White plague-like coral disease in remote reefs of the Western Caribbean

The health of coral reef communities has been decreasing over the last 50 years, due the negative effects of human activities combined with other natural processes. We present documentation of a White Plague Disease (WPD) outbreak in the Serrana Bank, an isolated Western Caribbean atoll with presumably inexistent pollutant inputs from local human settlements. In addition, this study summarizes seven years of observations on diseased corals in the nearby island of San Andrés, which in contrast is one of the most populated islands of the Caribbean. There was a massive coral mortality in the atoll lagoon (14°27’53.24”, 80°14’22.27” W, and 12m depth) due to WPD on May 4 of 2003. Seventeen species were found dead or largely affected by the disease. The information resulting from GPS and manta-tow transects revealed that approximately 5.8ha of reticulate Montastraea spp. patch reefs were lethally affected by the disease in the atoll. On May 8 of the same year we observed and calculated a mean coral cover of 7.03% (SD± 2.44), a mean diseased coral tissue cover of 5.5% (SD± 1.1) and a 13.4% (SD± 8.05) of recently dead coral covered with a thin filamentous algae layer; approximately 73% of mortalities caused by the disease occurred before the end of the outbreak. A rough estimate of 18.9% in recent coral cover reduction can be attributed to WPD. This represents about 82% of the total coral cover decline since 1995. Semi-enclosed environments such as atoll lagoons and the reticulate patch-reefs of Montastraea spp. seem to be particularly vulnerable to this kind of coral disease, which constitute an alert to increase the monitoring of the same kind of atoll environments. The WPD has been present in the area of the nearby island of San Andrés at a low prevalence level, with sporadic increasing peaks of disease proliferation. The peaks observed during 1999 and 2004 comprised increases of 266% and 355% respectively, suggesting an alarming progression of the disease in this area. This study includes new information of the epizoolotiology of White Plague Disease and documents the permanent prevalence and progression of the WPD in the area of San Andres Island. Rev. Biol. Trop. 58 (Suppl. 1): 145-154. Epub 2010 May 01.

Together with rain forests, coral reef ecosystems have the highest biodiversity on the planet (Sebens 1994).In fact, coral reefs exhibit greater animal diversity than any other marine ecosystem (Rohwer et al. 2002).The economic value of such remarkable biodiversity has been estimated to approach $375 billion of dollars per year (Constanza et al. 1997).However, it is not only their monetary value that makes coral reefs worth preserving, they play a critical role in the overall biological processes of the ocean and the entire planet as well.The health of coral reef communities has been significantly decreasing over the last 50 years, due the negative effects of human activities combined with other natural processes (Harvell et al. 2004).Right now levels of coral mortality are unprecedented (Garrison et al. 2003).Many biotic and abiotic factors acting alone or together, have been identified as causes of this decrease in coral reef coverage, e.g., temperature increase, higher ultraviolet radiation, toxic chemicals input, nutrient imbalance, predation, overgrowth of algae and infectious diseases (Hughes et al. 2003).Infectious diseases are now recognized as important modifying factors in natural systems, being involved in changes of reproduction rates, growth rates, community structure, species diversity and abundance, host genetic diversity and co-evolutionary processes of reef organisms associated with coral reef communities (Loya et al. 2001, Altizer et al. 2003).To date, up to 30 different coral diseases have been monitored worldwide, but only the pathogens of five of those diseases have been identified: Black Band Disease (Richardson et al. 1998, Weir et al. 2000, Nugues et al. 2004), Aspergillosis (Geiser et al. 1998), Bacterial Bleaching (Kushmaro et al. 2001), White Pox (Patterson et al. 2002) and White Plague Disease (Richardson et al. 1998, Drenner et al. 2003).Reservoirs are known for only three coral diseases: Black Band Disease, Aspergillosis, and White Plague Disease (Richardson et al. 1998, Weir et al. 2000, Denner et al. 2003, Nugues et al. 2004).
White Plague Disease (WPD) is one of the most common, virulent and prevalent diseases that has been observed affecting coral reefs in the Caribbean basin, which is now considered a marine disease hot spot (Harvell 1999, Weil et al. 2002, Santavy et al. 2001, Borger 2003).This disease has caused heavy losses on several coral species across this region (Richardson et al. 1998), and has created concern about the survival of coral reef communities due its rapid rate of tissue destruction, high level of contagiousness and the ability to cause widespread mortalities in most Caribbean coral species (Richardson et al. 2001, Nugues et al. 2004).
The Serrana Bank is located in the Southwestern Caribbean and belongs to the Archipelago of San Andres, Old Providence and Santa Catalina, Colombia.Its one of the few true oceanic atolls of the Caribbean surrounded by depths of thousands of meters (Sánchez et al. 2005).It has been inferred, for its location, that Serrana Bank has suffered little impact from local human activities (e.g.contamination).This bank was declared a Biosphere Reserve by UNESCO (Seaflower Biosphere Reserve), and active research has been developed to design a network of Marine Protected Areas-MPAs (Friedlander et al. 2003, Sánchez et al. 2005).One of the particularities of these atolls is the mid-depth (12-18m) lagoonal basin, usually covered by a dense reticulate patch-reef network (Diaz et al. 1997).These reef networks are mostly dominated by massive scleractinian corals, especially Montastraea annularis and M. faveolata.In this note we describe an extensive and lethal WPD outbreak observed in the lagoonal patch-reef areas of Serrana Bank.We also include the results from monitoring activity of the same disease over seven years in the nearby island of San Andrés, Colombia, which in contrast is one of the most populated islands of the Caribbean.

MATERIALS AND METHODS
During a coral reef survey at Serrana Bank and two other Southwestern Caribbean atolls, in April-May 2003, three diseases were observed and documented: White Plague Disease (Dustan 1977, Dustan & Halas 1987, Richardson et al. 1998), Bleaching, and Dark Spots (Gil-Agudelo & Garzon-Ferreira 2001).These diseases were present in different habitats throughout the banks but usually with low intensity, as it has been previously observed in these areas since the 1990s (see review in Garzon-Ferreira et al. 2001).However, WPD was particularly noticeable in the lagoonal habitats of Serrana bank towards the semi-enclosed lagoonal basins from the North and East elbowlike ends (Fig. 1; see area description in Sánchez et al. 2005).The mass coral mortality due to WPD was abrupt and extensive in the lagoon, around 14°27'53.24"N, 80°14'22.27"W (May 4, 2003), 12m depth (Fig. 1).In addition, three stations were surveyed to estimate the damage to the coral colonies and coral populations in the areas surrounding the affected zone (Fig. 3).Due to the severity and high incidence of WPD in the affected area, we returned to the area on May 8, 2003 (four days after the first observation) to perform a more detailed estimation of the damage caused to the coral reef by the pathogen.Photographs were taken of some of the affected colonies that had been photographed during the first visit to the area (Fig. 2 E-F).Additionally, this study included White Plague Disease data from the National Coral Reef Monitoring System of Colombia (SIMAC) that has been recorded since 1998 in a series of permanent transects at different depths and two sites in the nearby island of San Andres (Fig. 1).The stations are located West of the island, where the highest diversity and coral abundance is observed (Díaz et al. 2000).

RESULTS
At Serrana bank, the diseased colonies with portions of healthy tissue had a very sharp zone of interaction, which appeared as a white band of variable width, where tissue-less coral skeleton was perfectly visible.These observations were similar to those originally describing the White Plague Disease (Dustan 1977).Previously affected areas in coral colonies presented overgrowth of filamentous algae (Fig. 2).Seventeen coral species were observed affected by the disease on May 4, 2003.Mortality was up to 100% of recently dead coral on some of the sampled quadrants (Fig. 2).The information resulting from GPS and manta-tow transects revealed that approximately 5.8ha of reticulate Montastraea spp.patch reefs were uninterruptedly affected by the disease (Fig. 1).On May 8 of the same year we observed and calculated a mean coral cover of 7.03% (SD±2.44), a mean diseased coral tissue cover of 5.5% (SD±1.1)and a 13.4% (SD±8.05) of recently dead coral covered with a thin filamentous algae layer.This is approximately 73% of mortality caused by the disease before the end of the outbreak.A rough estimate of 18.9% in recent coral cover reduction can be attributed to WPD.Given that previously in 1995 there was ~38% of total coral cover in the same area of Serrana Bank (Diaz-Pulido et al. 2004), nearly ~81% of the recent coral mortality (ca.-30 % of coral cover) was caused before the end of the 2003 disease outbreak.Comparative photographs roughly revealed that the disease was growing at an approximate rate of 10mm per day (Fig. 2).
The disease outbreak was observed on adjoining colonies throughout the affected reef.Nonetheless, three species were not observed infected (Mycetophyllia ferox, Leptoseris cucullata, and Millepora alcicornis) and Siderastraea siderea appeared only bleached.Porites spp.had an overall low disease incidence and mortality (Fig. 3).In contrast, most of the other species presented >50% of their cover as recently dead (Fig. 3).The corals were observed as presumably becoming infected by the disease through contact with neighboring colonies due to the observed pattern along the patch reefs, which creates the potential of disease spread throughout the entire interconnected patch reef network.We also observed Acropora cervicornis with a white band-like disease (Fig. 2 F), this species has previously been reported as not suffering White Plague Disease (Sutherland et al. 2004).Since the disease starts at the edges of the colonies, which corresponds to the bases of branching corals, it is not possible to discern by observation between White Plague Disease and White Band in the case of A. cervicornis, particularly if these diseased colonies were in the middle of hundreds of diseased colonies with WPD.
The prevalence of WPD in the area of San Andrés ranged between a minimum value of 0.4% in 2000 and a maximum of 2.2% in 2004 (Fig. 4a), whereas the number of affected colonies ranged between 6 colonies/200m 2 and 88 colonies/200m 2 (Fig. 4b).Despite that the mean annual prevalence values usually did not exceed 1% throughout the monitoring program, these observations matched the prevalence ranges for other Caribbean localities (0.0-3.2%, Weil et al. 2002).The peaks observed during 1999 and 2004 comprised increases of 266% and 355% respectively, suggesting an alarming progression of the disease in this area.This pattern was also observed in a number of affected colonies (Fig. 4c).During the seven years of monitoring a total of 23 coral species have been observed diseased.Particularly during 2004, the worst year so far for the disease in San Andrés, 20 species were observed affected.These include the same species observed in Serrana (Fig. 3) and also Leptoseris cucullata, Millepora alcicornis and Mycetophyllia ferox, which were not noted as diseased in Serrana.

DISCUSSION
This is the first report of a White Plague Disease (WPD) outbreak in Serrana Bank, an isolated Western Caribbean atoll, with presumably inexistent pollutant inputs from local human settlements.In addition, this study summarizes seven years of observations on diseased corals in the nearby island of San Andrés.A similar disease outbreak has been reported by Nugues (2002) in the coral reefs from St. Lucia.Unfortunately, it is impossible to determine if a given outbreak is caused by the same kind of pathogen until a standard diagnostic procedure, such as the one proposed by Richardson et al. (2005), is widely used.Despite the increasing taxonomy in plague-like diseases based on symptomatic characteristics or in single species of bacteria, the key to this type of disease seems to be the disturbance of the microbial flora of the coral tissue due to changes in environmental conditions that can  both trigger the virulence of a pathogen and cause stress in the animal (Pantos et al. 2003).
The Serrana Bank lagoon has a semienclosed basin where water masses can reside for some period of time.This characteristic could be adverse for coral communities if the environmental conditions are different than normal (e.g., high temperature, nutrients, among others).Nonetheless, there were no high seawater surface temperature (SST) spots recorded in this area between April 29 and May 8, 2003 (University of South Florida, College of Marine Science, SST, ImaRS website).In the case of the 2003 WPD outbreak in Serrana Bank, there were two time-appealing coincidences with similar outbreaks at Corn Island (off the Nicaraguan coast: A. Hunt, pers.com.) in May, and the barrier reef off Belize (T.McClanahan, pers. com.) in July.Given the unlikeness of an eventual direct input of human locally produced pollutants in this area due its isolation from the land, it is however possible that a significant amount of nutrients and toxic compounds may have came from a remote source.It has been suggested and widely documented (Peters 1997, Goreau et al. 1998, Antonius & Ballesteros 1998, Geiser et al. 1998, Harvell 1999) that synthetic-organic chemicals and anthropogenic pollutants, viable microorganisms, macro and micronutrients, and trace metals are likely to be carried in the wind-dust air masses and deposited in the oceans (Garrison et al. 2003).These "dusttravelers" can change the local conditions of such an enclosed lagoon environments, and therefore facilitate the sporadic and unpredictable occurrence of WPD outbreaks in human isolated reefs (Garrison et al. 2003).However, it is unknown if the three places had the same kind of disease.Consequently, more observations (both oceanographic and microbiological/ genetic) and monitoring networks along Southwestern Caribbean reefs are needed to discern the epizootiology patterns producing mass disease outbreaks such as the ones observed in Serrana Bank and other Caribbean regions.
In the island of San Andrés, these results corroborated what was found by Garzón-Ferreira et al. (2001) and Weil et al. (2002), that the area of San Andres is an important focus of White Plague Disease prevalence.However, since Serrana Bank is considerably less affected by human impact than San Andres Island, the widespread outbreak observed in Serrana suggests that the nature of these events could be due to remote wind-transported particles (e.g.dust, toxic chemicals, microorganisms) or other ocean-wide anomalies.
This study included new information of the epizoolotiology of White Plague Disease.It documented as well the permanent prevalence and progression of the WPD in the area of San Andres Island.This study should also constitute an alert to increase the monitoring of the same kind of atoll environments (e.g., lagoonal reticulate patch-reef: Diaz et al.

Fig. 1 .
Fig. 1.Map showing the area affected by white plague-like disease in the Serrana Bank, Caribbean sea (see area details in Sánchez et al. 2005).

Fig. 4 .
Fig. 4. A) Percentage of white plague-like disease prevalence during 1998-2004 (bars are standard errors) in San Andrés.B) Number of colonies affected/200m 2 .C) Number of affected species per observed year.