Structure of Caribbean coral reef communities across a large gradient of fish biomass

The collapse of Caribbean coral reefs has been attributed in part to historic overfishing, but whether fish assemblages can recover and how such recovery might affect the benthic reef community has not been tested across appropriate scales. We surveyed the biomass of reef communities across a range in fish abundance from 14 to 593 g m⁻², a gradient exceeding that of any previously reported for coral reefs. Increased fish biomass was correlated with an increased proportion of apex predators, which were abundant only inside large marine reserves. Increased herbivorous fish biomass was correlated with a decrease in fleshy algal biomass but corals have not yet recovered.     

Downscaled projections of Caribbean coral bleaching that can inform conservation planning

Projections of climate change impacts on coral reefs produced at the coarse resolution (~1°) of Global Climate Models (GCMs) have informed debate but have not helped target local management actions. Here, projections of the onset of annual coral bleaching conditions in the Caribbean under Representative Concentration Pathway (RCP) 8.5 are produced using an ensemble of 33 Coupled Model Intercomparison Project phase‐5 models and via dynamical and statistical downscaling. A high‐resolution (~11 km) regional ocean model (MOM4.1) is used for the dynamical downscaling. For statistical downscaling, sea surface temperature (SST) means and annual cycles in all the GCMs are replaced with observed data from the ~4‐km NOAA Pathfinder SST dataset. Spatial patterns in all three projections are broadly similar; the average year for the onset of annual severe bleaching is 2040–2043 for all projections. However, downscaled projections show many locations where the onset of annual severe bleaching (ASB) varies 10 or more years within a single GCM grid cell. Managers in locations where this applies (e.g., Florida, Turks and Caicos, Puerto Rico, and the Dominican Republic, among others) can identify locations that represent relative albeit temporary refugia. Both downscaled projections are different for the Bahamas compared to the GCM projections. The dynamically downscaled projections suggest an earlier onset of ASB linked to projected changes in regional currents, a feature not resolved in GCMs. This result demonstrates the value of dynamical downscaling for this application and means statistically downscaled projections have to be interpreted with caution. However, aside from west of Andros Island, the projections for the two types of downscaling are mostly aligned; projected onset of ASB is within ±10 years for 72% of the reef locations.     

Reduced carbon emissions and fishing pressure are both necessary for equatorial coral reefs to keep up with rising seas

A rapid increase in sea-level rise is generating vertical accommodation space on modern coral reefs. Yet increases in sea-surface temperatures (SSTs) are reducing the capacity of coral reefs to keep up with sea-level rise. We use ensemble species distribution models of four coral species (Porites rus, Porites lobata, Acropora hyacinthus and Acropora digitifera) to gauge potential geographic differences in gross carbonate production. Net carbonate production was estimated by considering erosional rates of ocean acidification, increasing cyclone intensity, local pollution, fishing pressure and the projected burdens of increases in SSTs (under Representative Concentration Pathways (RCPs) 4.5, 6.0 and 8.5) through to the year 2100. Our models predict that only 4 ± 0.1% (~60 000 km²) of Indo-Pacific coral reefs are projected to keep up with sea-level rise by the year 2100 under RCP 8.5 – most of which will be located near the Equator. However, with drastic reductions in emissions (under RCPs 4.5 and 6.0 Wm⁻²), we predict that 15 ± 0.3% (~250 000 km²) (under RCP 4.5 Wm⁻²) and 12 ± 0.7% (~200 000 km²) (under RCP 6.0 Wm⁻²) of Indo-Pacific coral reefs, have the potential to keep up with sea-level rise by the year 2100. Yet the burdens of fishing pressure and its cascading effects are projected to be responsible for substantial reef erosion, nearly halving the number of reefs able to keep up with sea-level rise. If action is taken immediately and emissions are drastically reduced to RCPs 4.5 or 6.0 Wm⁻², and reef management reduces the burdens of local pollution and fishing pressure, then our model predicts that 21–27% (~350 000–470 000 km²) of Indo-Pacific coral reefs – most of which will be located near the Equator – would have the potential to keep up with sea-level rise by the year 2100.     

A coral reef refuge in the Red Sea

The stability and persistence of coral reefs in the decades to come is uncertain due to global warming and repeated bleaching events that will lead to reduced resilience of these ecological and socio‐economically important ecosystems. Identifying key refugia is potentially important for future conservation actions. We suggest that the Gulf of Aqaba (GoA) (Red Sea) may serve as a reef refugium due to a unique suite of environmental conditions. Our hypothesis is based on experimental detection of an exceptionally high bleaching threshold of northern Red Sea corals and on the potential dispersal of coral planulae larvae through a selective thermal barrier estimated using an ocean model. We propose that millennia of natural selection in the form of a thermal barrier at the southernmost end of the Red Sea have selected coral genotypes that are less susceptible to thermal stress in the northern Red Sea, delaying bleaching events in the GoA by at least a century.     

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.     

Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs

Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high‐latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high‐latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long‐term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst‐case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up‐to‐date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.     

Ocean acidification and warming will lower coral reef resilience

Ocean warming and acidification from increasing levels of atmospheric CO₂ represent major global threats to coral reefs, and are in many regions exacerbated by local‐scale disturbances such as overfishing and nutrient enrichment. Our understanding of global threats and local‐scale disturbances on reefs is growing, but their relative contribution to reef resilience and vulnerability in the future is unclear. Here, we analyse quantitatively how different combinations of CO₂ and fishing pressure on herbivores will affect the ecological resilience of a simplified benthic reef community, as defined by its capacity to maintain and recover to coral‐dominated states. We use a dynamic community model integrated with the growth and mortality responses for branching corals (Acropora) and fleshy macroalgae (Lobophora). We operationalize the resilience framework by parameterizing the response function for coral growth (calcification) by ocean acidification and warming, coral bleaching and mortality by warming, macroalgal mortality by herbivore grazing and macroalgal growth via nutrient loading. The model was run for changes in sea surface temperature and water chemistry predicted by the rise in atmospheric CO₂ projected from the IPCC's fossil‐fuel intensive A1FI scenario during this century. Results demonstrated that severe acidification and warming alone can lower reef resilience (via impairment of coral growth and increased coral mortality) even under high grazing intensity and low nutrients. Further, the threshold at which herbivore overfishing (reduced grazing) leads to a coral–algal phase shift was lowered by acidification and warming. These analyses support two important conclusions: Firstly, reefs already subjected to herbivore overfishing and nutrification are likely to be more vulnerable to increasing CO₂. Secondly, under CO₂ regimes above 450–500 ppm, management of local‐scale disturbances will become critical to keeping reefs within an Acropora‐rich domain.     

Microsatellite loci isolated from the Caribbean coral,Montastraea annularis

We report the isolation and characterization of seven microsatellite loci from the Caribbean reef‐building coral, Montastraea annularis. All loci are polymorphic with allele numbers ranging from five to 31 and observed heterozygosities from 0.17 to 0.89. These loci can be used in assessing gene flow patterns and diversity of this stony coral species both for local coral reef management purposes as well as for elucidating population connectivity within the greater Caribbean basin. These markers should also be applicable to other species of Montastraea and for resolving taxonomic relationships within the M. annularis species complex.     

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.     

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching

Biological feedbacks generated through patterns of disturbance are vital for sustaining ecosystem states. Recent ocean warming and thermal anomalies have caused pantropical episodes of coral bleaching, which has led to widespread coral mortality and a range of subsequent effects on coral reef communities. Although the response of many reef‐associated fishes to major disturbance events on coral reefs is negative (e.g., reduced abundance and condition), parrotfishes show strong feedbacks after disturbance to living reef structure manifesting as increases in abundance. However, the mechanisms underlying this response are poorly understood. Using biochronological reconstructions of annual otolith (ear stone) growth from two ocean basins, we tested whether parrotfish growth was enhanced following bleaching‐related coral mortality, thus providing an organismal mechanism for demographic changes in populations. Both major feeding guilds of parrotfishes (scrapers and excavators) exhibited enhanced growth of individuals after bleaching that was decoupled from expected thermal performance, a pattern that was not evident in other reef fish taxa from the same environment. These results provide evidence for a more nuanced ecological feedback system—one where disturbance plays a key role in mediating parrotfish–benthos interactions. By influencing the biology of assemblages, disturbance can thereby stimulate change in parrotfish grazing intensity and ultimately reef geomorphology over time. This feedback cycle operated historically at within‐reef scales; however, our results demonstrate that the scale, magnitude, and severity of recent thermal events are entraining the biological responses of disparate communities to respond in synchrony. This may fundamentally alter feedbacks in the relationships between parrotfishes and reef systems.     

High‐resolution imaging sheds new light on a multi‐tier symbiotic partnership between a “walking” solitary coral,a sipunculan,and a bivalve from East Africa

Marine symbioses are integral to the persistence of ecosystem functioning in coral reefs. Solitary corals of the species Heteropsammia cochlea and Heterocyathus aequicostatus have been observed to live in symbiosis with the sipunculan worm Aspidosiphon muelleri muelleri, which inhabits a cavity within the coral, in Zanzibar (Tanzania). The symbiosis of these photosymbiotic corals enables the coral holobiont to move, in fine to coarse unconsolidated substrata, a process termed as “walking.” This allows the coral to escape sediment cover in turbid conditions which is crucial for these light‐dependent species. An additional commensalistic symbiosis of this coral‐worm holobiont is found between the Aspidosiphon worm and the cryptoendolithic bivalve Jousseaumiella sp., which resides within the cavity of the coral skeleton. To understand the morphological alterations caused by these symbioses, interspecific relationships, with respect to the carbonate structures between these three organisms, are documented using high‐resolution imaging techniques (scanning electron microscopy and µCT scanning). Documenting multi‐layered symbioses can shed light on how morphological plasticity interacts with environmental conditions to contribute to species persistence.     

Global change and coral reefs: impacts on reefs, economies and human cultures

Coral reefs have reconstituted themselves after previous large sea-level variations, and climate changes. For the past 6000 years of unusually stable sea-level, reefs have grown without serious interruptions. During recent decades, however, new stresses threaten localized devastation of many reefs. A new period of global climate change is occurring, stimulated by anthropogenic increases in greenhouse gases. Coral reefs will cope well with predicted sea-level rises of 4.5 cm per decade, but reef islands will not. Higher sea levels will provide corals with greater room for growth across reef flats, but there are no foreseeable mechanisms for reef island growth to keep pace with sea-level rise, therefore many low islands may ultimately become uninhabitable. Climate change will introduce localized variations in weather patterns, but changes to individual reefs cannot be predicted. Reefs on average should cope well with regional climate change, as they have coped with similar previous fluctuations. Air temperature increases of 0.2–0.3 °C/decade will induce slower increases in sea-surface temperatures, which may cause localized, or regional increases in coral bleaching. Changes in rainfall will impact on reefs near land masses. Likewise, increased storms and variations in El Nino Southern Oscillation (ENSO) may stress some reefs, but not others. The greatest impact of climate change will be a synergistic enhancement of direct anthropogenic stresses (excessive sediment and pollution from the land; over-fishing, especially via destructive methods; mining of coral rock and sand; and engineering modifications), which currently cause most damage to coral reefs. Many of the world's reefs have been degraded and more will be damaged as anthropogenic impacts increase under the ‘demophoric’ increases in population (demos) and economic (phoric) activity. This biotic and habitat loss will result in severe economic and social losses. Reefs, however, have considerable recovery powers and losses can be minimized by effective management of direct human impacts and reducing indirect threats of global climate change.     

Paris Agreement could prevent regional mass extinctions of coral species

Coral reef ecosystems are expected to undergo significant declines over the coming decades as oceans become warmer and more acidic. We investigate the environmental tolerances of over 650 Scleractinian coral species based on the conditions found within their present-day ranges and in areas where they are currently absent but could potentially reach via larval dispersal. These “environmental envelopes” and connectivity constraints are then used to develop global forecasts for potential coral species richness under two emission scenarios, representing the Paris Agreement target (“SSP1-2.6”) and high levels of emissions (“SSP5-8.5”). Although we do not directly predict coral mortality or adaptation, the projected changes to environmental suitability suggest considerable declines in coral species richness for the majority of the world's tropical coral reefs, with a net loss in average local richness of 73% (Paris Agreement) to 91% (High Emissions) by 2080–2090 and particularly large declines across sites in the Great Barrier Reef, Coral Sea, Western Indian Ocean, and Caribbean. However, at the regional scale, we find that environmental suitability for the majority of coral species can be largely maintained under the Paris Agreement target, with 0%–30% potential net species lost in most regions (increasing to 50% for the Great Barrier Reef) as opposed to 80%–90% losses under High Emissions. Projections for subtropical areas suggest that range expansion will give rise to coral reefs with low species richness (typically 10–20 coral species per region) and will not meaningfully offset declines in the tropics. This work represents the first global projection of coral species richness under oceanic warming and acidification. Our results highlight the critical importance of mitigating climate change to avoid potentially massive extinctions of coral species.     

The threat to coral reefs from more intense cyclones under climate change

Ocean warming under climate change threatens coral reefs directly, through fatal heat stress to corals and indirectly, by boosting the energy of cyclones that cause coral destruction and loss of associated organisms. Although cyclone frequency is unlikely to rise, cyclone intensity is predicted to increase globally, causing more frequent occurrences of the most destructive cyclones with potentially severe consequences for coral reef ecosystems. While increasing heat stress is considered a pervasive risk to coral reefs, quantitative estimates of threats from cyclone intensification are lacking due to limited data on cyclone impacts to inform projections. Here, using extensive data from Australia's Great Barrier Reef (GBR), we show that increases in cyclone intensity predicted for this century are sufficient to greatly accelerate coral reef degradation. Coral losses on the outer GBR were small, localized and offset by gains on undisturbed reefs for more than a decade, despite numerous cyclones and periods of record heat stress, until three unusually intense cyclones over 5 years drove coral cover to record lows over >1500 km. Ecological damage was particularly severe in the central‐southern region where 68% of coral cover was destroyed over >1000 km, forcing record declines in the species richness and abundance of associated fish communities, with many local extirpations. Four years later, recovery of average coral cover was relatively slow and there were further declines in fish species richness and abundance. Slow recovery of community diversity appears likely from such a degraded starting point. Highly unusual characteristics of two of the cyclones, aside from high intensity, inflated the extent of severe ecological damage that would more typically have occurred over 100s of km. Modelling published predictions of future cyclone activity, the likelihood of more intense cyclones within time frames of coral recovery by mid‐century poses a global threat to coral reefs and dependent societies.     

Mass coral bleaching causes biotic homogenization of reef fish assemblages

Global climate change is altering community composition across many ecosystems due to nonrandom species turnover, typically characterized by the loss of specialist species and increasing similarity of biological communities across spatial scales. As anthropogenic disturbances continue to alter species composition globally, there is a growing need to identify how species responses influence the establishment of distinct assemblages, such that management actions may be appropriately assigned. Here, we use trait‐based analyses to compare temporal changes in five complementary indices of reef fish assemblage structure among six taxonomically distinct coral reef habitats exposed to a system‐wide thermal stress event. Our results revealed increased taxonomic and functional similarity of previously distinct reef fish assemblages following mass coral bleaching, with changes characterized by subtle, but significant, shifts toward predominance of small‐bodied, algal‐farming habitat generalists. Furthermore, while the taxonomic or functional richness of fish assemblages did not change across all habitats, an increase in functional originality indicated an overall loss of functional redundancy. We also found that prebleaching coral composition better predicted changes in fish assemblage structure than the magnitude of coral loss. These results emphasize how measures of alpha diversity can mask important changes in the structure and functioning of ecosystems as assemblages reorganize. Our findings also highlight the role of coral species composition in structuring communities and influencing the diversity of responses of reef fishes to disturbance. As new coral species configurations emerge, their desirability will hinge upon the composition of associated species and their capacity to maintain key ecological processes in spite of ongoing disturbances.     

Marine pollution and coral reefs

Coral reefs are exposed to many anthropogenic stresses increasing in impact and range, both on local and regional scales. The main ones discussed here are nutrient enrichment, sewage disposal, sedimentation, oil-related pollution, metals and thermal pollution. The stress comprising the main topic of this article, eutrophication, is examined from the point of view of its physiological and ecological mechanisms of action, on a number of levels. Nutrient enrichment can introduce an imbalance in the exchange of nutrients between the zooxanthellae and the host coral, it reduces light penetration to the reef due to nutrient- stimulated phytoplankton growth, and, most harmful of all, may bring about proliferation of seaweeds. The latter rapidly outgrow, smother and eventually replace, the slow-growing coral reef, adapted to cope with the low nutrient concentrations typical in tropical seas.
Eutrophication seldom takes place by itself. Sewage disposal invariably results in nutrient enrichment, but it also enriches the water with organic matter which stimulates proliferation of oxygen-consuming microbes. These may kill corals and other reef organisms, either directly by anoxia, or by related hydrogen sulfide production. Increased sediment deposition is in many cases associated with other human activities leading to eutrophication, such as deforestation and topsoil erosion.
Realistically achievable goals to ensure conservation, and in some instances, rehabilitation of coral reefs are listed.     

Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs

Around the globe, coral reefs and other marine ecosystems are increasingly overfished. Conventionally, studies of fishing impacts have focused on the population size and dynamics of targeted stocks rather than the broader ecosystem-wide effects of harvesting. Using parrotfishes as an example, we show how coral reef fish populations respond to escalating fishing pressure across the Indian and Pacific Oceans. Based on these fish abundance data, we infer the potential impact on four key functional roles performed by parrotfishes. Rates of bioerosion and coral predation are highly sensitive to human activity, whereas grazing and sediment removal are resilient to fishing. Our results offer new insights into the vulnerability and resilience of coral reefs to the ever-growing human footprint. The depletion of fishes causes differential decline of key ecosystem functions, radically changing the dynamics of coral reefs and setting the stage for future ecological surprises.     

Research challenges to improve the management and conservation of subtropical reefs to tackle climate change threats

This paper reports on a workshop conducted in Australia in 2010, entitled ‘Management, Conservation, and Scientific Challenges on Subtropical Reefs under Climate Change’. The workshop brought together 26 experts actively involved in the science and management of subtropical reefs. Its primary aim was to identify the areas of research that need to be most urgently addressed to improve the decision‐making framework for managers of subtropical reefs. The main findings of the workshop were a sustainable subtropical reefs declaration that highlights seven research priorities for subtropical reefs. These are to (i) conduct research and management activities across local government, state and bioregion borders; (ii) understand natural variability of environmental conditions; (iii) quantify socio‐economic factors and ecosystem services; (iv) benchmark cross‐realm connectivity; (v) know marine population connectivity; (vi) habitat mapping and ecological research; and (v) determine refugia. These findings are hoped to form a basis for focussing research efforts, leveraging funds and assisting managers with allocation of resources.