-tolerant corals from warmer patch reefs tended to have lower symbiont densities (Cornwell et al., 2021), and based on the oxidative stress theory of bleaching having higher concentrations of Symbiodiniaceae would put corals at a greater risk of bleaching due to the potentially increased positive feedback loop of reactive oxygen species from the Symbiodiniaceae during thermal stress (Cunning and Baker, 2012). Furthermore, there are alternative hypotheses of bleaching indicating that the coral-symbiont relationship may not be mutualistic but in fact a type of farming by the coral that can turn parasitic at times, and that altered carbon and nutrient cycling within the symbiosis during thermal stress leads to bleaching (Wooldridge, 2009; Ferrier-Pagès et al., 2018; Morris et al., 2019; Matz, 2024). A recent study also found no direct connection between Symbiodiniaceae photodamage and an increase in reaction oxygen species H₂O₂ concentration during thermally induced bleaching (Schlotheuber et al., 2024). Therefore, just having higher or lower concentrations of Symbiodiniaceae is not enough to induce thermal resilience based on the traditional reactive oxygen bleaching theory and there are definitely more intricate factors at play in the coral-symbiont interaction that conveys thermal tolerance. Further energetic and molecular analyses will be required to decipher the exact role the intertidal coral hosts play in the thermal tolerance seen in this study.

A significant limitation of the present study is that the Symbiodiniaceae communities hosted by the corals were not identified. Consequently, the physiological differences observed between habitats and species cannot be attributed solely to host-derived mechanisms. Thermal tolerance in corals is strongly influenced by the identity, composition, and functional traits of their associated Symbiodiniaceae communities. For example, some coral species were able to acquire increased thermal tolerance by hosting stress resistant Symbiodiniaceae species such as Durusdinium spp. and Cladocopium spp (Berkelmans and van Oppen, 2006; Stat and Gates, 2011; Levas et al., 2013; Hume et al., 2020). The shifts in the relative abundance of dominant symbionts in response to thermal stress or following thermal stress can affect the coral host thermal resilience (Jones et al., 2008; Silverstein et al., 2015; Cunning et al., 2017). Therefore, identifying the Symbiodiniaceae species hosted before, during, and after thermal stress would be essential to disentangle the relative contributions of the host physiology and the Symbiodiniaceae’s role in these coral’s thermal tolerance observed in this study.

4.5 Experimental considerations and future directions

Importantly, a fundamental limitation of this study is that temperatures after ramping remained constant, which does not mirror the natural ecological variability in daily thermal cycles, particularly in habitats such as intertidal rock pools. The use of uniform thermal stress regimes was intentional to enable clearer attribution of observed physiological changes directly to heat stress intensity, thereby improving experimental reproducibility and interpretability. Nonetheless, this represents a methodological caveat, as constant temperatures do not fully capture the dynamic thermal conditions corals experience in situ. Future studies should incorporate thermal profiles that mimic natural diurnal cycles and ecologically relevant daylight heating with nocturnal reprieves, as these designs offer more realistic assessments of coral thermal resilience (McLachlan et al., 2020; Voolstra et al., 2025).

Another key limitation of this study is that in situ temperature measurements nor turbidity, light, pH, wave action, dissolved oxygen, or nutrients were not collected concurrently from the intertidal and subtidal source habitats during the experimental period. Therefore, this study cannot isolate thermal pre-conditioning from multi-stressor pre-conditioning. Therefore, the observed physiological differences between habitats should be interpreted cautiously, as habitat-related variation may reflect the combined influence of multiple environmental factors rather than temperature variability alone. Furthermore, no genetic analyses were conducted to determine the extent of population connectivity or genetic differentiation between habitats. Consequently, it is not possible to distinguish whether the observed results reflect local adaptation, acclimatisation, or other forms of phenotypic plasticity associated with contrasting environmental conditions. Given the close spatial proximity of the habitats, larval exchange between populations is plausible. Future studies incorporating population genetic or genomic approaches would help clarify the relative contributions of genetic differentiation and environmental acclimatisation to thermal resilience in these corals.

The relatively low variability observed among replicate fragments may reflect aspects of the experimental design. Each experimental unit consisted of a small coral fragment containing multiple polyps, which likely averaged physiological responses within fragments and reduced polyp-level variability. In addition, colonies were collected from a relatively restricted geographic area, which may have limited genotypic diversity among sampled individuals. These factors may have contributed to the relatively consistent physiological responses observed across replicates. Despite incorporating tank replicate into the statistical models as covariates to account for potential tank-associated variation, the relatively small number of replicate tanks per treatment (n=3) inherently limited the precision with which tank-level variance could be estimated. Consequently, significant treatment effects should be interpreted with appropriate caution in the context of this limited tank replication.

Although cumulative mortality in intertidal P. verrucosa was marginally higher in the 28 °C treatment than in the 30 °C treatment after three months of heat stress, this pattern reflected the loss of only one additional fragment. As cumulative mortality values can accentuate relatively small numerical differences over time, the apparent deviation from a strictly dose-dependent mortality response should be interpreted cautiously. Furthermore, thermal exposure among replicate tanks within treatments was comparatively consistent, suggesting that the pattern was unlikely to result from major tank-level thermal inconsistencies. Instead, the observation most likely reflects normal biological variability associated with long-term coral thermal stress experiments. Further investigation into the biochemical and molecular mechanisms underpinning thermal stress responses in intertidal P. verrucosa may provide better insight into whether mortality responses differ across varying levels of chronic heat exposure.

Grottoli et al. (2021) recommends feeding corals during long-term bleaching experiments to mimic in situ conditions. Therefore, feeding the corals weekly made the study more realistic. However, the seawater used during this study was not filtered enough to remove microscopic organisms, which may have provided additional nutrition, especially to the thermally stressed fragments. Furthermore, the same quantity of coral nutrition was added to each tank throughout the experiment irrespective of fragment survival. Consequently, surviving fragments in treatments with higher mortality may have experienced relatively greater nutritional availability per fragment. The nutritional input from heterotrophy is believed to increase resilience to thermal stress by enabling the coral host to save photosynthates and essential nutrients (nitrogen and phosphorous) for the synthesis of antioxidants and heat-stress proteins to counteract cellular damage derived from oxidative and thermal stress (Houlbrèque et al., 2004; Lyndby et al., 2018; Brown et al., 2023). Heterotrophy was not accounted for in this study, and the results could have, therefore, been unintentionally affected by the additional nutrition, especially in A. irregularis since they rely more on heterotrophy than P. verrucosa (Smit, 2014; Boodraj and Glassom, 2022).

It is also noteworthy that shallow-water corals in situ can experience PAR levels which can exceed 500-1000 µmol m^-2 s^-1 (Dubinsky et al., 1990; Lehmann, 2022). In this study the peak midday PAR was only ~245 µmol m^-2 s^-1, which could have mitigated some of the thermal stress experienced by the corals since reduced light intensity has been found to ameliorate thermal stress effects in some corals (Rosic et al., 2020). Therefore, the bleaching responses and thermal thresholds observed under the present laboratory conditions must be interpreted with caution as they may underestimate the severity of responses that could occur under natural field conditions where elevated temperatures are typically coupled with substantially higher and more variable irradiance levels. Inorganic nutrients and oxygen concentrations in the tanks were also not measured during this study. Although all tanks were subjected to identical water circulation and water-exchange protocols, we cannot fully exclude the possibility that differences in dissolved oxygen or inorganic nutrient concentrations (especially nitrogen and phosphorus) may have influenced physiological outcomes. The use of closed recirculating aquaria may have influenced water chemistry over time through the accumulation of metabolic by-products such as dissolved organic matter and inorganic waste. Dissolved oxygen concentrations within the experimental holding tanks were also not monitored throughout the study and therefore potential interactions between thermal stress and background oxygen dynamics with the accumulation of metabolic by-products could not be directly assessed. Although regular water changes and continuous circulation were implemented to maintain water quality, such systems cannot fully replicate the dynamic flushing and dilution processes characteristic of in situ conditions. Especially in the elevated temperature tanks the dissolved oxygen concentrations may have been much lower due to increased respiration rates of the corals and possible increase accumulation of metabolic wastes and no additional active aeration was supplied to the tanks. Thus, some physiological responses observed may reflect the combined effects of thermal stress and shifts in organic content and dissolved oxygen in the water. This is an important caveat that should be considered when interpreting the physiological responses. Future experiments would benefit from routine monitoring of these parameters to improve mechanistic interpretation of coral thermal resilience since these parameters are known to influence coral-symbiont responses to thermal stress (Ezzat et al., 2016; Nelson and Altieri, 2019; Weis, 2019).

Similarly, the dissolved inorganic carbon and aragonite saturation state (Ωarag) were not monitored throughout the study which contribute to the broader carbonate chemistry system. Typically, natural seawater total alkalinity is around 2200 to 2400 µmol kg^-1, whereas the average seawater total alkalinity in this study was higher (~2870 µmol kg^-1). Elevated alkalinity can increase carbonate ion availability and potentially support coral calcification; however, the influence of alkalinity on calcification depends on the broader carbonate chemistry system, including the factor mentioned which were not comprehensively quantified in this study. Consequently, the potential contribution of carbonate chemistry to the observed skeletal growth responses cannot be fully excluded. The buoyant weight calculations assumed a constant aragonite density (2.94 g cm^-³) following standard methodology (Davies, 1989). However, skeletal architecture and porosity can vary among coral species and may change under thermal stress. Therefore, some uncertainty may exist in the absolute skeletal growth estimates, although the same calculation approach was applied consistently across all treatments and species.

Surface area measurements used to normalise physiological rates were determined at the conclusion of the experiment rather than at each sampling interval. This approach was used to minimise repeated handling and manipulation stress to the coral fragments during the prolonged experimental period. However, potential temporal changes in tissue expansion, contraction, partial mortality, or skeletal exposure during bleaching and recovery were therefore not incorporated into the surface area normalisation. Consequently, some uncertainty exists in the calculated area-normalised physiological rates across time, particularly in severely stressed fragments. Future studies would benefit from repeated non-destructive surface area measurements throughout long-term experiments.

4.6 Ecological implications and conservation relevance

Ultimately this study found that both temperature treatments caused bleaching in both species from both habitats, although the 30 °C treatment was more detrimental to the corals than the 28 °C treatment. This highlights that even the conservatively predicted increase in temperature along the South African east coast can detrimentally affect these corals. In terms of DHW, the corals in this study faced values far exceeding the thresholds of 4 and 8°C-weeks which are believed to cause low-level to severe bleaching (NOAA Coral Reef Watch; Leggat et al., 2022). Carilli et al. (2012) reported that some coral sites in the Gilbert Islands, Republic of Kiribati experienced DHW values as high as 24 °C-weeks and that corals regularly exposed to high and fluctuating temperatures can develop higher thermal tolerances. The degree to which the corals were physiologically affected by the temperature stress varied between species and habitats. Although subtidal corals and P. verrucosa in this study exhibited high susceptibility to thermal stress, with more mortalities, those that survived endured up to ~8 and ~21 °C-weeks of heat stress by the end of the study. This suggests that while high-latitude corals collectively exhibit notable thermal tolerance, there is considerable variation in tolerance across species and habitat, with some individuals demonstrating greater capacity to withstand prolonged thermal stress than others. The results of this study corresponded with McLachlan et al. (2021) proposal that there will be higher survival of corals that can modify their physiology when faced with climate change and local stressors. The intertidal corals of both species and A. irregularis appear to have increased tolerance to thermal stress over subtidal conspecifics and P. verrucosa. The results of this study partially support our hypotheses because recovery of photosynthesis, growth and tissue composition remained incomplete after two months and therefore thermal tolerance and only early recovery responses rather than complete resilience could be interpreted. Species-specific traits and habitat-driven thermal preconditioning were found to play critical roles in the coral’s tolerance to thermal stress. The ability to adjust their respiration rates and maintain higher symbiont cell proliferation, chlorophyll-a, and lipid concentrations may aid the intertidal corals to survive in their extreme habitats. These characteristics were able to help them persist with the long-term experimental thermal stress in this study. Interpretation of species-level differences should be made cautiously, as the comparison between the massive A. irregularis and branching P. verrucosa cannot isolate morphology from other interspecific traits, including host physiology, tissue structure, symbiont associations, and genetic differences. Consequently, morphology may contribute to the observed differences in thermal responses, but it is unlikely to represent the sole explanatory factor. Anomastraea irregularis appeared to be more resilient than the P. verrucosa possibly due to its thicker tissue which allowed for higher symbiont proliferation and lipid concentrations. The lower P:R ratios of A. irregularis, consistent with a more heterotrophic dependence, may have also increased their thermal tolerance. Marginal and extreme coral communities have important implications for the conservation and management of coral reefs and therefore, the results of this study are important. Identifying and conserving coral populations that naturally exhibit thermally tolerant characteristics, such as marginal and extreme communities, is essential for resilience-based reef management and restoration initiatives (Camp et al., 2018; Schoepf et al., 2023). These communities may serve as genetic and physiological refugia for coral adaptation, offering valuable material for restoration, assisted evolution and selective propagation initiatives aimed at enhancing reef recovery potential (van Oppen et al., 2015; Quigley, 2024). Furthermore, incorporating habitat-specific resilience data into predictive ecosystem models could improve the accuracy of climate impact forecasts for coral communities. Collectively, this study emphasises that conserving and investigating these understudied stress-tolerant coral communities is not only critical for their own persistence, but also for safeguarding the future adaptability and functionality of coral reef ecosystems under ongoing ocean warming.

It is also noteworthy that the lack of physiological and tissue content recovery after two months indicates that long recovery times may be required for these corals to return to healthy states. Rodrigues and Grottoli (2007) found that more than eight months may be required for full recovery of energy reserves in some corals. This is of concern since less time between bleaching events is predicted in the near future (Hoegh-Guldberg et al., 2023). The long-term effects of the tolerance on the fitness of these corals also need to be considered (Bove et al., 2022). For example, a year after recovering from the 2020 mass-bleaching event, Acropora millepora in the Keppel Islands had a 21% decrease in population-level reproductive output (Briggs et al., 2024). The decrease in reproductive output is concerning because it reduces the resilience of coral populations to withstand and recover from future bleaching events (Briggs et al., 2024).

5 Conclusion

This study offers insight into the physiological responses of two high-latitude coral species of different morphologies from two habitats of differing thermal regimes when exposed to prolonged experimental thermal stress. The impact of thermal stress varied between species and habitat. This study highlighted that coral resilience to thermal stress can be influenced by habitat of origin and possibly morphology. Corals from the intertidal habitat, with strong thermal fluctuations were more tolerant of thermal stress than conspecifics from the subtidal habitat and the massive corals were more resilient than branching corals. The greater physiological plasticity of intertidal corals (important to persist in their extreme environment) helped them to maintain of higher symbiont density, chlorophyll-a, and lipid concentrations, parameters associated with long-term tolerance to thermal stress in the present study. The massive species’ tolerance to long-term thermal stress may have resulted from also having tissue traits favouring the accumulation of symbiont cells and lipid reserves; and lower P:R ratios. Although respiration rates showed some improvement during the recovery period, other parameters did not recover after two months, indicating that restoration of physiological homeostasis following prolonged thermal stress likely requires substantially longer periods. Therefore, the patterns observed in this study should be interpreted as evidence of differential tolerance and early recovery responses rather than complete resilience. This study emphasises the need to further investigate and conserve coral communities from marginal latitudes and extreme environments, as they can possess stress-resilient characteristics that are crucial for the conservation of coral reefs in the face of global climate change.

References

• 1

  AinsworthT. D.HeronS. F.OritzJ. C.MumbyP. J.GrechA.OgawaD.et al. (2016). Climate change disables coral bleaching protection on the Great Barrier Reef. Science352, 338–342. doi: 10.1126/science.aac7125

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 2

  Al-SofyaniA. A.FloosY. A. M. (2013). Effect of temperature on two reef-building corals Pocillopora damicornis and P verrucosa in the Red Sea. Oceanologia55, 917–935. doi: 10.5697/oc.55-4.917

  • CrossRef
  • Google Scholar
  • View reference in article

• 3

  Alvarez-FilipL.Carricart-GanivetJ. P.Horta-PugaG.Iglesias-PrietoR. (2013). Shifts in coral-assemblage composition do not ensure persistence of reef functionality. Sci. Rep.3, 3486. doi: 10.1038/srep03486

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 4

  Alvarez-FilipL.GillJ.DulvyN. K.PerryA. L.WatkinsonA. R.CôtéI. M. (2011). Drivers of region-wide declines in architectural complexity on Caribbean reefs. Coral. Reefs.30, 1051–1060. doi: 10.1007/s00338-011-0795-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 5

  AndersonK. D.CantinN. E.CaseyJ. M.PratchettM. S. (2019). Independent effects of ocean warming versus acidification on the growth, survivorship and physiology of two Acropora corals. Coral. Reefs.38, 1225–1240. doi: 10.1007/s00338-019-01864-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 6

  AnthonyK. R. N.HoogenboomM. O.MaynardJ. A.GrottoliA. G.MiddlebrookR. (2009). Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct. Ecol.23, 539–550. doi: 10.1111/j.1365-2435.2008.01531.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 7

  BairdA. H.BhagooliR.RalphP. J.TakahashiS. (2009). Coral bleaching: the role of the host. Trends Ecol. Evol.24, 16–20. doi: 10.1016/j.tree.2008.09.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 8

  BakerD. M.FreemanC. J.KnowltonN.ThackerR. W.KimK.FogelM. L. (2015). Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses. ISME. J.9, 2620–2629. doi: 10.1038/ismej.2015.71

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 9

  BakerA. C. P.GlynnP. W.RieglB. (2008). Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf. Sci.80, 435–471. doi: 10.1016/j.ecss.2008.09.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 10

  BarshisD. J.BirkelandC.ToonenR. J.GatesR. D.StillmanJ. H. (2018). High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata. J. Exp. Biol.221, jeb188581. doi: 10.1242/jeb.188581

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 11

  BaumsI. B.BakerA. C.DaviesS. W.GrottoliA. G.KenkelC. D.KitchenS. A.et al. (2019). Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl.29, e01978. doi: 10.1002/eap.1978

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 12

  BayL. K.DoyleJ.LoganM.BerkelmansR. (2016). Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. R. Soc Open Sci.3, 160322. doi: 10.1098/rsos.160322

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 13

  BayR. A.PalumbiS. R. (2017). Transcriptome predictors of coral survival and growth in a highly variable environment. Ecol. Evol.7, 4794–4803. doi: 10.1002/ece3.2685

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 14

  BerkelmansR.van OppenM. J. H. (2006). The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc B.273, 2305–2312. doi: 10.1098/rspb.2006.3567

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 15

  BoodrajP.GlassomD. (2022). Microplastic ingestion in healthy and bleached Anomastraea irregularis and Pocillopora verrucosa corals. Mar. Biol.169, 1–14. doi: 10.1007/s00227-022-04038-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 16

  BoodrajP.GlassomD.VoslooD. (2024). Flexi-chambers and 3D photogrammetry effectively measure coral fragment physiology in situ. J. Exp. Mar. Biol. Ecol.572, 3–4. doi: 10.1016/j.jembe.2024.151986

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 17

  BoveC.-O.DaviesS. W.RiesJ. B.UmbanhowarJ.ThomassonB. C.FarquharE. B.et al. (2022). Global change differentially modulates Caribbean coral physiology. PloS One17, e0273897. doi: 10.1371/journal.pone.0273897

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 18

  BriggsN. D.PageC. A.GiulianoC.AlessiC.HoogenboomM.BayL. K.et al. (2024). Dissecting coral recovery: bleaching reduces reproductive output in Acropora millepora. Coral. Reefs.43, 557–569. doi: 10.1007/s00338-024-02483-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 19

  BrownB. (1997). Coral bleaching: causes and consequences. Coral. Reefs.16, 129–138. doi: 10.1007/s003380050249

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 20

  BrownK. T.GeninA.Mello-AthaydeM. A.BergstromE.CampiliA.ChaiA.et al. (2023). Marine heatwaves modulate the genotypic and physiological responses of reef-building corals to subsequent heat stress. Ecol. Evol.13, e10798. doi: 10.1002/ece3.10798

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 21

  CampE. F.SchoepfV.MumbyP. J.HardtkeL. A.Rodolfo-MetalpaR.SmithD. J.et al. (2018). The future of coral reefs subject to rapid climate change: Lessons from natural extreme environments. Front. Mar. Sci.5, 4. doi: 10.3389/fmars.2018.00004

  • CrossRef
  • Google Scholar
  • View reference in article

• 22

  CarilliJ.DonnerS. D.HartmannA. C. (2012). Historical temperature variability affects coral response to heat stress. PloS One7, e34418. doi: 10.1371/journal.pone.0034418

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 23

  CarilliJ. E.NorrisR. D.BlackB. A.WalshS. M.McFieldM.BogradS. J. (2009). Local Stressors reduce coral resilience to bleaching. PloS One4, e6324. doi: 10.1371/journal.pone.0006324

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 24

  ColesS. L.JokielP. L. (1977). Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar. Biol.43, 209–216. doi: 10.1007/bf00402313

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 25

  Colombo-PalottaM. F.Rodriguez-RomanA.Iglesias-PrietoR. (2010). Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral. Reefs.29, 899–907. doi: 10.1007/s00338-010-0638-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 26

  ConleyD. D.HollanderE. N. R. (2021). A non-destructive method to create a time series of surface area for coral using 3D photogrammetry. Front. Mar. Sci.8, 660846. doi: 10.3389/fmars.2021.660846

  • CrossRef
  • Google Scholar
  • View reference in article

• 27

  CornwellB.ArmstrongK.WalkerN. S.LippertM.NestorV.GolbuuY.et al. (2021). Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral Acropora hyacinthus in Palau. eLife10, e64790. doi: 10.7554/eLife.64790

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 28

  CunningR.BakerA. C. (2012). Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat. Clim. Change3, 259–262. doi: 10.1038/nclimate1711

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 29

  CunningR.SilversteinR. N.BakerA. C. (2017). Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral. Reefs.37, 145–152. doi: 10.1007/s00338-017-1640-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 30

  DandanS. S.FalterJ. L.LoweR. J.McCullochM. T. (2015). Resilience of coral calcification to extreme temperature variations in the Kimberley region, northwest Australia. Coral. Reefs.34, 1151–1163. doi: 10.1007/s00338-015-1335-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 31

  DaviesS. P. (1989). Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar. Biol.101, 389–395. doi: 10.1007/BF00428135

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 32

  DietzelA.BodeM.ConnollyS. R.HughesT. P. (2021). The population sizes and global extinction risk of reef-building coral species at biogeographic scales. Nat. Ecol. Evol.5, 663–669. doi: 10.1038/s41559-021-01393-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 33

  DownsC. A.FauthJ. E.HalasJ. C.DustanP.BemissJ.WoodleyC. M. (2002). Oxidative stress and seasonal coral bleaching. Free Radical Biol. Med.33, 533–543. doi: 10.1016/S0891-5849(02)00907-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 34

  DubinskyZ.StamblerN.Ben-ZionM.McCloskeyL.MuscatineL.FalkowskiP. (1990). The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc. R. Soc. Lond. B. Biol. Sci.239, 231–246. doi: 10.1098/rspb.1990.0015

  • CrossRef
  • Google Scholar
  • View reference in article

• 35

  EdmundsP.GatesR. (2002). Normalizing physiological data for scleractinian corals. Coral. Reefs.21, 193–197. doi: 10.1007/s00338-002-0214-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 36

  EzzatL.MaguerJ.-F.GroverR.Ferrier-PagèsC. (2016). Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean. Sci. Rep.6, 31768. doi: 10.1038/srep31768

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 37

  Ferrier-PagèsC.SauzéatL.BalterV. (2018). Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts. Global Change Biol.24, 3145–3157. doi: 10.1111/gcb.14141

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 38

  FosterT.ShortJ. A.FalterJ. L.RossC.McCullochM. T. (2014). Reduced calcification in Western Australian corals during anomalously high summer water temperatures. J. Exp. Mar. Biol. Ecol.461, 133–143. doi: 10.1016/j.jembe.2014.07.014

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 39

  FujiseL.YamashitaH.SuzukiG.SasakiK.LiaoL. M.KoikeK. (2014). Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from corals. PloS One9, 1–18. doi: 10.1371/journal.pone.0114321

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 40

  GambaA.PetrasD.LittleM.WhiteB.DorresteinP. C.RohwerF.et al. (2022). Applying tissue separation and untargeted metabolomics to understanding lipid saturation kinetics of host mitochondria and symbiotic algae in corals under high temperature stress. Front. Mar. Sci.9, 853554. doi: 10.3389/fmars.2022.853554

  • CrossRef
  • Google Scholar
  • View reference in article

• 41

  GatesR. D.EdmundsP. J. (1999). The physiological mechanisms of acclimatization in tropical reef corals. Am. Zool.39, 30–43. doi: 10.1093/icb/39.1.30

  • CrossRef
  • Google Scholar
  • View reference in article

• 42

  GrottoliA. G.RodriguesL. J.JuarezC. (2004). Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar. Biol.145, 621–631. doi: 10.1007/s00227-004-1337-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 43

  GrottoliA. G.RodriguesL. J.PalardyJ. E. (2006). Heterotrophic plasticity and resilience in bleached corals. Nature440, 1186–1189. doi: 10.1038/nature04565

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 44

  GrottoliA. G.TchernovD.WintersG. (2017). Physiological and biogeochemical responses of super-corals to thermal stress from the northern gulf of aqaba, red sea. Front. Mar. Sci.4, 215. doi: 10.3389/fmars.2017.00215

  • CrossRef
  • Google Scholar
  • View reference in article

• 45

  GrottoliA. G.ToonenR. J.van WoesikR.Vega ThurberR.WarnerM. E.McLachlanR. H.et al. (2021). Increasing comparability among coral bleaching experiments. Ecol. Appl.31, e02262. doi: 10.1002/eap.2262

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 46

  GuestJ. R.BairdA. H.MaynardJ. A.MuttaqinE.EdwardsA. J.CampbellS. J.et al. (2012). Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PloS One7, e33353. doi: 10.1371/journal.pone.0033353

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 47

  GuppyM.WithersP. (1999). Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev.74, 1–40. doi: 10.1017/s0006323198005258

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 48

  HelgoeJ.DavyS. K.WeisV. M.Rodriguez-LanettyM. (2024). Triggers, cascades, and endpoints: connecting the dots of coral bleaching mechanisms. Biol.99, 715–752. doi: 10.1111/brv.13042

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 49

  HelmuthB.MieszkowskaN.MooreP.HawkinsS. J. (2006). Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu. Rev. Ecol. Evol. Syst.37, 373–404. doi: 10.1146/annurev.ecolsys.37.091305.110149

  • CrossRef
  • Google Scholar
  • View reference in article

• 50

  Hoegh-GuldbergO.SkirvingW.DoveS. G.SpadyB. L.NorrieA.GeigerE. F.et al. (2023). Coral reefs in peril in a record-breaking year. Science382, 1238–1240. doi: 10.1126/science.adk4532

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 51

  HoulbrèqueF.Ferrier-PagèsC. (2009). Heterotrophy in tropical scleractinian corals. Biol.84, 1–17. doi: 10.1111/j.1469-185X.2008.00058.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 52

  HoulbrèqueF.TambuttéÉ.Ferrier-PagèsC. (2003). Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J. Exp. Mar. Biol. Ecol.296, 145–166. doi: 10.1016/S0022-0981(03)00259-4

  • CrossRef
  • Google Scholar
  • View reference in article

• 53

  HoulbrèqueF.TambuttéÉ.RichardC.Ferrier-PagèsC. (2004). Importance of a micro-diet for scleractinian corals. Mar. Ecol. Prog. Ser.282, 151–160. doi: 10.3354/meps282151

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 54

  HowellsE. J.BaumanA. G.VaughanG. O.HumeB. C. C.VoolstraC. R.BurtJ. A. (2020). Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol.29, 899–911. doi: 10.1111/mec.15372

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 55

  HuangW.MengL.XiaoZ.TanR.YangE.WangY.et al. (2024). Heat‐tolerant intertidal rock pool coral Porites lutea can potentially adapt to future warming. Mol. Ecol.33(5), e17273. doi: 10.1111/mec.17273

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 56

  HughesL.DeanA.SteffenW.RiceM. (2018). Lethal consequences: climate change impacts on the great barrier reef (Sydney, NSW, Australia: Climate Council of Australia Limited).

  • Google Scholar
  • View reference in article

• 57

  HumeB. C. C.Mejia-RestrepoA.VoolstraC. R.BerumenM. L. (2020). Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral. Reefs.39, 583–601. doi: 10.1007/s00338-020-01917-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 58

  IPCC (2023). “ Climate change 2023 synthesis report: summary for policymakers,” in Climate change 2023: synthesis report contribution of working groups I, II and III to the sixth assessment report of the intergovernmental panel on climate change intergovernmental panel on climate change. Eds. Core writing teamLeeH.RomeroJ. (Geneva, Switzerland: Intergovernmental Panel on Climate Change).

  • Google Scholar
  • View reference in article

• 59

  JacobsonL. M.EdmundsP. J.MullerE. B.NisbetR. M. (2016). The implications of reduced metabolic rate in resource-limited corals. J. Exp. Biol.219, 870–877. doi: 10.1242/jeb.136044

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 60

  JacquemontJ.HoulbrèqueF.TanvetC.Rodolfo-MetalpaR. (2022). Long-term exposure to an extreme environment induces species-specific responses in corals’ photosynthesis and respiration rates. Mar. Biol.169, 2–12. doi: 10.1007/s00227-022-04063-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 61

  JohannesR. E.WiebeW. J. (1970). Method for determination of coral tissue biomass and composition. Limnol. Oceanogr.15, 822–824. doi: 10.4319/lo.1970.15.5.0822

  • CrossRef
  • Google Scholar
  • View reference in article

• 62

  JonesR. J. (1997). Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Mar. Ecol. Prog. Ser.158, 51–59. doi: 10.3354/meps158051

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 63

  JonesA. M.BerkelmansR.Van OppenM. J. H.MieogJ. C.SinclairW. (2008). A community change in the algal symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimitization. Proc. R. Soc B.275, 1359–1365. doi: 10.1098/rspb.2008.0069

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 64

  JungE. M. U.StatM.ThomasL.KoziolA.SchoepfV. (2021). Coral host physiology and symbiont dynamics associated with differential recovery from mass bleaching in an extreme, macro-tidal reef environment in northwest Australia. Coral. Reefs.40, 893–905. doi: 10.1007/s00338-021-02094-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 65

  KavousiJ.DenisV.SharpV.ReimerJ. D.NakamuraT.ParkinsonJ. E. (2020). Unique combinations of coral host and algal symbiont genotypes reflect intraspecific variation in heat stress responses among colonies of the reef-building coral, Montipora digitata. Mar. Biol.167, 7–12. doi: 10.1007/s00227-019-3632-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 66

  KenkelC. D.MatzM. V. (2016). Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol.1, 0014. doi: 10.1101/059667

  • CrossRef
  • Google Scholar
  • View reference in article

• 67

  KimS. W.SommerB.BegerM.PandolfiJ. M. (2023). Regional and global climate risks for reef corals: Incorporating species-specific vulnerability and exposure to climate hazards. Global Change Biol.29, 4140–4151. doi: 10.1111/gcb.16739

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 68

  KramerW. E.Iglesias-PrietoR.EnriquezS. (2022). Evaluation of the current understanding of the impact of climate change on coral physiology after three decades of experimental research. Commun. Biol.5, 1418. doi: 10.1038/s42003-022-04353-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 69

  LachsL.DonnerS. D.MumbyP. J.BythellJ. C.HumanesA.EastH. K.et al. (2023). Emergent increase in coral thermal tolerance reduces mass bleaching under climate change. Nat. Commun.14, 4939. doi: 10.1038/s41467-023-40601-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 70

  LeggatW.HeronS. F.FordyceA.SuggettD. J.AinsworthT. D. (2022). Experiment Degree Heating Week (eDHW) as a novel metric to reconcile and validate past and future global coral bleaching studies. J. Environ. Manage.301, 113919. doi: 10.1016/j.jenvman.2021.113919

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 71

  LehmannW. (2022). “ Coral reef aquarium husbandry and health,” in Invertebrate medicine, 107–127. doi: 10.1002/9781119569831.ch6

  • CrossRef
  • Google Scholar
  • View reference in article

• 72

  LesserM. P. (1997). Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral. Reefs.16, 187–192. doi: 10.1007/s003380050073

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 73

  LesserM. P. (2013). Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things? Coral. Reefs.32, 25–33. doi: 10.1007/s00338-012-0993-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 74

  Le TissierM.BrownB. E. (1996). Dynamics of solar bleaching in the intertidal reef coral Goniastrea aspera at Ko Phuket, Thailand. Mar. Ecol. Prog. Ser.136, 235–244. doi: 10.3354/meps136235

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 75

  LevasS. J.GrottoliA. G.HughesA. D.OsburnC. L.MatsuiY. (2013). Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral porites lobata: implications for resilience in mounding corals. PloS One8, e63267. doi: 10.1371/journal.pone.0063267

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 76

  LoyaY.SakaiK.YamazatoK.NakanoY.SambaliH.van WoesikR. (2001). Coral bleaching: the winners and the losers. Ecol. Lett.4, 122–131. doi: 10.1046/j.1461-0248.2001.00203.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 77

  LyndbyN. H.HolmJ. B.WangpraseurtD.GroverR.RottierC.KühlM.et al. (2018). Effect of feeding and thermal stress on photosynthesis, respiration and the carbon budget of the scleractinian coral Pocillopora damicornis. BioRxiv, 378059. doi: 10.1101/378059

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 78

  MarshJ. A. (1970). Primary productivity of reef-building calcareous red algae. Ecology51, 255–263. doi: 10.2307/1933661

  • CrossRef
  • Google Scholar
  • View reference in article

• 79

  MatzM. V. (2024). Not-so-mutually beneficial coral symbiosis. Curr. Biol.34, R798–R801. doi: 10.1016/j.cub.2024.07.047

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 80

  McLachlanR. H.PriceJ. T.Muñoz-GarciaA.WeislederN. L.JuryC. P.ToonenR. J.et al. (2021). Environmental gradients drive physiological variation in Hawaiian corals. Coral. Reefs.40, 1505–1523. doi: 10.1007/s00338-021-02140-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 81

  McLachlanR. H.PriceJ. T.SolomonS. L.GrottoliA. G. (2020). Thirty years of coral heat-stress experiments: a review of methods. Coral. Reefs.39, 885–902. doi: 10.1007/s00338-020-01931-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 82

  McRaeC. J.KeshavmurthyS.MengP. J.RossetS. L.HuangW. B.ChenC. A.et al. (2022). Variable responses to chronic and acute elevated temperature of three coral species from reefs with distinct thermal regimes. Mar. Biol.169, 97. doi: 10.1007/s00227-022-04071-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 83

  MobergF.FolkeC. (1999). Ecological goods and services of coral reef ecosystems. Ecol. Econ.29, 215–233. doi: 10.1016/S0921-8009(99)00009-9

  • CrossRef
  • Google Scholar
  • View reference in article

• 84

  MorikawaM. K.PalumbiS. R. (2019). Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc. Natl. Acad. Sci.116, 10586–10591. doi: 10.1073/pnas.1721415116

  • Pubmed Abstract
  • CrossRef
  • Google Scholar
  • View reference in article

• 85

  MorrisL. A.VoolstraC. R.QuigleyK. M.BourneD. G.BayL. K. (2019). Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol.27, 678–689. doi: 10.1016/j.tim.2019.03.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 86

  Muller-ParkerG.D'EliaC. F.CookC. B. (2015). “ Interactions between corals and their symbiotic algae,” in Coral reefs in the anthropocene. Ed. BirkelandC. ( Springer, Dordrecht), 99–116.

  • Google Scholar

• 87

  MuscatineL. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. Ecosyst. World25, 75–87.

  • Google Scholar

• 88

  MuscatineL.McCloskeyR.MarianE. (1981). Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr.26, 601–611. doi: 10.4319/lo.1981.26.4.0601

  • CrossRef
  • Google Scholar

• 89

  NelsonH. R.AltieriA. H. (2019). Oxygen: the universal currency on coral reefs. Coral. Reefs.38, 177–198. doi: 10.1007/s00338-019-01765-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 90

  NOAA Coral Reef Watch Monthly Mean SST climatology (College Park, MD, USA: National Oceanic and Atmospheric Administration). Available online at: https://coralreefwatchnoaagov/product/5km/tutorial/crw06a_climatologyphp (Accessed January 22, 2022).

  • Google Scholar

• 91

  NystromM.NordemarI.TedengrenM. (2001). Simultaneous and sequential stress from increased temperature and copper on the metabolism of the hermatypic coral Porites cylindrica. Mar. Biol.138, 1225–1231. doi: 10.1007/s002270100549

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 92

  OburaD. O. (2005). Resilience and climate change: lessons from coral reefs and bleaching in the Western Indian Ocean. Estuar. Coast. Shelf. Sci.63, 353–372. doi: 10.1016/j.ecss.2004.11.010

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 93

  OliverT. A.PalumbiS. R. (2011). Do fluctuating temperature environments elevate coral thermal tolerance? Coral. Reefs.30, 429–440. doi: 10.1007/s00338-011-0721-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 94

  OnyangoC. A. (2020). Insights into the transcriptomic mechanisms underlying responses to heat stress and bleaching in two coral holobionts from Park Rynie, east coast South Africa. Doctor of philosophy in biological science thesis. School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa.

  • Google Scholar

• 95

  OsborneK.ThompsonA. A.ChealA. J.EmslieM. J.JohnsK. A.JonkerM. J.et al. (2017). Delayed coral recovery in a warming ocean. Global Change Biol.23, 3869–3881. doi: 10.1111/gcb.13707

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 96

  OsingaR.Iglesias-PrietoR.EnriquezS. (2012). “ Measuring photosynthesis in symbiotic invertebrates: A review of methodologies, rates and processes,” in Applied photosynthesis. Ed. NajafpourM. ( InTech, Rijeka, Croatia), 229–259.

  • Google Scholar

• 97

  PalumbiS. R.BarshisD. J.Traylor-KnowlesN.BayR. A. (2014). Mechanisms of reef coral resistance to future climate change. Science344, 895–898. doi: 10.1126/science.1251336

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 98

  PisapiaC.BurnD.YoosufR.NajeebA.AndersonK.PratchettM. (2016). Coral recovery in the central Maldives archipelago since the last major mass-bleaching, in 1998. Sci. Rep.6, 34720. doi: 10.1038/srep34720

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 99

  PorterS. N.SinkK. J.SchleyerM. H. (2021). The third global coral bleaching event on the marginal coral reefs of the southwestern Indian ocean and factors that contribute to their resistance and resilience. Diversity13, 10–17. doi: 10.3390/d13100464

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 100

  PupierC. A.GroverR.RottierC.Ferrier-PagèsC. (2024). Impact of seawater warming and nutrient deprivation on the physiology and energy metabolism of corals. Front. Mar. Sci.11. doi: 10.3389/fmars.2024.1423034

  • CrossRef
  • Google Scholar

• 101

  QuigleyK. M. (2024). Breeding and selecting corals resilient to global warming. Annu. Rev. Anim. Biosci.12, 209–332. doi: 10.1146/annurev-animal-021122-093315

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 102

  RädeckerN.PogoreutzC.GegnerH. M.CardenasA.RothF.BougoureJ.et al. (2021). Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl. Acad. Sci.118, e2022653118. doi: 10.1073/pnas.2022653118

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 103

  RazakT. B.RoffG.LoughJ. M.MumbyP. J. (2020). Growth responses of branching versus massive corals to ocean warming on the Great Barrier Reef, Australia. Sci. Tot. Environ.705, 135908. doi: 10.1016/j.scitotenv.2019.135908

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 104

  RodriguesL. J.GrottoliA. G. (2006). Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim. Cosmochim. Acta70, 2781–2789. doi: 10.1016/J.GCA.2006.02.014

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 105

  RodriguesL. J.GrottoliA. G. (2007). Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr.52, 1874–1882. doi: 10.4319/lo.2007.52.5.1874

  • CrossRef
  • Google Scholar

• 106

  RoikA.WallM.DobelmannM.NietzerS.BrefeldD.FiesingerA.et al. (2023). Trade-offs in a reef-building coral after six years of thermal acclimation. BioRxiv, 07. doi: 10.1101/2023.07.20.549699

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 107

  RosicN.RemondC.Mello-AthaydeM. A. (2020). Differential impact of heat stress on reef-building corals under different light conditions. Mar. Environ. Res.158, 104947. doi: 10.1016/j.marenvres.2020.104947

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 108

  SafaieA.SilbigerN. J.McClanahanT. R.PawlakG.BarshisD. J.HenchJ. L.et al. (2018). High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun.9, 1671. doi: 10.1038/s41467-018-04074-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 109

  SawallY.Al-SofyaniA.HohnS.Banguera-HinestrozaE.VoolstraC. R.WahlM. (2015). Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci. Rep.5, 8940. doi: 10.1038/srep08940

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 110

  SawallY.TeichbergM. C.SeemannJ.LitaayM.JompaJ.RichterC. (2011). Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia). Coral. Reefs.30, 841–853. doi: 10.1007/s00338-011-0764-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 111

  ScheufenT.Iglesias-PrietoR.EnríquezS. (2017). Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front. Mar. Sci.4, 2017. doi: 10.3389/fmars.2017.00309

  • CrossRef
  • Google Scholar

• 112

  SchleyerM. H.FlorosC.LaingS. C. S.MacdonaldA. H. H.Montoya-MayaP. H.MorrisT.et al. (2018). What can South African reefs tell us about the future of high-latitude coral systems? Mar. pollut. Bull.136, 491–507. doi: 10.1016/j.marpolbul.2018.09.014

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 113

  SchlotheuberM.VoolstraC. R.de BeerD.CampE. F.KlattJ. M.GhilardiM.et al. (2024). High temporal resolution of hydrogen peroxide (H₂O₂) dynamics during heat stress does not support a causative role in coral bleaching. Coral. Reefs.43, 119–133. doi: 10.1007/s00338-023-02448-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 114

  SchoepfV.BaumannJ. H.BarshisD. J.BrowneN. K.CampE. F.ComeauS.et al. (2023). Corals at the edge of environmental limits: A new conceptual framework to re-define marginal and extreme coral communities. Sci. Tot. Environ.884, 163688. doi: 10.1016/j.scitotenv.2023.163688

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 115

  SchoepfV.JungM. U.McCullochM. T.WhiteN. E.StatM.ThomasL. (2020). Thermally variable, macrotidal reef habitats promote rapid recovery from mass coral bleaching. Front. Mar. Sci.7, 245. doi: 10.3389/fmars.2020.00245

  • CrossRef
  • Google Scholar

• 116

  SchoepfV.SandersonH.LarcombeE. (2021). Coral heat tolerance under variable temperatures: Effects of different variability regimes and past environmental history vs. current exposure. Limnol. Oceanogr.67, 404–418. doi: 10.1002/lno.12000

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 117

  SchoepfV.StatM.FalterJ. L.McCullochM. T. (2015). Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci. Rep.5, 17639. doi: 10.1038/srep17639

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 118

  SiebeckU. E.MarshallN. J.KlüterA.Hoegh-GuldbergO. (2006). Monitoring coral bleaching using a colour reference card. Coral. Reefs.25, 453–460. doi: 10.1007/s00338-006-0123-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 119

  SilversteinR. N.CunningR.BakerA. C. P. (2015). Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Global Change Biol.21, 236–249. doi: 10.1111/gcb.12706

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 120

  SkirvingW. J.HeronS. F.MarshB. L.LiuG.De La CourJ. L.GeigerE. F.et al. (2019). The relentless march of mass coral bleaching: a global perspective of changing heat stress. Coral. Reefs.38, 547–557. doi: 10.1007/s00338-019-01799-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 121

  SmitK. (2014). Ecophysiology of intertidal corals along the east coast of South Africa: Coping in marginal habitats Masters of Biological Science dissertation (Durban, South Africa: School of Life Sciences, University of KwaZulu-Natal).

  • Google Scholar

• 122

  SmitK.GlassomD. (2017). Large fluctuations but constant mean temperatures allow corals to persist in intertidal rock pools on the east coast of South Africa. Helgol. Mar. Res.71, 1–9. doi: 10.1186/s10152-017-0482-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 123

  SpeelmanP. E.PargerM.SchoepfV. (2023). Divergent recovery trajectories of intertidal and subtidal coral communities highlight habitat-specific recovery dynamics following bleaching in an extreme macrotidal reef environment. PeerJ11, e15987. doi: 10.7717/peerj.15987

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 124

  StatM.BakerA. C.BourneD. G.CorreaA. M.ForsmanZ.HuggettM. J.et al. (2012). Molecular delineation of species in the coral holobiont. Adv. Mar. Biol.63, 1–65. doi: 10.1016/B978-0-12-394282-1.00001-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 125

  StatM.GatesR. D. (2011). Clade D Symbiodinium in scleractinian corals: a nugget of hope, a selfish opportunist, an omminus sign, or all of the above? J. Mar. Sci., 1–9. doi: 10.1155/2011/730715

  • CrossRef
  • Google Scholar

• 126

  StimsonJ.SakaiK.SembaliH. (2002). Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral. Reefs.21, 409–421. doi: 10.1007/s00338-002-0264-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 127

  SuzukiA.GaganM. K.FabriciusK. E.IsdaleP. J.YukinoI.KawahataH. (2003). Skeletal isotope microfiles of growth pertubations in Porites corals during the 1997-1998 mass bleaching event. Coral. Reefs.22, 357–369. doi: 10.1007/s00338-003-0323-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 128

  ThummasanM.CasaretoB. E.RamphulC.SuzukiT.ToyodaK.SuzukiY. (2021). Physiological responses (Hsps 60 and 32, caspase 3, H₂O₂ scavenging, and photosynthetic activity) of the coral Pocillopora damicornis under thermal and high nitrate stresses. Mar. pollut. Bull.171, 112737. doi: 10.1016/j.marpolbul.2021.112737

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 129

  TisthammerK. H.Timmins-SchiffmanE.SenecaF. O.NunnB. L.RichmondR. H. (2021). Physiological and molecular responses of lobe coral indicate nearshore adaptations to anthropogenic stressors. Sci. Rep.11, 3423. doi: 10.1038/s41598-021-82569-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 130

  TitlyanovE. A.TitlyanovaT. V. (2002). Reef-building corals - symbiotic autotrophic organisms: 1. General structure, feeding pattern, and light-dependent distribution in the shelf. Russ. J. Mar. Biol.28, S1–S15. doi: 10.1023/A:1021836204655

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 131

  TkachenkoK. S.SoongK. (2017). Dongsha Atoll: A potential thermal refuge for reef-building corals in the South China Sea. Mar. Environ. Res.127, 112–125. doi: 10.1016/j.marenvres.2017.04.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 132

  TremblayP.GoriA.MaguerJ. F.HoogenboomM.Ferrier-PagesC. (2016). Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Sci. Rep.6, 38112. doi: 10.1038/srep38112

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 133

  UlstrupK. E.KühlM.Van OppenM. J.CooperT. F.RalphP. J. (2011). Variation in photosynthesis and respiration in geographically distinct populations of two reef-building coral species. Aquat. Biol.12, 241–248. doi: 10.3354/ab00338

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 134

  van OppenM. J. H.OliverJ. K.PutnamH. M.GatesR. D. (2015). Building coral reef resilience through assisted evolution. Proc. Natl. Acad. Sci.112, 2307–2313. doi: 10.1073/pnas.1422301112

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 135

  VisramS.DouglasA. E. (2007). Resilience and acclimation to bleaching stressors in the scleractinian coral Porites cylindrica. J. Exp. Mar. Biol. Ecol.349, 35–44. doi: 10.1016/j.jembe.2007.04.014

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 136

  VoolstraC. R.AlderdiceR.ColinL.StaabS.ApprillA.RainaJ.-B. (2025). Standardized methods to assess the impacts of thermal stress on coral reef marine life. Annu. Rev. Mar. Sci.17, 4–15. doi: 10.1146/annurev-marine-032223-024511

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 137

  WeisV. M. (2008). Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol.211, 3059–3066. doi: 10.1242/jeb.009597

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 138

  WeisV. M. (2019). Cell biology of coral symbiosis: Foundational study can inform solutions to the coral reef crisis. Integr. Comp. Biol.59, 845–855. doi: 10.1093/icb/icz067

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 139

  WooldridgeS. A. (2009). A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis. Mar. Freshw. Res.60, 483–496. doi: 10.1071/mf08251

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 140

  WooldridgeS. A. (2014). Assessing coral health and resilience in a warming ocean: why looks can be deceptive. Bioessays36, 1041–1049. doi: 10.1002/bies.201400074

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 141

  WooldridgeS. A. (2017). Instability and breakdown of the coral–algae symbiosis upon exceedence of the interglacial pCO₂ threshold (>260 ppmv): the “missing” Earth-System feedback mechanism. Coral. Reefs.36, 1025–1037. doi: 10.1007/s00338-017-1594-5

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 142

  WrightR. M.MeraH.KenkelC. D.NayfaM.BayL. K.MatzM. V. (2019). Positive genetic associations among fitness traits support evolvability of a reef-building coral under multiple stressors. Global Change Biol.25, 3294–3304. doi: 10.1111/gcb.14764

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 143

  ZieglerM.RoderC. M.BuchelC.VoolstraC. R. (2014). Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea. Coral. Reefs.33, 1115–1129. doi: 10.1007/s00338-014-1192-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar