Delayed coral recovery in a warming ocean

Climate change threatens coral reefs across the world. Intense bleaching has caused dramatic coral mortality in many tropical regions in recent decades, but less obvious chronic effects of temperature and other stressors can be equally threatening to the long‐term persistence of diverse coral‐dominated reef systems. Coral reefs persist if coral recovery rates equal or exceed average rates of mortality. While mortality from acute destructive events is often obvious and easy to measure, estimating recovery rates and investigating the factors that influence them requires long‐term commitment. Coastal development is increasing in many regions, and sea surface temperatures are also rising. The resulting chronic stresses have predictable, adverse effects on coral recovery, but the lack of consistent long‐term data sets has prevented measurement of how much coral recovery rates are actually changing. Using long‐term monitoring data from 47 reefs spread over 10 degrees of latitude on Australia's Great Barrier Reef (GBR), we used a modified Gompertz equation to estimate coral recovery rates following disturbance. We compared coral recovery rates in two periods: 7 years before and 7 years after an acute and widespread heat stress event on the GBR in 2002. From 2003 to 2009, there were few acute disturbances in the region, allowing us to attribute the observed shortfall in coral recovery rates to residual effects of acute heat stress plus other chronic stressors. Compared with the period before 2002, the recovery of fast‐growing Acroporidae and of “Other” slower growing hard corals slowed after 2002, doubling the time taken for modest levels of recovery. If this persists, recovery times will be increasing at a time when acute disturbances are predicted to become more frequent and intense. Our study supports the need for management actions to protect reefs from locally generated stresses, as well as urgent global action to mitigate climate change.     

Turbid reefs moderate coral bleaching under climate‐related temperature stress

Thermal‐stress events that cause coral bleaching and mortality have recently increased in frequency and severity. Yet few studies have explored conditions that moderate coral bleaching. Given that high light and high ocean temperature together cause coral bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal‐stress events than corals at other localities. We analyzed coral bleaching, temperature, and turbidity data from 3,694 sites worldwide with a Bayesian model and found that K_d490, a measurement positively related to turbidity, between 0.080 and 0.127 reduced coral bleaching during thermal‐stress events. Approximately 12% of the world's reefs exist within this “moderating turbidity” range, and 30% of reefs that have moderating turbidity are in the Coral Triangle. We suggest that these turbid nearshore environments may provide some refuge through climate change, but these reefs will need high conservation status to sustain them close to dense human populations.     

Larval connectivity across temperature gradients and its potential effect on heat tolerance in coral populations

Coral reefs are increasingly exposed to elevated temperatures that can cause coral bleaching and high levels of mortality of corals and associated organisms. The temperature threshold for coral bleaching depends on the acclimation and adaptation of corals to the local maximum temperature regime. However, because of larval dispersal, coral populations can receive larvae from corals that are adapted to very different temperature regimes. We combine an offline particle tracking routine with output from a high‐resolution physical oceanographic model to investigate whether connectivity of coral larvae between reefs of different thermal regimes could alter the thermal stress threshold of corals. Our results suggest that larval transport between reefs of widely varying temperatures is likely in the Coral Triangle and that accounting for this connectivity may be important in bleaching predictions. This has important implications in conservation planning, because connectivity may allow some reefs to have an inherited heat tolerance that is higher or lower than predicted based on local conditions alone.     

Coral reef resilience to thermal stress in the Eastern Tropical Pacific

Coral reefs worldwide are threatened by thermal stress caused by climate change. Especially devastating periods of coral loss frequently occur during El Niño‐Southern Oscillation (ENSO) events originating in the Eastern Tropical Pacific (ETP). El Niño‐induced thermal stress is considered the primary threat to ETP coral reefs. An increase in the frequency and intensity of ENSO events predicted in the coming decades threatens a pan‐tropical collapse of coral reefs. During the 1982–1983 El Niño, most reefs in the Galapagos Islands collapsed, and many more in the region were decimated by massive coral bleaching and mortality. However, after repeated thermal stress disturbances, such as those caused by the 1997–1998 El Niño, ETP corals reefs have demonstrated regional persistence and resiliency. Using a 44 year dataset (1970–2014) of live coral cover from the ETP, we assess whether ETP reefs exhibit the same decline as seen globally for other reefs. Also, we compare the ETP live coral cover rate of change with data from the maximum Degree Heating Weeks experienced by these reefs to assess the role of thermal stress on coral reef survival. We find that during the period 1970–2014, ETP coral cover exhibited temporary reductions following major ENSO events, but no overall decline. Further, we find that ETP reef recovery patterns allow coral to persist under these El Niño‐stressed conditions, often recovering from these events in 10–15 years. Accumulative heat stress explains 31% of the overall annual rate of change of living coral cover in the ETP. This suggests that ETP coral reefs have adapted to thermal extremes to date, and may have the ability to adapt to near‐term future climate‐change thermal anomalies. These findings for ETP reef resilience may provide general insights for the future of coral reef survival and recovery elsewhere under intensifying El Niño scenarios.     

Interpreting the sign of coral bleaching as friend vs. foe

Coral bleaching is a major concern to researchers, conservationists and the general public worldwide. To date, much of the high profile attention for bleaching has coincided with major environmental impacts and for many the term coral bleaching is synonymously associated with coral mortality (so‐called ‘lethal’ bleaching episodes). While this synonymous association has undoubtedly been key in raising public support, it carries unfair representation: nonlethal bleaching is, and always has been, a phenomenon that effectively occurs regularly in nature as corals acclimatize to regular periodic changes in growth environment (days, seasons etc). In addition, corals can exhibit sublethal bleaching during extreme environmental conditions whereby mortality does not occur and corals can potentially subsequently recover once ambient environmental conditions return. Perhaps not surprisingly it is the frequency and extent of these non and sublethal processes that yield key evidence as to how coral species and reef systems will likely withstand environmental and thus climatic change. Observations of non and sublethal bleaching (and subsequent recovery) are arguably not as readily reported as those of lethal bleaching since (1) the convenient tools used to quantify bleaching yield major ambiguity (and hence high potential for misidentification) as to the severity of bleaching; and (2) lethal bleaching events inevitably receive higher profile (media) attention and so are more readily reported. Under‐representation of non and sublethal bleaching signs may over‐classify the severity of bleaching, under‐estimate the potential resilience of reefs against environmental change, and thus ultimately limit (if not depreciate) the validity and effectiveness of reef management policies and practices. While bleaching induced coral mortality must remain our key concern it must be better placed within the context of bleaching signs that do not result in a long‐term loss of reef viability.     

Century‐scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold

Coral bleaching, during which corals lose their symbiotic dinoflagellates, appears to be increasing in frequency and geographic extent, and is typically associated with abnormally high water temperatures and solar irradiance. A key question in coral reef ecology is whether local stressors reduce the coral thermal tolerance threshold, leading to increased bleaching incidence. Using tree‐ring techniques, we produced master chronologies of growth rates in the dominant reef builder, massive Montastraea faveolata corals, over the past 75–150 years from the Mesoamerican Reef. Our records indicate that the 1998 mass bleaching event was unprecedented in the past century, despite evidence that water temperatures and solar irradiance in the region were as high or higher mid‐century than in more recent decades. We tested the influence on coral extension rate from the interactive effects of human populations and thermal stress, calculated here with degree‐heating‐months (DHM). We find that when the effects of chronic local stressors, represented by human population, are taken into account, recent reductions in extension rate are better explained than when DHM is used as the sole predictor. Therefore, the occurrence of mass bleaching on the Mesoamerican reef in 1998 appears to stem from reduced thermal tolerance due to the synergistic impacts of chronic local stressors.     

The impact of ENSO on coral heat stress in the western equatorial Pacific

The Coral Triangle encompasses an extensive region of coral reefs in the western tropical Pacific with marine resources that support millions of people. As in all other reef regions, coral reefs in the Coral Triangle have been impacted by anomalously high ocean temperature. The vast majority of bleaching observations to date have been associated with the 1998 La Niña phase of ENSO. To understand the significance of ENSO and other climatic oscillations to heat stress in the Coral Triangle, we use a 5‐km resolution Regional Ocean Model System for the Coral Triangle (CT‐ROMS) to study ocean temperature thresholds and variability for the 1960–2007 historical period. Heat‐stress events are more frequent during La Niña events, but occur under all climatic conditions, reflecting an overall warming trend since the 1970s. Mean sea surface temperature (SST) in the region increased an average of ~ 0.1 °C per decade over the time period, but with considerable spatial variability. The spatial patterns of SST and heat stress across the Coral Triangle reflect the complex bathymetry and oceanography. The patterns did not change significantly over time or with shifts in ENSO. Several regions experienced little to no heat stress over the entire period. Of particular interest to marine conservation are regions where there are few records of coral bleaching despite the presence of significant heat stress, such as in the Banda Sea. Although this may be due to under‐reporting of bleaching events, it may also be due to physical factors such as mixing and cloudiness, or biological factors that reduce sensitivity to heat stress.     

Near‐term impacts of coral restoration on target species,coral reef community structure,and ecological processes

The global decline of corals has created an urgent need for effective, science‐based methods to augment coral populations and restore important ecosystem functions. To meet this challenge, the field of coral restoration has rapidly evolved over the past decade. However, despite widespread efforts to outplant corals and monitor survivorship, there is a shortage of information on the effects of coral restoration on reef communities or important ecosystem functions. To fill this knowledge gap, we examined the effects of restoration on three major criteria: diversity, community structure, and ecological processes. We conducted surveys of four restored sites in the Florida Keys ranging in restoration effort (500–2,300 corals outplanted) paired with surveys of nearby, unmanipulated control sites. Coral restoration successfully enhanced coral populations, increasing coral cover 4‐fold, but manifested in limited differences in coral and fish communities. Some restored sites had higher abundance of herbivorous fish, rates of herbivory, or more juvenile‐sized corals, but these effects were limited to individual reefs. Damselfish were consistently more abundant at restored compared to control sites. Despite augmenting target coral populations, 3 years of coral restoration has not facilitated many of the positive feedbacks that help reinforce coral success. In a time of increasingly frequent disturbances, it is urgent we hasten the speed at which reefs recover important ecological processes, such as herbivory and nutrient cycling, that make reefs more resistant and resilient if we are to achieve long‐term restoration success.     

Change in algal symbiont communities after bleaching,not prior heat exposure,increases heat tolerance of reef corals

Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral–algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to ‘bleaching’ (stress‐induced symbiosis breakdown), but stress‐tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32 °C for 10 days), corals hosting only stress‐sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress‐tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was also not observed in C3‐dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress. These findings indicate that increased thermotolerance post‐bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress.     

Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient?

Increased frequency of disturbances and anthropogenic activities are predicted to have a devastating impact on coral reefs that will ultimately change the composition of reef associated fish communities. We reviewed and analysed studies that document the effects of disturbance‐mediated coral loss on coral reef fishes. Meta‐analysis of 17 independent studies revealed that 62% of fish species declined in abundance within 3 years of disturbances that resulted in >10% decline in coral cover. Abundances of species reliant on live coral for food and shelter consistently declined during this time frame, while abundance of some species that feed on invertebrates, algae and/or detritus increased. The response of species, particularly those expected to benefit from the immediate loss of coral, is, however, variable and is attributed to erratic replenishment of stocks, ecological versatility of species and sublethal responses, such as changes in growth, body condition and feeding rates. The diversity of fish communities was found to be negatively and linearly correlated to disturbance‐mediated coral loss. Coral loss >20% typically resulted in a decline in species richness of fish communities, although diversity may initially increase following small declines in coral cover from high coverage. Disturbances that result in an immediate loss of habitat complexity (e.g. severe tropical storms), have a greater impact on fishes from all trophic levels, compared with disturbances that kill corals, but leave the reef framework intact (e.g. coral bleaching and outbreaks of Acanthaster planci). This is most evident among small bodied species and suggests the long‐term consequences of coral loss through coral bleaching and crown‐of‐thorn starfish outbreaks may be much more substantial than the short‐term effects currently documented.     

Gene expression profiles during short‐term heat stress in the red sea coral Stylophora pistillata

During the past several decades, corals worldwide have been affected by severe bleaching events leading to wide‐spread coral mortality triggered by global warming. The symbiotic Red Sea coral Stylophora pistillata from the Gulf of Eilat is considered an opportunistic ‘r’ strategist. It can thrive in relatively unstable environments and is considered a stress‐tolerant species. Here, we used a S. pistillata custom microarray to examine gene expression patterns and cellular pathways during short‐term (13‐day) heat stress. The results allowed us to identify a two‐step reaction to heat stress, which intensified significantly as the temperature was raised to a 32 °C threshold, beyond which, coping strategies failed at 34 °C. We identified potential ‘early warning genes’ and ‘severe heat‐related genes’. Our findings suggest that during short‐term heat stress, S. pistillata may divert cellular energy into mechanisms such as the ER‐unfolded protein response (UPR) and ER‐associated degradation (ERAD) at the expense of growth and biomineralization processes in an effort to survive and subsequently recover from the stress. We suggest a mechanistic theory for the heat stress responses that may explain the success of some species which can thrive under a wider range of temperatures relative to others.     

Global assessment of coral bleaching and required rates of adaptation under climate change

Elevated ocean temperatures can cause coral bleaching, the loss of colour from reef‐building corals because of a breakdown of the symbiosis with the dinoflagellate Symbiodinium. Recent studies have warned that global climate change could increase the frequency of coral bleaching and threaten the long‐term viability of coral reefs. These assertions are based on projecting the coarse output from atmosphere–ocean general circulation models (GCMs) to the local conditions around representative coral reefs. Here, we conduct the first comprehensive global assessment of coral bleaching under climate change by adapting the NOAA Coral Reef Watch bleaching prediction method to the output of a low‐ and high‐climate sensitivity GCM. First, we develop and test algorithms for predicting mass coral bleaching with GCM‐resolution sea surface temperatures for thousands of coral reefs, using a global coral reef map and 1985–2002 bleaching prediction data. We then use the algorithms to determine the frequency of coral bleaching and required thermal adaptation by corals and their endosymbionts under two different emissions scenarios. The results indicate that bleaching could become an annual or biannual event for the vast majority of the world's coral reefs in the next 30–50 years without an increase in thermal tolerance of 0.2–1.0°C per decade. The geographic variability in required thermal adaptation found in each model and emissions scenario suggests that coral reefs in some regions, like Micronesia and western Polynesia, may be particularly vulnerable to climate change. Advances in modelling and monitoring will refine the forecast for individual reefs, but this assessment concludes that the global prognosis is unlikely to change without an accelerated effort to stabilize atmospheric greenhouse gas concentrations.     

Overgrowth and killing of corals by the brown alga Lobophora hederacea (Dictyotales,Phaeophyceae) on healthy reefs in New Caledonia: A new case of the epizoism syndrome

Coral reef degradation is often associated with regime shifts from coral‐ to macroalgal‐dominated reefs. These shifts demonstrate that under certain conditions (e.g. coral mortality, decrease in herbivory, increased nutrients supply) some macroalgae may overgrow corals. The outcome of the competition is dependent on algal aggressiveness and the coral susceptibility. In undisturbed reefs, herbivore grazing is regulating macroalgal cover, thus preventing the latter from overgrowing corals. However, some macroalgae have evolved strategies not only to outcompete corals but also to escape herbivory to some extent, allowing overgrowth of some coral species in undisturbed reefs. Epizoism represents one of those successful strategies, and has been previously documented with red algae, cyanobacteria and Lobophora variegata (Dictyotales, Phaeophyceae). Here we report a new case of epizoism leading to coral mortality, involving a recently described species of Lobophora, L. hederacea, overgrowing the coral Seriatopora caliendrum (Pocilloporidae) in undisturbed reefs in New Caledonia.     

Long‐term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome

Scleractinian corals are assumed to be stenohaline osmoconformers, although they are frequently subjected to variations in seawater salinity due to precipitation, freshwater run‐off and other processes. Observed responses to altered salinity levels include differences in photosynthetic performance, respiration and increased bleaching and mortality of the coral host and its algal symbiont, but a study looking at bacterial community changes is lacking. Here, we exposed the coral Fungia granulosa to strongly increased salinity levels in short‐ and long‐term experiments to disentangle temporal and compartment effects of the coral holobiont (i.e. coral host, symbiotic algae and associated bacteria). Our results show a significant reduction in calcification and photosynthesis, but a stable microbiome after short‐term exposure to high‐salinity levels. By comparison, long‐term exposure yielded unchanged photosynthesis levels and visually healthy coral colonies indicating long‐term acclimation to high‐salinity levels that were accompanied by a major coral microbiome restructuring. Importantly, a bacterium in the family Rhodobacteraceae was succeeded by Pseudomonas veronii as the numerically most abundant taxon. Further, taxonomy‐based functional profiling indicates a shift in the bacterial community towards increased osmolyte production, sulphur oxidation and nitrogen fixation. Our study highlights that bacterial community composition in corals can change within days to weeks under altered environmental conditions, where shifts in the microbiome may enable adjustment of the coral to a more advantageous holobiont composition.     

Nearshore coral growth declining on the Mesoamerican Barrier Reef System

Anthropogenic global change and local stressors are impacting coral growth and survival worldwide, altering the structure and function of coral reef ecosystems. Here, we show that skeletal extension rates of nearshore colonies of two abundant and widespread Caribbean corals (Siderastrea siderea, Pseudodiploria strigosa) declined across the Belize Mesoamerican Barrier Reef System (MBRS) over the past century, while offshore coral conspecifics exhibited relatively stable extension rates over the same temporal interval. This decline has caused nearshore coral extension rates to converge with those of their historically slower growing offshore coral counterparts. For both species, individual mass coral bleaching events were correlated with low rates of skeletal extension within specific reef environments, but no single bleaching event was correlated with low skeletal extension rates across all reef environments. We postulate that the decline in skeletal extension rates for nearshore corals is driven primarily by the combined effects of long‐term ocean warming and increasing exposure to higher levels of land‐based anthropogenic stressors, with acute thermally induced bleaching events playing a lesser role. If these declining trends in skeletal growth of nearshore S. siderea and P. strigosa continue into the future, the structure and function of these critical nearshore MBRS coral reef systems is likely to be severely impaired.     

Boring sponges,an increasing threat for coral reefs affected by bleaching events

Coral bleaching is a stress response of corals induced by a variety of factors, but these events have become more frequent and intense in response to recent climate‐change‐related temperature anomalies. We tested the hypothesis that coral reefs affected by bleaching events are currently heavily infested by boring sponges, which are playing a significant role in the destruction of their physical structure. Seventeen reefs that cover the entire distributional range of corals along the Mexican Pacific coast were studied between 2005/2006, and later between 2009/2010. Most of these coral reefs were previously impacted by bleaching events, which resulted in coral mortalities. Sponge abundance and species richness was used as an indicator of bioerosion, and coral cover was used to describe the present condition of coral reefs. Coral reefs are currently highly invaded (46% of the samples examined) by a very high diversity of boring sponges (20 species); being the coral reef framework the substrate most invaded (56%) followed by the rubbles (45%), and the living colonies (36%). The results also indicated that boring sponges are promoting the dislodgment of live colonies and large fragments from the framework. In summary, the eastern coral reefs affected by bleaching phenomena, mainly provoked by El Niño, present a high diversity and abundance of boring sponges, which are weakening the union of the colony with the reef framework and promoting their dislodgment. These phenomena will probably become even more intense and severe, as temperatures are projected to continue to rise under the scenarios for future climate change, which could place many eastern coral reefs beyond their survival threshold.     

Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals

Reef corals are examples of metazoans that engage in mutualisms with a variety of microorganisms, including dinoflagellates, Bacteria, Archaea, and viruses. The high adaptive capacity of these microbial symbionts can be co‐opted by their coral hosts, and various emergent traits of these associations, such as thermotolerance, are undergoing strong selection due to climate change. This selection may spur the rise of microbial ‘disaster taxa’: opportunistic, cosmopolitan generalists that can proliferate and increase host survivorship following disturbances. Coral bleaching (a stress‐induced loss of dinoflagellates) constitutes one type of catastrophic disturbance for resident symbiont communities, and opens novel patches of host for colonization by microbial disaster taxa. Moreover, the compartmentalization of microbial symbionts within coral polyps reduces their effective population size and thus facilitates the spread of disaster taxa during times of environmental change. These phenomena suggest that, despite widespread loss of coral cover as a result of climate disturbances, the potential spread of resilient microbial disaster taxa in surviving colonies can have important implications for coral reef persistence over the coming decades.     

Density‐dependent effects on initial growth of a branching coral under restoration

Coral reef restoration aims to help threatened coral ecosystems recover from recent severe declines. Here we address whether coral fragments should be out‐planted individually or in larger aggregations. Theory suggests alternative possible outcomes: whereas out‐plants within aggregations might suffer from heightened negative interactions with neighbors (e.g. competition for space), they may alternatively benefit from positive interactions with neighbors (e.g. buffering wave disturbances). On a degraded reef in the Caribbean (St. Croix, USVI), using out‐plants of the critically endangered staghorn coral Acropora cervicornis, we experimentally tested how aggregation density (1–20 out‐planted coral fragments spaced at approximately 5 cm) influenced initial coral growth (over 3 months). Coral growth declined as a function of aggregation size, and out‐plants within larger aggregations had fewer and shorter secondary branches on average, indicative of horizontal competition for space. Our results therefore suggest that wide spacing of individuals will maximize the initial growth of out‐planted branching corals.