Peter W. Glynn

Widespread coral mortality and the 1982-83 EL Niño Warming event

The massive ‘bleaching’ (loss of zooxanthellae) and death of reef corals that occurred in one area (Gulf of Chiriqui) on the Pacific side of Panama and in the Galapagos Islands during February—April 1983 continued in these areas until September—October 1983, resulting in a catastrophic disturbance. Similar episodes have been reported subsequently throughout much of the tropical eastern Pacific region (Costa Rica, the entire Pacific coast of Panama, and Colombia), in the central and western Pacific Ocean, in parts of the western Atlantic Ocean (Caribbean coasts of Costa Rica, Panama, and Colombia), and in the Florida Keys and Bahama Islands.

Coral Mortality and Disturbances to Coral Reefs in the Tropical Eastern Pacific

Abstract Widespread bleaching and mortality of reef-building corals occurred in the tropical eastern Pacific region during the severe and prolonged El Nino-Southern Oscillation (ENSO) event of 1982-83. At the height of the 10 month sea warming period, Panamanian reefs experienced 2-3 bouts of coral bleaching (loss of symbiotic zooxanthellae), which resulted in coral death 2-4 weeks later. Coral reefs in Costa Rica, Panama and Colombia suffered up to 70-90% coral mortality; in the Galapagos Islands (Ecuador), most coral reefs experienced >95% mortality. The hypothesis that sea warming caused this disturbance is supported by (a) the coincidence between the warming event and stress responses of reef organisms, (b) the correlation between the magnitude of local temperature deviations and the extent of mortality, and (c) the El Nino simulation experiments that resulted in coral bleaching, mortality, and histopathological changes similar to those observed naturally. El Nino warming usually does not extend north of Ecuador where eastern Pacific coral reefs are best developed. A near-decadal (1976-1988) warming trend over much of the tropical and subtropical Pacific Ocean could have affected the susceptibility of reef corals during the short-term 1982-83 warming disturbance. Zooxanthellate corals were affected most severely in nearly all reef areas, however, other organisms – such as benthic algae, non-zooxanthellate scleractinian corals, black corals, molluscs, barnacles, and crustacean symbiotes of corals - often showed local negative responses associated with non-thermal, El Nino-related conditions (e.g., nutrient depletion, low plankton abundance, high sea level, and wave assault). Secondary disturbances included (a) the elimination of coral barriers, allowing the corallivore Acanthaster planci access to formerly protected coral prey, (b) increased external bioerosion of reef surfaces killed in 1983 because of post-El Nino increases in sea urchin densities, and (c) the establishment of damselfish territories on corals that experienced partial mortality in 1983. Such disturbances are currendy causing longer-term changes to their respective local communities. Estimates of the ages of massive corals that were killed or irreparably damaged, and the interruption of reef framework accumulation suggest that a disturbance comparable to that of 1982-83 probably has not occurred in the Galapagos Islands or Panama during the past 200 years. The initial damaging effects of the 1982-83 disturbance to reef coral populations, combined with persistent secondary disturbances and low coral recruitment, could prolong reef recovery for decades or possibly centuries. Periods of intense upwelling cause localized and moderate levels of coral mortality, but persistent ENSO-related sea warming causes widespread and catastrophic coral mortality. El Nino events of extreme severity may limit eastern Pacific reef growth and diversity as much as do distance and isolation of these reefs from the centers of reef development in the western Pacific.

Bioerosion and Coral Reef Growth: A Dynamic Balance

Bioerosion, involving the weakening and breakdown of calcareous coral reef structures, is due to the chemical and mechanical activities of numerous and diverse biotic agents. These range in size from minute, primarily intra-skeletal organisms, the microborers (e.g., algae, fungi, bacteria) to larger and often externally-visible macroboring invertebrate (e.g., sponges, polychaete worms, sipunculans, molluscs, crustaceans, echinoids) and fish (e.g., parrotfishes, acanthurids, pufferfishes) species. Constructive coral reef growth and destructive bioerosive processes are often in close balance. Dead corals are generally subject to higher rates of bioerosion than living corals, therefore, bioerosion and reef degradation can result from disturbances that cause coral mortality, such as sedimentation, eutrophication, pollution, temperature extremes, predation, and coral diseases. The effects of intensive coral reef bioerosion, involving El Nino-Southern Oscillation, Acanthaster predation, watershed alterations, and over-fishing, are re-examined after ~20 years (early 1990s–2010). We review the evidence showing that the biologically-mediated dissolution of calcium carbonate structures by endolithic algae and clionaid sponges will be accelerated with ocean acidification. The CaCO3 budget dynamics of Caribbean and eastern tropical Pacific reefs is reviewed and provides sobering case studies on the current state of coral reefs and their future in a high-CO2 world.

Global ecological consequences of the 1982-83 El Nino-Southern Oscillation

(Selection) Physical Aspects of the El Ni#o Event of 1982-1983. The global view. Some historical perspective. Development of the Event of 1982-1983. Nutrients and Productivity During the 1982/83 El Ni#o. Enso cycle. The basinwide setting. Western Pacific. Eastern Pacific normal conditions. Eastern Pacific anomalous conditions. Productivity effects of El Ni#o. Coral Mortality and Disturbances to Coral Reefs in the Tropical Eastern Pacific. Coral bleaching. mortality and environmental correlates. Community effects. Interrupted coral growth and reef framework accumulation: indicators of severe event occurrences. Discussion and conclusions. Summary. The Effects of the El Ni#o/Southern Oscillation on the Dispersal of Corals and Other Marine Organisms. Oceanic currents in the tropical and subtropical Pacific. Oceanic currents during the 1982-83 El Ni#o. Transport of marine organisms in oceanic currents. Coral Mortality Outside of the Eastern Pacific During 1982-1983: Relationship to El Ni#o. ENSO and coral mortality. Detailed case study - great barrier reef. Detailed case study - San Blas islands, Panama. El Ni#o and the History of Eastern Pacific Reef Building. Background. The 1982-1983 El Ni#o event and eastern Pacific reefs. Evidence for past El Ni#o events. Ocean conditions and past El Ni#o events. Urvina bay, Galapagos islands. Discussion. Reef-Building Corals and Identification of ENSO Warming Episodes. Study sites. Methods. Stable Isotope records in corals. Trace Element Indicators of Climate Variability in Reef-Building Corals. Minor and trace element geochemistry of corals. Sample sites. Methods. Oceanic markers of El Ni#o. Historical Aspects of El Ni#o/Southern Oscillation - Information from Tree Rings. Tree rings as a source of information on past climate. Tree rings and the southern oscillation: An example application. Future directions. Summary. Effects of El Ni#o 1982-83 on Benthos, Fish and Fisheries off the South American Pacific Coast. Principal abiotic changes induced by EN 1982-83. The pelagic subsystem. The benthic subsystem. Effects of the 1982-83 El Ni#o-Southern Oscillation Event on Marine Iguana (Amblyrhynchus Cristatus Bell, 1825) Populations on Galapagos. Study area. Methods. Results. Discussion. The Gulf of Panama and El Ni#o Events: The Fate of Two Refugee Boobies from the 1982-83 Event. Natural history of the boobies. The occurrence. El Ni#o events and the gulf of Panama. Seabirds and the 1982-1984 El Ni#o/Southern Oscillation. Results. Discussion of effects and evolutionary consequences of ENSO. Conclusions and future work. El Ni#os Effect on South American Pinniped Species. Galapagos fur seal. South American fur seal. How the seal lions in Galapagos and Punta San Juan survived the El Ni#o event. Summary and Conclusions. Bottoms Beneath Troubled Waters: Benthic Impacts of the 1982-1984 El Ni#o in the Temperate Zone. Biological effects of the 1982-84 El BNi#o on temperate pelagic ecosystems. ENSO effects of kelp forests.

Extensive «bleaching» and death of reef corals on the Pacific coast of Panamá

Recent ‘bleaching’ and death of hermatypic (reef-building) corals has occurred extensively in Pacific Ocean waters of Panama (Gulf of Chiriqui), near the Panama-Costa Rica border. All hydrocorals ( Millepora spp.) and scleractinian corals (5 genera) have been affected to some degree in the non-upwelling environment of Chiriqui. No other members of the macrobenthos showed signs of stress (lowered activities, morbidity) or reduced abundance. The affected area, including the mainland, nearshore and offshore islands, and adjacent waters, is about 10,000 km 2 . Further surveys in the Gulf of Chiriqui may reveal even more extensive mortality. This disturbance began in the dry season (January–April 1983), during a period of clear skies, low rainfall, and minimal river drainage. I first observed large, ‘bleached’ coral patches (up to 100 m 2 in area) in mid-March, and observations by others indicate that coral ‘bleaching’ occurred in February and possibly as early as mid-January. Normal and ‘bleached’ corals observed in mid-March were ‘bleached’ and dead, respectively, by the end of April, suggesting that the disturbance is protracted. By the end of the dry season, 80 to 95% of all corals in the affected areas were severely ‘bleached’ or dead.

Coral Reef Growth in the Galápagos: Limitation by Sea Urchins

The regular echinoid Eucidaris thouarsii is a conspicuous omnivore on coral bottoms in the Gal�pagos. Unlike Eucidaris in Panama and mainland Ecuador, Gal�pagos Eucidaris are large and abundant and graze heavily in the open on live corals day and night. These differences are probably due in large part to more intense predation by fishes on mainland compared with island urchin populations. An assessment of coral growth versus coral attrition from grazing shows that Eucidaris interferes with the establishment of pocilloporid reef frame and therefore reduces reef growth in the Gal�pagos.

Environmental influences on skeletal banding in eastern Pacific (Panama) corals

The timing of skeletal band formation and concomitant changes in calcification rates and linear skeletal extension were investigated in Pavona corals growing under two distinct thermal regimes along the Pacific coast of Panama: fluctuating, marked by seasonal upwelling (Gulf of Panama) and stable, nonupwelling (Gulf of Chiriqui). The purpose of this study was to test the hypothesis that banding in corals is largely mediated by seasonal variations in temperature (Highsmith 1979). Our results indicate that the timing of band formation is synchronous at these two environmentally distinct locations. The low density (LD) portion of the annual band is accreted over a five month period (January–June) and represents an increase in linear skeletal extension (mm/mo.) as well as a marked increase in calcification rate (g CaCO3 · cm-2 · mo-1) relative to the high density portion which forms over the remaining seven month period (July through December). In contrast to the predictions of the Highsmith model these findings indicate that variations in light levels rather than fluctuation in temperature is a better correlate to changes in skeletal density. Qualitatively, banding patterns were similar at the two sites; however, higher growth rates (particularly with respect to the LD band) for Pavona clavus in the Gulf of Panama indicate that lower water temperatures and higher productivity, or both, may be responsible for quantitative differences in banding between sites. We found that formation of the HD band corresponds to lower light levels and the production of gametes. We propose that banding in corals is a complex phenomenon governed by endogenous processes (e.g. reallocation of energy from growth to reproduction) which may be mediated by exogenous factors (e.g light and productivity).

Clipperton Atoll (eastern Pacific) : oceanography, geomorphology, reef-building coral ecology and biogeography

Coral reef geomorphology and community composition were investigated in the tropical northeastern Pacific during April 1994. Three areas were surveyed in the Revillagigedo Islands (Mexico), and an intensive study was conducted on Clipperton Atoll (1,300 km SW of Acapulco), including macro-scale surface circulation, sea surface temperature (SST) climatology, geomorphology, coral community structure, zonation, and biogeography. Satellite-tracked drifter buoys from 1979–1993 demonstrated complex patterns of surface circulation with dominantly easterly flow (North Equatorial Counter Current, NECC), but also westerly currents (South Equatorial Current, SEC) that could transport propagules to Clipperton from both central and eastern Pacific regions. The northernmost latitude reached by the NECC is not influenced by El Niño-Southern Oscillation (ENSO) events, but easterly flow velocity evidently is accelerated at such times. Maximum NECC flow rates indicate that the eastern Pacific barrier can be bridged in 60 to 120 days. SST anomalies at Clipperton occur during ENSO events and were greater at Clipperton in 1987 than during 1982–1983. Shallow (15–18 m)and deep (50–58 m) terraces are present around most of Clipperton, probably representing Modern and late Pleistocene sea level stands. Although Clipperton is a well developed atoll with high coral cover, the reef-building fauna is depauperate, consisting of only 7 species of scleractinian corals belonging to the generaPocillopora, Porites, Pavona andLeptoseris, and 1 species of hydrocoral in the genusMillepora. The identities of the one Pocilpopora species and one of the twoPorites species are still unknown. Two of the remaining scleractinians (Pavona minuta, Leptoseris scabra) and the hydrocoral (Millepora exaesa), all formerly known from central and western Pacific localities, represent new eastern Pacific records. Scleractinian corals predominate (10–100% cover) over insular shelf depths of 8 to 60m, and crustose coralline algae are dominant (5–40% cover) from 0.5 to 7m. Spur and groove features, constructed of alternating frameworks ofPocillopora andPorites, and veneered with crustose coralline algae, are generally well developed around most atoll exposures. Although crustose coralline algae predominate in the breaker zone (with up to 100% cover), a prominent algal ridge is absent with only a slight buildup (ca. 10 cm) to seaward. Frequent grazing by the pufferfishArothron meleagris results in the removal of large amounts of live tissue and skeleton fromPorites lobata. Acanthaster planci is present, but rare. The grazing of large diadematid sea urchins, (2 species each ofDiadema andEchinothrix) on dead corals cause extensive erosion in some areas. Large numbers of corals on the 15–18 m terrace had recently suffered partial (P. lobata, 60–70% maximum of all colonies sampled) or total (Pocillopora sp., 80% maximum) mortality. The lengths of regenerating knobs and the rates of linear skeletal growth inP. lobata, determined by sclerochronologic analysis, indicated a period of stress during 1987. Massive skeletal growth is significantly higher at intermediate (16–17 m) than shallow (6–8 m) depths with mean extension rates of 1.5 mm yr−1 inP. lobata and 1.4 mm yr−1 inP. minuta at intermediate depths. Skeletal growth inP. lobata was depressed during the 1987 El Nifio event at Clipperton. The branching coralPocillopora sp. demonstrated high and similar skeletal growth rates at both shallow (25.4 mm yr−1) and intermediate (26.5 mm yr−1) depths. The presence of widely distributed Indo-Pacific zooxanthellate corals at Clipperton and the Revillagigedo Islands indicates that these NE Pacific Islands probably serve as a stepping stone for dispersal into the far eastern Pacific region.

State of coral reefs in the Galápagos Islands: Natural vs anthropogenic impacts

Abstract Before the 1982–1983 El Nino disturbance event low diversity coral communities and small, actively accreting coral reefs were present on Galapagos shallow shelves in areas protected from strong upwelling. Prolonged El Nino 1982–1983 sea warming resulted in 95–99% coral mortality, virtually eliminating corals throughout the archipelago. The population size of an ubiquitous, large sea urchin species (Eucidaris thouarsii) was unaffected by the warming event. Urchins later showed increased abundance on dead coral colonies and frameworks, and caused bioerosion that exceeded the net calcification capacity of disturbed reefs. Known human impacts on corals result mainly from anchor damage, the collection of corals for sale as curios, and mechanical damage resulting from the activities of fishermen. An evaluation of natural and anthropogenic damage to Galapagos coral communities indicates that natural disturbances, especially strong ENSO episodes, are of greatest concern. However, rapidly increasing human pressures could exacerbate the recovery capacity of naturally perturbed coral communities.

Lipid decline in stressed corals and their crustacean symbionts

Total lipid levels, determined by the phosphosulphovanihin colorimetric method, declined significantly in ramose scleractinian corals and their xanthid crab symbionts during the 1983 El NiA±owarming event on the Pacific coast of Panama. This decline was observed in a controlled laboratory experiment, employing host corals (Pociiopora damicornis) and obligate crab symbionts (Trapezia coraiina and Trapezia ferruginea), concurrently with morbidity and mortality observed on coral reefs in the field. Lipid levels decreased from 0.59% (dry weight) to 0.34% in normal versus affected and dead corals, and from 4.54% (dry weight) to 1.20% in normal versus affected and dead crabs in a two-week period. Lipid depletion in corals accompanied the loss of zooxanthellae and increased morbidity and death; in crabs, a decrease in the number of egg-carrying females, a high emigration rate, a slight increase in mortality, and a decline in defensive behavior occurred. These findings suggest that symbiotic crabs were deprived of food from their coral hosts who initially lost zooxanthellae, an event correlated with the prolonged El Nub sea warming.