Spatially varying selection between habitats drives physiological shifts and local adaptation in a broadcast spawning coral on a remote atoll in Western Australia.

At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterizing the mechanisms of coral resilience to climate change. To explore these mechanisms in the reef coral Acropora tenuis, we collected samples from lagoon and reef slope habitats and combined whole-genome sequencing, ITS2 metabarcoding, experimental heat stress, and transcriptomics. Despite high gene flow across the atoll, we identified clear shifts in allele frequencies between habitats at relatively small linked genomic islands. Common garden heat stress assays showed corals from the lagoon to be more resistant to bleaching, and RNA sequencing revealed marked differences in baseline levels of gene expression between habitats. Our results provide new insight into the complex mechanisms of coral resilience to climate change and highlight the potential for spatially varying selection across complex coral reef seascapes to drive pronounced ecological divergence in climate-related traits.

A tale of two reef systems: Local conditions, disturbances, coral life histories, and the climate catastrophe.

Coral reefs have evolved over millennia to survive disturbances. Yet, in just a few decades chronic local pressures and the climate catastrophe have accelerated so quickly that most coral reefs are now threatened. Rising ocean temperatures and recurrent bleaching pose the biggest threat, affecting even remote and well-managed reefs on global scales. We illustrate how coral bleaching is altering reefs by contrasting the dynamics of adjacent reef systems over more than two decades. Both reef systems sit near the edge of northwest Australia's continental shelf, have escaped chronic local pressures and are regularly affected by tropical storms and cyclones. The Scott reef system has experienced multiple bleaching events, including mass bleaching in 1998 and 2016, from which it is unlikely to fully recover. The Rowley Shoals has maintained a high cover and diversity of corals and has not yet been impacted by mass bleaching. We show how the dynamics of both reef systems were driven by a combination of local environment, exposure to disturbances and coral life history traits, and consider future shifts in community structure with ongoing climate change. We then demonstrate how applying knowledge of community dynamics at local scales can aid management strategies to slow the degradation of coral reefs until carbon emissions and other human impacts are properly managed.

A quantitative comparison of towed-camera and diver-camera transects for monitoring coral reefs.

Novel tools and methods for monitoring marine environments can improve efficiency but must not compromise long-term data records. Quantitative comparisons between new and existing methods are therefore required to assess their compatibility for monitoring. Monitoring of shallow water coral reefs is typically conducted using diver-based collection of benthic images along transects. Diverless systems for obtaining underwater images (e.g. towed-cameras, remotely operated vehicles, autonomous underwater vehicles) are increasingly used for mapping coral reefs. Of these imaging platforms, towed-cameras offer a practical, low cost and efficient method for surveys but their utility for repeated measures in monitoring studies has not been tested. We quantitatively compare a towed-camera approach to repeated surveys of shallow water coral reef benthic assemblages on fixed transects, relative to benchmark data from diver photo-transects. Differences in the percent cover detected by the two methods was partly explained by differences in the morphology of benthic groups. The reef habitat and physical descriptors of the site-slope, depth and structural complexity-also influenced the comparability of data, with differences between the tow-camera and the diver data increasing with structural complexity and slope. Differences between the methods decreased when a greater number of images were collected per tow-camera transect. We attribute lower image quality (variable perspective, exposure and focal distance) and lower spatial accuracy and precision of the towed-camera transects as the key reasons for differences in the data from the two methods and suggest changes to the sampling design to improve the application of tow-cameras to monitoring.

Extreme seascape drives local recruitment and genetic divergence in brooding and spawning corals in remote north-west Australia.

Management strategies designed to conserve coral reefs threatened by climate change need to incorporate knowledge of the spatial distribution of inter- and intra-specific genetic diversity. We characterized patterns of genetic diversity and connectivity using single nucleotide polymorphisms (SNPs) in two reef-building corals to explore the eco-evolutionary processes that sustain populations in north-west Australia. Our sampling focused on the unique reefs of the Kimberley; we collected the broadcast spawning coral Acropora aspera (n = 534) and the brooding coral Isopora brueggemanni (n = 612) across inter-archipelago (tens to hundreds of kilometres), inter-reef (kilometres to tens of kilometres) and within-reef (tens of metres to a few kilometres) scales. Initial analysis of A. aspera identified four highly divergent lineages that were co-occurring but morphologically similar. Subsequent population analyses focused on the most abundant and widespread lineage, Acropora asp-c. Although the overall level of geographic subdivision was greater in the brooder than in the spawner, fundamental similarities in patterns of genetic structure were evident. Most notably, limits to gene flow were observed at scales <35 kilometres. Further, we observed four discrete clusters and a semi-permeable barrier to dispersal that were geographically consistent between species. Finally, sites experiencing bigger tides were more connected to the metapopulation and had greater gene diversity than those experiencing smaller tides. Our data indicate that the inshore reefs of the Kimberley are genetically isolated from neighbouring oceanic bioregions, but occasional dispersal between inshore archipelagos is important for the redistribution of evolutionarily important genetic diversity. Additionally, these results suggest that networks of marine reserves that effectively protect reefs from local pressures should be spaced within a few tens of kilometres to conserve the existing patterns of demographic and genetic connectivity.

Genetic signatures through space, time and multiple disturbances in a ubiquitous brooding coral.

The predominance of self-recruitment in many reef-building corals has fundamental and complex consequences for their genetic diversity, population persistence and responses to climate change. Knowledge of genetic structure over local scales needs to be placed within a broad spatial context, and also integrated with genetic monitoring through time to disentangle these consequences. Here, we examined patterns of genetic diversity over multiple spatio-temporal scales across tropical Australia in the ubiquitous brooding coral, Seriatopora hystrix. We also analysed complimentary environmental and demographic data to elucidate the seascape drivers of these patterns. Large genetic differences were detected between the east vs. west coasts of Australia. In northwest Australia, geographic differentiation dominated genetic structure over multiple scales. However, three sympatric lineages were detected at the largest offshore reef system (Scott Reef). Similar to the differences observed among putative species in eastern Australia, these lineages were associated with different levels of wave exposure. Local genetic structure within the Scott Reef system was relatively stable over 10 years, but temporal differences were observed that reflected small but important genetic changes over a few generations during recovery after severe bleaching. These results highlight the importance of self-recruitment together with occasional longer distance connectivity for the persistence of a metapopulation across spatially and temporally variable environments. Our multidimensional research provides a foundation for further long-term genetic monitoring to inform conservation strategies and highlights that sampling scales, ecological effects and cryptic diversity are important considerations to develop realistic understanding of the evolutionary resilience of corals.

Split spawning realigns coral reproduction with optimal environmental windows.

Split spawning in coral populations occurs when gamete maturation and mass spawning are split over two consecutive months. While split spawning has been observed at many reefs, little is known about the frequency and significance of these events. Here we show that split spawning occurred frequently and predictably over a decade at Scott Reef. Split spawning overlays the biannual spawning pattern in the region and occurs when the full moon falls in the first week of the usual spawning month, or the last week of the previous month. Additionally, in split years most species have their main spawning event after a 13-month lunar cycle, in the month following the usual spawning month. Without split spawning, spawn dates would shift by ~10 days each year to occur outside of optimal environmental windows. Our results suggest that split spawning is driven by a disconnect between lunar and seasonal cues, and is analogous with a 'leap year' in coral reproduction, realigning spawning dates with favourable conditions for reproduction.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño-Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.

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.

Biannual Spawning and Temporal Reproductive Isolation in Acropora Corals.

Coral spawning on the oceanic reef systems of north-western Australia was recently discovered during autumn and spring, but the degree to which species and particularly colonies participated in one or both of these spawnings was unknown. At the largest of the oceanic reef systems, the participation by colonies in the two discrete spawning events was investigated over three years in 13 species of Acropora corals (n = 1,855 colonies). Seven species spawned during both seasons; five only in autumn and one only in spring. The majority of tagged colonies (n = 218) spawned once a year in the same season, but five colonies from three species spawned during spring and autumn during a single year. Reproductive seasonality was not influenced by spatial variation in habitat conditions, or by Symbiodinium partners in the biannual spawner Acropora tenuis. Colonies of A. tenuis spawning during different seasons separated into two distinct yet cryptic groups, in a bayesian clustering analysis based on multiple microsatellite markers. These groups were associated with a major genetic divergence (G"ST = 0.469), despite evidence of mixed ancestry in a small proportion of individuals. Our results confirm that temporal reproductive isolation is a common feature of Acropora populations at Scott Reef and indicate that spawning season is a genetically determined trait in at least A. tenuis. This reproductive isolation may be punctuated occasionally by interbreeding between genetic groups following favourable environmental conditions, when autumn spawners undergo a second annual gametogenic cycle and spawn during spring.

Dynamic stability of coral reefs on the west Australian coast.

Monitoring changes in coral cover and composition through space and time can provide insights to reef health and assist the focus of management and conservation efforts. We used a meta-analytical approach to assess coral cover data across latitudes 10-35°S along the west Australian coast, including 25 years of data from the Ningaloo region. Current estimates of coral cover ranged between 3 and 44% in coral habitats. Coral communities in the northern regions were dominated by corals from the families Acroporidae and Poritidae, which became less common at higher latitudes. At Ningaloo Reef coral cover has remained relatively stable through time (∼28%), although north-eastern and southern areas have experienced significant declines in overall cover. These declines are likely related to periodic disturbances such as cyclones and thermal anomalies, which were particularly noticeable around 1998/1999 and 2010/2011. Linear mixed effects models (LME) suggest latitude explains 10% of the deviance in coral cover through time at Ningaloo. Acroporidae has decreased in abundance relative to other common families at Ningaloo in the south, which might be related to persistence of more thermally and mechanically tolerant families. We identify regions where quantitative time-series data on coral cover and composition are lacking, particularly in north-western Australia. Standardising routine monitoring methods used by management and research agencies at these, and other locations, would allow a more robust assessment of coral condition and a better basis for conservation of coral reefs.

Recovery of an isolated coral reef system following severe disturbance.

Coral reef recovery from major disturbance is hypothesized to depend on the arrival of propagules from nearby undisturbed reefs. Therefore, reefs isolated by distance or current patterns are thought to be highly vulnerable to catastrophic disturbance. We found that on an isolated reef system in north Western Australia, coral cover increased from 9% to 44% within 12 years of a coral bleaching event, despite a 94% reduction in larval supply for 6 years after the bleaching. The initial increase in coral cover was the result of high rates of growth and survival of remnant colonies, followed by a rapid increase in juvenile recruitment as colonies matured. We show that isolated reefs can recover from major disturbance, and that the benefits of their isolation from chronic anthropogenic pressures can outweigh the costs of limited connectivity.

Subtle genetic structure reveals restricted connectivity among populations of a coral reef fish inhabiting remote atolls.

We utilized a spatial and temporal analyses of genetic structure, supplemented with ecological and oceanographic analysis, to assess patterns of population connectivity in a coral reef fish Chromis margaritifer among the unique and remote atolls in the eastern Indian Ocean. A subtle, but significant genetic discontinuity at 10 microsatellite DNA loci was detected between atoll systems corresponding with a low (≤ 1%) probability of advection across the hundreds of kilometers of open ocean that separates them. Thus, although genetic connections between systems are likely maintained by occasional long-distance dispersal of C. margaritifer larvae, ecological population connectivity at this spatial scale appears to be restricted. Further, within one of these atoll systems, significant spatial differentiation among samples was accompanied by a lack of temporal pairwise differentiation between recruit and adult samples, indicating that restrictions to connectivity also occur at a local scale (tens of kilometers). In contrast, a signal of panmixia was detected at the other atoll system studied. Lastly, greater relatedness and reduced genetic diversity within recruit samples was associated with relatively large differences among them, indicating the presence of sweepstakes reproduction whereby a small proportion of adults contributes to recruitment in the next generation. These results are congruent with earlier work on hard corals, suggesting that local production of larvae drives population replenishment in these atoll systems for a range of coral reef species.

Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010-11.

BACKGROUND: Globally, coral bleaching has been responsible for a significant decline in both coral cover and diversity over the past two decades. During the summer of 2010-11, anomalous large-scale ocean warming induced unprecedented levels of coral bleaching accompanied by substantial storminess across more than 12° of latitude and 1200 kilometers of coastline in Western Australia (WA). METHODOLOGY/PRINCIPAL FINDINGS: Extreme La-Niña conditions caused extensive warming of waters and drove considerable storminess and cyclonic activity across WA from October 2010 to May 2011. Satellite-derived sea surface temperature measurements recorded anomalies of up to 5°C above long-term averages. Benthic surveys quantified the extent of bleaching at 10 locations across four regions from tropical to temperate waters. Bleaching was recorded in all locations across regions and ranged between 17% (±5.5) in the temperate Perth region, to 95% (±3.5) in the Exmouth Gulf of the tropical Ningaloo region. Coincident with high levels of bleaching, three cyclones passed in close proximity to study locations around the time of peak temperatures. Follow-up surveys revealed spatial heterogeneity in coral cover change with four of ten locations recording significant loss of coral cover. Relative decreases ranged between 22%-83.9% of total coral cover, with the greatest losses in the Exmouth Gulf. CONCLUSIONS/SIGNIFICANCE: The anomalous thermal stress of 2010-11 induced mass bleaching of corals along central and southern WA coral reefs. Significant coral bleaching was observed at multiple locations across the tropical-temperate divide spanning more than 1200 km of coastline. Resultant spatially patchy loss of coral cover under widespread and high levels of bleaching and cyclonic activity, suggests a degree of resilience for WA coral communities. However, the spatial extent of bleaching casts some doubt over hypotheses suggesting that future impacts to coral reefs under forecast warming regimes may in part be mitigated by southern thermal refugia.

Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience.

Coral reefs are in decline worldwide, and marine reserve networks have been advocated as a powerful management tool for maximizing the resilience of coral communities to an increasing variety, number, and severity of disturbances. However, the effective design of reserves must account for the spatial scales of larval dispersal that affect the demography of communities over ecological time frames. Ecologically relevant distances of dispersal were inferred from DNA microsatellite data in a broadcast-spawning (Acropora tenuis) and a brooding (Seriatopora hystrix) coral at isolated reef systems off northwest Australia. Congruent with expectations based on life histories, levels of genetic subdivision among populations were markedly higher in the brooder than in the broadcast spawner. Additionally, significant subdivision for both species between systems (>100 km), and between (>10 km) or within reefs (<10 km) within systems, indicated that many reefs or reef patches are demographically independent. There was also a clear distinction in the scale of genetic structure between the different systems; at the more geographically complex of the systems, a much finer scale structure was detected in both species. This suggested that the hydrodynamics associated with these complex reefs restrict distances regularly traveled by larvae. The primary implication is that short-term recovery of these coral communities after severe disturbance requires the input of larvae from viable communities kilometers to a few tens of kilometers away. Therefore, to be self-sustaining, we suggest that coral reef protected areas need to be large enough to encompass these routine dispersal distances. Further, to facilitate recovery from severe disturbances, protected areas need to be replicated over these spatial scales. However, specific designs also need to account for size, complexity, and isolation of reefs, which will either restrict or enhance dispersal within this range.