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.

Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral.

Sensitive molecular analyses show that most corals host a complement of Symbiodinium genotypes that includes thermo-tolerant types in low abundance. While tolerant symbiont types are hypothesized to facilitate tolerance to temperature and recovery from bleaching, empirical data on their distribution and relative abundance in corals under ambient and stress conditions are still rare. We quantified visual bleaching and mortality of coral hosts, along with relative abundance of C- and D-type Symbiodinium cells in 82 Acropora millepora colonies from three locations on the Great Barrier Reef transplanted to a central inshore site over a 13 month period. Our analyses reveal dynamic change in symbiont associations within colonies and among populations over time. Coral bleaching and declines in C- but not D-type symbionts were observed in transplanted corals. Survival and recovery of 25% of corals from one population was associated with either initial D-dominance or an increase in D-type symbionts that could be predicted by a minimum pre-stress D : C ratio of 0.003. One-third of corals from this population became D dominated at the bleached stage despite no initial detection of this symbiont type, but failed to recover and died in mid to late summer. These results provide a predictive threshold minimum density of background D-type symbionts in A. millepora, above which survival following extreme thermal stress is increased.

A population genetic assessment of coral recovery on highly disturbed reefs of the Keppel Island archipelago in the southern Great Barrier Reef.

Coral reefs surrounding the islands lying close to the coast are unique to the Great Barrier Reef (GBR) in that they are frequently exposed to disturbance events including floods caused by cyclonic rainfall, strong winds and occasional periods of prolonged above-average temperatures during summer. In one such group of islands in the southern GBR, the Keppel Island archipelago, climate-driven disturbances frequently result in major coral mortality. Whilst these island reefs have clearly survived such dramatic disturbances in the past, the consequences of extreme mortality events may include the loss of genetic diversity, and hence adaptive potential, and a reduction in fitness due to inbreeding, especially if new recruitment from external sources is limited. Here we examined the level of isolation of the Keppel Island group as well as patterns of gene flow within the Keppel Islands using 10 microsatellite markers in nine populations of the coral, Acropora millepora. Bayesian cluster analysis and assignment tests indicated gene flow is restricted, but not absent, between the outer and inner Keppel Island groups, and that extensive gene flow exists within each of these island groups. Comparison of the Keppel Island data with results from a previous GBR-wide study that included a single Keppel Island population, confirmed that A. millepora in the Keppel Islands is genetically distinct from populations elsewhere on the GBR, with exception of the nearby inshore High Peak Reef just north of the Keppel Islands. We compared patterns of genetic diversity in the Keppel Island populations with those from other GBR populations and found them to be slightly, but significantly lower, consistent with the archipelago being geographically isolated, but there was no evidence for recent bottlenecks or deviation from mutation-drift equilibrium. A high incidence of private alleles in the Keppel Islands, particularly in the outer islands, supports their relative isolation and contributes to the conservation value of the archipelago. The lack of evidence for genetic erosion, in combination with our observation that the North Keppel Island population samples collected in 2002 and 2008, respectively, exhibited a pairwise genetic distance of zero, supports previous published work indicating that, following bleaching, Acropora corals in the Keppel Islands predominantly recover from regrowth of small amounts of remaining live tissue in apparently dead coral colonies. This is likely supplemented by recruitment of larvae from genetically similar, less disturbed populations at nearby reefs, particularly following extreme flood events.

The use of climatologies and Bayesian models to link observations to outcomes; an example from the Torres Strait.

After widespread coral bleaching in the Torres Strait in 2009-2010 a monitoring program was established under the National Environmental Research Program and run by the Torres Strait Regional Authority to identify ocean conditions that may lead to future bleaching. One component of this program was a real time ocean monitoring station located between Thursday and Horn Islands in the south-western part of the Torres Strait. A key outcome of the project was to make the scientific data and knowledge available to the local communities in a form that they could engage with and with which they could act to instigate outcomes relevant to their needs. The project developed climatologies to give context to the temperature data allowing for historical limits to define the significance of the real time data as related to the longer term mean. This allowed the identification of 'normal', 'significant' and 'extreme' temperature events which could be linked into appropriate responses. Bayesian models were used to encapsulate the current scientific knowledge about the drivers and responses involved in coral bleaching. These models were used to convert the environmental parameters to an output index reflecting the current and future likelihood of coral bleaching occurring. Two web sites were used to integrate the real time data, climatology data and the bleaching indices generated from the Bayesian models. The first was a more technical site developed for the local environmental managers within the Torres Strait Regional Authority, the second was targeted at the general public with a display located within the local radio station and broadcast on a daily basis. Engagement with the project has been high to the point where additional monitoring stations and data display kiosks are to be installed in the near future. The combination of climatologies to give context and conceptual models to embody system knowledge has allowed the project to go from delivering simple measurements to being able to deliver knowledge about the system in a format that engages the local community and that can be used to facilitate environmental management outcomes.

Flood impacts in Keppel Bay, southern great barrier reef in the aftermath of cyclonic rainfall.

In December 2010, the highest recorded Queensland rainfall associated with Tropical Cyclone 'Tasha' caused flooding of the Fitzroy River in Queensland, Australia. A massive flood plume inundated coral reefs lying 12 km offshore of the Central Queensland coast near Yeppoon and caused 40-100% mortality to coral fringing many of the islands of Keppel Bay down to a depth of ∼8 m. The severity of coral mortality was influenced by the level of exposure to low salinity seawater as a result of the reef's distance from the flood plume and to a lesser extent, water depth and whether or not the reef faced the plume source. There was no evidence in this study of mortality resulting from pollutants derived from the nearby Fitzroy Catchment, at least in the short term, suggesting that during a major flood, the impact of low salinity on corals outweighs that of pollutants. Recovery of the reefs in Keppel Bay from the 2010/2011 Fitzroy River flood is likely to take 10-15 years based on historical recovery periods from a similar event in 1991; potentially impacting visitor numbers for tourism and recreational usage. In the meantime, activities like snorkeling, diving and coral viewing will be focused on the few shallow reefs that survived the flood, placing even further pressure on their recovery. Reef regeneration, restoration and rehabilitation are measures that may be needed to support tourism in the short term. However, predictions of a warming climate, lower rainfall and higher intensity summer rain events in the Central and Coastal regions of Australia over the next decade, combined with the current anthropogenic influences on water quality, are likely to slow regeneration with consequent impact on long-term reef resilience.

Historical thermal regimes define limits to coral acclimatization.

Knowledge of the degree to which corals undergo physiological acclimatization or genetic adaptation in response to changes in their thermal environment is crucial to the success of coral reef conservation strategies. The potential of corals to acclimatize to temperatures exceeding historical thermal regimes was investigated by reciprocal transplantation of Acropora millepora colonies between the warm central and cool southern regions of the Great Barrier Reef (GBR) for a duration of 14 months. Colony fragments retained at native sites remained healthy, whereas transplanted fragments, although healthy over initial months when temperatures remained within native thermal regimes, subsequently bleached and suffered mortality during seasonal temperature extremes. Corals hosting Symbiodinium D transplanted to the southern GBR bleached in winter and the majority suffered whole (40%; n=20 colonies) or partial (50%) mortality at temperatures 1.1 degrees C below their 15-year native minimum. In contrast, corals hosting Symbiodinium C2 transplanted to the central GBR bleached in summer and suffered whole (50%; n=10 colonies) or partial (42%) mortality at temperatures 2.5 degrees C above their 15-year native maximum. During summer bleaching, the dominant Symbiodinium type changed from C2 to D within corals transplanted to the central GBR. Corals transplanted to the cooler, southern GBR grew 74-80% slower than corals at their native site, and only 50% of surviving colonies reproduced, at least partially because of cold water bleaching of transplants. Despite the absence of any visual signs of stress, corals transplanted to the warmer, central GBR grew 52-59% more slowly than corals at their native site before the summer bleaching (i.e., from autumn to spring). Allocation of energy to initial acclimatization or reproduction may explain this pattern, as the majority (65%) of transplants reproduced one month earlier than portions of the same colonies retained at the southern native site. All parameters investigated (bleaching, mortality, Symbiodinium type fidelity, reproductive timing) demonstrated strong interactions between genotype and environment, indicating that the acclimatization potential of A. millepora populations may be limited by adaptation of the holobiont to native thermal regimes.

Environmental factors controlling the distribution of symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef.

BACKGROUND: The Symbiodinium community associated with scleractinian corals is widely considered to be shaped by seawater temperature, as the coral's upper temperature tolerance is largely contingent on the Symbiodinium types harboured. Few studies have challenged this paradigm as knowledge of other environmental drivers on the distribution of Symbiodinium is limited. Here, we examine the influence of a range of environmental variables on the distribution of Symbiodinium associated with Acropora millepora collected from 47 coral reefs spanning 1,400 km on the Great Barrier Reef (GBR), Australia. METHODOLOGY/PRINCIPAL FINDINGS: The environmental data included Moderate Resolution Imaging Spectroradiometer (MODIS) satellite data at 1 km spatial resolution from which a number of sea surface temperature (SST) and water quality metrics were derived. In addition, the carbonate and mud composition of sediments were incorporated into the analysis along with in situ water quality samples for a subset of locations. Analyses were conducted at three spatio-temporal scales [GBR (regional-scale), Whitsunday Islands (local-scale) and Keppel Islands/Trunk Reef (temporal)] to examine the effects of scale on the distribution patterns. While SST metrics were important drivers of the distribution of Symbiodinium types at regional and temporal scales, our results demonstrate that spatial variability in water quality correlates significantly with Symbiodinium distribution at local scales. Background levels of Symbiodinium types were greatest at turbid inshore locations of the Whitsunday Islands where SST predictors were not as important. This was not the case at regional scales where combinations of mud and carbonate sediment content coupled with SST anomalies and mean summer SST explained 51.3% of the variation in dominant Symbiodinium communities. CONCLUSIONS/SIGNIFICANCE: Reef corals may respond to global-scale stressors such as climate change through changes in their resident symbiont communities, however, management of local-scale stressors such as altered water quality is also necessary for maintenance of coral-Symbiodinium associations.

Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef.

Effective management of reef corals requires knowledge of the extent to which populations are open or closed and the scales over which genetic exchange occurs, information which is commonly derived from population genetic data. Such data are sparse for Great Barrier Reef (GBR) corals and other organisms, with the studies that are available being mostly based on a small number of sampling locations spanning only part of the GBR. Using 11 microsatellite loci, we genotyped 947 colonies of the reef-building coral Acropora millepora from 20 sites spanning almost the full length of the GBR (∼12° of latitude and ∼1550 km). The results show a major divide between the southernmost central to southern offshore populations and all other sampled populations. We interpret this divide as a signature of allopatric divergence in northern and southern refugia during the Pleistocene glaciations, from which the GBR was subsequently recolonized. Superimposed on this pattern is a cross-shelf genetic division, as well as a separation of inshore populations south of the Cape Clifton Front at ∼21.5-22°S. Most inshore populations north of this, as well as mid-shelf populations in the northern and far northern GBR, are open, exchanging recruits frequently. In contrast, inshore populations south of the Cape Clifton Front and offshore populations in the central and southern GBR are largely self-seeding, at least within the spatial resolution that was achieved given our sampling intensity. Populations that have been impacted by recent disturbance events causing extensive coral mortality show no evidence of reduced genetic diversity.

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.

Estimating the potential for adaptation of corals to climate warming.

The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetic basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermo-tolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT-PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming.

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.

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.

Coral bleaching indices and thresholds for the Florida Reef Tract, Bahamas, and St. Croix, US Virgin Islands.

It is well established that elevated sea temperatures cause widespread coral bleaching, yet confusion lingers as to what facet of extreme temperatures is most important. Utilizing long-term in situ datasets, we calculated nine thermal stress indices and tested their effectiveness at segregating bleaching years a posteriori for multiple reefs on the Florida Reef Tract. The indices examined represent three aspects of thermal stress: (1) short-term, acute temperature stress; (2) cumulative temperature stress; and (3) temperature variability. Maximum monthly sea surface temperature (SST) and the number of days >30.5 degrees C were the most significant; indicating that cumulative exposure to temperature extremes characterized bleaching years. Bleaching thresholds were warmer for Florida than the Bahamas and St. Croix, US Virgin Islands reflecting differences in seasonal maximum SST. Hind-casts showed that monthly mean SST above a local threshold explained all bleaching years in Florida, the Bahamas, and US Virgin Islands.

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 degrees 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.