The effects of thermal stress on the physiology of two high-latitude corals from the environmentally variable intertidal and moderate subtidal habitats.

Abstract

Corals are of great ecological and economic importance; however, they are increasingly threatened by mass bleaching events caused by ocean warming, which has become more frequent and is predicted to increase in frequency and severity in the coming years. The degree of coral bleaching, recoverability, and mortality is highly variable and considered to be affected by the coral’s physiological and antioxidant capacity and the thermal regimes they experience. These mechanisms are still poorly understood and need to be investigated in different coral species from varying environmental regimes when exposed to prolonged thermal stress and during recovery to better inform conservation measures. Coral communities found on the subtropical East Coast of South Africa can be defined as ‘extreme’ due to the sub-optimum environmental conditions experienced especially in intertidal habitats and ‘marginal’ since, ecologically, they are not true accretive reefs. Climate change has not caused severe bleaching in corals of this region, but the physiological mechanisms that influence their thermal resilience/susceptibility are yet to be investigated. Therefore, this thesis examined the thermal resilience/susceptibility of Anomastraea irregularis (massive morphology) and Pocillopora verrucosa (branching morphology) from the intertidal and subtidal zones of the understudied rocky shores of Treasure Beach, east coast KwaZulu-Natal province, South Africa using both laboratory and field studies. The intertidal pools in this region are highly dynamic, with large summer daytime fluctuations of more than 10°C at spring tide while the subtidal zone is notably more environmentally stable. These corals were maintained in closed recirculating aquaria and exposed to two constant thermal stress conditions (control: 26°C, thermal stress treatments: 28°C and 30°C) for three months and then were maintained at control conditions for two months to monitor recovery. Respiration, photosynthetic, and growth rates were measured monthly. The Symbiodiniaceae density, chlorophyll-a concentration, chlorophyll-a concentration per symbiont cell, lipid concentration, protein concentration, antioxidant enzyme activity (superoxide dismutase, catalase, glutathione peroxidase, glutathione s-transferase), and caspase 3 activity were analysed at the start and end of the thermal stress as well as at the end of the recovery period. The thermal stress treatments induced bleaching (significant decrease in Symbiodiniaceae density and chlorophyll-a concentrations) in both species from both habitats with associated significant decrease in photosynthetic and growth rates. Increased oxidative stress was also evident with the increased superoxide dismutase, catalase, glutathione peroxidase, and caspase 3 activity in fragments in both thermal stress treatments at the start and end of thermal stress and at the end of recovery. There were inherent physiological differences between the species and habitat that were maintained throughout the experiment, highlighting that variable thermal regimes and coral species can influence coral resilience to thermal stress. The intertidal corals were more resilient (less bleaching and fewer deaths) than their subtidal conspecifics, and A. irregularis appeared more resilient than P. verrucosa in both thermal stress treatments. The intertidal corals could lower their respiration rates to that of the control rates by the end of thermal stress and maintained higher Symbiodiniaceae densities, chlorophyll-a, and lipid concentrations than their= subtidal conspecifics throughout the study. Resilience of A. irregularis may be a result of its thicker tissue, which allowed higher Symbiodiniaceae density and lipid concentrations and lower P:R ratios demonstrative of a more heterotrophic nature. Overall, higher protein concentrations and lower antioxidant enzyme activities (superoxide dismutase, catalase, and glutathione peroxidase) were evident in intertidal fragments than subtidal fragments and A. irregularis than P. verrucosa when thermally stressed. The higher protein concentrations may have facilitated the corals’ physiological processes that made them more resilient to prolonged thermal stress. Therefore, these corals may have had lower antioxidant activities because of less oxidative stress. The results indicated much higher antioxidant activity in susceptible corals, suggesting that oxidative stress may be responsible for higher bleaching and mortalities. The photosynthetic and growth rates, Symbiodiniaceae density, chlorophyll-a concentration, and lipid concentration of both species from both habitats did not fully recover two months after thermal stress. Similarly, the antioxidant enzyme activities (superoxide dismutase, catalase, glutathione peroxidase), and caspase 3 activities of both species from both habitats did not decrease to control levels at the end of recovery, indicating that a longer period would be required for full recovery of the biochemical and physiological pathways of these corals. This has implications for coral reef recovery trajectories in situ since less time between mass bleaching events is predicted in the near future. Field studies are important for validating the physiological responses found during laboratory studies since the static nature of laboratory experiments cannot account for the dynamic environmental conditions corals encounter in situ. A pilot study was conducted to determine if the ‘flexi-chamber’ and photogrammetry could be used to track respiration, photosynthesis, and growth of A. irregularis and P. verrucosa fragments (3 cm > 4 cm) in the intertidal and subtidal habitats in Park Rynie, east coast KwaZulu-Natal province, South Africa. This study found that the two methods could be optimised to effectively measure the physiological processes of coral fragments in both habitats at relatively low cost and low complexity. To understand the physiological responses of these species when exposed to thermal stress in their natural habitats an in-situ experiment at Treasure Beach was conducted during the warmer austral spring and summer months where fragments of both species were reciprocally transplanted between the two habitats. Controls were established by placing fragments in their original habitats. Respiration, photosynthesis, growth rates, and coral health scores were measured monthly for six months. The physiological rates were measured using the optimised methods that were obtained during the pilot study. The Symbiodiniaceae density, chlorophyll-a concentration, chlorophyll-a concentration per symbiont cell, and lipid concentration were also analysed at the start and end of the study. Similar to the laboratory results, differential physiological responses between species and habitat were evident in response to the reciprocal transplantation. Intertidal A. irregularis and P. verrucosa transplanted into the subtidal habitat showed potential acclimation to the subtidal habitat. These fragments were able to adjust their P:R ratios and maintain higher Symbiodiniaceae cell density, Symbiodiniaceae chlorophyll-a concentration, and Symbiodiniaceae chlorophyll-a concentration per cell, and lipid content thereby experiencing less bleaching and mortalities. Anomastraea irregularis appeared more physiologically plastic (altering respiration rates and maintaining higher Symbiodiniaceae cell density and lipid concentration) and therefore more tolerant (less bleaching and mortalities) than P. verrucosa to the changes in environmental conditions. The laboratory and field results add to the limited knowledge of how high-latitude corals of different species and from habitats of differing environmental regimes react physiologically to long-term thermal stress. The results are promising since these resilient corals may be used in future conservation initiatives. The results of this thesis show the ability of some coral species to acclimatise and/or adapt to different environmental conditions, however, the potential for these corals to acclimatise/adapt to global climate change related stressors still warrants further investigation especially since several other stressors are also impacting reef systems.