coral bleaching

ate summer of 1987 seemed typi-cal for that time of year in theVirgin Islands. Huge, ßat-bot-

tomed cumulus clouds moved west-ward on light trade winds. Calm seaswere rarely disturbed by squalls sweep-ing into the northeastern Caribbean Seafrom the Atlantic Ocean. The only sug-gestion that something might be amisswas the water, which, though not sys-tematically measured, seemed unusual-ly warm to people swimming near theshallow coral reefs.

Something atypical had indeed oc-curred. The normally golden-brown,green, pink and gray corals, sea whipsand sponges had become pure white.In some cases, entire reefs were so daz-zlingly white that they could be seenfrom a considerable distance. In otherareas, pale corals punctuated the reefsurface while unbleached corals of thesame species grew as neighbors.

The phenomenon, which can be le-thal to coral, was not conÞned to theVirgin Islands. Observers at numerousmarine laboratories in the Caribbean

noted the same whitening. Nor was it the Þrst occurrence of such bleaching.In 1982 and 1983, after the atmosphericand oceanographic disturbance called ElNi�o/Southern Oscillation (ENSO), cor-als in certain areas of the Florida Keyswhitened and died, and oÝ the coast ofPanama mortality reached 50 percent.But it was only between 1987 and 1988,also an ENSO year, that reports of exten-sive bleaching became widespread. Theyhave increased in frequency ever since.

The association of coral bleachingwith ENSO, which ushers in warm wa-ter, and with water temperatures twoto three degrees Celsius above normalhas led some scientists to suggest thatthe bleaching is a manifestation of glob-al warming. Others point out that coralreefs have been studied only for a fewdecadesÑtoo short a time to permitgeneralized conclusions about a poorlyunderstood event.

Nevertheless, coral reefs around theworld are suÝering bouts of bleach-ing from which many do not recov-er. Although several factors can causethe processÑincluding disease, excessshade, increased ultraviolet radiation,sedimentation, pollution and changes insalinityÑthe episodes of the past de-cade have consistently been correlatedwith abnormally high seawater temper-atures. Understanding the complex pro-

BARBARA E. BROWN and JOHN C. OG-DEN work on international issues of coralreef ecology and management. Brown isdirector of the Centre for Tropical Coast-al Management and is reader in tropicalmarine biology at the University of New-castle upon Tyne in the U.K. She is alsoa founder of the International Societyfor Reef Studies. Ogden is the director ofthe Florida Institute of Oceanography andprofessor of biology at the University ofSouth Florida. He has served as a mem-ber of the faculty and as the director ofthe West Indies Laboratory in St. Croix,where he began his work on coral reefs.

64 SCIENTIFIC AMERICAN January 1993

Coral BleachingEnvironmental stresses can cause irreparableharm to coral reefs. Unusually high seawater

temperatures may be a principal culprit

by Barbara E. Brown and John C. Ogden

BOULDER CORAL has bleached only inpartsÑthe rest remains healthy for now.Although several factors cause potential-ly lethal whitening, recent bouts havebeen consistently correlated with higherthan average seawater temperatures.

Copyright 1992 Scientific American, Inc.

cess of bleaching can help pinpoint, andperhaps eventually deter, this threat tothe ecology of the reefs.

Tropical, shallow-water ecosystems,coral reefs are found around theworld in the latitudes that general-

ly fall between the southern tip of Flori-da and mid-Australia. They rank amongthe most biologically productive of allmarine ecosystems. Because they harbora vast array of animals and plants, coralreefs are often compared to tropical rainforests. Reefs also support life on landin several ways. They form and maintainthe physical foundation for thousandsof islands. By building a wall along thecoast, they serve as a barrier againstoceanic waves. And they sustain the Þsh-eries and tourist diving industries thathelp to maintain the economies of manycountries in the Caribbean and PaciÞc.

Although corals seem almost architec-tural in structureÑsome weigh manytons and stand between Þve and 10 meters highÑthey are composed ofanimals. Thousands of tiny creaturesform enormous colonies: indeed, nearly60 percent of the 220 living genera ofcorals do so. Each colony is made up ofmany individual coral animals, calledpolyps. Each polyp is essentially a hol-low cylinder, closed at the base and in-terconnected to its neighbors by the gutcavity. The polyps have one or morerings of tentacles surrounding a centralmouth. In this way, corals resemble seaanemones with skeletons. The soft ex-ternal tissues of the polyps overlie ahard structure of calcium carbonate.

Many of the splendid colors of coralscome from their symbionts, creaturesthat live in a mutually dependent re-lation with the coral. Symbiotic algae

called zooxanthellae reside in the oftentransparent cells of the polyps. Thereare between one and two million algaecells per square centimeter of coral tis-sue. Through photosynthesis the algaeproduce carbon compounds, which helpto nourish the coralÑsome species re-ceive 60 percent of their food from theiralgae. Algal photosynthesis also acceler-ates the growth of the coral skeleton bycausing more calcium carbonate to beproduced. The corals provide algae withnutrients, such as nitrogen and phos-phorus, essential for growth, as well aswith housing. The association enables al-gae to obtain compounds that are scarcein the nutrient-poor waters of the trop-ics (where warm surface waters overlieand lock in cold, nutrient-rich watersÑexcept in restricted areas of upwelling).

When corals bleach, the delicate bal-ance among symbionts is destroyed.

SCIENTIFIC AMERICAN January 1993 65Copyright 1992 Scientific American, Inc.


The corals lose algae, leaving their tis-sues so colorless that only the white,calcium carbonate skeleton is apparent.Other organisms such as anemones, seawhips and spongesÑall of which harboralgae in their tissueÑcan also whiten inthis fashion. Some of this loss is routine.A healthy coral or anemone continuous-ly releases algae, but in very low num-bers. Under natural conditions, less than0.1 percent of the algae in a coral islost during processes of regulation andreplacement. When subject to adverse

changes, such as temperature increas-es, however, the corals release increasednumbers of algae. For example, trans-ferring coral from a reef to a laboratorycan cause a Þvefold elevation in thenumbers of algae expelled.

The mechanism of algal release is notfully understood. Even deÞning bleach-ing remains tricky. The current deÞni-tion has its basis in laboratory mea-surements of the loss of algae and thereduction in algal pigments. The labo-ratory approach, however, is rarely, if

ever, applied in the Þeld. There judg-ment must rely on the naked eyeÕs abil-ity to detect loss of coloration. Althoughsuch methods may be reliable for in-stances of severe bleaching, a determi-nation that pale colonies are bleachedcan be extremely arbitrary, given thenatural variability of pigmentation.

In some cases, normal coral under-going an adaptive behavioral responsecan look bleached. In 1989, while work-ing at the Phuket Marine Biological Cen-ter in Thailand, one of us (Brown) ob-served that some intertidal coral spe-ciesÑthose that thrive in shallow waterand are exposed to the air at low tideÑ

CORAL REEFS (red) thrive around the world in tropical, shal-low watersÑthose areas falling between the lines. They are

the most biologically productive of all marine ecosystems.Coral reefs also support life on land by providing a barrier

Some of the SpeciesThat Thrive on Coral Reefs

SPINY LOBSTER QUEEN CONCH LOGGERHEAD SPONGE SEA ANEMONE BUTTERFLY FISH

PACIF IC OCEAN ATLANTIC OCEAN

CARIBBEANSEA

EQUATOR


appear completely white during lowspring tides. It became clear that thesecorals are able to pull back their exter-nal tissues, leaving their skeletons ex-posed; they do not lose their algae.This behavior should perhaps be moreaccurately described as blanching, a re-sponse that may reduce desiccation dur-ing exposure to air.

Despite the absence of an unassail-able deÞnition of the bleaching pro-cess, several mechanisms have beenproposed that may be at work. In 1928Sir Maurice Yonge and A. G. Nicholls,who participated in an expedition to theGreat Barrier Reef, were among the Þrst

to describe coral bleaching. They sug-gested that algae migrated through cor-al tissue in response to environmentalstress, before being released into thegut and ultimately expelled through themouth. The precise trigger for the re-lease and the stimulus causing the algaeto be so conveyed were unknown thenand remain largely unknown today.

One of the several theories proposedby Leonard Muscatine of the Universi-ty of California at Los Angeles is thatstressed coral polyps provide fewer nu-trients to the algae. According to thistheory, the algae would not necessar-ily be directly aÝected by, say, hightemperature, but the metabolism of thecoral would be lowered. Supplies ofcarbon dioxide, nitrogen and phospho-rus would become insuÛcient, and thisrationing would in turn cause the algaeto abandon their residence.

In addition, Muscatine, R. GrantSteen and Ove Hoegh-Guldberg, also atU.C.L.A., studied the response of anem-ones and corals to changes in temper-ature, light and salinity. They describedthe release of algae from the tissues intothe gut cavity and hypothesized that the coral was actually losing animal tissue along with the algal cells. Work by Suharsono at the University of New-castle upon Tyne supported this idea.He showed that anemones exposed towarmer temperatures in the laborato-ry lose their own cells and algal cells during bleaching. Thus, host tissuethinned signiÞcantly, perhaps reducingthe space available for the algae.

The direct release of algae into thegut, however, may be a mecha-nism of algal loss that results

only from the extreme shocks invokedin a laboratory. It is not yet clear thatalgae behave the same way in corals in situ. Under natural conditions, it isquite likely that algae are released by a variety of mechanisms. All experi-mental work carried out on bleachinghas involved exposure to extreme tem-perature changesÑthat is, increases ofsix degrees C or more over a period of16 to 72 hours. In nature the tempera-ture increases that induce bleachingare much smaller, about two degrees C,and may occur over several months.

Another hypothesis suggests that al-gae emit poisonous substances whenthey experience adverse conditions and

that these toxins may deleteriously af-fect the host. Algae produce oxygencompounds, called superoxide radicals,in concentrations that can damage thecoral. (Molecular oxygen is relativelyunreactive, but it can be chemically al-tered to form the superoxide radical.)An enzyme, superoxide dismutase, inthe coral detoxiÞes the radicals.

But Michael P. Lesser and his col-leagues at the University of Maine not-ed that in certain cases oxygen toxicitycould lead to bleaching. Although Les-ser and his team were unable to mea-sure the oxygen radicals directly, theyfollowed the production of superoxidedismutase. They found that exposureto elevated temperatures and to in-creased ultraviolet radiation indepen-dently spurred enzymatic activity. Theresearchers concluded that oxygen tox-icity could be responsible for bleachingbecause harmful oxygen radicals wereexported from the damaged algae tothe animal host.

Other biochemical changes may takeplace as well. David Miller of the Univer-sity of Leeds and students from BrownÕslaboratory suggest that alterations ingene expression occur as a response to deleterious environmental changes.These changes may involve the synthe-sis of heat-shock proteinsÑcompoundsfound in all living systems subject toadversity that serve to protect cells tem-porarily from heat damage. Miller deter-mined that these proteins are enhancedin anemones undergoing heat shock.Furthermore, in anemones that toleratetemperature increases, the presence ofproteins appears to be correlated withreduced bleaching during heat shock.

Genetic variability also plays an im-portant role in bleaching. Environmen-tal factors may aÝect species of algae orcoral in diÝerent ways. Of course, pre-dicting the ability of corals and their algae to adapt to increases in seawatertemperature or global climatic changemay be possible by identifying the typesof corals or algae at highest risk.

When working together at the Uni-versity of California at Santa Barbara,Robert K. Trench and Rudolf J. Blankshowed that diÝerent corals act as hoststo varied strains of algae. Subsequent-ly, Rob Rowan and Dennis A. Powers ofStanford University have found that al-gae living in a single species of coral aregenetically similar in composition but

SCIENTIFIC AMERICAN January 1993 67

against oceanic waves and by formingthe foundation for thousands of islands.

SEA CUCUMBER CROWN-OF-THORNS STARFISH PARROT FISH SQUID SEA URCHIN COMB JELLY TUBE WORM

ARABIANSEA

INDIANOCEAN


genetically diÝerent from algae in othercoral species. Certain algae may proveto be particularly sensitive to tempera-ture and may have varying temperaturetolerances. If so, Rowan and PowersÕsÞndings would help explain why relat-ed, but not identical, corals exposed towarmer temperatures frequently showdiÝerent susceptibilities to bleaching.

Alternatively, the variability may liewith the coral instead of the algae. Stud-ies of several species of coral have indi-cated that genetically dissimilar strainsexist within a species of coral. Suchstrains may have diÝerent environmen-tal tolerances, which could account forthe observation that one colony of aparticular species appears to have beenbleached while a nearby member of thesame species has not been.

The reports of bleaching in the Ca-ribbean in the 1980s seem to be relatedmost consistently to elevated sea tem-peratures. Coral reefs normally thrivebetween 25 and 29 degrees C, depend-ing on their location. When patternsdepicting coral diversity are plotted ona globe, it is apparent that diversity declines as the reefs get farther away

from two centersÑone in the Indo-Pa-ciÞc and the other in the Caribbean.The outlines of a map marking plum-meting diversity coincide with the con-tours of lower seawater temperatures.

The narrow temperature range forhealthy coral is very close to its upperlethal temperature: an increase of oneto two degrees above the usual sum-mer maximum can be deadly. Paul Joki-el and Stephen Coles of the Universityof Hawaii have shown that bleachingand coral mortality are not induced bythe shock of rapidly ßuctuating temper-atures but are a response to prevailinghigh temperatures and to signiÞcant de-viations above or below the mean.

Many times during a 10-monthperiod in 1982Ð1983, an unusu-ally severe ENSO warmed the

waters of the eastern PaciÞc three tofour degrees C over the seasonal aver-age. Peter W. Glynn and his colleaguesat the University of Miami tracked theevent and the subsequent developmentsin that region. As a result of elevatedtemperatures, coral reefs underwentbleaching. Between 70 and 90 percent

of the corals in Panama and Costa Ricaperished several weeks later; more than95 percent of the corals in the Gal�pa-gos were destroyed.

Glynn and Luis DÕCroz of the Univer-sity of Panama also linked coral mortal-ity with high temperatures in a series oflaboratory experiments that duplicatedÞeld conditions during ENSO. The ma-jor reef-building coral of the easternPaciÞc, Pocillopora damicornis, took thesame amount of time to die in the lab-oratory at 32 degrees C as it did in theÞeld, indicating that the experimentshad replicated the natural condition.Glynn and DÕCroz also suggested thatthe temperature disproportionately af-fected types of coral that normally expe-rienced seasonal upwelling of deep, coolwater in the Gulf of Panama.

Evidence for the 1987 warming of theseawater in the Caribbean is not as de-Þnitive. Donald K. Atwood and his col-leagues at the Atlantic Oceanographicand Meteorological Laboratory in Miamiexamined the National OceanographicData CenterÕs sea-surface temperaturerecords from 1932 to the present andfound no discernible long-term increasesin seawater temperature in the Caribbe-an. The monthly mean sea-surface tem-perature did not exceed 30.2 degrees Cin any of the regions examinedÑin otherwords, the water remained well below the32 degrees C required to induce bleach-ing in GlynnÕs laboratory experiments.

Atwood also examined the maps fromthe National Climate Data Center of theNational Oceanic and Atmospheric Ad-ministration (NOAA). These records pro-vide average monthly sea-surface tem-perature and track anomalies derivedfrom satellite data that are validated bymeasurements taken from ships. Themaps indicate that in 1987 the surfaceof the Caribbean was generally less than30 degrees C. Other groups examinedsimilar temperature records and con-cluded that the temperatures of somesectors of the Caribbean reached 31 de-grees C or more during 1990, anotheryear of bleaching.

The records, of course, are subject tointerpretation based on the geographicscale of the satellite measurements andthe integration of these data with in situmeasurements. Unfortunately, there areno long-term temperature records takenat the small geographic scale needed toclarify the cause of damage to corals.

The 1987 reports of coral bleachingcoincided with escalating concern aboutglobal warming. It was not surprising,therefore, that some scientists and oth-er observers reached the conclusionthat coral reefs served as the canary inthe coal mineÑthe Þrst indication ofan increase in global ocean tempera-


Anatomy of a Coral Polyp

he coral animal is essential-ly a digestive sac—including

related organelles, or mesenterialfilaments—overlying a skeleton

Tof calcium carbonate. Itstentacles pull in food fromthe seawater. Algae calledzooxanthellae thrive in asymbiotic relation with thecoral. The algae sustain thecoral with oxygen and foodand also stimulate produc-tion of the skeleton, whichcan grow 10 centimeters a year. The coral, in turn,provides a home for the al-gae in its tissues and makesavailable nutrients such asnitrogen and phosphorus.

STINGINGCELL

MESENTERIALFILAMENTS

SKELETON

ZOOXANTHELLAEGULLET

TENTACLES


SCIENTIFIC AMERICAN January 1993 69

tures. Although it appears that elevat-ed local seawater temperatures causedbleaching, linking this eÝect to globalwarming cannot be conclusive at thistime. With the support of the Nation-al Science Foundation, NOAA and theEnvironmental Protection Agency, reefscientists and climatologists convened inMiami in June 1991 to discuss coral reefsand global climatic change. The work-shop determined that reports of coralbleaching were indicative of threats tothe ecosystem and that bleaching did ap-pear to be associated with local tempera-ture increases. But the paucity of knowl-edge about the physiological responseof corals to stress and temperature, theinadequacy of seawater temperature rec-ords and the lack of standardized pro-tocol for Þeld studies made it impossi-ble to decide whether bleaching reßectsglobal climatic change in the ocean.

Several international monitoring ef-forts are now in progress or are plannedso that the appropriate data can begathered. For example, the CaribbeanCoastal Marine Productivity Program, acooperative research network of morethan 20 Caribbean marine research in-stitutions in 15 countries, was foundedin 1990 and began systematic observa-tions of coral reefs in 1992. Other net-works of marine laboratories have beenproposed in the central and westernPaciÞc Ocean.

Whatever its cause, bleaching hasimportant implications for thecommunity structure, growth

and accretion of coral reefs. Develop-ing countries are particularly dependenton coral reefs for food resources andhave made heavy investments in reef-related tourism. Bleaching, added tothe accumulated toll taken by pollutionand overÞshing, may seriously burdenthe future economies of many nations.

The death of coral over such a widegeographic range in the eastern Pacif-ic during the 1982Ð1983 ENSO had se-vere biological repercussions. Before thewidespread bleaching, Glynn and hiscolleagues noticed that large Þelds ofPocillopora served to protect more mas-sive coral species from the coral-feed-ing crown-of-thorns sea star (Acanthas-

ter planci ). The starÞsh did not ventureacross the dense coral stands, because

SEAWATER TEMPERATURE ßuctuationsin the Caribbean Sea in 1990 were trackedby satellite. Temperatures reached be-tween 31 and 32 degrees Celsius (red ) incertain areas during the months of Au-gust (top), September (middle) and Octo-ber (bottom). Such unusually warm wateris believed to cause coral reefs to bleach.



Pocillopora repelled it with the stingingcells of its tentacles. In addition, sever-al species of symbiotic shrimp and crabin the Pocillopora attacked the sea stars,driving them away. As a result of warm-er water, however, Pocillopora suÝeredhigher mortality and lower fecundi-ty, and large corals were consequentlyopen to attack by the sea star. The pred-atory crustaceans were also aÝected.Because they normally feed on the lip-id-rich mucus produced by the Pocillo-

pora coral, a decline in the quantityand lipid content of the mucus broughtabout by the thermal stress triggered adecrease in the crustacean population.

The massive reduction in coral coveron the reefs of Panama and the Gal�pa-gos in 1982 and 1983 also restrictedthe range of one species of hydrocoralcalled Millepora and caused the appar-ent extinction of another species of thesame genus. Glynn and W. H. de Weerdt,now at the University of Amsterdam Zoo-logical Museum, speculate that thesespecies of corals were most severely aÝected because of their limited rangeand extreme sensitivity to increases in temperature. The disturbance alsocaused a nearly complete interruptionin the long-term accumulation of calci-um carbonate on the reefs of the region.

The fact that healthy reefs ßourishedin the eastern PaciÞc Ocean before 1982indicates that an event of this magni-tude is rare. Glynn estimated the age oftwo species of corals that were killedor heavily damaged in the Gal�pagosby multiplying their radius by their an-

nual growth rate of approximately onecentimeter. He concluded that an ENSOlike that of 1982Ð1983 had not occurredin the Gal�pagos for at least 200 years,possibly 400. The estimate is similar forcorals in Panama. Interestingly, even attheir most healthy, the coral reefs of theeastern PaciÞc are less well developedthan those of the Caribbean. Their com-paratively meager development may bepartly explained by the relatively fre-quent high- and low-temperature dis-turbances over thousands of years.

The coral frameworks of the reefs of Panama and the Gal�pagos havechanged dramatically as a result of thebleaching. Large areas of dead coralhave become colonized by benthic al-gae, which in turn support increasedpopulations of herbivores, particularlysea urchins. Sea urchins are grazers;they scrape the coral rock surface of thereef as they feed, contributing to theerosion of the reef structure.

Glynn and Ian Macintyre of theSmithsonian Institution and Gerard M.Wellington of the University of Hous-ton have estimated the rates of cal-cium carbonate accretion and erosionon the reef. The rates of erosion af-ter the 1982Ð1983 ENSO attributable tosea urchins alone are greater than therates of accumulation on the healthyreefs before 1983. This Þnding sug-gests that without recovery of coral pop-ulations, these reefs will soon be re-duced to carbonate sediments. Becausethe grazers erode the reef surface, theymay also interfere with the recruitment

of new coral colonies, prolonging, oreven preventing, their recovery.

Coral became bleached at many oth-er places in the Indo-PaciÞc during the1982Ð1983 ENSO, including the Socie-ty Islands, the Great Barrier Reef, thewestern Indian Ocean and Indonesia.Brown and Suharsono noted widespreadbleaching and loss of as much as 80 or 90 percent of the coral cover on theshallow coral reefs of the Thousand Is-lands in the Java Sea. The corals mostaÝected were on the shallow reef tops.Five years later coral cover was only 50percent of its former level.

The extent of bleaching, environ-mental tolerances and the life-his-tory characteristics of the domi-

nant corals determine whether a reef re-covers from the loss of most of its livingcoral. So do the nature and timing of oth-er disturbances, such as predation andgrazing. When bleaching is severe or pro-longed, the coral may die. If the bleachingepisode is short, the coral can rebuild itsalgal population and continue to live,but biological processes such as growthand reproduction may be impaired.

Because we are only now forming net-works of sites that will conduct coop-erative observations, the extent of coralreef damage brought about by bleach-ing has not been globally assessed. In 1987 Ernest H. Williams, Jr., of the Uni-versity of Puerto Rico collected reports of bleaching from nearly every tropicalocean region. But until we have an ade-quate deÞnition of coral bleaching inthe Þeld and have standardized our ob-servations, the global impact of coralbleaching will remain a mystery.

If the temperature increase of one ortwo degrees C, predicted by the Inter-governmental Panel on Climate Change,does take place over the next 50 yearsin the tropical latitudes, the consequen-ces for coral reefs could be disastrous.Unlike the miners with the canary, wecannot yet link bleaching to a clearcause. But that does not mean we shouldignore the coralÕs message.

FURTHER READING

GLOBAL ECOLOGICAL CONSEQUENCES OFTHE EL NINO SOUTHERN OSCILLATION1982Ð83. Edited by Peter W. Glynn. El-sevier, Amsterdam, 1989.

CORAL BLEACHING. Edited by Barbara E.Brown. Special Issue of Coral Reefs, Vol.8, No. 4; April 1990.

WORKSHOP ON CORAL BLEACHING, COR-AL REEF ECOSYSTEMS AND GLOBALCHANGE: REPORT OF PROCEEDINGS. Or-ganized by Christopher F. DÕElia, Rob-ert W. Buddemeir and Stephen V. Smith.Maryland Sea Grant College, 1991.

INTERTIDAL CORALS in Thailand ÒblanchÓ when exposed to the air. Unlike bleach-ing, this phenomenon appears to be adaptive: the coral polyps retract their soft tis-sues during low tide, leaving the calcium carbonate skeleton exposed. When waterwashes over again, the polyps and tentacles expand to cover the skeleton.

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coral bleaching

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