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      Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment

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          Abstract

          Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.

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          Mechanisms of reef coral resistance to future climate change.

          Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
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            Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf

            Coral reefs are in rapid decline on a global scale due to human activities and a changing climate. Shallow water reefs depend on the obligatory symbiosis between the habitat forming coral host and its algal symbiont from the genus Symbiodinium (zooxanthellae). This association is highly sensitive to thermal perturbations and temperatures as little as 1°C above the average summer maxima can cause the breakdown of this symbiosis, termed coral bleaching. Predicting the capacity of corals to survive the expected increase in seawater temperatures depends strongly on our understanding of the thermal tolerance of the symbiotic algae. Here we use molecular phylogenetic analysis of four genetic markers to describe Symbiodinium thermophilum, sp. nov. from the Persian/Arabian Gulf, a thermally tolerant coral symbiont. Phylogenetic inference using the non-coding region of the chloroplast psbA gene resolves S. thermophilum as a monophyletic lineage with large genetic distances from any other ITS2 C3 type found outside the Gulf. Through the characterisation of Symbiodinium associations of 6 species (5 genera) of Gulf corals, we demonstrate that S. thermophilum is the prevalent symbiont all year round in the world's hottest sea, the southern Persian/Arabian Gulf.
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              Potential Costs of Acclimatization to a Warmer Climate: Growth of a Reef Coral with Heat Tolerant vs. Sensitive Symbiont Types

              One of the principle ways in which reef building corals are likely to cope with a warmer climate is by changing to more thermally tolerant endosymbiotic algae (zooxanthellae) genotypes. It is highly likely that hosting a more heat-tolerant algal genotype will be accompanied by tradeoffs in the physiology of the coral. To better understand one of these tradeoffs, growth was investigated in the Indo-Pacific reef-building coral Acropora millepora in both the laboratory and the field. In the Keppel Islands in the southern Great Barrier Reef this species naturally harbors nrDNA ITS1 thermally sensitive type C2 or thermally tolerant type D zooxanthellae of the genus Symbiodinium and can change dominant type following bleaching. We show that under controlled conditions, corals with type D symbionts grow 29% slower than those with type C2 symbionts. In the field, type D colonies grew 38% slower than C2 colonies. These results demonstrate the magnitude of trade-offs likely to be experienced by this species as they acclimatize to warmer conditions by changing to more thermally tolerant type D zooxanthellae. Irrespective of symbiont genotype, corals were affected to an even greater degree by the stress of a bleaching event which reduced growth by more than 50% for up to 18 months compared to pre-bleaching rates. The processes of symbiont change and acute thermal stress are likely to act in concert on coral growth as reefs acclimatize to more stressful warmer conditions, further compromising their regeneration capacity following climate change.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                02 December 2015
                2015
                : 5
                : 17639
                Affiliations
                [1 ]School of Earth and Environment and ARC Centre of Excellence for Coral Reef Studies, The University of Western Australia , Crawley, WA, Australia
                [2 ]UWA Oceans Institute, The University of Western Australia , Crawley, WA, Australia
                [3 ]The Western Australian Marine Science Institution , Perth, WA, Australia
                [4 ]Trace and Environmental DNA (TrEnD) Laboratory, Department of Environment and Agriculture, Curtin University , Perth, WA, Australia
                Author notes
                Article
                srep17639
                10.1038/srep17639
                4667274
                26627576
                92a038cf-caee-458c-953e-dd8aad9d7c4c
                Copyright © 2015, Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 01 May 2015
                : 03 November 2015
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