Ecological versatility and the decline of coral feeding fishes following climate driven coral mortality

Coral reefs are under threat due to climate-mediated coral mortality, which affects some reef coral genera more severely than others. The impact this has on coral reef fish is receiving increasing attention, with one focal area assessing impacts on fish that feed directly on live coral. It appears that the more specialised a species of corallivore, the more susceptible it is to coral declines. However data are sparse for the Indian Ocean, and little is known about why some corals are preferentially fed upon over others. Here I assess feeding specialisation in three species of coral feeding butterflyfish in the Chagos Archipelago, central Indian Ocean, assess the food quality of the coral genera they target and document patterns of decline in the Seychelles following a severe coral mortality event. Cheatodon trifascialis was the most specialised coral feeder, preferentially selecting for Acropora corals, however, when Acropora was scarce, individuals showed considerable feeding plasticity, particularly for the dominant Pocillopora corals. C. trifasciatus also preferentially fed on Acropora corals, but fed on a much more diverse suite of corals and also displayed some selectivity for Porites. C. auriga is a facultative corallivore and consumed ∼55% live coral, which lies within the wide range of coral dependence reported for this species. C:N ratio analysis indicated Lobophyllia and Acropora have the highest food quality, with Pocillopora having the lowest, which conforms with diet selection of corallivores and helps explain preferential feeding. Obligate specialist feeders displayed the greatest declines through coral mortality in the Seychelles with obligate generalists also declining substantially, but facultative feeders showing little change. Clearly a greater understanding of the species most vulnerable to disturbance, their habitat requirements and the functional roles they play will greatly assist biodiversity conservation in a changing climate.     

Long-term changes in coral colony size distributions on Kenyan reefs under different management regimes and across the 1998 bleaching event

Colony size is an important life-history characteristic of corals and changes in colony size will have significant effects on coral populations. This study summarizes ∼21,000 haphazard colony size measurements of 26 common coral taxa (mostly coral genera) collected annually between 1992 and 2006 in seven Kenyan reef lagoons. There was a major coral bleaching and mortality event in early 1998 and all seven reefs were affected. The seven locations include two long-protected Marine National Parks (Malindi and Watamu), one relatively recently established park (Mombasa), and four unprotected locations (Vipingo, Kanamai, Ras Iwatine, and Diani). They span about 150 km and represent three distinct fishery management regimes: old protected (OP), newly protected (NP), and unprotected (UP). Seventeen taxa had statistically significant different sizes for comparisons of the management regimes, with only one genus, Pavona, having larger sizes in the unprotected reefs. The size of eight coral genera showed a significant time and management interaction, and size frequency differences that existed in management areas prior to 1998 were further increased after the bleaching event. Time alone was a significant factor for eleven genera, and in all cases colonies were smaller after 1998. For most taxa, colony size distributions were significantly skewed and had right-tailed distributions. After 1998, the right-tailed distributions of Acropora, Hydnophora, and Montipora were significantly reduced. Most taxa had peaky distributions and only Acropora experienced a statistically significant change from peaky to flat. The mean sizes of taxa were not related to their mortality across 1998, which indicates that the size effect was within rather than between taxa. Astreopora and Platygyra were well-sampled taxa that did not show an effect of management, but had reduced median sizes across 1998. Consequently, no taxa were tolerant of both fishing and bleaching disturbances and the combined effect was to reduce the size of all corals.     

Coral mortality following extreme low tides and high solar radiation

Extreme tidal events are one of the most predictable natural disturbances in marine benthic habitats and are important determinants of zonation patterns in intertidal benthic communities. On coral reefs, spring low tides are recurrent disturbances, but are rarely reported to cause mass mortality. However, in years when extremely low tides coincide with high noon irradiances, they have the potential to cause widespread damage. Here, we report on such an event on a fringing coral reef in the central Great Barrier Reef (Australia) in September 2005. Visual surveys of colony mortality and bleaching status of more than 13,000 corals at 14 reef sites indicated that most coral taxa at wave-protected sites were severely affected by the event. Between 40 and 75% of colonies in the major coral taxa (Acropora, Porites, Faviidae, Mussidae and Pocilloporidae) were either bleached or suffered partial mortality. In contrast, corals at wave-exposed sites were largely unaffected (<1% of the corals were bleached), as periodic washing by waves prevented desiccation. Surveys along a 1–9 m depth gradient indicated that high coral mortality was confined to the tidal zone. However, 20–30% of faviid colonies were bleached throughout the depth range, suggesting that the increase in benthic irradiances during extreme low tides caused light stress in deeper water. Analyses of an 8-year dataset of tidal records for the area indicated that the combination of extended periods of aerial exposure and high irradiances occurs during May–September in most years, but that the event in September 2005 was the most severe. We argue that extreme low-tide, high-irradiance events are important structuring forces of intertidal coral reef communities, and can be as damaging as thermal stress events. Importantly, they occur at a time of year when risks from thermal stress, cyclones and monsoon-associated river run-off are minimal.     

Bleaching response of corals and their <Emphasis Type="Italic">Symbiodinium</Emphasis> communities in southern Africa

The high-latitude coral communities of southern Africa suffered minimal impacts during past mass bleaching events. Recent reports indicate an increase in bleaching frequency during the last decade, yet the actual levels of thermal stress and contributing factors in these bleaching events, and the degree of acclimatisation or adaptation on these reefs are poorly understood. During the 2005 warm-water anomaly in the southern Indian Ocean we conducted bleaching surveys and collected samples for genotyping of the algal symbiont communities at 21 sites in southern Mozambique and South Africa. Coral bleaching reached unprecedented levels and was negatively correlated with both latitude and water depths. Stylophora pistillata and Montipora were the most susceptible taxa, whereas three common branching corals had significantly different bleaching responses (Stylophora > Acropora > Pocillopora). Temperature records indicated that localised strong upwelling events coupled with persistent above-average seawater temperatures may result in accumulated thermal stress leading to bleaching. Symbiodinium in 139 scleractinian corals belonged almost exclusively to clade C, with clade D symbionts present in only 3% of the colonies. Two atypical C subclades were present in Stylophora and Pocillopora colonies and these were more abundant in shallow than deeper sites. Taxon-specific differences in bleaching responses were unrelated to different clades of algal symbionts and suggest that Symbiodinium C subtypes with diverse thermal tolerance, coupled with acclimatisation and morphology of the host colony influence the bleaching response. Additionally, the predominance of putatively thermal-sensitive Symbiodinium in southern African corals may reflect a limited experience of bleaching and emphasises the vulnerability of these reefs to moderate levels of thermal stress.     

Recovery of corals a decade after a bleaching event in Dubai, United Arab Emirates

Elevated sea surface temperatures in the late 1990s were associated with widespread coral mortality in the Arabian Gulf, particularly in Acropora dominated areas. This study investigates the composition, condition, and recruitment patterns of coral communities in Saih Al-Shaib, Dubai, United Arab Emirates, a decade after mass bleaching. Five statistically distinct communities were identified by cluster analysis, with grouping optimized from 17 significant indicator species. Overall, 25 species of scleractinian coral were observed, representing 35 ± 1.6% coral cover. Densities of recruits were low (0.8 ± 0.2 m⁻²), and composition generally reflected that of the surrounding adult community. Ten years after mass mortality, Acropora dominated assemblages were observed in three of the six sites examined and coral cover (41.9 ± 2.5%) was double post-bleaching cover. One shallow near-shore site appears to have had recovery of Acropora reset by a further bleaching event in 2002. However, the prevalence of young Acropora colonies here indicates that recovery may recur in several years. One area formerly dominated by Acropora is now dominated by faviids and poritids, with adult and juvenile composition suggesting this dominance shift is likely to persist. Porites lutea and Porites harrisoni dominated communities were negligibly impacted by the bleaching events, and the limited change in coral cover and composition in intervening years likely results from slow growth and low recruitment. Despite strong recovery of several dominant Acropora species, five formerly common species from this area were not observed suggesting local extinction. Dubai coral communities exhibit both resistance and resilience to elevated sea temperatures. The conservation of these patch reefs is warranted given the predicted increase in bleaching events, and the role that these communities may play in regional recovery.     

Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response

Coral bleaching events are often associated with higher levels of coral mortality but when this occurs in the chronology of individual bleaching events is poorly documented. Knowing when mortality occurs is important for understanding molecular mechanisms and the putative adaptive significance of the response (the Adaptive Bleaching Hypothesis). In a detailed study of a coral bleaching event on the Great Barrier Reef, involving weekly and twice weekly repetitive observations of >200 individually marked corals over an 18 month period (∼16,000 observations), it is shown that bleaching in Acropora latistella, A. subulata and Turbinaria mesenterina was an acute, rapid response, occurring within days of a peak in seawater temperatures exceeding previously described thresholds. Subsurface light levels, measured over the duration of the event, were not anomalous. Full bleaching (i.e. whole colonies turning bone-white) and partial bleaching (white patches) was observed in the Acropora spp. whilst the T. mesenterina colonies typically paled to a light brown colour. Algal densities in bleached corals were 10–30% of those of normally pigmented corals (∼2.5 × 10⁶ algae per cm²), and in this instance bleaching was clearly a sudden, isolated, stress event and not an extreme low-point in the seasonal fluctuation of the density of symbiotic algae. Bleached corals were associated with high levels of partial and whole-colony mortality, but mortality was exclusively limited to the two Acropora spp. Importantly, most of this mortality was recorded in surveys conducted 1 and 2 weeks after bleaching was first observed, and for A. latistella as little as 1 week after bleaching was first observed. This suggests that in this particular bleaching event, for the Acropora species, that bleaching and mortality were intimately linked: this in turn suggests it was a pathological phenomenon. The study highlights a problem in the adaptive bleaching hypothesis, whereby significant levels of mortality can occur in a bleaching event before any chance for subsequent recombination of the host-symbiont unit. It is argued that in order to further evaluate the significance of bleaching as a potentially adaptive mechanism, bleaching-induced and bleaching-related mortality have to be fully considered. It is necessary to incorporate the cost (in terms of mortality) of a bleaching event, the recurring cost of reverting to the original, mortal, stress–prone combination after the event, and the higher cost associated with forming a maladaptive combination.     

Microhabitat association in white-streaked grouper Epinephelus ongus: importance of Acropora spp.

Microhabitat associations are considered to be important for juvenile survivorship and growth of coral reef fishes. The aim of the study was to quantify microhabitat associations between juvenile and adult white-streaked grouper Epinephelus ongus, which supports important fisheries in coral reef areas. Underwater observations revealed that most juveniles were found in bottlebrush Acropora spp., staghorn Acropora spp. and coral rubble and there was a significant positive use of bottlebrush Acropora spp. and a significant negative use of coral rubble. For adults, most individuals were found in bottlebrush Acropora spp. and staghorn Acropora spp., and there was a significant positive use of staghorn Acropora spp. and significant negative use of coral rubble. A habitat choice experiment by using pre-settlement individuals revealed that both bottlebrush Acropora spp. and staghorn Acropora spp. were used as settlement sites, whereas coral rubble was rarely used as a settlement site. Results of the study suggest that juvenile and adult E. ongus showed significantly positive microhabitat associations with bottlebrush Acropora spp. and staghorn Acropora spp., respectively, in the field. Bottlebrush Acropora spp. has smaller inter-branch spaces than staghorn Acropora spp., which could drive patterns of microhabitat associations. In addition, post-settlement processes such as predation may influence the spatial distribution of juveniles. Because Acropora corals are very susceptible to coral bleaching, we predict that rising temperatures from climate change will negatively impact populations of E. ongus.     

Dynamics of a coral reef community after mass mortality of branching <Emphasis Type="Italic">Acropora</Emphasis> corals and an outbreak of anemones

Dynamics of a coral reef community at Tiao-Shi Reef, southern Taiwan were studied using permanent transects to examine coral recovery and successive cascades to collapse stage resulting from chronic anthropogenic impacts and typhoons. Three distinct zones were recognized within a relatively small study area (250 m across) formerly dominated by large stands of branching Acropora corals. The first zone still retains the dominance of branching Acropora corals, although they show a significant decreasing tendency. The second zone exhibits recovery with a significant increase in branching Montipora stellata, which is recruited and grows faster than branching Acropora corals. The third zone is occupied by anemone, Condylactis sp., and demonstrates a stable phase of coral deterioration without recovery. Such differences in coral reef community dynamics within a small spatial scale illustrate mosaic dynamics which have resulted from degradation of the water quality, patchy mortality of large branching Acropora thickets caused by typhoons, the rapid asexual fragmentation and growth of M. stellata making it a successful colonizer, and occupation by anemone, Condylactis sp., together with unstable remnants of dead Acropora rubbles have not allowed coral recruits to survive.     

Coral Bleaching and Global Climate Change: Scientific Findings and Policy Recommendations

Abstract: In 1998, tropical sea surface temperatures were the highest on record, topping off a 50-year trend for some tropical oceans. In the same year, coral reefs around the world suffered the most extensive and severe bleaching ( loss of symbiotic algae) and subsequent mortality on record. These events may not be attributable to local stressors or natural variability alone but were likely induced by an underlying global phenomenon. It is probable that anthropogenic global warming has contributed to the extensive coral bleaching that has occurred simultaneously throughout the reef regions of the world. The geographic extent, increasing frequency, and regional severity of mass bleaching events are an apparent result of a steadily rising baseline of marine temperatures, combined with regionally specific El Niño and La Niña events. The repercussions of the 1998 mass bleaching and mortality events will be far-reaching. Human populations dependent on reef services face losses of marine biodiversity, fisheries, and shoreline protection. Coral bleaching events may become more frequent and severe as the climate continues to warm, exposing coral reefs to an increasingly hostile environment. This global threat to corals compounds the effects of more localized anthropogenic factors that already place reefs at risk. Significant attention needs to be given to the monitoring of coral reef ecosystems, research on the projected and realized effects of global climate change, and measures to curtail greenhouse gas emissions. Even those reefs with well-enforced legal protection as marine sanctuaries, or those managed for sustainable use, are threatened by global climate change.     

Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo–Pacific coral Stylophora pistillata (Esper) after summer bleaching

Coral bleaching (the loss of symbiotic dinoflagellates from reef-building corals) is most frequently caused by high-light and temperature conditions. We exposed the explants of the hermatypic coral Stylophora pistillata to four combinations of light and temperature in late spring and also in late summer. During mid-summer, two NOAA bleaching warnings were issued for Heron Island reef (Southern Great Barrier Reef, Australia) when sea temperature exceeded the NOAA bleaching threshold, and a ‘mild’ (in terms of the whole coral community) bleaching event occurred, resulting in widespread S. pistillata bleaching and mortality. Symbiotic dinoflagellate biomass decreased by more than half from late spring to late summer (from 2.5×10⁶ to 0.8×10⁶ dinoflagellates cm² coral tissue), and those dinoflagellates that remained after summer became photoinhibited more readily (dark-adapted F _V : F _M decreased to (0.3 compared with 0.4 in spring), and died in greater numbers (up to 17% dinoflagellate mortality compared with 5% in the spring) when exposed to artificially elevated light and temperature. Adding exogenous antioxidants (d-mannitol and l-ascorbic acid) to the water surrounding the coral had no clear effect on either photoinhibition or symbiont mortality. These data show that light and temperature stress cause mortality of the dinoflagellate symbionts within the coral, and that susceptibility to light and temperature stress is strongly related to coral condition. Photoinhibitory mechanisms are clearly involved, and will increase through a positive feedback mechanism: symbiont loss promotes further symbiont loss as the light microenvironment becomes progressively harsher.     

Model of coral population response to accelerated bleaching and mass mortality in a changing climate

We model coral community response to bleaching and mass mortality events which are predicted to increase in frequency with climate change. The model was parameterized for the Arabian/Persian Gulf, but is generally applicable. We assume three species groups (Acropora, faviids, and Porites) in two life-stages each where the juveniles are in competition but the adults can enter a size-refuge in which they cannot be competitively displaced. An aggressive group (Acropora species) dominates at equilibrium, which is not reached due to mass mortality events that primarily disadvantage this group (compensatory mortality, >90% versus 25% in faviids and Porites) roughly every 15 years. Population parameters (N individuals, carrying capacity) were calculated from satellite imagery and in situ transects, vital rates (fecundity, mortality, and survival) were derived from the model, field observations, and literature. It is shown that populations and unaltered community structure can persist despite repeated 90% mortality, given sufficiently high fecundity of the remaining population or import from connected populations. The frequency of disturbance determines the dominant group—in low frequency Acropora, in high frequency Porites. This is congruent with field observations. The model of an isolated population was more sensitive to parameter changes than that of connected populations. Highest sensitivity was to mortality rate and recruitment rate. Community composition was sensitive to spacing of disturbances and level of catastrophic mortality. Decreased mortality led to Acropora dominance, increased mortality led to Acropora extinction. In nature, closely spaced disturbances have severely disadvantaged Acropora populations over the last decade. Unless a longer (>10 years) disturbance-free interval can be maintained, a permanent shift away from Acropora dominance will be observed. A mortality rate of 99% in Acropora, as observed in 1996, is not sustainable if repetitive and neither is a disturbance frequency <15 years—each leading to population collapse. This shows that the severity and/or the spacing of the 1996–1998–2002 disturbances were unusual in frequency and duration.     

The effects of an abnormal decrease in temperature on the Eastern Pacific reef-building coral Pocillopora verrucosa

Coral bleaching events are associated with abnormal increases in temperature, such as those produced during El Niño. Recently, a breakdown in the coral–dinoflagellate (genus Symbiodinium) endosymbiosis has been documented in corals exposed to anomalously cold-water temperatures associated with La Niña events. Given the ecological significance of such events, as well as the threat of global climate change, surprisingly little is known about the physiological response of corals to cold stress. This study evaluated some physiological effects of continuous temperature decline in colonies of the eastern Pacific reef-building coral Pocillopora verrucosa. Twenty days of incubation at 18.5–19.0 °C resulted in a substantial decrease in holobiont lipid and Chla content, as well as an increase in Symbiodinium density. These observations suggest a combination of symbiont acclimation due to the temperature decline and reallocation of carbon toward algal growth as opposed to translocation to the host coral. With a decreased availability of symbiont-derived carbon, the coral likely catabolized storage lipids in order to survive the stress event. Despite this stress and some tissue necrosis, no mortality was noted and corals recovered quickly when returned to the ambient temperature. As these results are in marked contrast to similar studies investigating elevated temperature on this coral from this same location, Pocillopora in the Mexican Central Pacific may be more prone to long-term damage and mortality during periods of ocean warming as opposed to ocean cooling.     

Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals,coral diseases and fish in the Arabian Gulf (Dubai,UAE)

Two positive sea-surface temperature anomalies occurred in the Arabian Gulf in short sequence. Between May and August 1996 and 1998, sea-surface temperatures in the southern Arabian Gulf were elevated by 2°C above average. The consequences for coral fauna, coral diseases and coral regeneration were studied in Dubai (United Arab Emirates) between Jebel Ali and Ras Hasyan. In 1996, coral death was widespread, affecting primarily the genus Acropora. In Acropora-dominated areas, live coral cover was reduced from 90% to about 26% in 1996, while in 1998 only a reduction from 26% to 22% of the remaining coral cover occurred. In the study area, all six Acropora species suffered total mortality in 1996, thus the coral fauna was reduced from 34 species to 27. The nearest areas with surviving Acropora were 30 km to the east (Deira) and 20 km to the west (Al Jazira). Massive coral species suffered negligible mortality, and slowly increased in space cover. The Acropora overkill turned 7.9 km² (19.7% of total coral-covered area) of previously lush coral gardens into a dead framework that was increasingly bioeroded. Acropora recruitment only started in 1998, average recruit size in 1999 was 7Dž cm, and recruits were rare. Prior to the mass mortality event, coral diseases were common and seasonal (14LJ% of corals, mainly Acropora, affected in summer, in winter 7Lj%, mainly massives), after the mortality event seasonality was lost and infection remained below winter levels (6LJ%, only massives infected). In fish, overall species richness decreased from 95 to 64 species in point counts, but frequency only decreased in one species (Pseudochromis persicus). Guild structure changed inasmuch as herbivores and planktivores increased, and invertivores decreased, although differences were not statistically significant. The most abundant family, both prior to and after the coral mass mortality, was Lutjanidae. It appears that even though much of the coral was dead, the maintenance of structural complexity allowed the fish assemblage to avoid a similar catastrophic change to that experienced by the coral assemblage.     

Coral mucus stable isotope composition and labeling: experimental evidence for mucus uptake by epizoic acoelomorph worms

Mucus released by scleractinian corals can act as an important energy and nutrient carrier in coral reef ecosystems, and a distinct isotopic signature would allow following the fate of this material. This study investigates the natural C and N stable isotopic signatures of mucus released by four scleractinian coral genera (Acropora, Fungia, Pocillopora and Stylophora) in comparison with those of suspended particulate organic matter (POM) in seawater of a Northern Red Sea fringing coral reef near Aqaba, Jordan. The natural δ¹³C and δ¹⁵N signatures of coral mucus differed significantly from seawater POM for the majority of seasonal comparisons, but were inappropriate for explicit tracing of mucus in the coral reef food web. Thus, a labeling technique using stable isotope tracers (¹³C and ¹⁵N) was developed that produced δ¹³C values of up to 122 ± 5‰ (mean ± SE) and δ¹⁵N of up to 2,100 ± 151‰ in mucus exuded by Fungia corals. ¹³C and ¹⁵N-enriched compounds were rapidly (within 3 h) and light-dependently transferred from the endosymbiotic zooxanthellae to the mucus-producing coral host. The traceability of ¹⁵N-labeled mucus was examined by evaluating its uptake and potential utilization by epizoic acoelomorph Waminoa worms naturally occurring on a range of scleractinian coral taxa. This tracer experiment resulted in uptake of coral mucus by the coral-associated acoelomorphs and further demonstrated the possibility to trace stable isotope-labeled coral mucus by revealing a new trophic pathway in coral reef ecosystems.     

Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak

Common Hawaiian and Enewetak corals were examined to determine the method and mining of reproduction. Of the 7 Hawaiian species examined for the release of planulae, only 2 have planulated in captivity, Pocillopora damicornis and Cyphastrea ocellina. Both planulate year-round and both are characteristic of reef flats. Four of the 5 species which did not planulate were found to contain eggs, but not planulate, when polyps were examined microscopically. These 5 species do not usually occur on reef flats. Seven of the 12 Enewetak species examined in June, July, August and January planulated; 4 of these were pocilloporids, all of which are common in shallow water. Only 3 of the 8 species of Acropora planulated, and these 3 occur solely in shallow water. A greater proportion of the Pocillopora spp. colonies than Acropora spp. colonies planulated and they released more planulae per head. In previous studies and in this one, coral species which have released planulae are characteristic of shallow-water environments such as reef flats. Most of the 10 species reported on here which failed to planulate in captivity are not commonly found on reef flats. The failure to detect planulation in so many species, particularly those of deeper water, suggests that common hermatypic corals may not all reproduce in the same way, and that mode of reproduction may be related to habitat.     

Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones

The hypothesis that intraspecific variation in coral bleaching is a result of the distribution of bleaching-susceptible clonal genotypes (genets) was addressed using photoquadrats recorded during the 1987 Caribbean bleaching event on a reef dominated by Montastraea annularis (Morphotype I), together with manipulative experiments with Porites porites. Nearest-neighbor analysis showed that bleached colonies (ramets) of M. annularis at 10 m depth had a high probability (0.80) of having a nearest bleached neighbor of the same genet rather than a bleached ramet of a different genet. Furthermore, the frequency distributions of bleached ramets of M. annularis in the photoquadrats was significantly different from a Poisson distribution, suggesting that bleached ramets were aggregated on the reef. Manipulative experiments with P. porites from 15 m depth showed that some genets were more susceptible to thermal bleaching than others, since three genets had significantly different rates of zooxanthellae loss when exposed to elevated temperatures in tanks receiving irradiances similar to those found in situ. These results suggest that the in situ patchy distribution of bleached ramets could correspond to the distribution of certain genets, and that adjacent genets can exhibit sufficiently different phenotypes to account for intraspecific variation in bleaching. Further studies of genet-specific coral bleaching may provide valuable insights into the causes and consequences of bleaching.     

The 1998 bleaching event and its aftermath on a coral reef in Belize

Widespread thermal anomalies in 1997-1998, due primarily to regional effects of the El Niño-Southern Oscillation and possibly augmented by global warming, caused severe coral bleaching worldwide. Corals in all habitats along the Belizean barrier reef bleached as a result of elevated sea temperatures in the summer and fall of 1998, and in fore-reef habitats of the outer barrier reef and offshore platforms they showed signs of recovery in 1999. In contrast, coral populations on reefs in the central shelf lagoon died off catastrophically. Based on an analysis of reef cores, this was the first bleaching-induced mass coral mortality in the central lagoon in at least the last 3,000 years. Satellite data for the Channel Cay reef complex, the most intensively studied of the lagoonal reefs, revealed a prolonged period of elevated sea-surface temperatures (SSTs) in the late summer and early fall of 1998. From 18 September to 1 October 1998, anomalies around this reef averaged +2.2°C, peaking at 4.0°C above the local HotSpot threshold. In situ temperature records from a nearby site corroborated the observation that the late summer and early fall of 1998 were extraordinarily warm compared to other years. The lettuce coral, Agaricia tenuifolia, which was the dominant occupant of space on reef slopes in the central lagoon, was nearly eradicated at Channel Cay between October 1998 and January 1999. Although the loss of Ag. tenuifolia opened extensive areas of carbonate substrate for colonization, coral cover remained extremely low and coral recruitment was depressed through March 2001. High densities of the sea urchin Echinometra viridis kept the cover of fleshy and filamentous macroalgae to low levels, but the cover of an encrusting sponge, Chondrilla cf. nucula, increased. Further increases in sponge cover will impede the recovery of Ag. tenuifolia and other coral species by decreasing the availability of substrate for recruitment and growth. If coral populations are depressed on a long-term basis, the vertical accretion of skeletal carbonates at Channel Cay will slow or cease over the coming decades, a time during which global-warming scenarios predict accelerated sea-level rise.     

Lag Effects in the Impacts of Mass Coral Bleaching on Coral Reef Fish, Fisheries, and Ecosystems

Abstract:  Recent episodes of coral bleaching have led to wide-scale loss of reef corals and raised concerns over the effectiveness of existing conservation and management efforts. The 1998 bleaching event was most severe in the western Indian Ocean, where coral declined by up to 90% in some locations. Using fisheries-independent data, we assessed the long-term impacts of this event on fishery target species in the Seychelles, the overall size structure of the fish assemblage, and the effectiveness of two marine protected areas (MPAs) in protecting fish communities. The biomass of fished species above the size retained in fish traps changed little between 1994 and 2005, indicating no current effect on fishery yields. Biomass remained higher in MPAs, indicating they were effective in protecting fish stocks. Nevertheless, the size structure of the fish communities, as described with size-spectra analysis, changed in both fished areas and MPAs, with a decline in smaller fish (<30 cm) and an increase in larger fish (>45 cm). We believe this represents a time-lag response to a reduction in reef structural complexity brought about because fishes are being lost through natural mortality and fishing, and are not being replaced by juveniles. This effect is expected to be greater in terms of fisheries productivity and, because congruent patterns are observed for herbivores, suggests that MPAs do not offer coral reefs long-term resilience to bleaching events. Corallivores and planktivores declined strikingly in abundance, particularly in MPAs, and this decline was associated with a similar pattern of decline in their preferred corals. We suggest that climate-mediated disturbances, such as coral bleaching, be at the fore of conservation planning for coral reefs.     

Effect of Macroalgal Expansion and Marine Protected Areas on Coral Recovery Following a Climatic Disturbance

Disturbance plays an important role in structuring marine ecosystems, and there is a need to understand how conservation practices, such as the designation of Marine Protected Areas (MPAs), facilitate postdisturbance recovery. We evaluated the association of MPAs, herbivorous fish biomass, substrate type, postdisturbance coral cover, and change in macroalgal cover with coral recovery on the fringing reefs of the inner Seychelle islands, where coral mortality after a 1998 bleaching event was extensive. We visually estimated benthic cover and fish biomass at 9 sites in MPAs where fishing is banned and at 12 sites where fishing is permitted in 1994, 2005, 2008, and 2011. We used analysis of variance to examine spatial and temporal variations in coral cover and generalized additive models to identify relations between coral recovery and the aforementioned factors that may promote recovery. Coral recovery occurred on all substrate types, but it was highly variable among sites and times. Between 2005 and 2011 the increase in coral cover averaged 1%/year across 21 sites, and the maximum increase was 4%/year. However, mean coral cover across the study area (14%) remained at half of 1994 levels (28%). Sites within MPAs had faster rates of coral recovery than sites in fished areas only where cover of macroalgae was low and had not increased over time. In MPAs where macroalgae cover expanded since 1998 there was no recovery. Where coral was recovering on granite reefs there was a shift in relative prevalence of colony life‐form from branching to encrusting species. This simplification of reef structure may affect associated reef fauna even if predisturbance levels of coral cover are attained. Efecto de la Expansión de Macroalgas y Áreas Marinas Protegidas sobre la Recuperación de Coral Después de una Perturbación Climática     

Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia

In April-May 1998, mass coral bleaching was observed in the lagoon of Rangiroa Atoll, Tuamotu Archipelago, French Polynesia. Six months later, the extent of bleaching-induced coral mortality was assessed at three sites. Corals in the fast-growing genus Pocillopora had experienced >99% mortality. Many large colonies of the slow-growing genus Porites (mean horizontal cross-sectional area 5.8 m²) had also died - a phenomenon not previously observed in French Polynesia and virtually unprecedented world-wide. At one site, 25% of colonies, or 44% of the pre-bleaching cover of living Porites, experienced whole-colony mortality. At the two other sites, recently dead Porites accounted for 41% and 82% of the pre-bleaching live cover. Mortality in Porites was negatively correlated with depth between 1.5 and 5 m. Using a 50-year dataset of mean monthly sea surface temperature (SST), derived from ship- and satellite-borne instruments, we show that bleaching occurred during a period of exceptionally high summer SST. 1998 was the first year in which mean monthly SSTs exceeded the 1961-1990 upper 95% confidence limit (29.4°C) for a period of three consecutive months. We suggest that the sustained 3-month anomaly in local summer SST was a major cause of coral mortality, but do not discount the synergistic effect of solar radiation. Recovery of the size-frequency distribution of Porites colonies to pre-bleaching levels may take at least 100 years.