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

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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 iden- tified 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 infec- tion 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 recog- nized 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 local- ized 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 con- tinued 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 photo- graphed 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 be- tween species. Spearman’s coefficient of rank correlation was calculated for each species to deter- mine 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 abun- dance 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 measure- ments 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.
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