George Roff

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.

Global disparity in the resilience of coral reefs

The great sensitivity of coral reefs to climate change has raised concern over their resilience. An emerging body of resilience theory stems largely from research carried out in a single biogeographic region; the Caribbean. Such geographic bias raises the question of transferability of concepts among regions. In this article, we identify factors that might predispose the Caribbean to its low resilience, including faster rates of macroalgal growth, higher rates of algal recruitment, basin-wide iron-enrichment of algal growth from aeolian dust, a lack of acroporid corals, lower herbivore biomass and missing groups of herbivores. Although mechanisms of resilience are likely to be ubiquitous, our analysis suggests that Indo-Pacific reefs would have to be heavily degraded to exhibit bistability or undergo coral-macroalgal phase shifts.

Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement.

The inshore reefs of the Great Barrier Reef (GBR) have undergone significant declines in water quality following European settlement (approx. 1870 AD). However, direct evidence of impacts on coral assemblages is limited by a lack of historical baselines prior to the onset of modern monitoring programmes in the early 1980s. Through palaeoecological reconstructions, we report a previously undocumented historical collapse of Acropora assemblages at Pelorus Island (central GBR). High-precision U-series dating of dead Acropora fragments indicates that this collapse occurred between 1920 and 1955, with few dates obtained after 1980. Prior to this event, our results indicate remarkable long-term stability in coral community structure over centennial scales. We suggest that chronic increases in sediment flux and nutrient loading following European settlement acted as the ultimate cause for the lack of recovery of Acropora assemblages following a series of acute disturbance events (SST anomalies, cyclones and flood events). Evidence for major degradation in reef condition owing to human impacts prior to modern ecological surveys indicates that current monitoring of inshore reefs on the GBR may be predicated on a significantly shifted baseline.

Regulation of bacterial communities through antimicrobial activity by the coral holobiont

Interactions between corals and associated bacteria and amongst these bacterial groups are likely to play a key role in coral health. However, the complexity of these interactions is poorly understood. We investigated the functional role of specific coral-associated bacteria in maintaining microbial communities on the coral Acropora millepora (Ehrenberg 1834) and the ability of coral mucus to support or inhibit bacterial growth. Culture-independent techniques were used to assess bacterial community structures whilst bacterial culture was employed to assess intra- and inter-specific antimicrobial activities of bacteria. Members of Pseudoalteromonas and ribotypes closely related to Vibrio coralliilyticus displayed potent antimicrobial activity against a range of other cultured isolates and grew readily on detached coral mucus. Although such bacterial ribotypes would be expected to have a competitive advantage, they were rare or absent on intact and healthy coral colonies growing in situ (analysed using denaturing gradient gel electrophoresis and 16S rRNA gene sequencing). The most abundant bacterial ribotypes found on healthy corals were Gammaproteobacteria, previously defined as type A coral associates. Our results indicate that this group of bacteria and specific members of the Alphaproteobacteria described here as ‘type B associates’ may be important functional groups for coral health. We suggest that bacterial communities on coral are kept in check by a combination of host-derived and microbial interactions and that the type A associates in particular may play a key role in maintaining stability of microbial communities on healthy coral colonies.

Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica

Coral bleaching occurs when the endosymbiosis between corals and their symbionts disintegrates during stress. Mass coral bleaching events have increased over the past 20 years and are directly correlated with periods of warm sea temperatures. However, some hypotheses have suggested that reef-building corals bleach due to infection by bacterial pathogens. The ‘Bacterial Bleaching’ hypothesis is based on laboratory studies of the Mediterranean invading coral, Oculina patagonica, and has further generated conclusions such as the coral probiotic hypothesis and coral hologenome theory of evolution. We aimed to investigate the natural microbial ecology of O. patagonica during the annual bleaching using fluorescence in situ hybridization to map bacterial populations within the coral tissue layers, and found that the coral bleaches on the temperate rocky reefs of the Israeli coastline without the presence of Vibrio shiloi or bacterial penetration of its tissue layers. Bacterial communities were found associated with the endolithic layer of bleached coral regions, and a community dominance shift from an apparent cyanobacterial-dominated endolithic layer to an algal-dominated layer was found in bleached coral samples. While bacterial communities certainly play important roles in coral stasis and health, we suggest environmental stressors, such as those documented with reef-building corals, are the primary triggers leading to bleaching of O. patagonica and suggest that bacterial involvement in patterns of bleaching is that of opportunistic colonization.

The Ecological Role of Sharks on Coral Reefs.

Sharks are considered the apex predator of coral reefs, but the consequences of their global depletion are uncertain. Here we explore the ecological roles of sharks on coral reefs and, conversely, the importance of reefs for sharks. We find that most reef-associated shark species do not act as apex predators but instead function as mesopredators along with a diverse group of reef fish. While sharks perform important direct and indirect ecological roles, the evidence to support hypothesised shark-driven trophic cascades that benefit corals is weak and equivocal. Coral reefs provide some functional benefits to sharks, but sharks do not appear to favour healthier reef environments. Restoring populations of sharks is important and can yet deliver ecological surprise.

Anticipative management for coral reef ecosystem services in the 21st century

Under projections of global climate change and other stressors, significant changes in the ecology, structure and function of coral reefs are predicted. Current management strategies tend to look to the past to set goals, focusing on halting declines and restoring baseline conditions. Here, we explore a complementary approach to decision making that is based on the anticipation of future changes in ecosystem state, function and services. Reviewing the existing literature and utilizing a scenario planning approach, we explore how the structure of coral reef communities might change in the future in response to global climate change and overfishing. We incorporate uncertainties in our predictions by considering heterogeneity in reef types in relation to structural complexity and primary productivity. We examine 14 ecosystem services provided by reefs, and rate their sensitivity to a range of future scenarios and management options. Our predictions suggest that the efficacy of management is highly dependent on biophysical characteristics and reef state. Reserves are currently widely used and are predicted to remain effective for reefs with high structural complexity. However, when complexity is lost, maximizing service provision requires a broader portfolio of management approaches, including the provision of artificial complexity, coral restoration, fish aggregation devices and herbivore management. Increased use of such management tools will require capacity building and technique refinement and we therefore conclude that diversification of our management toolbox should be considered urgently to prepare for the challenges of managing reefs into the 21st century.

Increased Prevalence of Ubiquitous Ascomycetes in an Acropoid Coral (Acropora formosa) Exhibiting Symptoms of Brown Band Syndrome and Skeletal Eroding Band Disease

ABSTRACT The prevalence of coral-associated fungi was four times higher in diseased Acropora formosa colonies than in healthy colonies. Since taxonomically related fungal species were isolated from diseased and healthy colonies, we suggest that their association with coral may be constitutive but that their abundance is dependent on coral health.

Linking Demographic Processes of Juvenile Corals to Benthic Recovery Trajectories in Two Common Reef Habitats

Tropical reefs are dynamic ecosystems that host diverse coral assemblages with different life-history strategies. Here, we quantified how juvenile (<50 mm) coral demographics influenced benthic coral structure in reef flat and reef slope habitats on the southern Great Barrier Reef, Australia. Permanent plots and settlement tiles were monitored every six months for three years in each habitat. These environments exhibited profound differences: the reef slope was characterised by 95% less macroalgal cover, and twice the amount of available settlement substrata and rates of coral settlement than the reef flat. Consequently, post-settlement coral survival in the reef slope was substantially higher than that of the reef flat, and resulted in a rapid increase in coral cover from 7 to 31% in 2.5 years. In contrast, coral cover on the reef flat remained low (~10%), whereas macroalgal cover increased from 23 to 45%. A positive stock-recruitment relationship was found in brooding corals in both habitats; however, brooding corals were not directly responsible for the observed changes in coral cover. Rather, the rapid increase on the reef slope resulted from high abundances of broadcast spawning Acropora recruits. Incorporating our results into transition matrix models demonstrated that most corals escape mortality once they exceed 50 mm, but for smaller corals mortality in brooders was double those of spawners (i.e. acroporids and massive corals). For corals on the reef flat, sensitivity analysis demonstrated that growth and mortality of larger juveniles (21–50 mm) highly influenced population dynamics; whereas the recruitment, growth and mortality of smaller corals (<20 mm) had the highest influence on reef slope population dynamics. Our results provide insight into the population dynamics and recovery trajectories in disparate reef habitats, and highlight the importance of acroporid recruitment in driving rapid increases in coral cover following large-scale perturbation in reef slope environments.

Characterizing the ecological trade‐offs throughout the early ontogeny of coral recruitment

Drivers of recruitment in sessile marine organisms are often poorly understood, due to the rapidly changing requirements experienced during early ontogeny. The complex suite of physical, biological, and ecological interactions beginning at larval settlement involves a series of trade-offs that influence recruitment success. For example, while cryptic settlement within complex microhabitats is a commonly observed phenomenon in sessile marine organisms, it is unclear whether trade-offs between competition in cryptic refuges and predation on exposed surfaces leads to higher recruitment.To explore the trade-offs during the early ontogeny of scleractinian corals, we combined field observations with laboratory and field experiments to develop a mechanistic understanding of coral recruitment success. Multiple experiments conducted over 15 months in Palau (Micronesia) allowed a mechanistic approach to study the individual factors involved in recruitment: settlement behavior, growth, competition, and predation, as functions of microhabitat and ontogeny. We finally developed and tested a predictive recruitment model with the broader aim of testing whether our empirical insights explained patterns of coral recruitment and quantifying the relative importance of each trade-off.Coral settlement was higher in crevices than exposed microhabitats, but post-settlement bottlenecks differed markedly in the presence (uncaged) and absence (caged) of predators. Incidental predation by herbivores on exposed surfaces at early post-settlement (<3 mm) stages and targeted predation by corallivores at late post-settlement (3–10 mm) stages exceeded competition in crevices as major drivers of mortality. In contrast, when fish were excluded, competition with macroalgae and heterotrophic invertebrates intensified mortality, particularly in crevices. As a result, post-settlement trade-offs were reversed, and recruitment was more than twofold higher on exposed surfaces than crevices. Once post-settlement bottlenecks were overcome, survival was higher on exposed surfaces regardless of fish exclusion. However, maximum recruitment occurred in crevices of uncaged treatments, being ninefold higher than caged treatments. Overall, we characterize recruitment success throughout the earliest life-history stages of corals and uncover some intriguing trade-offs between growth, competition and predation, highlighting how these change and even reverse during ontogeny and under alternate disturbance regimes.