Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high‐resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown‐of‐thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km², predicting a mean annual coral loss of ?0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner‐shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no‐take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.     

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.     

Population collapse dynamics in Acropora downingi,an Arabian/Persian Gulf ecosystem‐engineering coral,linked to rising temperature

As in the tropical Atlantic, Acropora populations in the southern Persian/Arabian Gulf plummeted within two decades after having been ecosystem engineers on most wave‐exposed reefs since the Pleistocene. Since 1996/1998 live coral cover in the Gulf declined by over 90% in many areas, primarily due to bleaching and diseases caused by rising temperatures. In the formerly dominant table‐coral species A. downingi, population dynamics corresponding to disturbance regimes was quantified in three transition matrices (lower disturbance pre‐1996; moderate disturbance from 1998 to 2010 and 2013 to 2017, disturbed in 1996/1998, 2010/11/12, 2017). Increased disturbance frequency and severity caused progressive reduction in coral size, cover, and population fecundity. Small size‐classes were bolstered more by partial colony mortality than sexual recruitment. Some large corals had a size refuge and resisted die‐back but were also lost with increasing disturbance. Matrix and biophysical larval flow models suggested one metapopulation. Southern, Arabian, populations could be connected to northern, Iranian, populations but this connectivity was lost under assumptions of pelagic larval duration at rising temperatures shortened to a third. Then, the metapopulation disintegrated into isolated populations. Connectivity required to avoid extinctions increased exponentially with disturbance frequency and correlation of disturbances across the metapopulation. Populations became unsustainable at eight disturbances in 15 years, when even highest theoretical recruitment no longer compensated mortality. This lethal disturbance frequency was 3‐fold that of the moderately disturbed monitoring period and 4‐fold of the preceding low‐disturbance period—suggesting ongoing shortening of the disturbance‐free period. Observed population collapse and environmental changes in the Gulf suggest that A. downingi is heading toward at least functional extinction mainly due to increasingly frequent temperature‐induced mortality events, clearly linked to climate change.     

Larvae of the coral eating crown‐of‐thorns starfish,Acanthaster planci in a warmer‐high CO2 ocean

Outbreaks of crown‐of‐thorns starfish (COTS), Acanthaster planci, contribute to major declines of coral reef ecosystems throughout the Indo‐Pacific. As the oceans warm and decrease in pH due to increased anthropogenic CO₂ production_, coral reefs are also susceptible to bleaching, disease and reduced calcification. The impacts of ocean acidification and warming may be exacerbated by COTS predation, but it is not known how this major predator will fare in a changing ocean. Because larval success is a key driver of population outbreaks, we investigated the sensitivities of larval A. planci to increased temperature (2–4 °C above ambient) and acidification (0.3–0.5 pH units below ambient) in flow‐through cross‐factorial experiments (3 temperature × 3 pH/pCO₂ levels). There was no effect of increased temperature or acidification on fertilization or very early development. Larvae reared in the optimal temperature (28 °C) were the largest across all pH treatments. Development to advanced larva was negatively affected by the high temperature treatment (30 °C) and by both experimental pH levels (pH 7.6, 7.8). Thus, planktonic life stages of A. planci may be negatively impacted by near‐future global change. Increased temperature and reduced pH had an additive negative effect on reducing larval size. The 30 °C treatment exceeded larval tolerance regardless of pH. As 30 °C sea surface temperatures may become the norm in low latitude tropical regions, poleward migration of A. planci may be expected as they follow optimal isotherms. In the absence of acclimation or adaptation, declines in low latitude populations may occur. Poleward migration will be facilitated by strong western boundary currents, with possible negative flow‐on effects on high latitude coral reefs. The contrasting responses of the larvae of A. planci and those of its coral prey to ocean acidification and warming are considered in context with potential future change in tropical reef ecosystems.     

Habitat dynamics,marine reserve status,and the decline and recovery of coral reef fish communities

Severe climatic disturbance events often have major impacts on coral reef communities, generating cycles of decline and recovery, and in some extreme cases, community‐level phase shifts from coral‐ to algal‐dominated states. Benthic habitat changes directly affect reef fish communities, with low coral cover usually associated with low fish diversity and abundance. No‐take marine reserves (NTRs) are widely advocated for conserving biodiversity and enhancing the sustainability of exploited fish populations. Numerous studies have documented positive ecological and socio‐economic benefits of NTRs; however, the ability of NTRs to ameliorate the effects of acute disturbances on coral reefs has seldom been investigated. Here, we test these factors by tracking the dynamics of benthic and fish communities, including the important fishery species, coral trout (Plectropomus spp.), over 8 years in both NTRs and fished areas in the Keppel Island group, Great Barrier Reef, Australia. Two major disturbances impacted the reefs during the monitoring period, a coral bleaching event in 2006 and a freshwater flood plume in 2011. Both disturbances generated significant declines in coral cover and habitat complexity, with subsequent declines in fish abundance and diversity, and pronounced shifts in fish assemblage structure. Coral trout density also declined in response to the loss of live coral, however, the approximately 2:1 density ratio between NTRs and fished zones was maintained over time. The only post‐disturbance refuges for coral trout spawning stocks were within the NTRs that escaped the worst effects of the disturbances. Although NTRs had little discernible effect on the temporal dynamics of benthic or fish communities, it was evident that the post‐disturbance refuges for coral trout spawning stocks within some NTRs may be critically important to regional‐scale population persistence and recovery.     

Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching

Nutrient loading is one of the strongest drivers of marine habitat degradation. Yet, the link between nutrients and disease epizootics in marine organisms is often tenuous and supported only by correlative data. Here, we present experimental evidence that chronic nutrient exposure leads to increases in both disease prevalence and severity and coral bleaching in scleractinian corals, the major habitat‐forming organisms in tropical reefs. Over 3 years, from June 2009 to June 2012, we continuously exposed areas of a coral reef to elevated levels of nitrogen and phosphorus. At the termination of the enrichment, we surveyed over 1200 scleractinian corals for signs of disease or bleaching. Siderastrea siderea corals within enrichment plots had a twofold increase in both the prevalence and severity of disease compared with corals in unenriched control plots. In addition, elevated nutrient loading increased coral bleaching; Agaricia spp. of corals exposed to nutrients suffered a 3.5‐fold increase in bleaching frequency relative to control corals, providing empirical support for a hypothesized link between nutrient loading and bleaching‐induced coral declines. However, 1 year later, after nutrient enrichment had been terminated for 10 months, there were no differences in coral disease or coral bleaching prevalence between the previously enriched and control treatments. Given that our experimental enrichments were well within the ranges of ambient nutrient concentrations found on many degraded reefs worldwide, these data provide strong empirical support to the idea that coastal nutrient loading is one of the major factors contributing to the increasing levels of both coral disease and coral bleaching. Yet, these data also suggest that simple improvements to water quality may be an effective way to mitigate some coral disease epizootics and the corresponding loss of coral cover in the future.     

Disease outbreaks, bleaching and a cyclone drive changes in coral assemblages on an inshore reef of the Great Barrier Reef

Coral disease is a major threat to the resilience of coral reefs; thus, understanding linkages between disease outbreaks and disturbances predicted to increase with climate change is becoming increasingly important. Coral disease surveys conducted twice yearly between 2008 and 2011 at a turbid inshore reef in the central Great Barrier Reef spanned two disturbance events, a coral bleaching event in 2009 and a severe cyclone (cyclone ‘Yasi’) in 2011. Surveys of coral cover, community structure and disease prevalence throughout this 4-yr study provide a unique opportunity to explore cumulative impacts of disturbance events and disease for inshore coral assemblages. The principal coral disease at the study site was atramentous necrosis (AtN), and it primarily affected the key inshore, reef-building coral Montipora aequituberculata. Other diseases detected were growth anomalies, white syndrome and brown band syndrome. Diseases affected eight coral genera, although Montipora was, by far, the genus mostly affected. The prevalence of AtN followed a clear seasonal pattern, with disease outbreaks occurring only in wet seasons. Mean prevalence of AtN on Montipora spp. (63.8 % ± 3.03) was three- to tenfold greater in the wet season of 2009, which coincided with the 2009 bleaching event, than in other years. Persistent wet season outbreaks of AtN combined with the impacts of bleaching and cyclone events resulted in a 50–80 % proportional decline in total coral cover. The greatest losses of branching and tabular acroporids occurred following the low-salinity-induced bleaching event of 2009, and the greatest losses of laminar montiporids occurred following AtN outbreaks in 2009 and in 2011 following cyclone Yasi. The shift to a less diverse coral assemblage and the concomitant loss of structural complexity are likely to have long-term consequences for associated vertebrate and invertebrate communities on Magnetic Island reefs.     

No-take reserves protect coral reefs from predatory starfish

The crown-of-thorns starfish, Acanthaster planci, is a predator of corals that is a major management issue on coral reefs [1]. It occurs throughout the Indo–Pacific and shows boom–bust population dynamics with low background densities and intermittent outbreaks. Three waves of population outbreaks have affected Australia's Great Barrier Reef (GBR) since the 1960s. The waves of outbreaks appear to start 15°S [2] and progress southward through the central GBR (Figure 1A), causing major losses of living coral on many reefs across a large area and dwarfing losses from other disturbances such as storms or coral bleaching over the same period [3]. Humans can potentially influence starfish population dynamics by exploiting predators, though evidence to date is circumstantial. Extensive surveys in the GBR Marine Park (GBRMP) show that protection from fishing affects the frequency of outbreaks: the relative frequency of outbreaks on reefs that were open to fishing was 3.75 times higher than that on no-take reefs in the mid-shelf region of the GBR, where most outbreaks occur, and seven times greater on open reefs if all reefs were included. Although exploited fishes are unlikely to prey on starfish directly, trophic cascades could favour invertebrates that prey on juvenile starfish.     

Coral population dynamics across consecutive mass mortality events

Annual coral mortality events due to increased atmospheric heat may occur regularly from the middle of the century and are considered apocalyptic for coral reefs. In the Arabian/Persian Gulf, this situation has already occurred and population dynamics of four widespread corals (Acropora downingi, Porites harrisoni, Dipsastrea pallida, Cyphastrea micropthalma) were examined across the first‐ever occurrence of four back‐to‐back mass mortality events (2009–2012). Mortality was driven by diseases in 2009, bleaching and subsequent diseases in 2010/2011/2012. 2009 reduced P. harrisoni cover and size, the other events increasingly reduced overall cover (2009: ?10%; 2010: ?20%; 2011: ?20%; 2012: ?15%) and affected all examined species. Regeneration was only observed after the first disturbance. P. harrisoni and A. downingi severely declined from 2010 due to bleaching and subsequent white syndromes, while D. pallida and P. daedalea declined from 2011 due to bleaching and black‐band disease. C. microphthalma cover was not affected. In all species, most large corals were lost while fission due to partial tissue mortality bolstered small size classes. This general shrinkage led to a decrease of coral cover and a dramatic reduction of fecundity. Transition matrices for disturbed and undisturbed conditions were evaluated as Life Table Response Experiment and showed that C. microphthalma changed the least in size‐class dynamics and fecundity, suggesting they were ‘winners’. In an ordered ‘degradation cascade’, impacts decreased from the most common to the least common species, leading to step‐wise removal of previously dominant species. A potentially permanent shift from high‐ to low‐coral cover with different coral community and size structure can be expected due to the demographic dynamics resultant from the disturbances. Similarities to degradation of other Caribbean and Pacific reefs are discussed. As comparable environmental conditions and mortality patterns must be expected worldwide, demographic collapse of many other coral populations may soon be widespread.     

Ecological analyses to inform management targets for the culling of crown-of-thorns starfish to prevent coral decline

The crown-of-thorns starfish (COTS), Acanthaster cf. solaris, is one of the main contributors to declines in coral cover on the Great Barrier Reef (GBR) and remains one of the major acute disturbances on coral reefs throughout much of the Indo-Pacific. Extensive control programs on the GBR involve manual culling of COTS in the field, and research is needed to inform these management efforts. Data from the Great Barrier Reef Marine Park Authority’s (GBRMPA) COTS control program provide near-real-time CPUE (Catch-Per-Unit-Effort, COTS culled per minute) data ideal for operational decision-making but these must be converted to density estimates before they can be related to ecological status of reefs or incorporated into ecological models. We developed conversions between common COTS field survey methods (i.e. manta tow, SCUBA transect searches) and COTS control program CPUE data using estimates of sightability and detectability. We used a population model and COTS size-structure data from COTS control program culling efforts to estimate that, on average, only 19% of 1-yr-old COTS (1–15 cm) are available to be culled. Finally, we developed a CPUE-COTS density relationship to estimate the threshold levels of COTS that prevent net growth of hard corals. Culling programs should therefore aim to achieve CPUEs below these ecological thresholds in order to effectively promote coral growth and recovery. These ecologically sustainable thresholds of COTS density varied depending on hard coral cover. For example, for 35% fast-growing coral cover, COTS culling needs to continue until CPUE decreases to below 0.05 COTS/min (1 COTS per 20 min) in order to prevent coral decline, whereas if coral cover is higher (80%), then a higher target threshold CPUE of ca. 0.08 COTS/min (ca. 3 COTS per 40 min) may be ecologically sustainable. These estimates underpin the current pest management rules being implemented by the GBRMPA in its COTS control program.

     

Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation

Population outbreaks of the coral-eating crown-of-thorns seastar, Acanthaster planci, continue to kill more coral on Indo-Pacific coral reefs than other disturbances, but the causes of these outbreaks have not been resolved. In this study, we combine (1) results from laboratory experiments where larvae were reared on natural phytoplankton, (2) large-scale and long-term field data of river floods, chlorophyll concentrations and A. planci outbreaks on the Great Barrier Reef (GBR), and (3) results from A. planci—coral population model simulations that investigated the relationship between the frequency of outbreaks and larval food availability. The experiments show that the odds of A. planci larvae completing development increases ~8-fold with every doubling of chlorophyll concentrations up to 3 μg l⁻¹. Field data and the population model show that river floods and regional differences in phytoplankton availability are strongly related to spatial and temporal patterns in A. planci outbreaks on the GBR. The model also shows that, given plausible historic increases in river nutrient loads over the last 200 years, the frequency of A. planci outbreaks on the GBR has likely increased from one in 50–80 years to one every 15 years, and that current coral cover of reefs in the central GBR may be 30–40% of its potential value. This study adds new and strong empirical support to the hypothesis that primary A. planci outbreaks are predominantly controlled by phytoplankton availability.     

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.     

The cumulative impact of annual coral bleaching can turn some coral species winners into losers

Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long‐term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species ‘winners’ into ‘losers’, and can also facilitate acclimation and turn some coral species ‘losers’ into ‘winners’. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long‐term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean.     

Associations between climate stress and coral reef diversity in the western Indian Ocean

Climatic–oceanographic stress and coral reef diversity were mapped in the western Indian Ocean (WIO) in order to determine if there were associations between high diversity coral reefs and regions with low‐to‐moderate climate stress. A multivariate stress model developed to estimate environmental exposure to stress, an empirical index of the coral community's susceptibility to stress, and field data on numbers of fish and corals taxa from 197 WIO sites were overlain to evaluate these associations. Exposure to stress was modeled from satellite data based on nine geophysical–biological oceanographic characteristics known to influence coral bleaching (i.e. temperature, light, and current variables). The environmental stress model and the coral community's susceptibility index were moderately correlated (r=?0.51) with southern and eastern parts of the WIO identified as areas with low environmental stress and coral communities with greater dominance of bleaching stress‐sensitive taxa. Numbers of coral and fish taxa were positive and moderately correlated (r=0.47) but high diversity regions for fish were in the north and west while diversity was highest for corals in central regions from Tanzania to northwestern Madagascar. Combining three and four of these variables into composite maps identified a region from southern Kenya to northern Mozambique across to northern–eastern Madagascar and the Mascarene Islands and the Mozambique–South Africa border as areas where low‐moderate environmental exposure overlaps with moderate‐high taxonomic diversity. In these areas management efforts aimed at maintaining high‐diversity and intact ecosystems are considered least likely to be undermined by climate disturbances in the near term. Reducing additional human disturbances, such as fishing and pollution, in these areas is expected to improve the chances for their persistence. These reefs are considered a high priority for increased local, national, and international management efforts aimed at establishing coral reef refugia for climate change impacts.     

Spatial and temporal genetic structure of Symbiodinium populations within a common reef‐building coral on the Great Barrier Reef

The dinoflagellate photosymbiont Symbiodinium plays a fundamental role in defining the physiological tolerances of coral holobionts, but little is known about the dynamics of these endosymbiotic populations on coral reefs. Sparse data indicate that Symbiodinium populations show limited spatial connectivity; however, no studies have investigated temporal dynamics for in hospite Symbiodinium populations following significant mortality and recruitment events in coral populations. We investigated the combined influences of spatial isolation and disturbance on the population dynamics of the generalist Symbiodinium type C2 (ITS1 rDNA) hosted by the scleractinian coral Acropora millepora in the central Great Barrier Reef. Using eight microsatellite markers, we genotyped Symbiodinium in a total of 401 coral colonies, which were sampled from seven sites across a 12‐year period including during flood plume–induced coral bleaching. Genetic differentiation of Symbiodinium was greatest within sites, explaining 70–86% of the total genetic variation. An additional 9–27% of variation was explained by significant differentiation of populations among sites separated by 0.4–13 km, which is consistent with low levels of dispersal via water movement and historical disturbance regimes. Sampling year accounted for 6–7% of total genetic variation and was related to significant coral mortality following severe bleaching in 1998 and a cyclone in 2006. Only 3% of the total genetic variation was related to coral bleaching status, reflecting generally small (8%) reductions in allelic diversity within bleached corals. This reduction probably reflected a loss of genotypes in hospite during bleaching, although no site‐wide changes in genetic diversity were observed. Combined, our results indicate the importance of disturbance regimes acting together with limited oceanographic transport to determine the genetic composition of Symbiodinium types within reefs.     

Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef

Coral reefs are increasingly threatened by various disturbances, and a critical challenge is to determine their ability for resistance and resilience. Coral assemblages in Moorea, French Polynesia, have been impacted by multiple disturbances (one cyclone and four bleaching events between 1991 and 2006). The 1991 disturbances caused large declines in coral cover (~51% to ~22%), and subsequent colonization by turf algae (~16% to ~49%), but this phase-shift from coral to algal dominance has not persisted. Instead, the composition of the coral community changed following the disturbances, notably favoring an increased cover of Porites, reduced cover of Montipora and Pocillopora, and a full return of Acropora; in this form, the reef returned to pre-disturbance coral cover within a decade. Thus, this coral assemblage is characterized by resilience in terms of coral cover, but plasticity in terms of community composition.     

Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss

While it is generally assumed that specialist species are more vulnerable to disturbance compared with generalist counterparts, this has rarely been tested in coastal marine ecosystems, which are increasingly subject to a wide range of natural and anthropogenic disturbances. Habitat specialists are expected to be more vulnerable to habitat loss because habitat availability exerts a greater limitation on population size, but it is also possible that specialist species may escape effects of disturbance if they use habitats that are generally resilient to disturbance. This study quantified specificity in use of different coral species by six coral‐dwelling damselfishes (Chromis viridis, C. atripectoralis, Dascyllus aruanus, D. reticulatus, Pomacentrus moluccensis, and P. amboinensis) and related habitat specialization to proportional declines in their abundance following habitat degradation caused by outbreaks of the coral eating starfish, Acanthaster planci. The coral species preferred by most coral‐dwelling damselfishes (e.g., Pocillopora damicornis) were frequently consumed by coral eating crown‐of‐thorns starfish, such that highly specialized damselfishes were disproportionately affected by coral depletion, despite using a narrower range of different coral species. Vulnerability of damselfishes to this disturbance was strongly correlated with both their reliance on corals and their degree of habitat specialization. Ongoing disturbances to coral reef ecosystems are expected, therefore, to lead to fundamental shifts in the community structure of fish communities where generalists are favored over highly specialist species.     

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.