REVIEWS Coral diseases: what is really known? Laurie L. Richardson uring the International Reports of new and emerging coral Research in the late 1970s and Year of the Reef (1997) and diseases have proliferated in recent years. early 1980s followed the same de- continuing into the Inter- Such coral diseases are often cited as scriptive approach. New results, Dnational Year of the Ocean contributing to coral reef decline. Many of however, included the first quan- (1998), much attention and activity these diseases, however, have been titative study of disease preva- have been focused on evaluating described solely on the basis of field lence, and it was determined that the current status of coral reefs1–6. characteristics, and in some instances white band disease was relent- The uniform conclusion of these there is disagreement as to whether an lessly eliminating the important multiple assessments is that coral observed coral condition is actually a reef-forming acroporid corals of reef ecosystems are degrading, disease. A disease pathogen has been shallow Caribbean waters13. This and that this is most likely a com- identified for only three coral diseases, was the first case in which the po- bined result of global warming, and for only two of these has the pathogen tential severity of coral diseases ozone depletion, overfishing, eutro- been shown (in the laboratory) to be the was verified. phication, poor land-use practices disease agent. In one case, the same Further efforts were made and other manifestations of human disease name has been used for several to identify pathogens associated activities. All of these reports have widely varying coral syndromes, with specific diseases, and ad- emphasized that an increase in whereas in another multiple disease ditional causative agents were coral disease is contributing to reef names have been applied to symptoms proposed14–16. For black band dis- degradation, a conclusion based that may be caused by a single disease. ease, the postulated primary largely on an observed increase in Despite the current confusion, rapid pathogens included one species the numbers of diseased coral col- progress is being made. of cyanobacteria Oscillatoria sub- onies. Recent rigorous studies of membranaceae16 (renamed Phor- coral disease at both the mecha- midium corallyticum17) and a nism and ecosystem levels are Laurie Richardson is at the marine fungus18, in addition to the finally beginning to provide infor- Dept of Biological Sciences, Florida International sulfate-reducing bacteria (pre- University, Miami, FL 33199, USA mation that will define the role of ([email protected]). sumed to be of the genus Desulfo- coral disease in reef decline. vibrio11) and sulfide-oxidizing bac- teria (Beggiatoa spp.10) noted in The first coral diseases the 1970s. Most of the studies Investigations into the nature of coral diseases are rela- included the observation that all of these microorganisms tively recent, with the first descriptive reports appearing were present within black band. Black band disease was in the 1970s of coral tissue degradation occurring on stony, also newly reported to infect gorgonians19,20 (soft corals), reef-building corals (scleractinians). Two disease patterns in addition to the scleractinian, or ‘stony’, corals targeted were recognized in these initial studies, which were charac- in all previous studies, and was for the first time observed terized by either a sharply demarcated interface between on reefs of the Indo-Pacific21 and the Red Sea22, thus widely healthy and unhealthy coral tissue or a distinctive band expanding the previously known range of black band dis- (mm to cm wide). Each moved across coral colonies while ease (in the Caribbean and Western Atlantic). completely destroying coral tissue. The first coral disease A new, histological approach was applied to the study reported (in 1973) – ‘black band’ disease7 – consisted of a of white band disease by Peters et al.23 in 1983. Their work dark band that was present between apparently healthy revealed ‘packets’ of gram negative bacteria associated with coral tissue and freshly exposed coral skeleton (Fig. 1). The white-band-diseased tissue (as well as healthy) from col- second two coral diseases reported (in 1977) –‘white band’ onies of Acropora palmata at two sites in the Caribbean23. disease of branching acroporid corals8 and ‘plague’ (Fig. 2) Within five years up to 95% of all colonies on these study of massive and plate-forming corals9 – each appeared as a reefs died. Laboratory culturing and isolation attempts sharp boundary between coral tissue and exposed skel- yielded inconsistent results and no specific pathogen was eton, with no apparent microbial biomass. All three diseases postulated. progressively destroyed coral tissue at rates of several milli- Dustan’s report9 on plague in 1977 documented tissue meters per day. loss rates of up to 3.1 mm per day, with mortality of indi- vidual colonies occurring within four months. Microscopic Coral disease pathogens: early attempts at observation revealed the presence of gram-negative uni- characterization cellular and flexi-bacteria in diseased tissue, but no at- In the 1970s limited efforts were made to identify coral tempts were made to culture or isolate potential pathogens. disease pathogens. These efforts routinely consisted of Two additional coral afflictions were also reported in the microscopic observations of diseased tissue, all of which 1980s. The first was an extremely rapid pattern of tissue loss revealed the presence of various bacteria. Heterotrophic on scleractinian corals, which affected an entire colony at and phototrophic (for black band disease) bacteria were once (termed ‘shut down reaction’)16. Although no micro- observed, and both photosynthetic and heterotrophic bac- biological studies were conducted, exposure of healthy cor- teria were proposed as potential agents of coral disease7,9–11. als to sloughed-off, necrotic coral tissue elicited the same There were no reports of attempts to apply the established symptoms. The second report described tissue hyperpla- methods of medical microbiology (Koch’s postulates, Box 1) sia of gorgonian corals associated with nodules that con- to coral diseases. tained the filamentous green alga Entocladia endozoica24. 438 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00 PII: S0169-5347(98)01460-8 TREE vol. 13, no. 11 November 1998 REVIEWS Neither tissue degradation nor colony mortality oc- curred, however, and in- fected gorgonians recovered by encapsulating affected areas24. Currently, this syn- drome is not considered to be a disease (W.M. Goldberg, pers. commun.). Therefore, by 1984, four tissue-degrading coral dis- eases (plus the algal nod- ules of gorgonians) had been studied at a descriptive level: black band, white band, plague and shut down reac- tion. Of the four, the identity of only one primary causa- tive pathogen had been pro- posed – the cyanobacterium P. corallyticum found in black band disease17. This was pro- posed even though there was no success in obtaining an axenic (bacteria-free) cul- ture and the disease state Fig. 1. Black band disease on Colpophyllia natans. Two active infections are present, revealing the characteristic dark band separating healthy coral tissue and exposed coral skeleton (exposed as the result of coral tissue degradation could only be initiated by during the disease process). The band is dark because of high concentrations of the red pigment phycoerythrin, a inoculation using the cyano- light-harvesting pigment found in the dominant member of the black band community (the cyanobacterium Phormidium bacterium with other asso- corallyticum). The disease is found on reefs world-wide and targets nonacroporid scleractinian corals. Disease pro- ciated black-band-disease mi- gression is at a rate of 0.3–1 cm per day, and can kill a coral colony over several months. The sulfide-oxidizing bacterium Beggiatoa spp., another member of the black band community, is often present on the band surface as sulfide accumu- crobes. Despite the fact that lates within the band. Populations of this genus appear white, the result of intracellular accumulation of highly refractile Koch’s postulates were not elemental sulfur (a by-product of the sulfide oxidation). The black band community is now known to consist of a microbial fulfilled (Box 1), it was ac- community similar to those found in other illuminated aquatic environments that contain steep gradients of oxygen cepted for many years that and sulfide. the black-band disease agent was known. Characterization of coral diseases in the 1990s Research progress has accelerated in the 1990s as investigators have become interested in specific aspects of coral disease etiology. White band disease. Recently, Ritchie and Smith25 have demonstrated that there are two patterns of tissue-loss associated with white band disease, which they have termed white band type I and white band type II. Type I exhibits a disease line of ac- tive tissue necrosis, whereas type II has a variable zone between active tissue death and exposed coral skeleton, where coral tissue can be bleached but not necrotic. Differentiation between the Fig. 2. Plague on Dichocoenia stokesi. Type II is shown here. This coral is the most susceptible of 17 affected coral two types requires close species of the Florida reef tract (USA). Tissue loss occurs at rates of up to 2 cm per day, and because it affects small scrutiny over time, because coral colonies (normally ,10 cm in diameter) it routinely kills entire colonies in two to three days. Plague type II is the the bleached tissue area of most virulent and destructive scleractinian coral disease yet documented. Long-term effects on the reef are unknown. type II at times ‘catches up’ Epizootics of plague have occurred on Florida reefs in the 1970s, 1980s and 1990s and were recently reported in the with the necrotic zone, thus Caribbean in the 1990s. appearing identical to type I. TREE vol. 13, no. 11 November 1998 439 REVIEWS 11 weeks31.