Climate change impacts on coral reefs: Synergies with local effects,possibilities for acclimation,and management implications

Most reviews concerning the impact of climate change on coral reefs discuss independent effects of warming or ocean acidification. However, the interactions between these, and between these and direct local stressors are less well addressed. This review underlines that coral bleaching, acidification, and diseases are expected to interact synergistically, and will negatively influence survival, growth, reproduction, larval development, settlement, and post-settlement development of corals. Interactions with local stress factors such as pollution, sedimentation, and overfishing are further expected to compound effects of climate change.     

A demographic approach to monitoring the health of coral reefs

Inshore coral reefs adjacent to the wet tropics in North Queensland, Australia, are regularly exposed to flood plumes from coastal river systems. Changes in the nature of these plumes have been linked to the declining health of coral reefs in the region. The effect of flood plumes on the health of inshore corals was investigated by quantifying aspects of the demography of populations of corymbose and digitate Acropora at three groups of Island reefs along a gradient of exposure and decreasing water quality (High Island >Frankland's >Fitzroy). The size-structures of colonies, the rates of sexual recruitment, and the growth and survival of juveniles, all varied among the Island reefs. Juvenile and adult sized colonies were far more abundant at the Fitzroy Island reefs, than at the High or Frankland Island reefs that were more exposed to flood plumes. Additionally, there were up to eight times as many sexual recruits at the Fitzroy Island reefs, compared with the High Island reefs. However, the rates of growth and survival of the juvenile sized corals at the Fitzroy Island reefs were lower than at the more exposed reefs. The comparatively low abundance of adult corals at the exposed reefs is most likely due to their histories of disturbance from crown-of-thorns and coral bleaching, but the lack of subsequent recovery due to their low levels of larval recruitment. If a stock-recruitment relationship is typical for these groups of reefs, then the low rates of recruitment may be linked to the low density of adult colonies. Alternately, direct or indirect effects of chronic exposure to poor water quality may have resulted in less suitable substrata for larval settlement. We discuss these results and provide examples of how information about population structure and dynamics can be used in simple matrix models to quantify the current and future health of populations of corals under various scenarios.     

Macroalgae in the coral reefs of Eilat (Gulf of Aqaba, Red Sea) as a possible indicator of reef degradation

The current state of health of the coral reefs in the northern Gulf of Aqaba (Red Sea), notably the Eilat reefs, is under debate regarding both their exact condition and the causes of degradation. A dearth of earlier data and unequivocal reliable indices are the major problems hinder a clear understanding of the reef state. Our research objective was to examine coral-algal dynamics as a potential cause and an indication of reef degradation. The community structure of stony corals and algae along the northern Gulf of Aqaba reveal non-seasonal turf algae dominancy in the shallow Eilat reefs (up to 72%), while the proximate Aqaba reefs present negligible turf cover (<6%). We believe that turf dominancy can indicate degradation in these reefs, based on the reduction in essential reef components followed by proliferation of perennial turf algae. Our findings provide further evidence for the severe state of the Eilat coral reefs.     

Modern microbialites and their environmental significance, Meiji reef atoll, Nansha (Spratly) Islands, South China Sea

Meiji (Mischief) coral atoll, in Nansha (Spratly) Islands, South China Sea, consists of an annular reef rim surrounding a central lagoon. On the atoll rim there are either protuberant 'motu' (small coral patch reefs on the rim of atoll) islets or lower sandy cays that contain modern microbialite deposits on the corals in pinnacles and surrounding bottoms of the atoll. Microbialites, including villiform, hairy, and thin spine growth forms, as well as gelatinous masses, mats and encrustation, developed on coral colonies and atoll rim sediments between 0 and 15 m deep-water settings. The microbialites were produced by natural populations of filamentous cyanobacteria and grew on (1) bulbous corals together with Acropora sp., (2) on massive colonies of Galaxea fascicularis, (3) on dead Montipora digitata, and (4) on dead Acropora teres, some hairy microbialite growing around broken coral branches. This study demonstrates that microbial carbonates are developed in coral reefs of South China Sea and indicates that microbial processes may be important in the construction of modern reef systems. The results have significance in the determination of nature and composition in microorganisms implied in the formation ancient microbialites, and permit evaluation of the importance of microbial deposits in mo-dern coral reefs and of 'microbialites' in biogeochemical cycles of modern coral reef systems. The re-sults also provide evidence of modern analogues for ancient microbialites in shallow-water settings, and combine with sedimentological studies of ancient microbialites to understand their controls.     

Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia

The threats of wide-scale coral bleaching and reef demise associated with anthropogenic climate change are widely known. Here, the additional role of poor water quality in lowering the thermal tolerance (i.e. bleaching ‘resistance’) of symbiotic reef corals is considered. In particular, a quantitative linkage is established between terrestrially-sourced dissolved inorganic nitrogen (DIN) loading and the upper thermal bleaching thresholds of inshore reefs on the Great Barrier Reef, Australia. Significantly, this biophysical linkage provides concrete evidence for the oft-expressed belief that improved coral reef management will increase the regional-scale survival prospects of corals reefs to global climate change. Indeed, for inshore reef areas with a high runoff exposure risk, it is shown that the potential benefit of this ‘local’ management imperative is equivalent to ∼2.0-2.5 °C in relation to the upper thermal bleaching limit; though in this case, a potentially cost-prohibitive reduction in end-of-river DIN of >50-80% would be required. An integrated socio-economic modelling framework is outlined that will assist future efforts to understand (optimise) the alternate tradeoffs that the water quality/coral bleaching linkage presents.     

Impact of sea-level rise and coral mortality on the wave dynamics and wave forces on barrier reefs

A one-dimensional wave model was used to investigate the reef top wave dynamics across a large suite of idealized reef-lagoon profiles, representing barrier coral reef systems under different sea-level rise (SLR) scenarios. The modeling shows that the impacts of SLR vary spatially and are strongly influenced by the bathymetry of the reef and coral type. A complex response occurs for the wave orbital velocity and forces on corals, such that the changes in the wave dynamics vary reef by reef. Different wave loading regimes on massive and branching corals also leads to contrasting impacts from SLR. For many reef bathymetries, wave orbital velocities increase with SLR and cyclonic wave forces are reduced for certain coral species. These changes may be beneficial to coral health and colony resilience and imply that predicting SLR impacts on coral reefs requires careful consideration of the reef bathymetry and the mix of coral species.     

Identification of bacteria-derived urease in the coral gastric cavity

Nitrogen cycle is critical to maintain a healthy coral reef ecosystem. Urea can provide a source of nitrogen for coral holobiont and is important for coral calcification through degradation by urease. Despite the involvement of coral-associated bacteria in nitrogen fixation, nitrification and denitrification are well recognized, to what extend urea degradation by bacteria contributing to the urea utilization by coral holobiont remains to be investigated. In this study, we demonstrate that the urea utilization is a common feature of Halomonas spp. that is a dominant genus in cultivable coral-associated bacteria. A urease operon was characterized by genome sequencing and gene knock-out technique in Halomonas meridiana SCSIO 43005, isolated from the gastric cavity of healthy scleractinian coral Galaxea fascicularis. H. meridiana showed high urease activity which was induced by urea and deletion of the urease operon reduced the capability to use urea as solo nitrogen source. Furthermore,approximately 1/3 coral-associated bacteria in the IMG/M database possess complete urease operons indicating the involvement of bacteria-derived ureases in coral holobiont. These results suggest that urease from coral-associated bacteria might be important player in the nitrogen cycling of coral reefs.     

Introductory perspective on the COREF Project

Abstract Coral reefs are tropic to subtropic, coastal ecosystems comprising very diverse organisms. Late Quaternary reef deposits are fossil archives of environmental, tectonic and eustatic variations that can be used to reconstruct the paleoclimatic and paleoceanographic history of the tropic surface oceans. Reefs located at the latitudinal limits of coral‐reef ecosystems (i.e. those at coral‐reef fronts) are particularly sensitive to environmental changes – especially those associated with glacial–interglacial changes in climate and sealevel. We propose a land and ocean scientific drilling campaign in the Ryukyu Islands (the Ryukyus) in the northwestern Pacific Ocean to investigate the dynamic response of the corals and coral‐reef ecosystems in this region to Late Quaternary climate and sealevel change. Such a drilling campaign, which we call the COREF (coral‐reef front) Project, will allow the following three major questions to be evaluated: (i) What are the nature, magnitude and driving mechanisms of coral‐reef front migration in the Ryukyus? (ii) What is the ecosystem response of coral reefs in the Ryukyus to Quaternary climate changes? (iii) What is the role of coral reefs in the global carbon cycle? Subsidiary objectives include (i) the timing of coral‐reef initiation in the Ryukyus and its causes; (ii) the position of the Kuroshio current during glacial periods and its effects on coral‐reef formation; and (iii) early carbonate diagenetic responses as a function of compounded variations in climate, eustacy and depositional mineralogies (subtropic aragonitic to warm‐temperate calcitic). The geographic, climatic and oceanographic settings of the Ryukyu Islands provide an ideal natural laboratory to address each of these research questions.     

Cellular diagnostics and coral health: declining coral health in the Florida Keys

Coral reefs within the Florida Keys are disappearing at an alarming rate. Coral cover in the Florida Keys National Marine Sanctuary declined by 38% from 1996 to 2000. In 2000, populations of Montastraea annularis at four sites near Molasses Reef within the Florida Keys National Marine Sanctuary and one reef within Biscayne National Park were sampled on a quarterly basis. Anecdotal observations showed corals at Alina's Reef in Biscayne National Park appeared healthy in March, but experienced an acute loss of coral cover by August. Cellular Diagnostic analysis indicated that Alina's Reef corals were in distress: they had been afflicted with a severe oxidative damaging and protein-denaturing stress that affected both the corals and their symbiotic zooxanthellae. This condition was associated with a significant xenobiotic detoxification response in both species, reflecting probable chemical contaminant exposure. These results demonstrate that applying a Cellular Diagnostic approach can be effective in helping to identify stress and its underlying causes, providing diagnostic and prognostic biomarkers of coral health.     

Is proximity to land-based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract

Localized declines in coral condition are commonly linked to land-based sources of stressors that influence gradients of water quality, and the distance to sources of stressors is commonly used as a proxy for predicting the vulnerability and future status of reef resources. In this study, we evaluated explicitly whether proximity to shore and connections to coastal bays, two measures of potential land-based sources of disturbance, influence coral community and population structure, and the abundance, distribution, and condition of corals within patch reefs of the Florida Reef Tract. In the Florida Keys, long-term monitoring has documented significant differences in water quality along a cross-shelf gradient. Inshore habitats exhibit higher levels of nutrients (DIN and TP), TOC, turbidity, and light attenuation, and these levels decrease with increasing distance from shore and connections to tidal bays. In clear contrast to these patterns of water quality, corals on inshore patch reefs exhibited significantly higher coral cover, higher growth rates, and lower partial mortality rates than those documented in similar offshore habitats. Coral recruitment rates did not differ between inshore and offshore habitats. Corals on patch reefs closest to shore had well-spread population structures numerically dominated by intermediate to large colonies, while offshore populations showed narrower size-distributions that become increasingly positively skewed. Differences in size-structure of coral populations were attributed to faster growth and lower rates of partial mortality at inshore habitats. While the underlying causes for the favorable condition of inshore coral communities are not yet known, we hypothesize that the ability of corals to shift their trophic mode under adverse environmental conditions may be partly responsible for the observed patterns, as shown in other reef systems. This study, based on data collected from a uniform reef habitat type and coral species with diverse life-history and stress-response patterns from a heavily exploited reef system, showed that proximity to potential sources of stressors may not always prove an adequate proxy for assigning potential risks to reef health, and that hypothesized patterns of coral cover, population size-structure, growth, and mortality are not always directly related to water quality gradients.     

Sewage impacts coral reefs at multiple levels of ecological organization

Against a backdrop of rising sea temperatures and ocean acidification which pose global threats to coral reefs, excess nutrients and turbidity continue to be significant stressors at regional and local scales. Because interventions usually require local data on pollution impacts, we measured ecological responses to sewage discharges in Surin Marine Park, Thailand. Wastewater disposal significantly increased inorganic nutrients and turbidity levels, and this degradation in water quality resulted in substantial ecological shifts in the form of (i) increased macroalgal density and species richness, (ii) lower cover of hard corals, and (iii) significant declines in fish abundance. Thus, the effects of nutrient pollution and turbidity can cascade across several levels of ecological organization to change key properties of the benthos and fish on coral reefs. Maintenance or restoration of ecological reef health requires improved wastewater management and run-off control for reefs to deliver their valuable ecosystems services.     

Coral Transplantation: A Useful Management Tool or Misguided Meddling?

The primary objectives of coral transplantation are to improve reef ‘quality' in terms of live coral cover, biodiversity and topographic complexity. Stated reasons for transplanting corals have been to: (1) accelerate reef recovery after ship groundings, (2) replace corals killed by sewage, thermal effluents or other pollutants, (3) save coral communities or locally rare species threatened by pollution, land reclamation or pier construction, (4) accelerate recovery of reefs after damage by Crown-of-thorns starfish or red tides, (5) aid recovery of reefs following dynamite fishing or coral quarrying, (6) mitigate damage caused by tourists engaged in water-based recreational activities, and (7) enhance the attractiveness of underwater habitat in tourism areas. Whether coral transplantation is likely to be effective from a biological standpoint depends on, among other factors, the water quality, exposure, and degree of substrate consolidation of the receiving area. Whether it is necessary (apart from cases related to reason 3 above), depends primarily on whether the receiving area is failing to recruit naturally.

The potential benefits and dis-benefits of coral transplantation are examined in the light of the results of research on both coral transplantation and recruitment with particular reference to a 4.5 year study in the Maldives. We suggest that in general, unless receiving areas are failing to recruit juvenile corals, natural recovery processes are likely to be sufficient in the medium to long term and that transplantation should be viewed as a tool of last resort. We argue that there has been too much focus on transplanting fast-growing branching corals, which in general naturally recruit well but tend to survive transplantation and re-location relatively poorly, to create short-term increases in live coral cover, at the expense of slow-growing massive corals, which generally survive transplantation well but often recruit slowly. In those cases where transplantation is justified, we advocate that a reversed stance, which focuses on early addition of slowly recruiting massive species to the recovering community, rather than a short-term and sometimes short-lived increase in coral cover, may be more appropriate in many cases.     

Coral bleaching and mortality on artificial and natural reefs in Maldives in 1998, sea surface temperature anomalies and initial recovery

The bleaching and subsequent mortality of branching and massive corals on artificial and natural reefs in the central atolls of Maldives in 1998 are examined with respect to sea surface temperature (SST) anomalies. SST normally peaks in April-May in Maldives. The UK Meteorological Office's Global sea-Ice and SST data set version 2.3 b shows that in 1998 monthly mean SST was 1.2-4 S.D. above the 1950-1999 average during the warmest months (March-June), with the greatest anomaly in May of +2.1 degrees C. Bleaching was first reported in mid-April and was severe from late April to mid-May with some recovery evident by late-May. At least 98% of branching corals (Acroporidae, Pocilloporidae) on artificial structures deployed on a reef flat in 1990 died whereas the majority of massive corals (Poritidae, Faviidae, Agariciidae) survived the bleaching. The pre-bleaching coral community on the artificial reefs in 1994 was 95% branching corals and 5% massives (n = 1589); the post-bleaching community was 3% branching corals and 97% massives (n = 248). Significant reductions in live coral cover were seen at all natural reefs surveyed in the central atolls, with average live coral cover decreasing from about 42% to 2%, a 20-fold reduction from pre-bleaching levels. A survey of recruitment of juvenile corals to the artificial structures 10 months after the bleaching event showed that 67% of recruits (> or = 0.5 cm diameter) were acroporids and pocilloporids and 33% were from massive families (n = 202) compared to 94% and 6%, respectively, in 1990-1994 (n = 3136). Similar post-bleaching dominance of recruitment by branching corals was seen on nearby natural reef (78% acroporids and pocilloporids; 22% massives). A linear regression of April mean monthly SST against year was highly significant (p < 0.001) and suggests a rise of 0.16 degree C per decade. If this trend continues, by 2030 mean April SST in the central atolls will normally exceed the anomaly level at which corals appear there are susceptible to mass bleaching.     

Effects of algal turfs and sediment on coral settlement

Successful settlement and recruitment of corals is critical to the resilience of coral reefs. Given that many degraded reefs are dominated by benthic algae, recovery of coral populations after bleaching and other disturbances requires successful settlement amidst benthic algae. Algal turfs often accumulate sediments, sediments are known to inhibit coral settlement, and reefs with high inputs of terrestrial sediments are often dominated by turfs. We investigated the impacts of two algal turf assemblages, and of sediment deposits, on settlement of the coral Acropora millepora (Ehrenberg). Adding sediment reduced coral settlement, but the effects of different algal turfs varied. In one case, algal turfs inhibited coral settlement, whereas the other turf only inhibited settlement when combined with sediments. These results provide the first direct, experimental evidence of effects of filamentous algal turfs on coral settlement, the variability in those effects, and the potential combined effects of algal turfs and trapped sediments.     

Long-term community changes on a high-latitude coral reef in the Greater St Lucia Wetland Park, South Africa

South African coral reefs are limited in size but, being marginal, provide a model for the study of many of the stresses to which these valuable systems are being subjected globally. Soft coral cover, comprising relatively few species, exceeds that of scleractinians over much of the reefs. The coral communities nevertheless attain a high biodiversity at this latitude on the East African coast. A long-term monitoring programme was initiated in 1993, entailing temperature logging and image analysis of high resolution photographs of fixed quadrats on representative reef. Sea temperatures rose by 0.15 degrees C p.a. at the site up to 2000 but have subsequently been decreasing by 0.07 degrees C p.a. Insignificant bleaching was encountered in the region during the 1998 El Nino Southern Oscillation (ENSO) event, unlike elsewhere in East Africa, but quantifiable bleaching occurred during an extended period of warming in 2000. Peak temperatures on the South African reefs thus appear to have attained the coral bleaching threshold. While this has resulted in relatively little bleaching thus far, the increased temperatures appear to have had a deleterious effect on coral recruitment success as other anthropogenic influences on the reefs are minimal. Recruitment success diminished remarkably up to 2004 but appears again to be improving. Throughout, the corals have also manifested changes in community structure, involving an increase in hard coral cover and reduction in that of soft corals, resulting in a 5.5% drop in overall coral cover. These "silent" effects of temperature increase do not appear to have been reported elsewhere in the literature.     

Photosystem II herbicide pollution in Hong Kong and its potential photosynthetic effects on corals

Photosystem II (PSII) herbicides have been shown to affect the photosynthesis of corals at low, environmentally relevant concentrations. The recent detection of the PSII herbicide Irgarol-1051 in coastal waters of Hong Kong at concentrations above the EC(50) for reduction of photosynthesis of corals prompted further investigation into the extent of PSII herbicide pollution in coral reefs of Hong Kong. Snap-shot and passive samples were taken from coral reef sites and evaluated via HPLC/MS-MS and a novel bioanalytical technique. Low concentrations (less than 10 ng L(-1)) of diuron and atrazine were found at all study sites. Extracts from these samples concentrated by a factor of 10 were found to reduce the photosynthetic yield of zooxanthellae. It appears unlikely that herbicide pollution is a key issue in isolation but may act synergistically with other stressors to reduce the viability of Hong Kong's coral reefs. The study has also demonstrated the feasibility of combining sample extraction techniques with a coral specific bioanalytical technique for a sensitive assessment of risks associated with herbicide exposure in corals.     

Impacts of human activities on coral reef ecosystems of southern Taiwan: a long-term study

In July 2001, the National Museum of Marine Biology and Aquarium, co-sponsored by the Kenting National Park Headquarters and Taiwan's National Science Council, launched a Long-Term Ecological Research (LTER) program to monitor anthropogenic impacts on the ecosystems of southern Taiwan, specifically the coral reefs of Kenting National Park (KNP), which are facing an increasing amount of anthropogenic pressure. We found that the seawater of the reef flats along Nanwan Bay, Taiwan's southernmost embayment, was polluted by sewage discharge at certain monitoring stations. Furthermore, the consequently higher nutrient and suspended sediment levels had led to algal blooms and sediment smothering of shallow water corals at some sampling sites. Finally, our results show that, in addition to this influx of anthropogenically-derived sewage, increasing tourist numbers are correlated with decreasing shallow water coral cover, highlighting the urgency of a more proactive management plan for KNP's coral reefs.     

Environmental impacts of dredging and other sediment disturbances on corals: A review

A review of published literature on the sensitivity of corals to turbidity and sedimentation is presented, with an emphasis on the effects of dredging. The risks and severity of impact from dredging (and other sediment disturbances) on corals are primarily related to the intensity, duration and frequency of exposure to increased turbidity and sedimentation. The sensitivity of a coral reef to dredging impacts and its ability to recover depend on the antecedent ecological conditions of the reef, its resilience and the ambient conditions normally experienced. Effects of sediment stress have so far been investigated in 89 coral species (～10% of all known reef-building corals). Results of these investigations have provided a generic understanding of tolerance levels, response mechanisms, adaptations and threshold levels of corals to the effects of natural and anthropogenic sediment disturbances. Coral polyps undergo stress from high suspended-sediment concentrations and the subsequent effects on light attenuation which affect their algal symbionts. Minimum light requirements of corals range from <1% to as much as 60% of surface irradiance. Reported tolerance limits of coral reef systems for chronic suspended-sediment concentrations range from <10mgL(-1) in pristine offshore reef areas to >100mgL(-1) in marginal nearshore reefs. Some individual coral species can tolerate short-term exposure (days) to suspended-sediment concentrations as high as 1000mgL(-1) while others show mortality after exposure (weeks) to concentrations as low as 30mgL(-1). The duration that corals can survive high turbidities ranges from several days (sensitive species) to at least 5-6weeks (tolerant species). Increased sedimentation can cause smothering and burial of coral polyps, shading, tissue necrosis and population explosions of bacteria in coral mucus. Fine sediments tend to have greater effects on corals than coarse sediments. Turbidity and sedimentation also reduce the recruitment, survival and settlement of coral larvae. Maximum sedimentation rates that can be tolerated by different corals range from <10mgcm(-2)d(-1) to >400mgcm(-2)d(-1). The durations that corals can survive high sedimentation rates range from <24h for sensitive species to a few weeks (>4weeks of high sedimentation or >14days complete burial) for very tolerant species. Hypotheses to explain substantial differences in sensitivity between different coral species include the growth form of coral colonies and the size of the coral polyp or calyx. The validity of these hypotheses was tested on the basis of 77 published studies on the effects of turbidity and sedimentation on 89 coral species. The results of this analysis reveal a significant relationship of coral sensitivity to turbidity and sedimentation with growth form, but not with calyx size. Some of the variation in sensitivities reported in the literature may have been caused by differences in the type and particle size of sediments applied in experiments. The ability of many corals (in varying degrees) to actively reject sediment through polyp inflation, mucus production, ciliary and tentacular action (at considerable energetic cost), as well as intraspecific morphological variation and the mobility of free-living mushroom corals, further contribute to the observed differences. Given the wide range of sensitivity levels among coral species and in baseline water quality conditions among reefs, meaningful criteria to limit the extent and turbidity of dredging plumes and their effects on corals will always require site-specific evaluations, taking into account the species assemblage present at the site and the natural variability of local background turbidity and sedimentation.     

A continuous,real-time water quality monitoring system for the coral reef ecosystems of Nanwan Bay,Southern Taiwan

The coral reef ecosystems of Nanwan Bay, Southern Taiwan are undergoing degradation due to anthropogenic impacts, and as such have resulted in a decline in coral cover. As a first step in preventing the continual degradation of these coral reef environments, it is important to understand how changes in water quality affect these ecosystems on a fine-tuned timescale. To this end, a real-time water quality monitoring system was implemented in Nanwan Bay in 2010. We found that natural events, such as cold water intrusion due to upwelling, tended to elicit temporal shifts in coral spawning between 2010 and 2011. In addition, Degree Heating Weeks (DHWs), a commonly utilized predictor of coral bleaching, were 0.92 and 0.59 in summer 2010 and 2011, respectively. Though this quantity of DHW was below the presumed stress-inducing value for these reefs, a rise in DHWs in the future may stress the resident corals.