Spread of a Black-Band Disease Epizootic Through the Coral Reef System in St

BULLETIN OF MARINE SCIENCE, 61(3): 919–928, 1997 CORAL REEF PAPER

SPREAD OF A BLACK-BAND DISEASE EPIZOOTIC THROUGH THE CORAL REEF SYSTEM IN ST. ANN’S BAY, JAMAICA

Andrew W. Bruckner, Robin J. Bruckner and Ernest H. Williams, Jr.

ABSTRACT The distribution, abundance and dispersion patterns of black-band disease (BBD) [Phormidium corallyticum (Cyanobacterium)] were determined on four shallow reefs located on the north coast of Jamaica. Between January 1992 and August 1993, 5.2% of the total population of massive corals, including the dominant reef-building species Diploria clivosa, D. strigosa, Montastrea annularis, M. cavernosa and Siderastrea siderea, became infected within 20 sites (6280 m2 total area). Black-band disease was first identified in the back reef; over 19 mo, the abundance of BBD increased dramatically, and infections spread 3 km in the direction of the predominant current. The distribution of diseased corals appeared to be clumped, with infections progressing from one individual to adjacent corals which were attached by contiguous skeleton but unconnected by live tissue. Black-band disease occurred on 8.6% of the S. siderea colonies; this species was impacted by excessive run-off associated with abnormally high rainfall. In contrast, M. annularis, the coral reported to be most susceptible to the disease, had a lower frequency (2.2%) of infection. Migration of a black-band disease epizootic across a coral reef has not been previously documented.

Massive scleractinian corals that form major reef systems are susceptible to black-band disease (BBD) (Fig. 1), an infection caused by the cyanobacterium Phormidium corallyticum (Rützler and Santavy, 1983). Black-band disease has been observed on massive corals throughout the Caribbean (Garrett and Ducklow, 1975; Rützler et al., 1983; Peters, 1993), the Indo-Pacific (Antonius, 1985a), the Red Sea (Antonius, 1988), and recently, on acroporid corals from the Great Barrier Reef (Dinsdale, 1994; Glazebrook and Streiner, 1994). BBD may also occur on gorgonians and milleporids (Antonius, 1985b; Feingold, 1988). This disease characteristically forms a circular or crescent-shaped band of darkly pigmented filaments that separates white, denuded skeleton from living coral tissue. In the disease process, BBD may advance several millimeters per day across a coral’s surface, killing an entire colony during one active season or after a repeat infection the following year (Rützler et al., 1983; Richardson and Carlton, 1993). On most reefs, 0.5-1.0% of the susceptible coral colonies are affected by BBD at a given time, with infections distributed throughout the reef (Garrett and Ducklow, 1975; Antonius, 1981; Edmunds, 1991). Recently, localized outbreaks have been reported from the Bahamas, Belize, the Cayman Islands, Florida (USA) and St. Vincent (Peters, 1988, 1993; Williams and Bunkley-Williams, 1990). The appearance of a BBD outbreak may be associated with environmental perturbations (Dustan, 1977; Antonius, 1981). Taylor (1983) noted that development of BBD was dependent on abnormal physiological stress or trauma that lowered a coral’s resistance. Antonius (1988) observed an increase of BBD in industrialized areas, and found that corals which were normally resistant to the disease succumbed to BBD in polluted water (1988). Major changes in the coral reef community structure, including a progressive loss of live coral and concurrent increase of macroalgae, have been documented in Jamaica over the last 20 yrs (Goreau, 1992; Hughes, 1994). The degradation of these reefs has been

919 920 BULLETIN OF MARINE SCIENCE, 61(3): 919–928, 1997

Fig. 1. Progression of Black-Band Disease on Diploria strigosa. The upper surface of the colony was previously killed and colonized by filamentous algae. The coral was invaded by BBD on June 30, 1992; to follow disease progression two nails were placed at the trailing edge of the band, in dead coral skeleton. (A) BBD as of 22 September, 1992. Two separate bands are visible. (B) BBD 7 d later, 29 September, 1992. Bands have merged; the infection continued to spread down the colony. L = live coral; D = bare coral skeleton, exposed by BBD. attributed to anthropogenic and natural causes, however BBD was not previously recognized as a contributing factor. Liddell and Olherst (1992) noted that BBD was sporadic and in low abundance on Jamaica’s north coast. During the 1990s, we have observed an abrupt increase in the incidence of BBD on north coast reefs, and have documented localized outbreaks from widely separated areas (unpubl. obs.). In this study, we describe an outbreak of BBD that developed in a sheltered back reef and spread in the direction of the prevailing water current. Evidence is presented suggesting that the high incidence of BBD on these reefs is a result of adverse environmental conditions and physiological stress to the corals.

MATERIALS AND METHODS

The distribution of black-band disease and sequence of BBD transmission was followed for 20 mo along 5 km of reef substrata in St. Ann’s Bay, Jamaica. Corals with BBD were identified during snorkel and SCUBA surveys conducted on 11 reefs between 0-15 m depth (Fig. 2b). Initial surveys were conducted in July 1991. A monitoring program was established in December 1991, and continued through August 1993. Each reef was visually surveyed a minimum of one time every 30 d. Upon identification of a BBD infected coral, the disease interface was marked by inserting markers in the tissue-stripped skeleton immediately behind the disease/tissue interface. Samples of BBD material were collected during each survey for microscopic confirmation of P. corallyticum. All corals with BBD were photographed using a Nikonos V (28 or 35 mm lens and close-up attach- ment), and the length and width of the BBD was measured. To determine whether a relationship existed between the apparent health of a coral and the appearance of BBD, the condition of each coral was categorized according to the following characteristics: 1) unblemished (absence of algae, injuries and other disease signs); 2) injured; 3) bleached; 4) progressive overgrowth by inverte- brates; 5) presence of algal turf; 6) necrotic tissue, white-band disease or shutdown reaction (Antonius, 1981); 7) a combination of the above features. On each reef experiencing a BBD outbreak (Lee, TI, Fig Tree and UC reefs), five permanent, non-overlapping study sites were established (Fig. 2c). Study sites were patterned to represent all BRUCKNER ET AL.: SPREAD OF BBD EPIZOOTIC IN JAMAICA 921

Fig. 2. (A) Location of study area on the north coast of Jamaica (18° 27' N, 77° 13' W). (B) Eleven reefs of St. Ann’s Bay, Jamaica surveyed for BBD. Land areas stippled; bricks represent rocky shore and squares indicate sand. Total number of BBD infections identified in 20 mo are given (in parenthesis) for each reef. Contour line represents the edge of the reef; reefs were 1-7 m deep, bordered by sand, red mangrove Rhizophora mangle L. or turtle grass Thalassia testudinum Koenig and Sims. (C) Migration of the BBD epizootic from Lee Reef through adjacent reef environments. Twenty 314 m2 sites were chosen within Lee, TI, Fig Tree and UC reefs (5 per reef). Numbers increase sequentially to represent the date BBD first appeared in each site as follows: (1) Jul 91; (2) Dec 91; (3) Jan 92; (4) Mar 92; (5) May 92; (6) Jun 92; (7) Jul 92; (8) Feb 93; (9) Jun 93; (10) Jul 93; (11) Aug 93. An outbreak of BBD was not observed east of Lee Reef. The predominant current flows from east to west. 922 BULLETIN OF MARINE SCIENCE, 61(3): 919–928, 1997 areas within each reef, and encompassed approximately 10% of the total reef surface. A study site consisted of a circular area (10 m radius, 314 m2) surrounding a coral haphazardly selected and designated as the central point of the site. The total number of uninfected or BBD-infected colonies of the species Diploria clivosa (Ellis and Solander), D. strigosa (Dana), Montastrea annularis (Ellis and Solander), M. cavernosa (Linnaeus) and Siderastrea siderea (Ellis and Solander) were recorded within each site. M. annularis was differentiated into two morphotypes (Knowlton et al., 1992); morphotype 3 was absent from all sites. Agaricia agaricites (Linnaeus) and Meandrina meandrites (Linnaeus) were identified with BBD, but are not included in counts because these species were uncommon, and rarely became infected. All corals with BBD were tagged and photographed when first identified; additional photographs were taken monthly for the duration of each infection. Progression of BBD was monitored at 7-14 d intervals through August 1993 in each site. For statistical analyses, the frequency distribution of the number of BBD infections was obtained by pooling data from the 20 sites located on four reefs. A G-test (Sokal and Rohlf, 1981) was used to determine whether the number of infected colonies versus non-infected colonies differed between species. Spearman’s coefficient of rank correlation was calculated for each species to determine if the number of corals infected with BBD was correlated with colony density. To determine whether BBD infections varied seasonally among individual coral species, differences in the abundance of active BBD infections between months were analyzed using a G-test; the incidence of BBD was compared with monthly mean reef temperatures and rain data. Temperature measurements were taken at the same time each day at 5 m depth with a hand-held mercury thermometer; all temperatures were recorded to the nearest tenth of a degree, and data was averaged for each 30- d period. The pattern of dispersion of BBD infections was examined by mapping the position of infected corals. The sequence of disease spread was compared with water circulation patterns of St. Ann’s Bay, and the detachment and movement of dislodged BBD material. Distance and compass bear- ings between infected corals were obtained using the central colony within the nearest permanent site as a reference point. Each colony was assigned a number to denote the date of initial infection, and each coral’s position was plotted. Directions of water movement were estimated by releasing fluorescein dye near 20 BBD-infected corals during a period of moderate wave surge, and again during calm seas; dye was also released in the water column, 1 m above 10 BBD-infected corals. Dye studies were conducted within permanent sites (five measurements per reef), and the direction of dye transport was tracked with a hand-held compass. Portions of the microbial mat from BBD- infected corals were observed to exfoliate in the summer and fall of 1992 during rough seas. Move- ment of dislodged BBD material from 16 corals was followed for up to 15 min, and subsequent direction and distance of transport was determined.

RESULTS

In July 1991, during initial surveys of 11 reefs within St. Ann’s Bay, black-band disease was identified on M. annularis (morphotype 1, n = 3; morphotype 2, n = 1) and D. strigosa (n = 1). Infections were confined to the back reef (Lee and SABR; Fig. 2). At the onset of the permanent monitoring program (December 1991), BBD existed only on M. annularis, morphotype 1 (n = 6); infected corals included three colonies observed with BBD in July 1991, and three additional colonies. During December 1991, BBD was restricted to Lee Reef; no infections were found on other reefs. The number of infected colonies increased dramatically during 1992 at the eastern end of Lee Reef (site 1; Fig. 2c), midway along the St. Ann’s Bay reef system. Between January and June 1992, 24% of the D. strigosa population (n = 12) and 20% of the M. annularis colonies (morphotype 1, n = 14) became infected with BBD in this site. Infec- tions gradually spread to the west, occurring throughout Lee Reef by March 1992 among BRUCKNER ET AL.: SPREAD OF BBD EPIZOOTIC IN JAMAICA 923

Ts.1elba IncidenceofBBDinfectionsamongthespecieDiploriaclivosa,Diploriastrigosa, Montastreaannularis,MontastreacavernosaandSiderastreasiderealocatedonfourreefsinSt. Ann'sBay,JamaicabetweenDecember1991andAugust1993.Countsarepooledfromfivenon- overlapping314m2studysiteswithineachreef.NumberofcoloniesinfectedwithBBDare followedbytotalnumberofcoloniesinparenthesis.DataforD.clivosaandD.strigosahave beencombined.

NumberofBBDinfectionsoneachreef CforalSpeciesLfeeReeTeIReeFCigTreUfeeRlTota S.siderea4)1(122)7)1(6524)8(5392)5(847185(2160 M.cavernosa4)(16)2)5(8492)4(8131)(6754(1745 M.annularis2)1(345)5)(2693)(6481)(8630(1348 Diplorias)pp.1)8(1584)(1170)(141)(2223(301 T)otal8)4(6411)05(18877)5(20142)8(1022292(5564

the coral species D. clivosa, D. strigosa, M. annularis (morphotype 1), M. cavernosa and S. siderea. Black-band disease first appeared on fringing reefs to the west of Lee Reef in May 1992. The BBD epizootic advanced through TI and Fig Tree Reefs, infecting 2.9% of the M. cavernosa colonies (n = 49) and 8.2% of the S. siderea colonies (n = 106) located within the 10 sites. The disease also developed on A. agaricites (n = 5), D. strigosa (n = 4), M. annularis (morphotype 1, n = 6; morphotype 2, n = 2), and M. meandrites (n = 6). In February 1993, BBD invaded UC Reef, 3 km west of the initial outbreak. The disease spread primarily among S. siderea on this reef. Black-band disease was uncommon on six reefs surveyed to the east of Lee Reef; in 20 mo a total of 28 corals (< 0.5%) became infected with BBD on these reefs (Fig. 2c). Between December 1991 and August 1993, BBD infections occurred on 5.2% of 5564 massive corals in 20 sites (6280 m2 total area) (Table 1). Inspection of BBD dispersion patterns within individual sites gave the qualitative impression that BBD corals were aggregated. Black-band disease occurred simultaneously on a maximum of 15 corals in one site; up to 31 colonies became infected in each site in 20 mo (mean = 15.2 , SD = 8.7). Over the duration of the infection, BBD frequently (10.7%) spread to multiple, isolated locations on the same colony. Thirty corals (10.3%) previously afflicted with BBD exhibited reactivation of the BBD pathogen after a period of dormancy, either later in the season or the following year. Furthermore, BBD advanced from one colony to a neigh- boring coral; 11.6% of the colonies which became infected with BBD consisted of con- specific groups of adjacent, unconnected corals. Black-band disease infected 292 corals in 20 sites during this study. By August 1993, 32 BBD corals died, 156 suffered partial mortality before the disease disappeared, and 104 colonies continued to be afflicted with BBD. Significant differences in the percent of BBD infections between species were present (G-test, G = 40.23, df = 3, P < 0.001). Post-hoc analysis (Student-Newman-Keuls [SNK] test) showed that this was due to a much higher abundance of BBD on S. siderea. Other species were equally infected (SNK). The percent of colonies infected with BBD (pooled

species) was not correlated with coral density (rs = 0.655, n = 80, P < 0.0005). However, analysis of individual species demonstrated that BBD was a function of colony density in

S. siderea (rs = 0.3594, n = 20, P > 0.1). In the other species, a low incidence of BBD versus a high unit area colony abundance suggests that these infections were density ≤ ≤ independent (rs 0.69, n = 20, P 0.01). 924 BULLETIN OF MARINE SCIENCE, 61(3): 919–928, 1997

Using data from the 20 sites (pooled for 60-d intervals) statistical analyses revealed that the temporal abundance of BBD infections varied between coral species. Of the four species, M. annularis (morphotype 1 and 2 pooled) had the lowest frequency of infections, and there were no significant differences between months (G-test, G = 13.01, df = 9, P > 0.1) for infected M. annularis colonies (mean = 5.3, SD = 1.8; Fig. 3c). Abundance of BBD on M. cavernosa and Diploria spp. varied between months (G-test, G = 1002.95 and 251.37, respectively, df = 9, P < 0.0001), with a significant increase in BBD on these species during warm water periods of 1992 (Fig. 3b). BBD infections were also signifi- cantly different between months for S. siderea (G-test, G = 415.36, df = 9, P < 0.0001). No seasonal decline was observed during the winter of 1992. In contrast, this species showed a significant increase in BBD than observed during the previous summer. S. siderea suffered the highest rate of infection (8.6%), with a dramatic elevation in BBD during 1993 (Fig. 3a). Comparisons of photographs taken of individual BBD corals revealed that the visual appearance of the BBD (band width and area of recently exposed, white coral skeleton) varied between survey periods. The bands became wider and coral tissue mortality was most severe between May and September, particularly when infections coincided with calm weather. The width of the BBD was visibly reduced immediately after a storm. During periods of moderate surge portions of the BBD mat were observed to exfoliate from the site of infection. Sixteen dislodged fractions (10-30 mm diameter) were followed. The BBD material contacted an algal-covered boulder less than 1 m away (n = 3), landed on the substrata 1 - 3 m away (n = 6), washed over the reef crest (n = 2), or was transported up in the water column and to the west (n = 5). Fluorescein dye was conveyed in a manner which was similar to patterns of BBD dis- persal. Fluorescein dye released above corals moved primarily towards the west, parallel to the reef crest. Waves associated with afternoon trade winds conveyed the dye to the southwest, from the reef crest towards the back reef, or from open water into protected coves. When released on exposed reefs, the dye was dispersed with a back and forth motion. Negligible transport of dye was observed during calm periods, especially in back reef environments. Black-band disease was consistently found on corals suffering from environmental and physiological stress. Shallow reefs surveyed for BBD are experiencing a dramatic shift from coral to algae. Corals in a progressive state of overgrowth by algae were most susceptible to BBD; infections initiated most frequently at the margin of living coral tissue and algal turf (n = 188). Between October 1992 and May 1993, coral populations were exposed to excessive sedimentation associated with flood rains and runoff. Rainfall exceeded 230 cm during this period, representing the highest level reported for St. Ann’s Bay in 40 yrs (mean precipitation, 1951 - 1991 = 144 cm year-1, SD = 36.17). On shallow fringing reefs (TI and FT) which were subjected to excessive turbidity, corals (>10%) experienced tissue necrosis, white-band disease and bleaching; the highest incidence of BBD also occurred on these reefs during 1993. Colonies of D. clivosa and M. cavernosa (n = 10) suffered from tissue necrosis and shutdown reaction (Antonius, 1981) during development and progression of BBD. Black-band disease infected S. siderea colonies which bleached (n = 21), had necrotic, tissue-stripped areas (n = 29) or were being overgrown by sponges (Cliona sp. or Anthosigmella sp.) or fire coral (Millepora complenata, n = 44). In contrast, BBD did not occur on unblemished corals or corals with minor injuries. M. annularis (morphotype 1, n = 46) and D. strigosa (n = 63) colo- BRUCKNER ET AL.: SPREAD OF BBD EPIZOOTIC IN JAMAICA 925

Fig. 3. Variation between months in number of BBD infections within Lee, TI, Fig Tree and UC reefs. BBD infections were averaged over 2 mo periods (4 surveys/reef) between December 1991 and August 1993. (A) Total number of active BBD infections on Diploria clivosa, Diploria strigosa, Montastraea annularis, Montastraea cavernosa and Siderastrea siderea, and BBD infections on Siderastrea siderea only. (B) Bimonthly variation in the number of active BBD infections on Montastraea cavernosa and Diploria spp. (D. clivosa and D. strigosa are pooled). Daily reef temperatures measured at 5 m depth were averaged from the four study sites for each 2 mo period. (C) Active BBD infections on Montastraea annularis (morphotypes 1 and 2 are pooled) for the same period. 926 BULLETIN OF MARINE SCIENCE, 61(3): 919–928, 1997 nies which sustained injuries from anchors, dive fins, fish pots or parrotfish were monitored for 90 d; none became infected with BBD.

DISCUSSION

Wave surge and water currents appeared to be important mechanisms responsible for intercolonial transfer of BBD in shallow water. Fringing and barrier reefs in St. Ann’s Bay are influenced by northeast trade winds and a predominant westward water current; trade winds become more pronounced between April and December (Goreau, 1959; Grant and Wyatt, 1980). The BBD epizootic migrated primarily in the direction of water transport, and BBD remained uncommon in locations east of the initial outbreak, confirming that the BBD epizootic had not been transmitted against the prevailing current. Further- more, wave surge provided sufficient energy to lift portions of the BBD mat from infected corals located in shallow areas. Dislodged portions of these mats were carried back and forth, broken into smaller fragments, and deposited one to several meters from their point of origin. These observations may explain the appearance of multiple intracolonial infections, and the localized spread of BBD from one colony to adjacent, unconnected corals. Peters (1984) observed multiple infections on adjacent D. strigosa colonies located in a confined portion of the reef crest in St. Croix; she suggested that the high incidence of BBD is due to heavy wave surge sediment resuspension. Disease epizootics typically manifest as a series of oscillations. Once a host population loses most of its susceptible individuals, the remaining individuals have an increased capacity for counteracting the disease, and infections diminish (Kinne, 1980). In St. Ann’s Bay, the initial appearance of BBD in one site was followed by a rapid rise in the number of infected corals located in close proximity. During the initial outbreak 26 colonies of D. strigosa and M. annularis were infected in a localized area. The number of new infections occurring on these species declined in 1993. Black-band disease was observed infrequently on S. siderea in 1992. This species is thought to be highly resistant to BBD, and is described as having a powerful ciliary- mucus system which may remove infections (Antonius, 1981). During 1993, S. siderea colonies exhibited a dramatic increase in bleaching, stress-related necrosis (Peters, 1984) and BBD. The decline of S. siderea populations may be attributed to run-off, reef silt- ation and excessive water turbidity associated with flood rains (>200 cm) which occurred in northeastern Jamaica between October 1992 and May 1993. Similar levels of abnormally high precipitation have occurred four times in the past 40 yrs (1958, 1960, 1963 and 1986). In addition to BBD, algal and invertebrate overgrowth of corals, periodic coral reef bleaching and frequent colony mortality is reducing live coral cover on St. Ann’s Bay reefs (pers. obs.). These factors are coupled with a gradual shift from a reef dominated by corals to a reef composed primarily of macro algae. Modifications in the community structure of Jamaican reefs have been attributed to hurricanes, over fishing and the Diadema antillarum mass mortality (Done, 1992; Goreau, 1992). The combined effects of physi- cal damage, reduced or absent herbivore populations and disease have destroyed most corals on Jamaican reefs (Hughes, 1994); the compromised condition of the remaining colonies may increase the likelihood of additional BBD epizootics on these reefs. BRUCKNER ET AL.: SPREAD OF BBD EPIZOOTIC IN JAMAICA 927

This documented outbreak of BBD not only damaged a reef system, but it moved across the coral reef in a manner not previously recognized. The distribution and spread of BBD was caused by wave surge and currents. In 20 mo, the effects of BBD extended over 3 km of shallow reef terrace, and the epizootic continued to spread down current; no outbreak of BBD has been observed up current. Previous reports of BBD epizootics have been largely anecdotal, and quantitative studies have described a low incidence of BBD (Garrett and Ducklow, 1975; Edmunds, 1991). The data presented elevates black-band disease from a minor enzootic condition to an invasive epizootic threat that can move across and between coral reefs.

ACKNOWLEDGMENTS

We thank Hofstra University Marine Laboratory and Columbus Beach Cottages, Priory, Jamaica for facilities and N. Campbell for boat use. The Jamaica Meteorological Office provided precipitation data from the parish of St. Ann. Critical comments on earlier versions of the manuscript by P. Yoshioka, D. Ballantine and J. Morelock are gratefully acknowledged. The comments of two anony- mous reviewers greatly improved this manuscript.

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DATE ACCEPTED: May 24, 1996.

ADDRESS: Caribbean Aquatic Animal Health Project, Department of Marine Sciences, University of Puerto Rico, P.O. Box 908, Lajas, Puerto Rico 00667-0908. Phone (787) 899-2048; Fax (787) 899-5500.