Diversity among Macroalgae-Consuming Fishes on Coral Reefs: A Transcontinental Comparison

Despite high diversity and abundance of nominally herbivorous fishes on coral reefs, recent studies indicate that only a small subset of taxa are capable of removing dominant macroalgae once these become established. This limited functional redundancy highlights the potential vulnerability of coral reefs to disturbance and stresses the need to assess the functional role of individual species of herbivores. However, our knowledge of species-specific patterns in macroalgal consumption is limited geographically, and there is a need to determine the extent to which patterns observed in specific reefs can be generalised at larger spatial scales. In this study, video cameras were used to quantify rates of macroalgae consumption by fishes in two coral reefs located at a similar latitude in opposite sides of Australia: the Keppel Islands in the Great Barrier Reef (eastern coast) and Ningaloo Reef (western coast). The community of nominally herbivorous fish was also characterised in both systems to determine whether potential differences in the species observed feeding on macroalgae were related to spatial dissimilarities in herbivore community composition. The total number of species observed biting on the dominant brown alga Sargassum myriocystum differed dramatically among the two systems, with 23 species feeding in Ningaloo, compared with just 8 in the Keppel Islands. Strong differences were also found in the species composition and total biomass of nominally herbivorous fish, which was an order of magnitude higher in Ningaloo. However, despite such marked differences in the diversity, biomass, and community composition of resident herbivorous fishes, Sargassum consumption was dominated by only four species in both systems, with Naso unicornis and Kyphosus vaigiensis consistently emerging as dominant feeders of macroalgae.     

Coral reef mesopredators switch prey,shortening food chains,in response to habitat degradation

Diet specificity is likely to be the key predictor of a predator's vulnerability to changing habitat and prey conditions. Understanding the degree to which predatory coral reef fishes adjust or maintain prey choice, in response to declines in coral cover and changes in prey availability, is critical for predicting how they may respond to reef habitat degradation. Here, we use stable isotope analyses to characterize the trophic structure of predator–prey interactions on coral reefs of the Keppel Island Group on the southern Great Barrier Reef, Australia. These reefs, previously typified by exceptionally high coral cover, have recently lost much of their coral cover due to coral bleaching and frequent inundation by sediment‐laden, freshwater flood plumes associated with increased rainfall patterns. Long‐term monitoring of these reefs demonstrates that, as coral cover declined, there has been a decrease in prey biomass, and a shift in dominant prey species from pelagic plankton‐feeding damselfishes to territorial benthic algal‐feeding damselfishes, resulting in differences in the principal carbon pathways in the food web. Using isotopes, we tested whether this changing prey availability could be detected in the diet of a mesopredator (coral grouper, Plectropomus maculatus). The δ¹³C signature in grouper tissue in the Keppel Islands shifted from a more pelagic to a more benthic signal, demonstrating a change in carbon sources aligning with the change in prey availability due to habitat degradation. Grouper with a more benthic carbon signature were also feeding at a lower trophic level, indicating a shortening in food chains. Further, we found a decline in the coral grouper population accompanying a decrease in total available prey biomass. Thus, while the ability to adapt diets could ameliorate the short‐term impacts of habitat degradation on mesopredators, long‐term effects may negatively impact mesopredator populations and alter the trophic structure of coral reef food webs.     

Branching coral as a macroalgal refuge in a marginal coral reef system

Marginal coral reef systems may provide valuable insights into the nature of ecosystem processes in systems on the trajectory towards a phase shift to an alternate ecosystem state. This study investigates the process of herbivory in a marginal coral reef system in the Keppel Islands at the southern end of the Great Barrier Reef. Branching Acropora coral and the brown macroalga Lobophora variegata occupied up to 95% of the reef crest substratum at the three surveyed reefs. Feeding rates of herbivorous fishes and removal rates of Lobophora were directly quantified within areas of branching Acropora and on planar surfaces. Feeding rates by herbivorous fishes were habitat dependent with the highest bite rates being found in planar habitats for both Lobophora and the epilithic algal matrix (EAM) by 1–2 orders of magnitude, respectively. Feeding rates on Lobophora were, however, much lower than rates on the EAM. The low rates of Lobophora removal and significantly lower rates of herbivory in branching habitats were consistent with the high biomass of this brown alga throughout the Keppel Islands and with its distribution on reef crests, where Lobophora biomass was 20 times greater in branching than in planar habitats. This lack of feeding by herbivorous fishes within branching coral habitats in the Keppel Islands contrasts with the typical role of coral and topographic complexity on herbivores on coral reefs and highlights the potential for complex interactions between algae, corals and fishes on coral reefs. On marginal systems, herbivory may modify algal distributions but may be unable to contain the proliferation of algae such as Lobophora.     

Flood Impacts in Keppel Bay,Southern Great Barrier Reef in the Aftermath of Cyclonic Rainfall

In December 2010, the highest recorded Queensland rainfall associated with Tropical Cyclone ‘Tasha’ caused flooding of the Fitzroy River in Queensland, Australia. A massive flood plume inundated coral reefs lying 12 km offshore of the Central Queensland coast near Yeppoon and caused 40–100% mortality to coral fringing many of the islands of Keppel Bay down to a depth of ∼8 m. The severity of coral mortality was influenced by the level of exposure to low salinity seawater as a result of the reef''s distance from the flood plume and to a lesser extent, water depth and whether or not the reef faced the plume source. There was no evidence in this study of mortality resulting from pollutants derived from the nearby Fitzroy Catchment, at least in the short term, suggesting that during a major flood, the impact of low salinity on corals outweighs that of pollutants. Recovery of the reefs in Keppel Bay from the 2010/2011 Fitzroy River flood is likely to take 10–15 years based on historical recovery periods from a similar event in 1991; potentially impacting visitor numbers for tourism and recreational usage. In the meantime, activities like snorkeling, diving and coral viewing will be focused on the few shallow reefs that survived the flood, placing even further pressure on their recovery. Reef regeneration, restoration and rehabilitation are measures that may be needed to support tourism in the short term. However, predictions of a warming climate, lower rainfall and higher intensity summer rain events in the Central and Coastal regions of Australia over the next decade, combined with the current anthropogenic influences on water quality, are likely to slow regeneration with consequent impact on long-term reef resilience.     

Satellite observation of Keppel Islands (Great Barrier Reef) 2002 coral bleaching using IKONOS data

An examination of IKONOS satellite imagery of the Keppel Islands (Great Barrier Reef) acquired before and during a coral bleaching event indicates that severe bleaching of reefs can be detected as an increase in brightness in the band 1 (blue) and band 2 (green) IKONOS spectral bands (4-m resolution). The bleaching was not detected in band 3 (red), band 4 (near-infrared), or in the 1-m panchromatic band data. A total of 0.74 km² of bleached coral was identified, with detection occurring in waters as deep as 15 m. The procedure requires that one of the scenes be radiometrically normalized to match the reference scene prior to image differencing. A relative radiometric normalization was used in this case because variable cloud cover present in the image acquired during the bleaching event prevented reliable modeling of atmospheric effects. The success at coral bleaching detection at Keppel Islands represents both a best-case and a cloud-challenged scenario. It was a best-case scenario in that coral cover was extensive (70–90% live coral cover, mostly acroporids) and the bleaching level was extreme (92–95% of coral cover white bleached). It was a cloud-challenged scenario in terms of having extensive and highly variable cloud cover present in the image acquired during the bleaching event. Color difference images reveal extensive areas of bleached coral at sites away from our study area, indicating that this platform and methodology may be a valuable tool for mapping high coral cover areas during bleaching events. Additional studies and technique refinements would be required to test the detection limits of bleaching with IKONOS imagery or to develop a spectrally based bleaching detection index.An erratum to this article can be found at     

Building resilience into practical conservation: identifying local management responses to global climate change in the southern Great Barrier Reef

Climate change is now considered the greatest long-term threat to coral reefs, with some future change inevitable despite mitigation efforts. Managers must therefore focus on supporting the natural resilience of reefs, requiring that resilient reefs and reef regions be identified. We develop a framework for assessing resilience and trial it by applying the framework to target management responses to climate change on the southern Great Barrier Reef. The framework generates a resilience score for a site based on the evaluation of 19 differentially weighted indicators known or thought to confer resilience to coral reefs. Scores are summed, and sites within a region are ranked in terms of (1) their resilience relative to the other sites being assessed, and (2) the extent to which managers can influence their resilience. The framework was applied to 31 sites in Keppel Bay of the southern Great Barrier Reef, which has a long history of disturbance and recovery. Resilience and ‘management influence potential’ were both found to vary widely in Keppel Bay, informing site selection for the staged implementation of resilience-based management strategies. The assessment framework represents a step towards making the concept of resilience operational to reef managers and conservationists. Also, it is customisable, easy to teach and implement and effective in building support among local communities and stakeholders for management responses to climate change.     

A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization

The symbiosis between reef-building corals and their algal endosymbionts (zooxanthellae of the genus Symbiodinium) is highly sensitive to temperature stress, which makes coral reefs vulnerable to climate change. Thermal tolerance in corals is known to be substantially linked to the type of zooxanthellae they harbour and, when multiple types are present, the relative abundance of types can be experimentally manipulated to increase the thermal limits of individual corals. Although the potential exists for this to translate into substantial thermal acclimatization of coral communities, to date there is no evidence to show that this takes place under natural conditions. In this study, we show field evidence of a dramatic change in the symbiont community of Acropora millepora, a common and widespread Indo-Pacific hard coral species, after a natural bleaching event in early 2006 in the Keppel Islands (Great Barrier Reef). Before bleaching, 93.5% (n=460) of the randomly sampled and tagged colonies predominantly harboured the thermally sensitive Symbiodinium type C2, while the remainder harboured a tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving tagged colonies that were initially C2 predominant changed to D or C1 predominance. Colonies that were originally C2 predominant suffered high mortality (37%) compared with D-predominant colonies (8%). We estimate that just over 18% of the original A. millepora population survived unchanged leaving 29% of the population C2 and 71% D or C1 predominant six months after the bleaching event. This change in the symbiont community structure, while it persists, is likely to have substantially increased the thermal tolerance of this coral population. Understanding the processes that underpin the temporal changes in symbiont communities is key to assessing the acclimatization potential of reef corals.     

Dead bleached coral provides new surfaces for dinoflagellates implicated in ciguatera fish poisonings

Synopsis Dead sections of bleached corals in the United States Virgin Islands and British Virgin Islands were found to be colonized by filamentous algae harboring epiphytic dinoflagellates implicated in ciguatera fish poisonings. The dinoflagellates Ostreopsis lenticularis, Prorocentrum concavum, and P. lima were found in association with filamentous algae growing on dead sections of bleached Montastrea annularis and Acropora cervicornis. Several fish species from the families Acanthuridae, Pomacentridae, and Scaridae were observed to readily consume this filamentous algae/epiphytic dinoflagellate food source. Such fishes are common prey for large piscivores inhabiting tropical reefs. An increased incidence of ciguatoxic fishes may occur on reefs where bleaching events have caused significant coral mortality.     

Freeze coring as a method of collecting unconsolidated lake sediments

The paper describes a method of collecting unconsolidated lake sediment by freezing the in situ sediment to the outer surface of an aluminium tube. This prevents any disturbance and disruption of the stratigraphy which would otherwise occur because of the release of dissolved gas resulting from the pressure and temperature change on bringing the sediment to the surface. Sampling methods were tested on the laminated sediments of Lake Barrine, North Queensland.     

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.     

Coral population trajectories,increased disturbance and management intervention: a sensitivity analysis

Coral reefs distant from human population were sampled in the Red Sea and one‐third showed degradation by predator outbreaks (crown‐of‐thorns‐starfish = COTS observed in all regions in all years) or bleaching (1998, 2010). Models were built to assess future trajectories. They assumed variable coral types (slow/fast growing), disturbance frequencies (5,10,20 years), mortality (equal or not), and connectivity (un/connected to un/disturbed community). Known disturbances were used to parameterize models. Present and future disturbances were estimated from remote‐sensing chlorophyll and temperature data. Simulations and sensitivity analysis suggest community resilience at >20‐year disturbance frequency, but degradation at higher frequency. Trajectories move from fast‐grower to slow‐grower dominance at intermediate disturbance frequency, then again to fast‐grower dominance. A similar succession was observed in the field: Acropora to Porites to Stylophora/Pocillopora dominance on shallow reefs, and a transition from large poritids to small faviids on deep reefs. Synthesis and application: Even distant reefs are impacted by global changes. COTS impacts and bleaching were key driver of coral degradation, coral population decline could be reduced if these outbreaks and bleaching susceptibility were managed by maintaining water quality and by other interventions. Just leaving reefs alone, seems no longer a satisfactory option.     

Fauna of anemonefishes (Pomacentridae,Amphiprioninae) and their host sea anemones (Cnidaria,Actiniaria) on reefs of Phu Quy,Con Son,and An Thoi Islands (South China Sea,South Vietnam,and Gulf of Thailand) and a review of these groups from the coastal waters of Vietnam

A full species composition of anemonefishes (Pomacentridae, Amphiprioninae) and their host sea anemones (Cnidaria, Actiniaria) from reefs of Phu Quy and Con Son Islands (off South Vietnam) and An Thoi Islands (northeastern Gulf of Thailand) is presented for the first time. A comparison of the faunas of anemonefishes and their host sea anemones is conducted in the coastal waters of Vietnam and adjacent waters. The presence of intermittent ranges of the anemonefishes in the coastal waters of Vietnam is demonstrated. For example, the ranges of two species, Amphiprion clarkii and A. frenatus, include the coastal waters of Vietnam, excluding the Gulf of Thailand, where they are not found even at the eastern border of the gulf. A. perideraion is absent in the Gulf of Tonkin, but it is distributed to the south along the entire coastal zone of Vietnam, including the Gulf of Thailand. In the coastal waters of Vietnam, A. sandaracinos is distributed only between the Gulf of Tonkin and Gulf of Thailand. A. polymnus is reliably indicated in the coastal waters of Vietnam between 12°50′ and 9°54′ N, but, most likely, its range is continuous along the entire Vietnamese coast. The richness of species composition of host sea anemones decreases (from nine to three species) in the southern direction, from Central Vietnam to the eastern border of the Gulf of Thailand.     

How much time can herbivore protection buy for coral reefs under realistic regimes of hurricanes and coral bleaching?

Coral reefs have been more severely impacted by recent climate instability than any other ecosystem on Earth. Corals tolerate a narrow range of physical environmental stress, and increases in sea temperature of just 1 °C over several weeks can result in mass coral mortality, often exceeding 95% of individuals over hundreds of square kilometres. Even conservative climate models predict that mass coral bleaching events could occur annually by 2050. Unfortunately, managers of coral‐reef resources have few options available to meet this challenge. Here, we investigate the role that fisheries conservation tools, including the designation of marine reserves, can play in altering future trajectories of Caribbean coral reefs. We use an individual‐based model of the ecological dynamics to test the influence of spatially realistic regimes of disturbance on coral populations. Two major sources of disturbance, hurricanes and coral bleaching, are simulated in contrasting regions of the Caribbean: Belize, Bonaire, and the Bahamas. Simulations are extended to 2099 using the HadGEM1 climate model. We find that coral populations can maintain themselves under all levels of hurricane disturbance providing that grazing levels are high. Regional differences in hurricane frequency are found to cause strikingly different spatial patterns of reef health with greater patchiness occurring in Belize, which has less frequent disturbance, than the Bahamas. The addition of coral bleaching led to a much more homogenous reef state over the seascape. Moreover, in the presence of bleaching, all reefs exhibited a decline in health over time, though with substantial variation among regions. Although the protection of herbivores does not prevent reef degradation it does delay rates of coral loss even under the most severe thermal and hurricane regimes. Thus, we can estimate the degree to which local conservation can help buy time for reefs with values ranging between 18 years in the Bahamas and over 50 years in Bonaire, compared with heavily fished systems. Ultimately, we demonstrate that local conservation measures can benefit reef ecosystem services but that their impact will vary spatially and temporally. Recognizing where such management interventions will either help or fail is an important step towards both achieving sustainable use of coral‐reef resources and maximizing resource management investments.     

Climatological context for large-scale coral bleaching

Large-scale coral bleaching was first observed in 1979 and has occurred throughout virtually all of the tropics since that time. Severe bleaching may result in the loss of live coral and in a decline of the integrity of the impacted coral reef ecosystem. Despite the extensive scientific research and increased public awareness of coral bleaching, uncertainties remain about the past and future of large-scale coral bleaching. In order to reduce these uncertainties and place large-scale coral bleaching in the longer-term climatological context, specific criteria and methods for using historical sea surface temperature (SST) data to examine coral bleaching-related thermal conditions are proposed by analyzing three, 132 year SST reconstructions: ERSST, HadISST1, and GISST2.3b. These methodologies are applied to case studies at Discovery Bay, Jamaica (77.27°W, 18.45°N), Sombrero Reef, Florida, USA (81.11°W, 24.63°N), Academy Bay, Galápagos, Ecuador (90.31°W, 0.74°S), Pearl and Hermes Reef, Northwest Hawaiian Islands, USA (175.83°W, 27.83°N), Midway Island, Northwest Hawaiian Islands, USA (177.37°W, 28.25°N), Davies Reef, Australia (147.68°E, 18.83°S), and North Male Atoll, Maldives (73.35°E, 4.70°N). The results of this study show that (1) The historical SST data provide a useful long-term record of thermal conditions in reef ecosystems, giving important insight into the thermal history of coral reefs and (2) While coral bleaching and anomalously warm SSTs have occurred over much of the world in recent decades, case studies in the Caribbean, Northwest Hawaiian Islands, and parts of other regions such as the Great Barrier Reef exhibited SST conditions and cumulative thermal stress prior to 1979 that were comparable to those conditions observed during the strong, frequent coral bleaching events since 1979. This climatological context and knowledge of past environmental conditions in reef ecosystems may foster a better understanding of how coral reefs will respond in future, ocean warming scenarios.     

The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef

The development of parentage analysis to track the dispersal of juvenile offspring has given us unprecedented insight into the population dynamics of coral reef fishes. These tools now have the potential to inform fisheries management and species conservation, particularly for small fragmented populations under threat from exploitation and disturbance. In this study, we resolve patterns of larval dispersal for a population of the anemonefish Amphiprion melanopus in the Keppel Islands (southern Great Barrier Reef). Habitat loss and fishing appear to have impacted this population and a network of no‐take marine reserves currently protects 75% of the potential breeders. Using parentage analysis, we estimate that 21% of recruitment in the island group was generated locally and that breeding adults living in reserves were responsible for 79% (31 of 39) of these of locally produced juveniles. Overall, the network of reserves was fully connected via larval dispersal; however, one reserve was identified as a critical source of larvae for the island group. The population in the Keppel Islands also appears to be well‐connected to other source populations at least 60 km away, given that 79% (145 of 184) of the juveniles sampled remained unassigned in the parentage analysis. We estimated the effective size of the A. melanopus metapopulation to be 745 (582–993 95% CI) and recommend continued monitoring of its genetic status. Maintaining connectivity with populations beyond the Keppel Islands and recovery of local recruitment habitat, potentially through active restoration of host anemone populations, will be important for its long‐term persistence.     

Coral bleaching, reef fish community phase shifts and the resilience of coral reefs

The 1998 global coral bleaching event was the largest recorded historical disturbance of coral reefs and resulted in extensive habitat loss. Annual censuses of reef fish community structure over a 12-year period spanning the bleaching event revealed a marked phase shift from a prebleach to postbleach assemblage. Surprisingly, we found that the bleaching event had no detectable effect on the abundance, diversity or species richness of a local cryptobenthic reef fish community. Furthermore, there is no evidence of regeneration even after 5–35 generations of these short-lived species. These results have significant implications for our understanding of the response of coral reef ecosystems to global warming and highlight the importance of selecting appropriate criteria for evaluating reef resilience.     

Coral Reef Community Composition in the Context of Disturbance History on the Great Barrier Reef,Australia

Much research on coral reefs has documented differential declines in coral and associated organisms. In order to contextualise this general degradation, research on community composition is necessary in the context of varied disturbance histories and the biological processes and physical features thought to retard or promote recovery. We conducted a spatial assessment of coral reef communities across five reefs of the central Great Barrier Reef, Australia, with known disturbance histories, and assessed patterns of coral cover and community composition related to a range of other variables thought to be important for reef dynamics. Two of the reefs had not been extensively disturbed for at least 15 years prior to the surveys. Three of the reefs had been severely impacted by crown-of-thorns starfish outbreaks and coral bleaching approximately a decade before the surveys, from which only one of them was showing signs of recovery based on independent surveys. We incorporated wave exposure (sheltered and exposed) and reef zone (slope, crest and flat) into our design, providing a comprehensive assessment of the spatial patterns in community composition on these reefs. Categorising corals into life history groupings, we document major coral community differences in the unrecovered reefs, compared to the composition and covers found on the undisturbed reefs. The recovered reef, despite having similar coral cover, had a different community composition from the undisturbed reefs, which may indicate slow successional processes, or a different natural community dominance pattern due to hydrology and other oceanographic factors. The variables that best correlated with patterns in the coral community among sites included the density of juvenile corals, herbivore fish biomass, fish species richness and the cover of macroalgae. Given increasing impacts to the Great Barrier Reef, efforts to mitigate local stressors will be imperative to encouraging coral communities to persist into the future.     

Large-scale bleaching of corals on the Great Barrier Reef

 The Great Barrier Reef (GBR) experienced its most intensive and extensive coral bleaching event on record in early 1998. Mild bleaching commenced in late January and intensified by late February/early March 1998. Broad-scale aerial surveys conducted of 654 reefs (∼23% of reefs on the GBR) in March and April 1998, showed that 87% of inshore reefs were bleached at least to some extent (>1% of coral cover) compared to 28% of offshore (mid- and outer-shelf) reefs. Of inshore reefs 67% had high levels of bleaching (>10% of coral) and 25% of inshore reefs had extreme levels of bleaching (>60% of coral). Fewer offshore reefs (14%) showed high levels of bleaching while none showed extreme levels of bleaching. Ground-truth surveys of 23 reefs, which experienced bleaching in intensities ranging from none to extreme, showed that the aerial survey data are likely to be underestimates of the true extent and intensity of bleaching on the GBR. The primary cause of this bleaching event is likely to be elevated sea temperature and solar radiation, exacerbated by lowered salinity on inshore and some offshore reefs in the central GBR. Accepted: 30 July 1998     

Historical temperature variability affects coral response to heat stress

Coral bleaching is the breakdown of symbiosis between coral animal hosts and their dinoflagellate algae symbionts in response to environmental stress. On large spatial scales, heat stress is the most common factor causing bleaching, which is predicted to increase in frequency and severity as the climate warms. There is evidence that the temperature threshold at which bleaching occurs varies with local environmental conditions and background climate conditions. We investigated the influence of past temperature variability on coral susceptibility to bleaching, using the natural gradient in peak temperature variability in the Gilbert Islands, Republic of Kiribati. The spatial pattern in skeletal growth rates and partial mortality scars found in massive Porites sp. across the central and northern islands suggests that corals subject to larger year-to-year fluctuations in maximum ocean temperature were more resistant to a 2004 warm-water event. In addition, a subsequent 2009 warm event had a disproportionately larger impact on those corals from the island with lower historical heat stress, as indicated by lower concentrations of triacylglycerol, a lipid utilized for energy, as well as thinner tissue in those corals. This study indicates that coral reefs in locations with more frequent warm events may be more resilient to future warming, and protection measures may be more effective in these regions.