Bleaching and Reef Community Change in Jamaica: 1951-1991

AMER. ZOOL., 32:683-695 (1992)

Bleaching and Reef Community Change inJamaica: 1951-1991'

THOMAS J. GOREAU

Global Coral Reef Alliance, 324 North Bedford Road,Chappaqua, New York 10514

SYNOPSIS. Coral reefs have deteriorated at an accelerating pace during40 years of ecological study at 11 sites around Jamaica. This is due to avariety of causes, whose effects are analyzed by comparing sites withknown and divergent histories of environmental change. Degradative fac-tors include overgrowth by algae, sponges, and soft corals, eutrophicationby sewage nutrients, reduced herbivory due to overfishing and naturalcauses, hurricanes, sedimentation, diver and boat damage, and coralbleaching. These stresses have very different histories and gradients atdifferent sites, allowing separation of their effects. Mass coral bleachingis apparently a novel phenomenon of the past decade. Non-parametricstatistical analysis of relative stresses at the 11 sites shows that its patternin space and time is unrelated to previously existing stresses.

METHODS

Diving as a long-term ecological researchtool was started in Jamaica in 1951 by thelate Thomas F. Goreau. Its use by his col-leagues and students may make Jamaicanreefs the longest directly observed sub-marine ecosystem. During the 1950s and1960s reefs all around Jamaica were pho-tographed, mapped, bathymetrically pro-filed, and their species and ecology described(Goreau, 1956, 1959; Goreau and Goreau,1973; Goreau, unpublished). Detailed fieldnotes provide unique baseline data for eval-uating changes during the 1970s and 1980s.Before dying in 1970, T. F. Goreau startedthe Port Royal Marine Laboratory on theSouth Coast and the Discovery Bay MarineLaboratory on the North Coast. Over 500subsequent publications from those labs arewell known, but these important contribu-tions are not reviewed here as many focuson single sites or species, over relatively shortperiods.

Reefs were studied with numerous col-leagues by a variety of methods, includingsnorkeling, SCUBA diving, photography,photographic quadrats, line transects, sonar

1 From the Symposium on Long-Term Dynamics ofCoral Reefs presented at the Annual Meeting of theAmerican Society of Zoologists, 27-30 December 1991,at Atlanta, Georgia.

profiling, side-scan sonar (P. Goreau, 1990),drilling, and other techniques. Direct fieldobservations have been repeated as fre-quently as circumstances permitted, andsupplemented by detailed discussions withlarge numbers of individual divers, fisher-men, and scientists with long and reliableknowledge of particular sites. The primarytechnique used is detailed and sustainedobservation of species distributions, naturalhistory, and environmental history. Thefocus has been on corals, the major pro-ducers of reef framework, along with algae,which now dominate biomass at many sites.Large areas of reefs are surveyed by snor-keling long distances, observing coral andalgal species abundance and distributionpatterns (e.g., Table 1), and supplementedby close-up observation of all corals andalgae during dives at representative sitesbased on snorkel surveys. Species lists canbe used to record numbers, variants, anddistribution patterns of individual species.Species distribution patterns are inferredfrom what are effectively thousands ofobservations. Interactions between speciesand environmental gradients affecting coralcover and growth rates are noted. Coralgrowth rates in Jamaica have been studiedby repeated observation, photography, res-pirometry (Goreau, 1956, 1963; Porter,1985), radio-isotopes (Goreau and Goreau,

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684 THOMAS J. GOREAU

TABLE 1. Negril coral abundances and bleaching.'

Coral species

Millepora complanata*Millepora squarrosa*Millepora alcicornis*Stylaster roseusStephanocoenia micheliniiAcropora palmataAcropora cervicornisAcropora proliferaMadracis decactisMadracis mirabilisMadracis pharensisMadracis formosaAgaricia agaricites*Agaricia lenuifoliaAgaricia undaiaAgaricia fragilis*Agaricia lamarcki*Agaricia grahamaeHelioseris cucullataSiderastrea siderea*Siderastrea radians*Porites porites*Porites furcataPonies divancataPorites astroides*Porites brannenFavia fragum*Diploria strigosa*Diplona clivosa*Diploria labyrinthiformis*Maniana areolata*Colpophyllia nalans*Montastrea annularis*Montastrea cavernosa*Solenastrea hyadesAstrangia solitariaPhyllangia americanaOculina dtffusaOculina valenciennesiiMeandrina meandrites*Dichoecenia stokesiDendrogyra cyhndrus*Mussa angulosaIsophyllia sinuosaIsophyllastrea rigidaMycelophyllia lamarckanaMycetophyllia feroxMycetophyllia aliciaeMycelophyllia danaanaMycetophyllia reesiEusmilia fastigiata*Tubastrea coccineaScolymia laceraScolymia cubensisCladocora arbuscula

Aug. I960

commonnot reportednot reporteduncommondeeper waterabundantcommonnot reporteduncommoncommonnot seennot seencommonnot reportednot reportedcommonnot reportednot reportedcommoncommoncommonuncommoncommonnot reportedabundantnot reportedcommoncommoncommoncommoncommoncommoncommoncommonnot seencommoncommonnot seennot seencommoncommonrarecommoncommoncommoncommonnot reportednot reportednot reportednot reportedcommonnot seennot reportednot reportednot reported

Nov. 1991

commonnot seencommonuncommonuncommonrarerarenot seennot seencommonnot seennot seencommonnot seencommoncommoncommonnot seennot seencommoncommonuncommoncommonuncommonabundantnot seencommoncommoncommoncommoncommoncommoncommonvery commonnot seennot seennot seennot seennot seencommoncommonrareuncommoncommoncommoncommonnot identifiednot identifiednot identifiednot identifiedcommonnot seenuncommonnot seennot seen

Bleaching

2-2--11--1--1-233--9612-2-43213227-----53I-232----1-1--

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CORAL REEF CHANGE IN JAMAICA 685

1959, 1960), sclerochronology (Dodge et ai,1974; Goreau, 1977; Huston, 1985; Teal,1986; Goreau et ai, 1988; Goreau andDodge, unpublished), non-destructive in situgrowth measurements (Goreau and Mac-farlane, 1990), and other techniques.

Many species which are relativelyuncommon, have broad distribution ranges,or are sporadic in distribution, provide littleenvironmental information. Some havepuzzling patterns: the brown alga Turbi-naria turbinata was very common, van-ished for no obvious cause, and was laterreplaced by Turbinaria tricostata. A num-ber of species tend to be more abundant incertain areas which are shallow, deep, rough,calm, near to or away from freshwater, orare more tolerant or intolerant of sediment,nutrient, or temperature stress (Goreau,1959). Changes in the abundances of theseindicator species can be strongly indicativeof changing environmental conditions. Somealgae are strong indicators of herbivorybecause of different feeding preferences ofmajor herbivores (Sammarco, 1982a, b;Lewis, 1986; Liddell and Ohlhorst, 1986;Hughes et ai, 1987; Goreau and Goreau,1988). The red alga Liagora is normally veryrare but quickly becomes dominant overlarge areas for about a year after hurricanes.Many algae are sharply zoned along stressgradients, making them useful for charac-terizing degree of eutrophication stress fromexternal nutrients. Sewage stimulates greenalgae such as Enteromorpha, Ulva, Chae-tomorpha, and other species capable ofpolyphosphate storage, which dominate nearsewage outfalls. With distance green, red,and then brown algae generally predomi-nate. In submarine springs with high nitrateand low phosphorus contents, red algae,

including Ceramium, Acanthophora, andHypnea co-dominate with greens like Cla-dophora and Bryopsis. Algal overgrowth ofthe reef is seen in reef habitats where nitrateis as low as a few micromoles per liter(Lapointe et ai, 1988). Good indicator spe-cies of sediment and sewage stress are alsofound among some sponges which are zonedalong stress gradients (Goreau, 1992).

This paper summarizes general island-wide changes over the past 40 years seen byrepeated direct observation, focusing oneleven sites (Fig. 1). These sites, about a fifthof those examined, were chosen because theyare representative of larger areas or havestrong gradients in various stress factors.Their ecological history has been followedover all or most of the period. Although allstresses probably act to some degree at allsites, their intensity and duration varygreatly among sites, allowing effects of majorstresses to be separated.

COMPARATIVE ENVIRONMENTAL HISTORIESOF SITES

1) HellshireHellshire is the most intensely and longest

stressed reef site in Jamaica. Over a millionpeople, or half the island's population, livenearby. Kingston Harbour outflow is pusheddirectly towards these reefs by currents.These reefs are exposed to the most pollutedwaters in Jamaica, into which almost all thecountry's industrial wastes, commercialpollutants, ship traffic, hydrocarbons, andsewage effluents flow. The area is stronglyaffected by high turbidity from erosion ofdeforested mountains around Kingston, andby sediment plumes from the Yallahs Riverto the East during rainy seasons. Dredging

1 Coral species as listed in T. F. Goreau, 1960, generally ammended for later species name changes. Therestill remains taxonomic uncertainty in certain genera, particularly Agaricia, Montastrea, and Mycetophyllia.Underlined species have either undergone largest reductions in abundance, or are the most abundant specieswhich were highly bleached. Species marked by asterisks have been greatly affected by bleaching in Jamaicaduring severe episodes, and may have largely recovered at the time of the survey (late November 1991, afterstrong storms had lowered water temperatures). Relative abundances were noted on long transects by SCUBAor snorkelling. Bleaching frequency was estimated on a 10 point scale, where - indicates the species was notseen or too rare for bleaching frequency to be meaningful, 1 indicates that at least one of those seen were bleached,and 10 indicates that all coral heads showed signs of bleaching over part or all of their surface. Most speciesnot seen bleached were very rare or are small solitary coral species which lack symbiotic algae. Estimates arepooled based on all observations, and are probably accurate to within plus or minus 10%.

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LIMESTONE JAMAICA

CURRENTKILOMETRES

10 20 30 40

URBAN AREAS

<50,000 •

>50,000 •

>1,000,000FIG. 1. Map of Jamaica showing sites discussed in text. Major population centers are indicated by size. Coastalcurrent directions are indicated by arrows. North is at top. Map by Dr. Peter D. Goreau.

for airport construction and ship channelmaintenance has caused episodic impactsfrom resuspended sediment plumes. In theearly 1950s the reefs of Hellshire were sub-ject primarily to high turbidity, and hadprobably been so for at least three centuries.Dominant corals were those adapted to highenergy and high turbidity. Open exposureto the east causes heavy wave activity underall but calmest conditions. Much damageoccurred after Hurricane Charlie in 1951(Goreau, 1956). During the 1950s these reefswere gradually overgrown by algae, and bythe mid 1960s were largely dead.

2) Port Royal CaysThe Port Royal Cays, a few kilometers

east of Hellshire, are reefs around smallsandy islands on the sediment-impactedSouth coastal shelf (Goreau and Burke,1966). Strong westward currents place themupcurrent of the harbour mouth, so they

receive only a tiny fraction of the land-derived pollution in the Hellshire area. Beingnear the ship channel entrance, they are pre-sumably affected by ship-derived hydrocar-bon emissions. Although off the driest partof the island (less than 70 cm rain per year),turbidity is high due to current-transport oferoded soils, resuspended sediment, andflocculent organic particles. Turbidity isespecially high during rainy seasons, sincethe area is downcurrent from the mouth ofthe Yallahs River, which drains some of thesteepest and most erodible soils in Jamaica.Catastrophic landslides have occurred, withone town completely buried by slumping ofa mountainside in 1692. Deforestation bythe current coffee boom is once again push-ing up to the crests of the highest mountainsin the island, deforested and then aban-doned during the coffee boom which endedin the early 1800s, and likely to increaseerosion further. These reefs were strongly

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affected by Hurricane Charlie, but largebanks of Acropora occurred in the 1950s,especially in southern parts (Goreau, 1956).Following hurricane rains in 1963, exten-sive local bleaching occurred (Goreau,1964). Very little Acropora is now to be seen,sediment stress is very high, the coral faunais primarily made up of sediment-tolerantcorals, and the sponge and gorgonian bio-mass exceeds that of corals. Mass coralbleaching has only slightly affected thesereefs. During the 1989 bleaching event, whenaround 80% of corals along the north coastwere bleached, frequency of bleaching in theCays was no more than 5%, and water tem-peratures were noticeably colder on the southcoast reefs.

3) Eastern PortlandThese reefs lie along the most exposed

coasts on the island, subject to full force ofhurricanes and tropical storms arriving overopen water. Wave action is dangerouslystrong at most times, and reflected by mas-sive boulders and slumped reef blocksunderwater (Goreau, 1956; Goreau andGoreau, 1973). The corals are a veneer ofwave-adapted species rather than a trueconstructional reef framework. This area isupstream from all human influence inJamaica, and lies near the rainiest part ofthe island (over 7 meters per year, around2 centimeters per day). The area is virtuallyuninhabited, densely-forested limestonemountains with little soil. Tourism isextremely low due to isolation, poor roads,and heavy rains. Rivers draining non-lime-stone areas to the southwest contributeminor sediment, and the major freshwaterinfluence is from strong groundwater springs,driven by high rainfall and steep hydraulicgradients. Nitrate contents of these springsare only one tenth that of limestone aquiferson the north coast (Lapointe and Goreau,in preparation). The area has bleached syn-chronously with reefs all along the NorthCoast of Jamaica, and sites in Cayman,Florida, and the Bahamas. Little deterio-ration has been noted in this area except formass bleaching.

4) Ocho RiosThese reefs were among the first to have

species composition and zonation described

in detail (Goreau, 1956, 1959). There is nosurface drainage, but strong groundwatersprings occur underwater and on land, con-taining very high levels of nitrate (UNDP,1974; Goreau et al., 1988). In the early 1950sthese were among the best reefs in Jamaica,with vigorous reef growth, high speciesdiversity, and stunning underwater cavesand canyons (Goreau, 1956, 1959). Tour-ism was minor, and the town had only ahandful of wooden buildings, some shore-front cottages, no more than a few hundredpeople, and trees covered the hills down tothe beach. By the late 1950s hotels hadexpanded rapidly and most of the reef wasdying from sediment stress as hills weredeforested, buildings constructed, and reefsediment dredged on a large scale for landfillto create hotel land and port facilities abovethe previously living back reef. Expandingemployment turned Ocho Rios into one ofthe country's largest towns (around 50,000),resulting in urban commercial and slumareas. Treatment facilities are inadequate todeal with all raw sewage, and much passesdirectly into the bay. Remaining reefs in thebay are largely dead and overgrown withalgae. Mass bleaching has taken place inheavily used tourist resort reefs to the eastand west of the town center.

5) Runaway BayReefs here have vigorous coral growth on

a steep limestone slope, producing caves,canyons, and vertical drop offs. There is lit-tle local surface drainage, but submarinesprings occur. Two small rivers less than 10km upcurrent are fed by high nitrategroundwater springs, known from dye stud-ies to be fed by rivers disappearing under-ground in central Jamaica. Their waters arenormally clear but turn muddy for days toweeks after flood rains a few times perdecade, so sediment stress is rare. Popula-tion densities are moderate, the area beingprimarily used for low-density holiday vil-las or pasture. The resort area receives lessthan 3% of the island's visitors, and the townis small. Septic tanks release nutrients intogroundwater, with some primary and sec-ondary treatment by larger hotels. Reefsremain in fairly good condition in deeperareas, but there is considerable anchor anddiver damage at tourist dive sites and in

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shallow back reef areas from high densitypleasure boat traffic. The area has beenheavily affected by mass bleaching. Algalovergrowth of reefs is moderately severe,with large amounts ofLobophora, Dictyota,and Halimeda, on the fore reef and Peyson-nelia in caverns.

6) Discovery BayDiscovery Bay reefs were analogous to

those of Runaway Bay, with extremely welldeveloped Acropora zones on the shallowfore reef until these were destroyed by Hur-ricanes Allen (Woodley et al., 1981; Porteretai, 1981;Rnowlton^a/., 1990) and Gil-bert. Acropora are now slowly regeneratingin deeper water (10 to 25 meters). DiscoveryBay is sheltered by reefs and had well devel-oped back reef habitats with highly produc-tive submarine spring communities (Goreauet ai, 1986). Species diversity has beenaffected by overfishing, which has severelyreduced catches of most fish species, and byinadequately controlled collection of organ-isms by visitors to the Discovery Bay MarineLab, especially in the west back reef zone,often used for ecological studies. There isvery little tourism in Discovery Bay, a fewholiday villas, a small town focused onbauxite mining offices, and a small dock forbauxite ships. Anchor and diver damage isminor. Sediment stress is apparent mainlywithin the hundred meters next to the baux-ite dock. The nearest corals are largely dead,and fine-grained red bauxite mud has pro-moted dominance by sediment-tolerantMadracis, Porites and other genera. Sedi-ment stress is confined to a very small partof the bay as there is no surface drainage ornearby rivers. Algal overgrowth has beensevere in the last decade, with major coralovergrowers being Lobophora variegata indeep water, Ceramium nitens on the reefcrest, and Chaetomorpha linum in the backreef. During this period fore-reef algal bot-tom cover and biomass has changed frombeing very minor (except for Halimeda andDictyota) to exceeding that of corals. Muchof this was due to the sharp reduction of themajor sea urchin herbivore, Diadema antil-larum following massive disease-inducedmortality in 1983 (Liddell and Ohlhorst,

1986; Hughes et al, 1987). However algalovergrowth has continued to increase despitelack of significant further change in herbi-vores. Strong growth response of local algaeto nitrate concentrations similar to thoseintroduced into reef waters by submarinesprings (Lapointe et al., 1988), concentriczonation of algae around springs, and theirspread outwards from them indicates thatalgal populations are undergoing eutrophi-cation from nutrients in groundwatersources. Local freshwater-induced bleach-ing has not been noted at Discovery Bay,but mass bleaching has been severe. Growthrates of bleached and unbleached popula-tions of different color morphs of Montas-trea annularis were followed from 1987 to1991. Bleached corals cease growth (Goreauand Macfarlane, 1990), and many are beingovergrown by algae, especially in damselfishterritories (Goreau, in preparation).

7) Rio BuenoThis site is only a few miles downcurrent

from Discovery Bay. There is no tourism,a very small old town in ruins, and a formersugar port whose heyday had passed by1850. Reef growth is exceptionally vigor-ous, and submarine relief is spectacular.Conditions differ from nearby DiscoveryBay since a large river enters the bay. Itssource is an inland spring derived from riv-ers vanishing into sinkholes in centralJamaica. The watershed is largely forested,with small farms in valleys, and some cattlegrazing. River water is usually clear or green,but turns red following heavy rains. Thereis a strong freshwater stress gradient in thebay, and strong but episodic sediment stress.These reefs underwent severe local bleach-ing following Hurricane Gilbert, beingaffected by muddy freshwater flows for sev-eral weeks. Reefs upcurrent from the rivermouth were not affected. Rio Bueno reefshave also been affected by mass bleaching,and thus have bleached now for five yearsin a row (1987-1991). Bleached Siderastreasiderea colonies are unable to clean them-selves of sediment filling their calices, andmany large colonies appear to be succumb-ing. Several species ofMontastrea and Agar-icia which bleach strongly at Discovery Bay

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have brightly colored populations in RioBueno which are not affected. Hurricaneimpacts varied greatly at different sites afterHurricane Allen and Gilbert (T. Hughes,personal communication).

8) Montego BayReefs to the north and east of Montego

Bay are free from sediment influence, butto the west they are affected by high sedi-ment loads from the Great River, whichdrains interior sugar plantations and smallfarms. The town, one of the largest inJamaica with 70,000 people, was a majorsugar port for 300 years, and its hotelsreceive over a third of all visitors to theisland. Tourism began in the late 1940s, butmost visitor growth, hotel construction, andpopulation growth has been within the last15 years. Extensive dredging and landfilldumping in the 1960s on top of reefs createdport facilities and caused extensive sedi-ment damage. Tourism and populationgrowth greatly exceeded sewage treatmentcapacity, and much raw sewage flows straightinto the bay. Around half the coral in shal-lower areas is dead, and most of the rest isstrongly stressed by sediment or algal over-growth. Bleaching has been severe at bettersites near resort areas, and algal overgrowthis a general problem, as elsewhere along theNorth Coast. Spectacular relief providesgood diving at deeper upcurrent reef sites,but anchor and diver damage are clear atmany locations due to mass diving opera-tions and heavy pleasure boat activities. Portfacilities for cruise ships result in illicit gar-bage dumping and hydrocarbon releases.The area is the second most polluted afterKingston, but with an intensity that is prob-ably at least an order of magnitude lowerdue to the smaller population and negligibleindustry.

9) Western HanoverThese reefs are among the richest and most

pristine in Jamaica and show minimum dis-turbance. Coastal population densities arelow, based on subsistence farming and fish-ing, and the area is one of the poorest onthe island. Tourism is almost absent. Coralreefs, except just downstream from river

mouths, have extremely high species diver-sity, large colonies, morphologies indicatingvigorous growth, and high biomass. Coralgrowth rates are the most rapid measuredin Jamaica (Goreau et ah, 1988). Reefs areaffected primarily by fishing and by massbleaching. Sediment stress is confined tolocal river mouth sites, where local bleach-ing may also have occurred. Algal over-growth appears relatively low. Because thesemay be some of the best reefs in Jamaicathey need to be closely monitored for longterm and short term changes, and protectedbefore they are damaged by external stresses.

10) NegrilReefs at Negril include offshore bank reefs,

lagoonal patch reefs, and fringing reefs onrocky shores. Negril was the most isolatedand unpopulated part of Jamaica until 1960,when a road was built first providing landaccess to the 12 km long beach. In that yearcanals were dug to drain swamps whichblocked landward access to the beach, andlarge amounts of organic peat sediment isdischarged onto reefs at both ends of thebay. The area has transformed since 1960from entirely unpopulated to the island'sthird major resort area: the beach is nowalmost continuous resorts. Boat and divingtraffic is very heavy. Diver and anchor dam-age are high, but have been nearly elimi-nated by installation of moorings and edu-cation efforts by dive operators. Sewagetreatment is inadequate to deal with existinghotel outputs, so much is discharged rawinto the bay. Septic tanks are used by localresidents in the hills. Detailed ecologicalsurveys of the Negril area in 1960 (Goreau,1960), before the advent of tourism, allowcomparison of current conditions withundisturbed ones (Table 1). Formerly abun-dant Acropora reefs are now almost entirelydead. Areas near sewage inputs have beenkilled by algal overgrowth. In 1986 algalovergrowth of corals was confined near rivermouths, but five years later affected theentire bay. Reefs near drainage canals arestrongly affected by sediment and brown,peat-stained freshwater from swamps, whichdepress coral growth by reducing light levels(Dallmeyer et al, 1982). Peat debris forms

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organic sediments which are easily resus-pended. A petroleum spill was caused byrupture of a storage tank into Negril Riverin late 1991 (K. Thacker, personal com-munication). Study of coral cores fromNegril showed a small, but statistically sig-nificant decline in growth rates from 1940to 1980 (Hendry et ai, 1992). A regionalsurvey of coral growth rates in Negril in1986 found growth rates to be declining atmuch faster rates between 1970 and 1985,and rates of decrease were directly propor-tional to growth, so fastest growing coralswere slowing most rapidly (Goreau et ai,1988). Expanding sediment stress was thelikely cause of growth reduction, since algalovergrowth was then confined near rivermouths. Since 1986, mass bleaching or localbleaching has occurred every year. Bleach-ing of Montastrea annularis in November1991 was about half as frequent in the moststressed parts of Negril Bay as in nearbyareas free from sediment, freshwater, sew-age, and boat damage (Goreau, 1992). Manycolonies were brightly colored andunbleached, and several species have colorsin common, which are unusual in other partsof Jamaica, that may indicate bleaching-resistant algal symbionts. By the end of 1991most Caribbean reef species were still pres-ent, but corals were being steadily over-grown. With the exception of stable coral-sponge symbionts (Goreau and Hartman,1966), corals were losing ground whereverthey contacted sponges, algae, soft corals,and Millepora (Goreau, 1992). Someencrusting sponges are especially effectiveat overgrowing corals, but large masses ofalgae are also responsible, especially Sar-gassum hystrix, Lobophora variegata, andseveral Dictyota and Halimeda species indeeper water. In 1960 the inshore area wasalmost devoid of algae, but in 1991 massesof Chaetomorpha linum up to 2 or 3 meterslong smothered large areas of seagrass andpatch reefs. Algal species composition,zonation, and spread outwards from sewageinputs suggest eutrophication. Withoutprompt tertiary sewage treatment, algae andsponges are likely to overgrow most of thebay's reefs within a few years, as in Hell-shire, Ocho Rios, and Montego Bay.

11) Western WestmorelandThe coastline in this area has only recently

been connected by road, and is one of theleast populated and developed shorelines inJamaica. Reefs are not affected by stressesfrom Negril Bay because of strong currentflow. Reef growth is vigorous but shallow.The shore line is rocky, with few beaches.The exposed location and large amounts ofAcropora rubble indicate past hurricanedamage. Species diversity is very high andmost unbleached corals are healthy. Fishingis limited by low population, strong cur-rents, and distance from fishermen'sbeaches. Algal biomass is moderate, andalgal overgrowth does not appear to be aproblem, except Lobophora, which may beinfluenced by groundwater spring inputs andreduced Diadema abundance. Algal speciesdiversity is fairly high and dominated byrelatively oligotrophic brown and green algalspecies. The area has been affected by massbleaching events. In November 1991, afterone of the mildest mass bleaching events todate, nearly half the corals were bleached,including virtually all the dominant Mon-tastrea cavernosa and Siderastrea siderea.The former were bleached to grey. Most ofthe latter bleached to blue colors, but abouta tenth had partial bleaching: pale polka-dots on a dark brown background. Bleach-ing to white was rare. A small proportionof other abundant corals such as Montastreaannularis, Diploria, Agaricia, and Myceto-phyllia species were partially bleached.Bleaching was about twice as common asin Negril Bay at the same time, in markedcontrast to the high anthropogenic stressesat the latter area. Almost all species of her-matypic corals had at least some partiallybleached individuals (Table 1), but theseestimates are certainly too low because mostbleached corals were in recovery phases, andmany had recovered in previous weeks aftera long period of very hot, calm weather wasended by a severe storm with record floods.

DISCUSSION

Of the many stress factors operating ateach site, only two, hurricane damage andepidemic mortality of Diadema, have had

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TABLE 2. Estimated magnitudes of reef stress factors at each site.*

Site

123456789

1011

RI

MHLMVL0VHHMH0

ss00VHHMH0VLL0H

SD

VHVHLMLVLVHHMVHVL

sw

VHLVLHLLLHVLMVL

PO

VHM0MLLLHVLM0

OF

VHVHMVHVHVHHVHVHHM

DR

VH00VHVLH0VH000

CC

LMVLVHHMLVHVLLVL

BD

LH0VHHL0VH0VH0

AL

VHMLVHHHMVHLHL

SC

HHLHLLMMLHL

LB

HH0000VHMLL0

MB

LLVHVHVHVHVHHVHMVH

* Relative reef stresses listed are rivers (RI), submarine springs (SS), sedimentation (SD), sewage (SW), in-dustrial pollution (PO), overfishing (OF), dredging (DR), curio collection (CC), boat, anchor and diver damage(BD), algal overgrowth (AL), sponge and soft coral overgrowth (SC), local bleaching (LB), mass bleaching (MB).Factors are ranked as absent (0), very low (VL), low (L), moderate (M), high (H), or very high (VH).

fairly uniform island-wide impacts. Theothers show great variability between sites.Table 2 shows the relative importance of 13stress factors at the 11 sites. The factorsreflect magnitude of, and proximity to,stresses from rivers (RI), submarine springs(SS), terrigenous sedimentation (SD), sew-age (SW), industrial pollution (PO), over-fishing (OF), dredging (DR), curio collection(CC), boat, anchor and diver damage (BD),algal overgrowth (AL), sponge and soft coralovergrowth (SC), local bleaching (LB), massbleaching (MB). These factors ranked asnone (0), very low (VL), low (L), moderate(M), high (H), or very high (VH). Values areassigned based on direct observations at allsites over 4 decades, photographs, and dis-cussions with individuals working in eacharea. The latest observations are used, butsome sites have been examined at differenttimes and with differing frequency. Valuesgenerally represent the entire area andinclude the full range of habitats in each.Many factors vary considerably from placeto place within each area, including forexample both upstream and downstreamreef areas at sites with river inputs, or sitesnear and far from sewage outfalls. Manystress factors are strongly episodic, so rank-ings are based on maximum impactsobserved, which have happened at differenttimes in different places, for example dredg-ing or population growth impacts such assewage. Rankings are internally consistent,but relative and somewhat subjective, so it

is possible that other observers with the samefield experience might rank some of themslightly differently. The relative importanceof these factors should only be comparedby non-parametric statistics.

The non-parametric Spearman rank ordercorrelation coefficients and their statisticalsignificances for all pairs of factors in Table2 are shown in Table 3. Considering cor-relations to be significant at the 0.05 prob-ability level, to be strong at the 0.01 level,and very strong at the 0.001 level, the pairinteractions of factors are:

1) Significantly positive: RISC, SW-CC,OF-DR, SS-MB, PO-DR, OF-CC, PO-SD,PO-CC, DR-CC, BD-SC.

2) Strongly positive: RI-LB, PO-BD, SC-SD, PO-SC, SW-DR, CC-BD, SW-BD, CC-AL, SW-SC, BD-AL.

3) Very strongly positive: RI-SD, LB-SD,SW-PO, SW-AL, PO-AL, DR-AL.

4) Significantly negative: PO-SS, SC-SS,SD-MB, LB-MB.

5) Strongly negative: RI-SS, PO-MB, SC-MB.

6) Very strongly negative: SD-SS, LB-SS.Some of these correlations are related to

common patterns of human activity in cer-tain areas. For example, erosion, pollution,sewage, dredging, boat and anchor damage,and curio collection stresses correlate witheach other because they are most intensenear cities and resort areas. Proximity torivers is not a direct measure of terrigenoussedimentation impact because South Coast

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sites are fairly distant from rivers, butundergo severe episodic sedimentation whenextremely high erosion occurs in upcurrentwatersheds during flood rains.

The positive significant Spearman cor-relations support field observations alongstress gradients which suggest that rivers andsedimentation are related to local bleachingand shifts towards sponge, gorgonian, andsoft coral dominance. Sedimentationappears to have caused species shifts ratherthan eliminated coral reefs, even at siteswhere sediment stress has continued for over300 years. Sewage is strongly associated withpollution and algal overgrowth. Nutrientinputs stimulate algal overgrowth of corals,and have caused expanding rings of dead orovergrown coral reef framework aroundmajor nutrient sources to the coastal zone.

The negative correlations in Table 3 arealso especially revealing, as all significantnegative correlations involve either massbleaching or submarine springs. All signif-icant correlations of mass bleaching and ofsubmarine springs are negative, except onlyfor their mutual correlation, which is pos-itive. Submarine springs are most commonat less-populated and less stressed sites(except for Ocho Rios) where mass bleach-ing is especially prevalent. Submarinesprings generally carry little or no sediment.A natural "stress," they appear to haveminor negative impacts on reefs unlessnutrient levels are excessive.

Mass coral reef bleaching has a uniquepattern. It first appeared in Jamaica in 1987,followed by repeated events in 1989, 1990,and 1991 (Table 4). Mass bleaching did notoccur in Jamaica from 1951 through 1986,and it is not possible that it could have hap-pened without our knowledge because offrequent field work and regular contact withdivers and fishermen around the island. Theonly year since 1987 without mass bleach-ing was 1988, but local bleaching occurredthat year. Hurricane Gilbert, whose eyepassed the length of the island, generatedfloods which caused local bleaching at sitessuch as Rio Bueno. The distribution of masscoral bleaching in space and time is entirelyunlike patterns of other known stresses,which all show clear environmental stressgradients increasing towards obvious sources

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like towns and rivers. In contrast, massbleaching has been intense all around thenorth, east, and west of Jamaica, but onlymild or rare on the south coast, site of mostsediment, sewage, and pollution inputs tothe coastal zone. Detailed study of bleachingalong freshwater, sediment, and sewagestress gradients in western Jamaica duringlate 1991 showed unpolluted reefs hadhigher coral cover and lower algal, sponge,and soft coral overgrowth than chronicallystressed reefs, but frequency of bleachingwas about half as high in the most stressedareas than at pristine sites (Goreau, 1991).This implies that the standard local anthro-pogenic stresses are not a cause of bleaching,and that corals which are routinely subjectto them appear to be less susceptible to thestresses which cause mass bleaching. In con-trast, the intensity of bleaching in Jamaicais extremely similar to high sea surface tem-perature anomalies since 1987, recorded byboth in situ temperature measurements andby satellite radiometer data (Goreau et al,1992). This suggests that many Jamaicanreefs may have only passed their tempera-ture tolerance thresholds in the last decade.

CONCLUSIONS

Major observed changes in Jamaican coralreef community structure and health from1951 to 1991 suggest:

1) Clear signs of reef degradation in termsof changing reef community composition,coral cover, or coral growth rates are presentat all sites;

2) The rate and character of reef degra-dation depends on the type, intensity, andduration of stresses;

3) Hurricanes have played a major rolein eliminating Acropora palmata and Acro-pora cervicornis zones which previouslydominated most shallow reefs all around theisland;

4) The intensity and extent of reef stressfrom sewage, sediment, pollution, overfish-ing, boat anchor, and divers have steadilyincreased;

5) Algal overgrowth of corals is a seri-ously escalating problem in most Jamaicanreefs;

6) This is due to a combination of reducedherbivory due to overfishing and disease,

TABLE 4. Coral bleaching in Jamaica, 1951-1991.'

Year

19511952195319541955195619571958195919601961196219631964196519661967196819691970197119721973197419751976197719781979198019811982198319841985198619871988198919901991

Hurricane

Charlie

++

+

Flora+

+

+

+Allen

Gilbert

Localbleaching

?

X

?

X

Massbleaching

**

****

**

1 Major hurricanes whose eye hit Jamaica directlyare named. Minor hurricanes or those hitting periph-erally are marked by +. Reported local freshwaterbleaching is indicated by x, and possible occurenceswhich were not reported are indicated by ?. Massregional bleaching along North Coast reefs are shownby **.

and to increased fertilization by nutrientsderived from inappropriate land and sewagemanagement practices;

7) Increased sediment and organic mat-

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ter loading correlates with coral overgrowthby sponges and soft corals;

8) Local bleaching occurred in shallowreefs downstream from rivers after majorhurricanes;

9) Mass bleaching did not take placebefore 1987;

10) The primary deep water reef buildingspecies in the genera Montastrea, Sideras-trea, Diploria, Agaricia, along with other lessabundant genera, are among those moststrongly impacted by mass bleaching in thepast decade;

11) The spatial and temporal distribu-tion of bleaching is opposed to that of allmajor reef stress patterns;

12) Bleaching is most frequent on reefswhich previously escaped degradationbecause they were remote from local stresses;

13) The spatial and temporal patterns ofmass bleaching correlate with mean monthlyopen sea water temperatures above 30°C;

14) All stresses act to reduce coral areacoverage and/or coral growth rates;

15) The net impact of all stresses is accel-erating decline of reef health around theisland, especially during the last five years.

ACKNOWLEDGMENTS

All work described is based on pioneeringresearch by the late Thomas F. Goreau. Theauthor is deeply indebted to Nora Goreau,Peter Goreau, Stefan Goreau, and the lateThomas F. Goreau for repeated discussionsof many points in this paper over the past4 decades. This work could not have beenpossible without their shared commitmentto long term knowledge. Special thanks alsogo to large numbers of divers, fishermen,scientists, and others who have helpedgreatly by discussing their own observa-tions. They are unfortunately far too numer-ous to name here, and to mention just a fewwould be unfair. Peter Goreau kindly draftedFigure 1. This paper is dedicated to NoraGoreau, for single-handedly preserving pastinformation under most difficult circum-

stances.

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