Biological Conservation 96 (2000) 347±361
The signi®cance of coral disease epizootiology for coral reef conservation Edmund P. Green a,*, Andrew W. Bruckner b a UNEP-WCMC, 219 Huntingdon Road, Cambridge CB3 0DL, UK NOAA, National Marine Fisheries Service, 1315 East-West Highway, Silver Spring, MD 20910, USA
Received 26 January 2000; received in revised form 28 April 2000; accepted 3 May 2000
Abstract There are many aspects of coral disease that are poorly understood. The relationship, if any, between human activities and the incidence of coral disease is particularly important since it is frequently assumed that the number and prevalence of diseases are increasing, and are indicative of a general decline in the marine environment. Certainly a good understanding of these issues would assist in the conservation of coral reefs by identifying targets for mitigating management programmes. In situ observations of coral disease and associated mortality were therefore compiled from more than 150 sources, and reviewed. Although there have been cases where disease has caused major changes in the composition and structure of reefs, most notably in the Caribbean, these are exceptions when compared to the number of locations at which disease has been observed. With the exception of white-band disease, most frequently observed diseases do not appear to be speci®c in their host requirements, aecting species in many dierent genera. The overwhelming majority of disease in the Caribbean (97% of locations) has been recorded from coral reefs where human activities are expected to have medium to high impacts. Regional scale patterns in the incidence of coral disease may therefore be suitable bio-indicators of disturbance to coral reefs. This potential relationship should be investigated further with a view to using patterns of disease to monitor speci®c sources of stress on reefs. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Coral; Disease; Mortality; Incidence; Epizootiology
1. Introduction Bacteria were ®rst observed within coral tissue in the early 1900s (Duerden, 1902), but the ®rst reports of disease aecting scleractinian corals did not appear until the early 1970s. Increasingly frequent observations of coral diseases in the wild have been given added importance by the lack of previous observations even on wellstudied reefs. Therefore the possibility exists that the present widespread occurrence of coral diseases is a manifestation of a decline in the integrity of the wider marine environment. Thirty-four mass mortalities, each aecting >10% of a population, have been recorded in groups as diverse as sponges, seagrasses, cetaceans, urchins, ®sh and molluscs, as well as corals, and there is some indirect evidence to suggest that marine epidemics are becoming more frequent (Harvell et al., 1999). Diseases may be suitable bio-indicators (sensu Risk, 1999) of disturbance to coral reefs if a link to speci®c human
* Corresponding author. Fax:+44-1223-277-136. E-mail address: [email protected]
activities exists. This possibility continues to fuel the production of an extensive and varied literature. There is good direct (Gladfelter, 1982; Aronson and Precht, 1997) and indirect (Garzon-Ferreira and Zea, 1992) evidence that mortality arising from disease has modi®ed the composition and structure of coral reefs across the Caribbean by removing common and locally abundant species. Furthermore, the results of some ®eld monitoring programmes do suggest that the occurrence of disease, at least in the Florida Keys, has increased dramatically in the last few years (Porter et al., 1999). For most of the world's reefs a consensus of opinion exists that conditions during the past 20 years have been very dierent to those prevailing during the two decades prior to 1980. Although the exact nature of this global environmental change remains unknown it is tempting to speculate, as many have done, that direct and indirect human impacts on reefs are responsible. However, beyond tantalising glimpses provided by studies that have attempted to examine the relationship between disease and water pollution (e.g. Mitchell and Chet, 1975; Antonius, 1981), the role of anthropogenic in¯uence is extremely unclear. Indeed Richardson (1998)
0006-3207/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(00)00073-2
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
concludes in her review that this is one of the most important yet most poorly understood aspects of coral diseases. General aspects of coral disease have been summarised already (e.g. Peters, 1997; Goreau et al., 1998) and the etiology (the relationship between the host and disease-causing pathogen) of biotic diseases has been concisely reviewed by Richardson (1998). She emphasises that the procedure by which a presumed disease pathogen is demonstrated to be the causative agent, Koch's postulates, has not been ful®lled for most coral diseases so that they should be regarded as potential disease states rather than true diseases. This applies to all diseases mentioned here except aspergillosis and white plague type II. Other authors conclude that a disease may be abiotic as well as biotic, and in the case of abiotic diseases the cause could be an environmental stressor and not a micro-organism (Santavy and Peters, 1997; Peters, 1997). Coral bleaching is widely believed to be caused by a combination of elevated water temperatures and ultra-violet radiation. In this sense bleaching is an abiotic disease because it is not usually caused by a pathogen [although a bacterium has been shown to cause bleaching in Oculina paragonica, a Mediterranean species (see Toren et al., 1998)]. This review includes only those diseases which are presently believed to be biotic. Epidemiology is de®ned as the study of the incidence, distribution, abundance and control of disease, and an analysis of the interactions of a disease-causing agent and its host. It is most usually applied to human diseases. The equivalent term for animals is epizootiology, which is the study of the factors involved in the occurrence of animal diseases. The epizootiology of coral diseases is poorly understood, mainly because an analysis of the occurrence and distribution of diseases has not been carried out and because the factors that govern their spread remain largely unknown. If there is a link between anthropogenic in¯uence on reefs and the incidence and distribution of coral diseases then their occurrence is unlikely to be uniformly or randomly distributed at regional scales. An understanding of the global epizootiology of coral diseases would constitute a ®rst step in examining whether any relationship exists. This paper therefore complements the etiological review by Richardson (1998) by summarising all the in situ observations of the `major' diseases, and by providing data on the range of species aected, the geographical distribution, incidence and mortality caused. 2. A global coral disease database We present here data obtained from 155 separate sources which provide details of direct observations of
coral disease in the ®eld: 98 are articles from peerreviewed journals or conference proceedings; eight are postings on the electronic coral discussion list provided by the USA Department of Commerce National Oceanic and Atmospheric Administration (http: //coral.aoml.noaa. gov/lists/coral-list.html); seven are articles published on the internet; nine are non-reviewed conference proceedings or abstracts; two are popular magazine articles. Personal communications of coral disease or unpublished data, 34 in total, were included if referenced in a peerreviewed publication. A global coral disease database was created at WCMC (available at http//www.wcmc.org.uk/marine/ coraldis) and populated with records of coral disease from these sources. The occurrence of a disease on a coral species (or genus) was recorded for each location and date on which it was observed. Where the authors had assessed the incidence of the disease quantitatively this too was recorded as the percentage of colonies aected or number of aected colonies per m2. If the authors had not assessed the prevalence of the disease quantitatively then a qualitative assessment was carried out by assigning observations into one of four categories: no information on the extent of the disease, an observation of the disease on only one specimen or colony, an observation of the disease on a few (<50) specimens or colonies, an observation of the disease on many (>50) specimens or colonies. Mortality arising from disease was recorded in the database in a similar way: quantitatively, where the original observations permitted, as percentage of colonies suering complete mortality or number of dead colonies per m2, or qualitatively into four categories Ð no information on mortality, no mortality from the disease occurred (i.e. there was complete recovery of all infected tissue), partial mortality (<50% of living tissue) of infected colonies occurred, severe mortality (>50% of living tissue) of infected colonies occurred. 3. Global aspects of coral disease A total of 2076 records of coral disease were obtained in this manner. Coral diseases have been observed in 102 dierent species and in seven instances in colonies not identi®ed beyond genus (Echinopora spp., Eunicea spp., Favia spp., Favites spp., Fungia spp., Goniastrea spp., Goniopora spp.). Their occurrence is unquestionably global as coral diseases have been recorded on reefs in 54 dierent nations. However a disproportionate number of records, 66%, describe observations of disease in 38 nations of the Wider Caribbean (Table 1) although these constitute only 8% of the world's total coral reef area (Spalding and Grenfell, 1997). There is also a substantial number of observations of disease in the Red Sea and Gulf of Arabia. The dierence between
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361 Table 1 Records and sources of coral disease Region
Records of disease
Number of sources
Wider Caribbean Red Sea and Gulf of Arabia Paci®c and South East Asia Indian Ocean
1375 494 174 24
125 9 15 3
these two areas is that the majority (86%) of the observations of disease in the Red Sea and Gulf of Arabia were made by one individual in four papers (Antonius, 1985a,b, 1987, 1988) whereas there are 125 dierent sources for observations of disease in the Caribbean. 4. A plethora of names Richardson (1998) drew attention to the confusion that has been created by the many reports of new diseases during the 1990s. The variety of similar names for dierent diseases and the uncertainty that what is being described is actually a disease (Hayes and Goreau, 1998) contributes further to this situation. Indeed a total of 29 dierently named diseases have been recorded in the literature. Clearly, a method of meaningfully categorising this varied terminology is essential in attempting to assess
the global implications of coral disease. Twenty diseases (231 observations; Table 2) were excluded from further consideration in this article for one or more of the following reasons: 1. The name was assigned on the basis of very few or single observations, e.g. dark spot disease, white blotch, yellow pox disease, white syndrome, white spot disease, black and white purple spots, yellow to white spots. 2. There has been no documentation of tissue destruction and/or mortality (see Table 1 in Richardson, 1998), e.g. red band disease. 3. Controversy as to whether the name refers to a state which is caused by a pathogen or some other cause, e.g. damage from parrot®sh bites (Bruckner and Bruckner, 1998) has been referred to as rapid wasting disease or syndrome (Cervino et al., 1997). 4. The condition referred to as white-band disease (WBD) has been used to describe similar signs in massive and plating corals on Caribbean reefs. This condition has also been referred to as white plague and white death (Peters, 1997). To avoid confusion, all reports of WBD from the western Atlantic for corals other than the acroporids have been combined with records of white plague. 5. Corals are referred to simply as `diseased' with no further speci®c details.
Table 2 Diseases not included in this review Recorded disease name
Rapid wasting disease Blistering necrosis Patchy necrosis Yellow-band disease
34 32 24 22
8 1 3 7
Shut down reaction Red-band disease
White line disease White pox Dark spot disease Yellow-blotch disease
8 5 4 4
3 4 3 3
Abnormal development Skeleton eroding band Tissue necrosis White blotch Yellow pox disease White syndrome White spot disease Black and white purple spots Yellow to white spots
3 3 3 2 2 1 1 1 1
3 1 1 1 1 1 1 1 1
Antonius and Weiner (1982); Glynn et al. (1989); Dinsdale (1994); Santavy et al. (1999); Bruckner and Bruckner (1999) Cervino et al. (1997); Bruckner and Bruckner (1998) Peters (1984) Bruckner and Bruckner (1997a,b); Raghukumar and Raghukumar (1991) Cervino et al. (1997); Korrubel and Riegl (1998); Bruckner and Bruckner (1999) Antonius and Riegl (1997); Antonius (1988) Richardson (1992); Rutzler et al. (1983); also personal communications cited in Santavy and Peters (1997) Two coral list postings, one internet article Bruckner and Bruckner (1997c); Williams (1997) Goreau et al. (1998); Gil-Agudelo and Garzon-Ferreira (1999) Cervino and Smith (1997); McGrath and Smith personal communication cited in Cervino and Smith (1997) Personal communications and unpublished data cited in Peters et al. (1986) Antonius and Riegl (1997) Peters (1984) Dinsdale (1994) One internet article Antonius and Riegl (1998) One coral list posting ReefCheck data ReefCheck data
N, number of observations; P, number of dierent sources.
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
More than 1800 observations of the diseases in Table 3 were reviewed and aspects of the disease such as species infected, location and mortality recorded. Tissue destruction and/or mortality has been documented for all these diseases (see Table 1 in Richardson, 1998) with the exception of tumours, hyperplasia and neoplasia. These are grouped here in a general category called growth abnormalities because they have been widely observed and there is some evidence that they have been associated with necrosis (Glynn et al., 1989). Goreau et al. (1998) provide a useful summary of the diagnostic signs associated with coral diseases, and there are also good pictures and descriptions available on the internet (http://ourworld.compuserve.com/homepages/ mccarty_and_peters/coraldis.htm) and from the second author. 4.1. Black-band Disease Black-band disease (BBD) has been observed on 42 dierent species a total of 568 times (Table 4). A further 116 observations have been recorded on corals only identi®ed to genus. Black-band disease has been observed in 26 dierent countries, 19 of which are in the
Wider Caribbean Region (Fig. 1). Half of the species on which BBD has been observed are from this area, 16 scleractinians and ®ve octocorals. Observations in other areas exist but are rare Ð only 21% originate from reefs in the Red Sea or Paci®c. There were 51 quantitative observations of the incidence of BBD. In most cases (34) between 1 and 10% of colonies were infected equating to an occurrence of the disease of ca. 0.01±1 diseased colonies per m2. Occasionally infection rates would be lower (e.g. Garret and Ducklow, 1975; Edmunds, 1991) or slightly higher (e.g. Taylor, 1983; Bruckner and Bruckner, 1997a). Widespread infection of ca. 50% of colonies has been observed once, for Montastrea annularis in Key Largo, Florida (Richardson and Carlton, 1993). This corresponded to an incidence rate of 0.8 diseased colonies per m2. Overall it was possible to assess the incidence of black band disease quantitatively in half of the published observations. In these cases 17% of all observations recorded BBD as occurring on single coral colonies, 29% on <50 colonies and 7% on >50 colonies. Similarly, there were 27 quantitative observations of mortality occurring from BBD. Approximately half
Table 3 Diseases included in this review Recorded disease name
White-band disease type II White plague type I White plague type II
2 40 26
2 8 4
Yellow-blotch disease Aspergillosis Tumour
4 57 61
3 4 19
Garret and Ducklow (1975); Ducklow and Mitchell (1979); Antonius (1981, 1988); Antonius and Weiner (1982); Ramos-Flores (1983); Rutzler and Santavy (1983); Rutzler et al. (1983); Taylor (1983); Guzman and Cortes (1984); Peters (1984); Antonius (1985a,b); Rogers (1985); Dustan (1987); Williams and Bunkley-Williams (1990); Edmunds (1991); Liddell and Ohlhorst (1992); Porter and Meier (1992); Richardson and Carlton (1993); Bythell et al. (1993); Dustan (1993); Garzon-Ferreira and Kielman (1993); Dinsdale (1994); Glazebrook and Steiner (1994); Kuta and Richardson (1994, 1996, 1997); Santavy et al. (1994); Carlton and Richardson (1995); Littler and Littler (1996); Miller (1996); Richardson (1996 (1997); Richardson et al. (1997); Briggs et al. (1999); Bruckner and Bruckner (1997a,b, 1998); Grosholz and Ruiz (1997); Feingold (1988); Fenner (1998); Korrubel and Riegl (1998); Franklin (1998) Gladfelter et al. (1977); Antonius (1981); Bak and Criens (1981); Knowlton et al. (1981); Antonius and Weiner (1982); Gladfelter (1982); Peters et al. (1983); Laydoo (1984); Peters (1984); Antonius (1985a,b, 1987, 1988); Rogers (1985); Davis et al. (1986); Jaap et al. (1988); Korrubel and Riegl (1998); Gladfelter (1990); Williams and Bunkley-Williams (1990); Goenaga and Boulon (1992); Bythell and Sheppard (1993); Coles (1994); Ritchie and Smith (1995); Santavy et al. (1995); Smith and Ritchie (1995); Antonius and Riegl (1997); Aronson and Precht (1997); Bruckner and Bruckner (1997b); Bruckner et al. (1997); Aronson et al. (1998); Peters (1988); Williams et al. (1999) Richardson (1998); Ritchie and Smith (1998) Dustan (1977, 1987, 1993); Dustan and Halas (1987); Bruckner and Bruckner (1997b,c, 1998) Richardson et al. (1998b); Feingold and Richardson (1999); also Nedimyer personal communication cited in Richardson et al. (1998a) Cervino and Smith (1997); McGrath and Smith cited in Cervino and Smith (1997) Merkel et al. (1997); Nagelkerken et al. (1997a,b); Smith et al. (1998) Cheney (1975); Goldberg and Makemson (1981); Morse et al. (1981); Laydoo (1983); Peters (1984); Glynn et al. (1989); Liddell and Ohlhorst (1992); Dinsdale (1994); also Land and Bak, personal communication cited in Cheney (1975); Catala, Cheney, Goreau and Lang, Goreau, Hemmes, Lang, Neumann, Spencer-Davies, Wellington, personal communications cited in Peters et al. (1986) Loya et al. (1984); Peters (1984) Squires (1965); Cheney (1975); Morse et al. (1977); Bak (1983); Peters (1984); Coles and Seapy (1998)
N, number of observations; P, number of dierent sources.
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
Table 4 Species and genera of coral on which black band disease has been observed, and the countries in which these observations were madea Species Montastrea annularis Diploria strigosa Montastrea cavernosa Colpophylima natans Siderastrea siderea Gorgonia ¯abellum Gorgonia ventalina Diploria clivosa Diploria labyrinthiformis Dichocoenia stokesii Favia fragum Pseudopterogorgia acerosa Goniastrea pectinata Platygyra lamellina Meandrina meandrites Montastrea faveolata Plexaura ¯exuosa Plexaura homomalla Colpophyllia breviseria1isc Favia favus Favia pallida Favia stelligera Favites petagona Goniastrea retiformis Hydnophora microconos Leptoria phrygia Pseudopterogorgia americana Montastrea franksi Stephanocoenia intersepta Acropora hyacinthus Acropora nobilis Montastrea meandrites Acropora clathrata Acropora cytherea Acropora formosa Montipora aequituberculata Montipora ¯orida Pachyseris gemmae Porites astreoides Siderastrea radians Stephanocoenia micheliniid Turbinaria mesenterina Total a b c d
Nb 91 81 63 41 37 30 29 24 23 12 12 10 9 9 8 8 7 7 6 5 5 5 5 5 5 5 4 3 3 2 2 2 1 1 1 1 1 1 1 1 1 1
Genus Favia spp. Favites spp. Diploria spp. Montastrea spp. Colpophyllia spp. Acropora spp. Agaricia spp. Montipora spp. Porites spp. Gorgonia spp. Siderastrea spp.
N 35 35 14 14 8 2 2 2 2 1 1
Florida, USA Saudi Arabia Puerto Rico Virgin Islands Belize Bermuda Jamaica US Virgin Islands Bahamas Philippines Australia Egypt Bonaire Curacao Colombia Venezuela Cayman Islands St. Lucia British Virgin Islands Netherlands Antilles Costa Rica India St. Vincent Turks & Caicos Islands United Arab Emirates Fiji
171 106 84 68 56 53 32 31 25 18 13 9 8 8 8 4 3 2 2 2 1 1 1 1 1 1
There is some overlap between observations for M. annularis and those for M. faveolata and/or M. franksi. N, number of observations. Colpophyllia breviserialis=Colpophyllia natans. Stephanocoenia michelinii=Stephanocoenia intersepta.
these observations recorded mortality in 5% of colonies, or less (e.g. Feingold, 1988; Bruckner and Bruckner. 1997a). Seven observations have recorded mortality of between 10 and 30% (e.g. Antonius and Weiner, 1982). Bruckner and Bruckner (1997a) noted that a relatively small proportion of the colonies aected by BBD die from a single infection event, with mortality occurring primarily to small colonies. Siderastrea siderea colonies in St. Ann's Bay, Jamaica, lost 50% of their living tissue in 2±3 years with mean colony size falling from 2700 to
890 cm2. Over the same period the area of live Montastrea cavernosa declined by 68%,with mean colony size falling from 2100 to 470 cm2. This mortality occurred at multiple points on single corals so that the surviving larger colonies sub-divided into patches of live tissue physiologically separated by dead skeleton (Bruckner and Bruckner, 1997a). Mortality caused by BBD has varied markedly at dierent times for the same species at some locations. For example, <3% of Pseudopterogorgia acerosa colonies (from 0.1 diseased colonies per
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
Fig. 1. The locations of observations of black band disease on coral reefs (orange) in the Caribbean (the disease may have been observed at the same location more than once and on more than one species).
m2) on Sands Key, FL, were killed in 1987: 15% (from 0.48 diseased colonies per m2) died in 1998 (Feingold, 1988). 4.2. White-band disease types I and II White-band disease type II was recorded for the ®rst time in 1997 and can closely resemble type I with time (Ritchie and Smith, 1998). Presumably there is a good possibility that some of the cases described prior to 1998 were actually type II and not type I. For this reason, and because the recent description of type II means that there have been very few observations recorded, the two are treated together here. White-band disease (WBD) in the Caribbean is now believed only to infect corals in the genus Acropora. Within this region most observations of WBD have been made in the US and British Virgin Islands (Table 5). A substantial number of observations of WBD have been made elsewhere on 34 species in nine countries (Table 6). Many of these records are not from Acroporid species: disease signs appear similar to those reported for white plague, but plague has not been reported from outside the Caribbean. The majority of records in Table 6 were made in the Red Sea and Philippines during studies which attempted to demonstrate that active WBD in a coral is a precondition for the development of BBD (Antonius, 1985a, b). However, BBD has been studied extensively in many dierent species (Table 4) with no signs of disease which resemble
WBD (e.g. Edmunds, 1991; Bruckner and Bruckner, 1997a) and it is likely that WBD was misidenti®ed in these cases. The distribution of occurrences of WBD on Acroporid corals in the Wider Caribbean Region is plotted in Fig. 2. The most common Caribbean Acroporid corals are Acropora cervicornis and A. palmata. Infection rates on these species have varied substantially within the region with Davis et al. (1986) recording that between 5 and 26% of colonies were infected with white band disease Table 5 White band disease observed on Caribbean Acroporids Species Acropora palmata Acropora cervicornis
Na 77 43
N, number of observations.
US Virgin Islands British Virgin Islands Florida, USA Puerto Rico Belize Netherlands Antilles Bermuda Virgin Islands Jamaica Bahamas Bermuda Tobago Guadeloupe Nicaragua St. Lucia
25 21 18 11 10 9 6 6 4 3 3 2 1 1 1
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361 Table 6 White-band disease observations outside of the Caribbean Species
Goniastrea retiformis Plazygyra lamellina Hydnophora microconos Leptoria phiygia Acropora prolifera Favia stelligera Acropora humilis Acropora hyacinthus Acropora squarrosa Acropora variabilis Favia favus Favia pallida Favites petagona Goniastrea pectinata Pocillopora damicornis Stylophora pistillata Lobophyllia corymbosa Porites lutea Pocillopora verrucosa Leptoseris mycetoseroides Echinopora gemmacea Acropora hemprichi Leptoseris glabra Acropora capillaris Acropora pharaonis Mycedium elephantotus Podabacia crustacea Montipora ehrenbergi Acropora palifera Symphyllia radians Acropora nobilis Platygyra daedalea Montipora aequituberculata Total a
24 23 21 19 12 10 9 9 9 9 9 9 9 9 9 9 9 9 9 9 6 5 5 5 5 5 4 4 4 1 1 1 1 282
Saudi Arabia Philippines Egypt Oman Australia Guam India United Arab Emirates
305 108 25 6 2 1 1 1
ease as occurring on single coral colonies, 30% on <50 colonies and 5% on >50 colonies. Mortality arising from WBD has also varied substantially. Between 3 and 15% of Acropora palmata colonies were killed at sites in Puerto Rico (Antonius and Weiner, 1982). In the US Virgin Islands mortality in Acropora palmata as low as 3% (Antonius and Weiner, 1982) and as high as 33% (Gladfelter, 1982) has occurred. From 1977 to 1979 about 5 ha of reef at Buck Island Reef National Monument in St. Croix USVI were aected by WBD, although the incidence was highly variable (Gladfelter, 1982); within 10 years, populations declined from 85% cover to 5% primarily from WBD (Gladfelter, 1990). In the British Virgin Islands, the mortality was even greater with 50% of colonies dying in 1984 (Davis et al., 1986). Elsewhere, in Oman, mortality averaged 40% for colonies in six different genera (Coles, 1994). The highest mortality has been observed in Florida (Jaap et al., 1988) and the US Virgin Islands (Peters, 1988) where in excess of 90% of Acropora cervicornis and A. palmata died, respectively. On the shallow forereefs of south western Puerto Rico in 1992 the volume of living Acropora spp. tissue was only 0.05% of the volume measured in the mid 1970s, the near complete obliteration of these formerly dominant species being attributed to a combination of WBD, bleaching and bio-erosion from the boring sponge, Cliona langae (Williams et al., 1999). 4.3. White plague types I and type II
N, number of observations.
at various locations within the British Virgin Islands. In the US Virgin Islands the incidence of this disease has varied from 1±2% (Gladfelter et al., 1977; Antonius and Weiner, 1982) to 25% (Gladfelter, 1982) and as high as 64% in 1981 (Peters et al., 1983). In Tague Bay, USVI, the number of infected colonies of Acropora cervicornis has been recorded at 0.88 diseased colonies per m2 and the number of infected A. palmata colonies at 1.28 diseased colonies per m2. White-band disease has also been reported on other less abundant species, such as Agaricia agaricites and Stephanocoenia michelinii, at much lower incidence Ð 0.02 diseased colonies per m2 (Peters, 1984) but here these records have been combined with those for white plague. The highest recorded incidence of white band disease was in Jamaica and the Netherlands Antilles in 1980 where >80% of Acropora spp. colonies were infected (Rogers, 1985). Overall it was possible to assess the incidence of WBD quantitatively in just under half of all published observations. In these cases, 6% of all observations recorded white-band dis-
White plague type I has only been reported from the Bahamas (13 times), Puerto Rico (16) and Florida (11), and type II only in Florida (26 times). Type I is known to have infected 12 dierent species, type II 17 (Table 7). When studying disease epizootiology it is most sensible to treat white plague types I and II together because they were dierentiated only recently (Richardson et al., 1998a) and the two cannot be distinguished in situ. The term WBD has also been used in some cases to describe white plague in non-Acroporid corals. As a result, a total of 281 observations of WBD disease have been made on Caribbean non-acroporid corals (Table 8). Therefore the distribution of white plague is probably wider than just the Bahamas, Puerto Rico and Florida and should include the observations in Table 8. In the ®rst description of white plague type I at Carysfort Reef, FL, Dustan recorded it as occurring on 7% of Siderastrea siderea colonies and 24% of Mycetophyllia ferox: elsewhere, the proportion of infected Mycetophyllia ferox was even greater, 54% on French Reef and 73% on Molasses Reef (Dustan, 1977). More recently, type I has been observed in Puerto Rico on 47% of Diploria labyrinthiformis colonies, or 0.24 diseased colonies per m2, although this high incidence was con®ned to a single patch reef while outlying areas had a
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
Fig. 2. The locations of observations of white band disease on coral reefs (orange) in the Caribbean (the disease may have been observed at the same location more than once and on more than one species).
much lower prevalence of disease (Bruckner and Bruckner, 1997b). Only one quantitative observation has been made of the occurrence of type II: 9 and 38% of Dichocoenia spp. colonies at two reefs in Florida (Feingold and Richardson, 1999). Only Dustan (1993) has quantitatively assessed the mortality arising from white plague (type I) at <1% of coral colonies. Dustan had previously observed a high incidence of white plague in 1977 among Mvcetophyllia ferox, M. lamarckana and Colpophyllia spp. (Dustan, 1977). In 1982 these species were absent from a number of transects on the same reefs, although dead algalencrusted skeletons were still present. The authors discounted physical disturbance as the means of death because of the presence of these skeletons and attributed the mortality to disease (Dustan and Halas, 1987). 4.4. Yellow-blotch disease Yellow-blotch disease (YBD) is a relatively newly described condition that aects faviid corals in the genus Montastraea on western Atlantic reefs. This condition, formerly called yellow-band disease (Santavy et al., 1999), was ®rst identi®ed in 1994 in the lower Florida Keys (Reeves, 1994; Quirolo, cited in Santavy and Peters, 1997) and since then has been reported from Panama (Santavy et al., 1999), the United Arab Emirates (Korrubel and Riegl, 1998), Curacao (Bruckner and Bruckner, 1999), Bonaire and Puerto Rico (Bruckner, unpublished data). Yellow-blotch disease is a
necrotic event where concentric tissue margins have a pale yellow border 1±10 cm wide separating denuded skeleton from apparently healthy tissue. Richardson (1998) referred to yellow-blotch as a potential disease state because at the time it was not known to result in tissue mortality. However monitoring eorts near Key West have recorded an increased incidence of this disease and accompanied mortality (Quirolo, pers. comm.). Reef Care Curacao identi®ed an incidence of YBD of 20% on reefs in eastern Curacao during 1997, in an area that was apparently free from disease in 1993 (Coral-list server, 9 July 1998). Bruckner and Bruckner (1999) reported an incidence of 22% on four reefs in eastern and western Curacao during 1997±1998; they noted that YBD advances across a coral at 7±11 cm per year. 4.5. Aspergillosis Aspergillosis is a disease of soft corals and has only been recorded on two species Gorgonia ¯abellum and G. ventalina which occur in the Caribbean (Table 9). The disease has been observed throughout the region, although no records exist for continental Central America (Fig. 3). Nagelkerken et al. (1997b) have surveyed the occurrence of aspergillosis throughout the Caribbean. They recorded that 22±60% of colonies in various locations in the Bahamas were infected, 59±75% in the British Virgin Islands, 32±39% in the Netherlands Antilles and in the region of 50% in the Cayman Islands, Dominican
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361 Table 7 Species and genera of coral on which white plague types I and II has been observeda Species
Type I Siderastrea siderea Acropora palmata Monrastrea annularis Mycetophyllia ferox Acropora cervicornis Agaricia agaricires Colpophyllia natans Diploria labyrinthiformis Montastrea cavernosa Montastrea faveolata Mycerophyllia lamarckiana Stephanocoenia michelinii c Total
4 3 3 3 2 2 2 2 1 1 1 1
Colpophyllia spp. Dendrogyra spp. Diploria spp. Montastrea spp. Siderastrea spp. Porites spp.
Type II Dichocoenia stokesii Agaricia agaricites Agaricia lamarcki Colpophyllia natans Dendrogyra cylindrus Diploria labyrinthiformis Dmploria strigosa Eusmilia fastigiata Madracis decactis Madracis mirabilis Manicina areolata Meandrina meandrites Montastrea annularis Montastrea cavernosa Siderastrea siderea Solenastrea bournonii Stephanocoenia micheliniia Total
8 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 26
N 2 2 2 2 2 1
11 Dichocoenia spp.
Table 8 Observations of white-band disease on non-acroporid corals in the Caribbeana Species Montastrea cavernosa Diploria strigosa Diploria labyrinthiformis Montastrea annularis Agaricia agaricites Mycetophyllia ferox Mycetophyllia lamarckiana Porites astreoides Siderastrea radians Agaricia tenuifolia Siderastrea siderea Favia fragum Dichocoenia stokesii Stephanocoenia michelinii c Total
Nb 54 43 42 42 13 12 12 12 12 12 12 12 2 1
Country US Virgin Islands British Virgin Islands Florida, USA Puerto Rico Belize Netherlands Antilles Bermuda Virgin Islands Jamaica Bahamas Bermuda Tobago Guadeloupe Nicaragua St. Lucia
N 25 21 18 11 10 9 6 6 4 3 3 2 1 1 1 121
a It is likely that the disease described as WBD was actually white plague, and so these records have been combined with those of white plague in Fig. 2. b N, number of observations. c Stephanocoenia michelinii=Stephanocoenia intersepta.
Table 9 Countries in which aspergillosis has been observed aecting gorgoniansa
a There is some overlap between observations for M. annularis and those for M. faveolata and/or M. franksi. All observations are from the western Atlantic. b N, number of observations. c Stephanocoenia michelinii=Stephanocoenia intersepta.
Republic, Florida and Jamaica. The lowest incidence of aspergillosis that they recorded was 12% in Puerto Rico, the highest was 90% in the Lesser Antilles (Nagelkerken et al., l997b). There have been no quantitative records of mortality of Gorgonia spp. colonies from aspergillosis. 4.6. Abnormal development Tumours, neoplasia and hyperplasia have been recorded on corals throughout the world on several dierent species. Tumours have been observed on 20 species predominantly from the Paci®c and Caribbean, neoplasia on nine and hyperplasia on 12 (Table 10). The distribution of Caribbean records is shown in Fig. 4.
Bahamas Netherlands Antilles Lesser Antilles British Virgin Islands Florida, USA Trinidad Puerto Rico Jamaica Dominican Republic Cayman Islands US Virgin Islands Cuba Colombia
14 6 6 6 4 3 3 3 3 3 2 2 2
No records have been made outside the western Atlantic. N, number of observations.
Tumours have been recorded as having occurred on 1±10% of colonies of nine species of coral, including Pseudoplexaura spp., at two locations in Florida (Glynn et al., 1989). On other reefs in Florida between 20 and 55% of Pseudoplexaura spp. colonies have had tumours (Goldberg and Makemson, 1981). Elsewhere in the Caribbean ca. 20% of colonies have had tumours, e.g. Pseudoplexaura ¯agellosa in the Netherlands Antilles (Morse et al., 1981) and Gorgonia ventalin in Trinidad (Laydoo, 1983). Tumours have occasionally been recorded on nearly every colony observed [Gorgonia
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
Fig. 3. The locations of observations of aspergillosis on coral reefs (orange) in the Caribbean (the disease may have been observed at the same location more than once and on more than one species).
ventalina in the Netherlands Antilles (Morse et al., 1981]. There has only been one quantitative observation of hyperplasia, on Platygyra sinensis and P. pini in Australia where 18 and 24% of colonies were aected respectively (Loya et al., 1984). There has also only been one quantitative observation of neoplasia, on Gorgonia ventalin in Trinidad where 35 colonies over a 5 m2 area were aected (Morse et al., 1977). 4.7. A qualitative assessment of coral diseases A qualitative measure of incidence and mortality was only possible for the ®ve diseases in Table 11, as there were too few observations of white plague type II, yellow blotch disease, neoplasia and hyperplasia. Two conclusions can be drawn from Table 11: (i) that it is rare for any of these diseases to be observed in isolation on just a single colony, which is to be expected if infectious pathogens are responsible for the disease signs being observed, and (ii) that complete recovery of all infected tissue (zero mortality) has never been recorded. There is always some tissue loss associated with these diseases. 5. Discussion Corals are not the only group of animals to be suffering from outbreaks of diseases at global scales:
populations of amphibians have declined rapidly as a result of disease (Vial and Saylor, 1993). There are some similarities between the mass mortalities which have been observed in these two groups: (i) they were ®rst observed about 20 years ago; (ii) the diseases can cause 50±100% mortality and the extirpation of previously abundant species; (iii) a variety of age classes, including older individuals, are aected; (iv) there is no correlation to obvious sources of pollution, and; (v) global climate change may increase the eects of diseases (Carey, 2000). In both groups, the possibility exists that increased vulnerability to disease has arisen from the evolution of more virulent pathogens or from diminished immune responses in the hosts, or both. However, the available evidence seems to indicate that new marine diseases have emerged through range shifts of known pathogens, frequently human-facilitated (Harvell et al., 1999). However, important dierences exist in our ability to understand the epizootiology of diseases in these two groups. Unravelling the global implications of disease in amphibians has been assisted by a good comprehension of their immune systems (e.g. Carey et al., 1999), and by numerous programmes at many locations around the world which have monitored populations both before and after outbreaks. Consequently, data exist for amphibian populations which have, and have not, declined through disease (Carey et al., 2000). This same situation does not exist for corals although initiatives such as ReefCheck (Hodgson, 1999) and the Global
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361 Table 10 Species and genera of coral on which abnormal development (taken here to include tumours, neoplasia and hyperplasia) has been observed, and the countries in which these observations were made Species Tumour Acropora formosa Acropora palmata Gorgonia ventalina Pseudoplexaura porosa Porites astreoides Dipioria strigosa Dichocoenia stokesi Siderastrea siderea Plexaura homomalla Plexaura ¯exuosa Pavona gigantea Montipora verrucosa Montipora patula Millepora alcicornis Favia valenciennesii Agaricia lannarcki Acropora virgata Acropora nobilis Total Neoplasia Acropora formosa Acropora valenciennesii Acropora palmata Pseudoplexaura Plexaura homomalla Madrepora kauaiensis Gorgonia ventalina Acropora valida Acropora clathrata Total Hyperplasia Stephanocoenia Siderastrea siderea Siderastrea radians Porites porites Porites astreoides Montastrea annularis Favia fragum Diploria strigosa Colpophyllia natans Acropora cervicornis Plasygyra sinensis Platygyra pini Total a
Na Genus 9 4 3 3 2 2 2 I 1 1 1 1 1 1 1 1 I 1
Pseudoplexaura spp. 15 Florida, USA 25 Gorgonia spp. 3 Marshall Islands 5 Eunicea spp. 2 Jamaica 5 Plexaura spp. 1 Puerto Rico 4 Fungia spp. 1 Netherlands Antilles 4 Diploria spp. 1 Trinidad 2 Acropora spp. 1 Mariana Islands 2 Hawaii 2 Caroline Islands 2 US Virgin Islands 1 New Caledonia 1 Micronesia 1 Maldive Islands 1 Costa Rica 1 British Virgin 1 Belize 1 Bay of Panama 1 Australia 1
8 3 3 1 1 1 1 1 1
Mariana Islands Oman Netherlands Antilles Trinidad Hawaii Florida, USA
4 4 4 4 4 4 4 4 4 4 1 1 42
8 5 4 1 1 1
Puerto Rico US Virgin Islands Australia
30 10 2
N, number of observations.
Coral Reef Monitoring Network (GCRMN, 1998) have the potential to provide ®eld data on coral diseases at truly global scales. Until this happens the scienti®c literature is the best source of information available for an assessment of the future implications of geographically widespread diseases. Therefore, we must recognise that any conclusions on the epizootiology of coral diseases that are based solely upon observations recorded in the scienti®c literature must be considered in the light of biases inherent in this
approach, principally because scienti®c journals do not function as a monitoring mechanism. This has two consequences. First, the records of coral disease which we have summarised here represent the locations at which the authors are working, rather than the distribution of diseased colonies itself. Second, a simple observation of coral disease would not merit publication in a scienti®c journal, or even perhaps in most grey literature, so many observations may not have been placed in the public domain. Acknowledging these limitations, it is nevertheless possible to draw six simple conclusions on the global epizootiology of coral diseases. (i) The majority of disease has been recorded as occurring in the wider Caribbean region. Undoubtedly there has been a greater volume of coral reef research carried out there than in the Red Sea, for example, but it is interesting to note the relative scarcity of observations of disease in other areas of active research and monitoring, especially the Paci®c and South East Asia. It would appear that coral diseases have been particularly prevalent in the wider Caribbean region. (ii) Only one disease has caused a major change in the composition and structure of reefs: white-band disease has been the most signi®cant source of mortality to Acroporid corals over large areas of the Caribbean (e.g. Gladfelter, 1982; Williams et al., 1999). Other diseases have been observed in many locations throughout the region (147 in total) but have not caused permanent changes in community structure. (iii) Only a few studies have quanti®ed the prevalence of disease or the mortality arising from disease at any instant, and still fewer have monitored incidence or mortality on individual colonies over time. As a result, while complete or partial mortality of coral colonies is often attributed to disease, it is not usually possible to determine whether disease was indeed the cause. (iv) The occurrence of diseases may be increasing, but certainty over this fact will always be dicult as it is impossible to know what is normal. In general, reefs are not being devastated by biotic diseases in the same way that many were aected by bleaching during the 1997± 1998 event (Wilkinson, 1999). (v) Therefore the global implications of diseases on coral reefs may not be as severe as bleaching at this time (Hoegh-Guldberg, 1999). However, it would foolish to discount diseases as being unimportant. Outbreaks of coral diseases and mass mortality on reefs could be marine harbingers of world-wide environmental decline as has been claimed for amphibians on land and in freshwater ecosystems (Barinaga, 1990; Philips, 1990). (vi) Black-band disease, white plague and abnormal developments aect a large number of dierent sceleractinian corals. These diseases do not therefore appear to be very speci®c in their host requirements, aecting species in many dierent genera. However, it is possible that the same disease sign actually re¯ects dierent
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
Fig. 4. The locations of observations of abnormal developments on coral reefs (orange) in the Caribbean (abnormal developments may have been observed at the same location more than once and on more than one species).
Table 11 Percentage of observations recording disease incidence or mortality, arranged qualitatively into three categories (omitting observations which did not record any information on incidence or mortality)a Incidence
Black band disease White band disease White plague type I Aspergillosis Tumour
Single (1) colony
Few (2±50) colonies
Many (50+) colonies
No (0%) mortality
Partial (<50%) mortality
Severe (>50%) mortality
33 15 ± ± 3
54 73 53 44 66
13 12 47 56 31
± ± ± ± ±
49 54 ± 100 ±
49 42 100 ± ±
a Thus, 33% of observations which recorded the incidence of black band disease recorded it as occurring on just a single colony, etc. There were too few observations of white plague type II, neoplasia and hyperplasia to generate meaningful percentages.
etiologies, as a coral may manifest signs of disease in a limited number of ways. Without a doubt there will be a variety of environmental factors which govern the epizootiology of coral diseases, and they will interact in complex and variable ways. This review suggests that it would be sensible to investigate the potential geographic relationship between patterns of disease occurrence and various human disturbances within the wider Caribbean region. Not only may diseases be more prevalent in the Caribbean than elsewhere, but the threats to coral reefs vary widely in intensity across the whole region. A recent map-based indicator of four potential threats to corals (coastal development, marine-based pollution,
overexploitation and destructive ®shing, land-based pollution) has calculated that 39% of the Caribbean's reefs are at low risk of degradation from anthropogenic in¯uences, 32% at medium risk and 29% at high (Bryant et al., 1998). A preliminary comparison between the threat data of Bryant et al. (1998) and the distribution of coral diseases revealed that <3% of the locations at which disease has been observed in the Caribbean (Figs. 1±4) were on reefs judged to be at a low risk from environmentally damaging human activities. Although this low ®gure re¯ects reduced sampling of more remote locations, the possibility nonetheless exists that the incidence of disease may be a suitable bio-indicator (sensu Risk, 1999) of disturbance to coral reefs at
E.P. Green, A.W. Bruckner / Biological Conservation 96 (2000) 347±361
regional scales, and may perhaps ultimately ®ngerprint and date sources of stress. Future research should be directed to ascertaining whether ®eld observations of disease are consistent with this potential relationship, and to relating the epizootiology of coral diseases to speci®c factors. Only then can management and conservation programmes hope to address the regional implications of coral disease with remedial action. Acknowledgements The following people are warmly thanked for assisting in this work: Lucy Conway, for research and data entry; Mary Edwards, for map production; Anna Morton for editing the references; Mark Spalding and Tom Hourigan, for a review of the manuscript. Compilation of disease records and creation of the Global Coral Disease database was funded in part by the National Oceanic and Atmospheric Administration's National Marine Fisheries Service (#40AANF803496).
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