Ray Berkelmans

The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change

The ability of coral reefs to survive the projected increases in temperature due to global warming will depend largely on the ability of corals to adapt or acclimatize to increased temperature extremes over the next few decades. Many coral species are highly sensitive to temperature stress and the number of stress (bleaching) episodes has increased in recent decades. We investigated the acclimatization potential of Acropora millepora, a common and widespread Indo-Pacific hard coral species, through transplantation and experimental manipulation. We show that adult corals, at least in some circumstances, are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D. Our data suggest that the change in symbiont type in our experiment was due to a shuffling of existing types already present in coral tissues, not through exogenous uptake from the environment. The level of increased tolerance gained by the corals changing their dominant symbiont type to D (the most thermally resistant type known) is around 1–1.5 °C. This is the first study to show that thermal acclimatization is causally related to symbiont type and provides new insight into the ecological advantage of corals harbouring mixed algal populations. While this increase is of huge ecological significance for many coral species, in the absence of other mechanisms of thermal acclimatization/adaptation, it may not be sufficient to survive climate change under predicted sea surface temperature scenarios over the next 100 years. However, it may be enough to ‘buy time’ while greenhouse reduction measures are put in place.

Global warming and recurrent mass bleaching of corals

During 2015–2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization

The symbiosis between reef-building corals and their algal endosymbionts (zooxanthellae of the genus Symbiodinium) is highly sensitive to temperature stress, which makes coral reefs vulnerable to climate change. Thermal tolerance in corals is known to be substantially linked to the type of zooxanthellae they harbour and, when multiple types are present, the relative abundance of types can be experimentally manipulated to increase the thermal limits of individual corals. Although the potential exists for this to translate into substantial thermal acclimatization of coral communities, to date there is no evidence to show that this takes place under natural conditions. In this study, we show field evidence of a dramatic change in the symbiont community of Acropora millepora, a common and widespread Indo-Pacific hard coral species, after a natural bleaching event in early 2006 in the Keppel Islands (Great Barrier Reef). Before bleaching, 93.5% (n=460) of the randomly sampled and tagged colonies predominantly harboured the thermally sensitive Symbiodinium type C2, while the remainder harboured a tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving tagged colonies that were initially C2 predominant changed to D or C1 predominance. Colonies that were originally C2 predominant suffered high mortality (37%) compared with D-predominant colonies (8%). We estimate that just over 18% of the original A. millepora population survived unchanged leaving 29% of the population C2 and 71% D or C1 predominant six months after the bleaching event. This change in the symbiont community structure, while it persists, is likely to have substantially increased the thermal tolerance of this coral population. Understanding the processes that underpin the temporal changes in symbiont communities is key to assessing the acclimatization potential of reef corals.

Large-scale bleaching of corals on the Great Barrier Reef

Abstract The Great Barrier Reef (GBR) experienced its most intensive and extensive coral bleaching event on record in early 1998. Mild bleaching commenced in late January and intensified by late February/early March 1998. Broad-scale aerial surveys conducted of 654 reefs (∼23% of reefs on the GBR) in March and April 1998, showed that 87% of inshore reefs were bleached at least to some extent (>1% of coral cover) compared to 28% of offshore (mid- and outer-shelf) reefs. Of inshore reefs 67% had high levels of bleaching (>10% of coral) and 25% of inshore reefs had extreme levels of bleaching (>60% of coral). Fewer offshore reefs (14%) showed high levels of bleaching while none showed extreme levels of bleaching. Ground-truth surveys of 23 reefs, which experienced bleaching in intensities ranging from none to extreme, showed that the aerial survey data are likely to be underestimates of the true extent and intensity of bleaching on the GBR. The primary cause of this bleaching event is likely to be elevated sea temperature and solar radiation, exacerbated by lowered salinity on inshore and some offshore reefs in the central GBR.

Doom and Boom on a Resilient Reef: Climate Change, Algal Overgrowth and Coral Recovery

Background Coral reefs around the world are experiencing large-scale degradation, largely due to global climate change, overfishing, diseases and eutrophication. Climate change models suggest increasing frequency and severity of warming-induced coral bleaching events, with consequent increases in coral mortality and algal overgrowth. Critically, the recovery of damaged reefs will depend on the reversibility of seaweed blooms, generally considered to depend on grazing of the seaweed, and replenishment of corals by larvae that successfully recruit to damaged reefs. These processes usually take years to decades to bring a reef back to coral dominance. Methodology/Principal Findings In 2006, mass bleaching of corals on inshore reefs of the Great Barrier Reef caused high coral mortality. Here we show that this coral mortality was followed by an unprecedented bloom of a single species of unpalatable seaweed (Lobophora variegata), colonizing dead coral skeletons, but that corals on these reefs recovered dramatically, in less than a year. Unexpectedly, this rapid reversal did not involve reestablishment of corals by recruitment of coral larvae, as often assumed, but depended on several ecological mechanisms previously underestimated. Conclusions/Significance These mechanisms of ecological recovery included rapid regeneration rates of remnant coral tissue, very high competitive ability of the corals allowing them to out-compete the seaweed, a natural seasonal decline in the particular species of dominant seaweed, and an effective marine protected area system. Our study provides a key example of the doom and boom of a highly resilient reef, and new insights into the variability and mechanisms of reef resilience under rapid climate change.

Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef

Abstract Experimental studies of the upper thermal limits of corals from Orpheus Island, an inshore reef in the central Great Barrier Reef, show that Acropora formosa has a 5-day 50%-bleaching threshold of between 31 and 32 °C in summer, only 2 to 3 °C higher than local mean summer temperatures (29 °C). Summer bleaching thresholds for Pocillopora damicornis and A. elseyi were 1 °C higher (between 32 and 33 °C). The winter bleaching threshold of Pocillopora damicornis was 1 °C lower than its summer threshold, indicating that seasonal acclimatisation may take place. This seasonal difference raises the possibility that at least some corals may be capable of short-term thermal acclimatisation. Neither P. damicornis nor A. elseyi showed habitat-specific (reef flat versus reef slope) differences in bleaching thresholds. Further, colonies of P. damicornis collected from sites 3 km apart also showed no difference in bleaching threshold despite populations of this species responding differently at these two sites during a natural bleaching event. The bleaching thresholds determined in this study are best considered as the maximum tolerable temperatures for local populations of these species because they were determined in the absence of additional stressors (e.g. high light) which often co-occur during natural bleaching events. We consider the 5-day 50% bleaching thresholds determined in these experiments to be fair indicators of upper thermal limits, because >50% of a sample population died when allowed to recover in situ. We found a delay of up to a month in the bleaching response of corals following thermal stress, a result that has implications for identifying the timing of stressful conditions in natural bleaching events.

Source of trace element variability in Great Barrier Reef corals affected by the Burdekin flood plumes

Abstract Massive corals in the Great Barrier Reef, analyzed at high-resolution for Sr/Ca (thermal ionization mass spectrometry) and trace elements such as Ba and Mn (laser ablation inductively coupled plasma mass spectrometry), can provide continuous proxy records of dissolved seawater concentrations, as well as sea surface temperature (SST). A 10-yr record (1989 to 1998) from Pandora Reef, an inshore reef regularly impacted by the freshwater plumes of the Burdekin River, is compared with an overlapping record from a midshelf reef, away from runoff influences. Surface seawater samples, taken away from river plumes, show little variability for Sr/Ca (8484 ± 10 μmol/mol) and Ba (33.7 ± 0.7 nmol/kg). Discrete Ba/Ca peaks in the inshore coral coincide with flood events. The magnitude of this Ba/Ca enrichment is most likely controlled by the amount of suspended sediments delivered to the estuary, which remains difficult to monitor. The maximum flow rate at peak river discharge is used here as a proxy for the sediment load and is shown to be strongly correlated with coral Ba/Ca (r = 0.97). After the wet summer of 1991, the coral Ba/Ca flood peak is followed by a plateau that lingers for several months after dissipation of plume waters, signifying an additional flux of Ba that may originate from submarine groundwater seeps and/or mangrove reservoirs. Both Mn and Y are enriched by a factor of ∼5 in inshore relative to midshelf corals. Mn/Ca ratios show a seasonal cycle that follows SST (r = 0.7), not river discharge, with an additional high variability in summer suggesting a link with biological activity. P and Cd show no significant seasonal variation and are at a low level at both inshore and midreef locations. However, leaching experiments suggest that part of the coral P is not lattice bound.

ReefTemp: An interactive monitoring system for coral bleaching using high‐resolution SST and improved stress predictors

Anomalously high sea surface temperatures (SST) have led to repeated mass coral bleaching events on a global scale. Existing satellite-based systems used to monitor conditions conducive to bleaching are based on low-resolution (0.5°, ∼50 km) SST data. While these systems have served the research and management community well, they have inherent weaknesses that limit their capacity to predict stress on coral reefs at local scales, over which bleaching severity is known to vary dramatically. Here we discuss the development and testing of ReefTemp, a new operational remote sensing application for the Great Barrier Reef that assesses bleaching risk daily using: high-resolution (2 km) SST, regionally validated thermal stress indices, and color-graded legends directly related to past observations of bleaching severity. Given projections of sea temperature rise, ReefTemp is timely as it can accurately predict bleaching severity at a local scale and therefore help to give focus to future research and monitoring efforts.

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.

The Roles and Interactions of Symbiont, Host and Environment in Defining Coral Fitness

Background Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments. Methodology/Principal Findings Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31–35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora. Conclusions/Significance These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.