Successive marine heatwaves cause disproportionate coral bleaching during a fast phase transition from El Niño to La Niña.

The frequency and intensity of marine heatwaves that result in coral bleaching events have increased over recent decades and led to catastrophic losses of reef-building corals in many regions. The high-latitude coral assemblages at Lord Howe Island, which is a UNESCO listed site is the world southernmost coral community, were exposed to successive thermal anomalies following a fast phase-transition of the record-breaking 2009 to 2010 warm pool El Niño in the Central Pacific to a strong La Niña event in late 2010. The coral community experienced severe and unprecedented consecutive bleaching in both 2010 and 2011. Coral health surveys completed between March 2010 and September 2012 quantified the response and recovery of approximately 43,700 coral colonies to these successive marine heatwaves. In March 2010, coral bleaching ranged from severe, with 99% of colonies bleached at some shallow lagoon sites, to mild at deeper reef slope sites, with only 17% of individuals affected. Significant immediate mortality from thermal stress was evident during the peak of the bleaching event. Overall, species in the genera Pocillopora, Stylophora, Seriatopora and Porites were the most affected, while minimal bleaching and mortality was recorded among members of other coral families (e.g. Acroporidae, Dendrophyllidae & Merulinidae). Surviving corals underwent a subsequent, but much less intense, thermal anomaly in 2011 that led to a disproportionate bleaching response among susceptible taxa. While this observation indicates that the capacity of thermally susceptible high-latitude corals to acclimatize to future ocean warming may be limited, particularly if bleaching events occur annually, our long-term survey data shows that coral cover at most sites recovered to pre-bleaching levels within three years in the absence of further thermal anomalies.

Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp.

Climate change is driving global declines of marine habitat-forming species through physiological effects and through changes to ecological interactions, with projected trajectories for ocean warming and acidification likely to exacerbate such impacts in coming decades. Interactions between habitat-formers and their microbiomes are fundamental for host functioning and resilience, but how such relationships will change in future conditions is largely unknown. We investigated independent and interactive effects of warming and acidification on a large brown seaweed, the kelp Ecklonia radiata, and its associated microbiome in experimental mesocosms. Microbial communities were affected by warming and, during the first week, by acidification. During the second week, kelp developed disease-like symptoms previously observed in the field. The tissue of some kelp blistered, bleached and eventually degraded, particularly under the acidification treatments, affecting photosynthetic efficiency. Microbial communities differed between blistered and healthy kelp for all treatments, except for those under future conditions of warming and acidification, which after two weeks resembled assemblages associated with healthy hosts. This indicates that changes in the microbiome were not easily predictable as the severity of future climate scenarios increased. Future ocean conditions can change kelp microbiomes and may lead to host disease, with potentially cascading impacts on associated ecosystems.

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.

Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals.

Reef-building corals possess a range of acclimatisation and adaptation mechanisms to respond to seawater temperature increases. In some corals, thermal tolerance increases through community composition changes of their dinoflagellate endosymbionts (Symbiodinium spp.), but this mechanism is believed to be limited to the Symbiodinium types already present in the coral tissue acquired during early life stages. Compelling evidence for symbiont switching, that is, the acquisition of novel Symbiodinium types from the environment, by adult coral colonies, is currently lacking. Using deep sequencing analysis of Symbiodinium rDNA internal transcribed spacer 2 (ITS2) PCR amplicons from two pocilloporid coral species, we show evidence consistent with de novo acquisition of Symbiodinium types from the environment by adult corals following two consecutive bleaching events. Most of these newly detected symbionts remained in the rare biosphere (background types occurring below 1% relative abundance), but one novel type reached a relative abundance of ~33%. Two de novo acquired Symbiodinium types belong to the thermally resistant clade D, suggesting that this switching may have been driven by consecutive thermal bleaching events. Our results are particularly important given the maternal mode of Symbiodinium transmission in the study species, which generally results in high symbiont specificity. These findings will cause a paradigm shift in our understanding of coral-Symbiodinium symbiosis flexibility and mechanisms of environmental acclimatisation in corals.

Defining critical habitats of threatened and endemic reef fishes with a multivariate approach.

Understanding critical habitats of threatened and endemic animals is essential for mitigating extinction risks, developing recovery plans, and siting reserves, but assessment methods are generally lacking. We evaluated critical habitats of 8 threatened or endemic fish species on coral and rocky reefs of subtropical eastern Australia, by measuring physical and substratum-type variables of habitats at fish sightings. We used nonmetric and metric multidimensional scaling (nMDS, mMDS), Analysis of similarities (ANOSIM), similarity percentages analysis (SIMPER), permutational analysis of multivariate dispersions (PERMDISP), and other multivariate tools to distinguish critical habitats. Niche breadth was widest for 2 endemic wrasses, and reef inclination was important for several species, often found in relatively deep microhabitats. Critical habitats of mainland reef species included small caves or habitat-forming hosts such as gorgonian corals and black coral trees. Hard corals appeared important for reef fishes at Lord Howe Island, and red algae for mainland reef fishes. A wide range of habitat variables are required to assess critical habitats owing to varied affinities of species to different habitat features. We advocate assessments of critical habitats matched to the spatial scale used by the animals and a combination of multivariate methods. Our multivariate approach furnishes a general template for assessing the critical habitats of species, understanding how these vary among species, and determining differences in the degree of habitat specificity.

Spatial and temporal patterns of eastern Australia subtropical coral communities.

Despite increases in the frequency and intensity of disturbances on coral reefs over the past few decades, the response of subtropical coral assemblages to climate change is poorly understood. To address this knowledge gap on Australian reefs and provide a baseline for future comparisons, we quantified spatial (10-100's of kilometres) and temporal (decadal) patterns of benthic assemblages across a latitudinal gradient along the east Australian coastline (23.5° S to 31.5° S). Benthic community composition was quantified at six locations from the southern Great Barrier Reef, Queensland (Heron Reef, 23.5° S, 152° E) to northern New South Wales (31° S, 153.1° E) and at Lord Howe Island (31.5° S, 159.1° E). Our results indicate significant latitudinal differences in benthic assemblages, while community composition at some sites was more similar to those hundreds of kilometres away than to that of neighbouring reefs. A general trend was observed with decreasing cover of Acroporidae with increasing latitude, corresponding with an increasing cover of Pocilloporidae and Dendrophylliidae. Heron Reef comprised a high proportion of Acropora corals (43% total coral cover) and coralline algae (44%). In contrast, high-latitude reefs were dominated by mixed coral assemblages (0-52%) and high macroalgal cover (16-27%). Decadal comparisons of high-latitude reefs showed regional stability of benthic assemblages (9 out of 11 assemblages remained stable at > 75% similarity), during a period of warming oceans (0.15-0.24°C per decade). Such temporal stability suggests that eastern Australian subtropical communities may be more resistant than tropical reef communities that have experienced assembly shifts caused by perturbations associated with recent global climate change. Despite the clear differences in the structure of coral assemblages evident in our spatial surveys, we suggest that the temporal stability of high-latitude reefs may provide a limited refuge for tropical coral populations in an increasingly uncertain future.

Monitoring the sea change: preliminary assessment of the conservation value of nearshore reefs, and existing impacts, in a high-growth, coastal region of subtropical eastern Australia.

In northern NSW, Australia, coastal populations are forecast to increase dramatically over the next 25 years (the "sea change"). However, management of the effects of development on marine communities is hampered by the lack of data on key habitats. Consequently, we developed a protocol to assess the biodiversity and current human impacts on nearshore reefs, habitats that will be readily affected by coastal development. We assessed four reefs adjacent to each of three population centres targeting fish, mollusc and sessile benthic communities, and debris loads. Community structure was highly variable over all spatial scales indicating that reefs should not be considered equivalent within the planning framework. While, debris loads were relatively low on most reefs, those with highest conservation value also had the highest debris loads suggesting potential conflict between human use and long-term sustainability of reefal communities. Without intervention, this situation will be exacerbated in the future.