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.     

Cushion star (Culcita schmideliana) preys on coral polyps in Gulf of Mannar,Southeast India

Corallivore animals play vital role in coral reef ecology. Predation on corals by other organisms has not been studied properly in the Indian waters. This study reports the first observation of predation by cushion star (Culcita schmideliana) on coral polyps in Gulf of Mannar (GoM), southeast India. During our regular underwater surveys in GoM, C. schmideliana was found preying on hard coral Acropora formosa and soft coral Sarcophyton sp. at a depth of 3 m in Vilanguchalli patch reef. Though C. schmideliana has been sighted often under water, it has not been observed to predate on corals in GoM before. The area where predation was observed has a major population of hard corals (50.21%) besides seagrasses (8.36%) and soft corals (6.11%). Temperature anomalies and the consequent coral bleaching could be the factors making C. schmideliana prefer coral polyps.     

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.     

Effects of disturbance on coral communities: bleaching in Moorea,French Polynesia

This study examines patterns of susceptibility and short-term recovery of corals from bleaching. A mass coral bleaching event began in March, 1991 on reefs in Moorea, French Polynesia and affected corals on the shallow barrier reef and to >20 m depth on the outer forereef slope. There were significant differences in the effect of the bleaching among common coral genera, with Acropora, Montastrea, Montipora, and Pocillopora more affected than Porites, Pavona, leptastrea or Millepora. Individual colonies of the common species of Acropora and Pocillopora were marked and their fate assessed on a subsequent survey in August, 1991 to determine rates of recovery and mortality. Ninety-six percent of Acropora spp. showed some degree of bleaching compared to 76% of Pocillopora spp. From March to August mortality of bleached colonies of Pocillopora was 17%, 38% recovered completely, and many suffered some partial mortality of the tissue. In contrast, 63% of the Acropora spp. died, and about 10% recovered completely. Generally, those colonies with less than 50% of the colony area affected by the bleaching recovered at a higher rate than did those with more severe bleaching. Changes in community composition four months after the event began included a significant decrease only in crustose algae and an increase in cover of filamentous algae, much of which occupied plate-like and branching corals that had died in the bleaching event. Total coral cover and cover of susceptible coral genera had declined, but not significantly, after the event.     

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.     

Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce

Corals are an essential and threatened habitat for a diverse range of reef-associated animals. Episodes of coral bleaching are predicted to increase in frequency and intensity over coming decades, yet the effects of coral-host bleaching on the associated animal communities remain poorly understood. The present study investigated the effects of host-colony bleaching on the obligate coral-dwelling crab, Trapezia cymodoce, during a natural bleaching event in the lagoon of Lizard Island, Australia. Branching corals, which harbour the highest diversity of coral associates, comprised 13% of live coral cover at the study site, with 83% affected by bleaching. Crabs on healthy and bleached colonies of Pocillopora damicornis were monitored over a 5-week period to determine whether coral bleaching affected crab density and movement patterns. All coral colonies initially contained one breeding pair of crabs. There was a significant decline in crab density on bleached corals after 5 weeks, with many corals losing one or both crabs, yet all healthy colonies retained a mating pair. Fecundity of crabs collected from bleached and healthy colonies of P. damicornis was also compared. The size of egg clutches of crabs collected from bleached hosts was 40% smaller than those from healthy hosts, indicating a significant reduction in fecundity. A laboratory experiment on movement patterns found that host-colony bleaching also prompted crabs to emigrate in search of more suitable colonies. Emigrant crabs engaged in aggressive interactions with occupants of healthy hosts, with larger crabs always usurping occupants of a smaller size. Decreased densities and clutch sizes, along with increased competitive interactions, could potentially result in a population decline of these important coral associates with cascading effects on coral health.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.     

Taxonomic patterns of bleaching within a South African coral assemblage

In 1998, the Indian Ocean coral reefs suffered a severe and extensive mass bleaching event. The thermal tolerances of corals were exceeded and their photosynthetic symbionts (zooxanthellae) lost. Mortalities of up to 90% were recorded on the reefs of Seychelles, Maldives, Kenya and Tanzania. South African coral reefs were among the few that largely escaped the 1998 mass bleaching event, but may be threatened in the future if global warming increases. This study assessed the extent of coral bleaching and partial recovery at Sodwana Bay, South Africa during 2000 and 2001. Bleaching levels in this study varied over the course of a year, which suggested that seasonally varying parameters such as sea temperature were the most likely cause of bleaching. Bleaching levels were highest at the shallowest site. However, these bleaching levels were very low in comparison with those of reefs elsewhere in the Indian Ocean. The greater volume of water over the relatively deeper reefs of Sodwana Bay may have protected the reefs from severe bleaching. Field measurements on the three reefs indicated that, although the reefs at Sodwana Bay are still healthy, bleaching increased from <1% in 1998 to 5–10% in 2002. Bleaching occurred in 26 coral genera. The Alcyonacea were highly susceptible to bleaching, especially Sarcophyton sp. Among the hard corals, Montipora spp. were the species most susceptible to bleaching. The sensitivity of these genera to early and slight increases in temperature suggests that they can forewarn of a possible greater bleaching event. In contrast, the coral genera Turbinaria and Stylophora were most resistant to bleaching.     

Chronic parrotfish grazing impedes coral recovery after bleaching

Coral bleaching, in which corals become visibly pale and typically lose their endosymbiotic zooxanthellae (Symbiodinium spp.), increasingly threatens coral reefs worldwide. While the proximal environmental triggers of bleaching are reasonably well understood, considerably less is known concerning physiological and ecological factors that might exacerbate coral bleaching or delay recovery. We report a bleaching event in Belize during September 2004 in which Montastraea spp. corals that had been previously grazed by corallivorous parrotfishes showed a persistent reduction in symbiont density compared to intact colonies. Additionally, grazed corals exhibited greater diversity in the genetic composition of their symbiont communities, changing from uniform ITS2 type C7 Symbiodinium prior to bleaching to mixed assemblages of Symbiodinium types post-bleaching. These results suggest that chronic predation may exacerbate the influence of environmental stressors and, by altering the coral-zooxanthellae symbiosis, such abiotic-biotic interactions may contribute to spatial variation in bleaching processes.     

Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals

Background

Coral reefs worldwide are in decline. Much of the mortality can be attributed to coral bleaching (loss of the coral''s intracellular photosynthetic algal symbiont) associated with global warming. How corals will respond to increasing oceanic temperatures has been an area of extensive study and debate. Recovery after a bleaching event is dependent on regaining symbionts, but the source of repopulating symbionts is poorly understood. Possibilities include recovery from the proliferation of endogenous symbionts or recovery by uptake of exogenous stress-tolerant symbionts.

Methodology/Principal Findings

To test one of these possibilities, the ability of corals to acquire exogenous symbionts, bleached colonies of Porites divaricata were exposed to symbiont types not normally found within this coral and symbiont acquisition was monitored. After three weeks exposure to exogenous symbionts, these novel symbionts were detected in some of the recovering corals, providing the first experimental evidence that scleractinian corals are capable of temporarily acquiring symbionts from the water column after bleaching. However, the acquisition was transient, indicating that the new symbioses were unstable. Only those symbiont types present before bleaching were stable upon recovery, demonstrating that recovery was from the resident in situ symbiont populations.

Conclusions/Significance

These findings suggest that some corals do not have the ability to adjust to climate warming by acquiring and maintaining exogenous, more stress-tolerant symbionts. This has serious ramifications for the success of coral reefs and surrounding ecosystems and suggests that unless actions are taken to reverse it, climate change will lead to decreases in biodiversity and a loss of coral reefs.     

Predicted disappearance of coral-reef ramparts: a direct result of major ecological disturbances

Two coral cays near La Parguera, Puerto Rico, have large, exposed coral ramparts composed almost entirely of loose pieces of elkhorn coral Acropora palmata (88% of horizontal transects, 98% of vertical transects). The total volume of elkhorn coral in the ramparts of the two cays was estimated at 3600 and 12 800 m³. The present volume of living elkhorn coral on these two reefs was estimated at 7 and 14 m³ and previous volumes at 11 000 and 34 900 m³. White-band disease was found on 8.5% of living elkhorn colonies. Lang’s boring sponge Cliona langae covered 10.8% of the total transect area, overgrowing both dead and living corals. White-band disease and coral-reef bleaching have drastically reduced the populations of elkhorn coral, thus, skeletal coral materials to replenish the plate ramparts are severely reduced, disrupting the process of forming and maintaining these coral reef ramparts. We predict that the next series of major storms striking these prominent cay ramparts will remove them. These disappearances will represent a quick, obvious and permanent consequence of global disturbances. Loss of cay ramparts will modify the environments on and around Atlantic coral reefs. Ramparts may be similarly lost from Indo-Pacific reefs. The lack of any other indisputable definitive indicators of long-term, major disturbances on coral reefs makes the distinct loss of coral-reef ramparts an important physical sign.     

Severity of the 1998 and 2005 bleaching events in Venezuela, southern Caribbean

This study describes the severity of the 2005 bleaching event at 15 reef sites across Venezuela and compares the 1998 and 2005 bleaching events at one of them. During August and September 2005, bleached corals were first observed on oceanic reefs rather than coastal reefs, affecting 1 to 4% of coral colonies in the community (3 reef sites, n = 736 colonies). At that time, however, no bleached corals were recorded along the eastern coast of Venezuela, an area of seasonal upwelling (3 reefs, n = 181 colonies). On coastal reefs, bleaching started in October but highest levels were reached in November 2005 and January 2006, when 16% of corals were affected among a wide range of taxa (e.g. scleractinians, octocorals, Millepora and zoanthids). In the Acropora habitats of Los Roques (an oceanic reef),no bleached was recorded in 2005 (four sites,n = 643 colonies). At Cayo Sombrero, a coastal reef site, bleaching was less severe in 1998 than in 2005 (9% of the coral colonies involving 2 species vs. 26% involving 23 species, respectively). Our results indicate that bleaching was more severe in 2005 than in 1998 on Venezuelan reefs; however, no mass mortality was observed in either of these two events.     

Caribbean massive corals not recovering from repeated thermal stress events during 2005–2013

Massive coral bleaching events associated with high sea surface temperatures are forecast to become more frequent and severe in the future due to climate change. Monitoring colony recovery from bleaching disturbances over multiyear time frames is important for improving predictions of future coral community changes. However, there are currently few multiyear studies describing long‐term outcomes for coral colonies following acute bleaching events. We recorded colony pigmentation and size for bleached and unbleached groups of co‐located conspecifics of three major reef‐building scleractinian corals (Orbicella franksi, Siderastrea siderea, and Stephanocoenia michelini; n = 198 total) in Bocas del Toro, Panama, during the major 2005 bleaching event and then monitored pigmentation status and changes live tissue colony size for 8 years (2005–2013). Corals that were bleached in 2005 demonstrated markedly different response trajectories compared to unbleached colony groups, with extensive live tissue loss for bleached corals of all species following bleaching, with mean live tissue losses per colony 9 months postbleaching of 26.2% (±5.4 SE) for O. franksi, 35.7% (±4.7 SE) for S. michelini, and 11.2% (±3.9 SE) for S. siderea. Two species, O. franksi and S. michelini, later recovered to net positive growth, which continued until a second thermal stress event in 2010. Following this event, all species again lost tissue, with previously unbleached colony species groups experiencing greater declines than conspecific sample groups, which were previously bleached, indicating a possible positive acclimative response. However, despite this beneficial effect for previously bleached corals, all groups experienced substantial net tissue loss between 2005 and 2013, indicating that many important Caribbean reef‐building corals will likely suffer continued tissue loss and may be unable to maintain current benthic coverage when faced with future thermal stress forecast for the region, even with potential benefits from bleaching‐related acclimation.     

The effect of species and colony size on the bleaching response of reef-building corals in the Florida Keys during the 2005 mass bleaching event

Understanding the variation in coral bleaching response is necessary for making accurate predictions of population changes and the future state of reefs in a climate of increasing thermal stress events. Individual coral colonies, belonging to inshore patch reef communities of the Florida Keys, were followed through the 2005 mass bleaching event. Overall, coral bleaching patterns followed an index of accumulated thermal stress more closely than in situ temperature measurements. Eight coral species (Colpophyllia natans, Diploria strigosa, Montastraea cavernosa, M. faveolata, Porites astreoides, P. porites, Siderastrea siderea, and Stephanocoenia intersepta), representing >90% of the coral colonies studied, experienced intense levels of bleaching, but responses varied. Bleaching differed significantly among species: Colpophyllia natans and Diploria strigosa were most susceptible to thermal stress, while Stephanocoenia intersepta was the most tolerant. For colonies of C. natans, M. faveolata, and S. siderea, larger colonies experienced more extensive bleaching than smaller colonies. The inshore patch reef communities of the Florida Keys have historically been dominated by large colonies of Montastraea sp. and Colpophyllia natans. These results provide evidence that colony-level differences can affect bleaching susceptibility in this habitat and suggest that the impact of future thermal stress events may be biased toward larger colonies of dominant reef-building species. Predicted increases in the frequency of mass bleaching and subsequent mortality may therefore result in significant structural shifts of these ecologically important communities.     

Wave exposure shapes reef community composition and recovery trajectories at a remote coral atoll

In a time of unprecedented ecological change, understanding natural biophysical relationships between reef resilience and physical drivers is of increasing importance. This study evaluates how wave forcing structures coral reef benthic community composition and recovery trajectories after the major 2015/2016 bleaching event in the remote Chagos Archipelago, Indian Ocean. Benthic cover and substrate rugosity were quantified from digital imagery at 23 fore reef sites around a small coral atoll (Salomon) in 2020 and compared to data from a similar survey in 2006 and opportunistic surveys in intermediate years. Cluster analysis and principal component analysis show strong separation of community composition between exposed (modelled wave exposure > 1000 J m⁻³) and sheltered sites (< 1000 J m⁻³) in 2020. This difference is driven by relatively high cover of Porites sp., other massive corals, encrusting corals, soft corals, rubble and dead table corals at sheltered sites versus high cover of pavement and sponges at exposed sites. Total coral cover and rugosity were also higher at sheltered sites. Adding data from previous years shows benthic community shifts from distinct exposure-driven assemblages and high live coral cover in 2006 towards bare pavement, dead Acropora tables and rubble after the 2015/2016 bleaching event. The subsequent recovery trajectories at sheltered and exposed sites are surprisingly parallel and lead communities towards their respective pre-bleaching communities. These results demonstrate that in the absence of human stressors, community patterns on fore reefs are strongly controlled by wave exposure, even during and after widespread coral loss from bleaching events.

     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Climate‐change refugia in the sheltered bays of Palau: analogs of future reefs

Coral bleaching and mortality are predicted to increase as climate change‐induced thermal‐stress events become more frequent. Although many studies document coral bleaching and mortality patterns, few studies have examined deviations from the expected positive relationships among thermal stress, coral bleaching, and coral mortality. This study examined the response of >30,000 coral colonies at 80 sites in Palau, during a regional thermal‐stress event in 2010. We sought to determine the spatial and taxonomic nature of bleaching and examine whether any habitats were comparatively resistant to thermal stress. Bleaching was most severe in the northwestern lagoon, in accordance with satellite‐derived maximum temperatures and anomalous temperatures above the long‐term averages. Pocillopora populations suffered the most extensive bleaching and the highest mortality. However, in the bays where temperatures were higher than elsewhere, bleaching and mortality were low. The coral‐community composition, constant exposure to high temperatures, and high vertical attenuation of light caused by naturally high suspended particulate matter buffered the corals in bays from the 2010 regional thermal‐stress event. Yet, nearshore reefs are also most vulnerable to land‐use change. Therefore, nearshore reefs should be given high conservation status because they provide refugia for coral populations as the oceans continue to warm.     

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.     

Augmented coral reef monitoring using a stationary reef monitoring system

Coral reef monitoring is a reliable tool to assess the effect of climate change as corals are sensitive to increases in water temperatures between 30 °C and 35 °C resulting in bleaching - a whitening process when the corals lose their color and the reefs begin to die. Existing satellite-based monitoring products facilitate coral bleaching monitoring over large spatial scales, but their use in predicting local scale stress that influences the bleaching severity across reefs is limited. In this paper, we describe a Stationary Reef Monitoring System (SRMS) that monitors the time evolution of coral reefs through the photography of nearby coral clusters. Simultaneously, the SRMS measures and records environmental parameters such as temperature, solar irradiance (PAR), and salinity in the waters surrounding the coral colonies. When deployed in the sea, the SRMS detected a 0.1–0.4 °C variability in temperature between the in situ and satellite datasets. The SRMS uses color photography along with quantitative data on environmental parameters to monitor the health of corals and eliminates the need for physical/visual verification of coral health by a diver. By this approach, one can determine the stress thresholds of corals and identify the vulnerable and resilient reefs so as to prioritize conservation efforts.