Global coral disease prevalence associated with sea temperature anomalies and local factors

Coral diseases are taking an increasing toll on coral reef structure and biodiversity and are important indicators of declining health in the oceans. We implemented standardized coral disease surveys to pinpoint hotspots of coral disease, reveal vulnerable coral families and test hypotheses about climate drivers from 39 locations worldwide. We analyzed a 3 yr study of coral disease prevalence to identify links between disease and a range of covariates, including thermal anomalies (from satellite data), location and coral cover, using a Generalized Linear Mixed Model. Prevalence of unhealthy corals, i.e. those with signs of known diseases or with other signs of compromised health, exceeded 10% on many reefs and ranged to over 50% on some. Disease prevalence exceeded 10% on 20% of Caribbean reefs and 2.7% of Pacific reefs surveyed. Within the same coral families across oceans, prevalence of unhealthy colonies was higher and some diseases were more common at sites in the Caribbean than those in the Pacific. The effects of high disease prevalence are potentially extensive given that the most affected coral families, the acroporids, faviids and siderastreids, are among the major reef-builders at these sites. The poritids and agaricids stood out in the Caribbean as being the most resistant to disease, even though these families were abundant in our surveys. Regional warm temperature anomalies were strongly correlated with high disease prevalence. The levels of disease reported here will provide a much-needed local reference point against which to compare future change.     

Algal contact as a trigger for coral disease

Diseases are causing alarming declines in reef‐building coral species, the foundation blocks of coral reefs. The emergence of these diseases has occurred simultaneously with large increases in the abundance of benthic macroalgae. Here, we show that physical contact with the macroalga Halimeda opuntia can trigger a virulent disease known as white plague type II that has caused widespread mortality in most Caribbean coral species. Colonies of the dominant coral Montastraea faveolata exposed to algal transplants developed the disease whereas unexposed colonies did not. The bacterium Aurantimonas coralicida, causative agent of the disease, was present on H. opuntia sampled close to, and away from diseased corals, indicating that the alga serves as a reservoir for this pathogen. Our results suggest that the spread of macroalgae on coral reefs could account for the elevated incidence of coral diseases over past decades and that reduction of macroalgal abundance could help control coral epizootics.     

Coral diseases on Philippine reefs: genus Porites is a dominant host

While it is generally assumed that Indo-Pacific reefs are not widely affected by diseases, limited data suggest a number of diseases and syndromes that appear to differ from those currently under study in the Caribbean. This report presents the results of a baseline survey of coral diseases in 2 regions in the Philippines: the Central Visayas and the Lingayen Gulf. Mean prevalence for all diseases observed was 8.3 +/- 1.2% (mean +/- SE; n = 8 reefs), with Central Visayas reefs showing higher disease prevalence (11.6 +/- 2.8%; n = 4 reefs) than those of Lingayen Gulf (5.1 +/- 1.4%; n = 4 reefs). Five diseases and syndromes were described; 3 of these-Porites ulcerative white spot disease (PUWS) (prevalence = 8.96 +/- 2.2%), tumors (prevalence = 1.0 +/- 0.5%) and pigmentation response (prevalence = 0.5 +/- 0.2%)--occurred frequently in both regions and targeted the genus Porites. Correlation between disease prevalence and number of Porites colonies was fairly strong (r2 = 43.4), though not significant, and no correlation was seen between prevalence and either the amount or diversity of hard coral. Porites is a major reef-builder in the Indo-Pacific comprising 30% of hard coral colonies on our surveyed reefs, and is generally thought to be a hardy, long-lived genus. Diseases targeting this robust group present an as yet unquantified risk to Philippine reefs and could result in major changes in reef structure.     

Coral disease outbreak at Navassa,a remote Caribbean island

In November 2004, a high prevalence of coral disease was observed at several sites around Navassa, an uninhabited Caribbean island between Haiti and Jamaica. At least fifteen mounding and foliaceous scleractinian species were affected with ‘white disease’ signs. Coral disease incidence was observed to be absent in quantitative surveys in 2002, but in 2004 average prevalence (i.e., % of colonies) of active disease ranged up to 15% and an additional 19% prevalence of colonies with patterns of recent mortality consistent with disease. Large and/or Montastraea spp. colonies were disproportionately affected and the anticipated loss of these large, reef-building colonies will impact coral community structure. One or more potential factors may influence the initiation and persistence of disease outbreak conditions at Navassa including recent hurricane disturbance, regional patterns of increasing disease impact in deep or remote Caribbean reefs, or vectoring of disease by the corallivorous worm, Hermodice carunculata.     

Non-colonial coral macro-borers as indicators of coral reef status in the South Pacific of Costa Rica

Coral reef status was surveyed in three south Pacific coral reefs of Costa Rica, one in Ca?o Island and two in Golfo Dulce, and the density, richness and distribution of non-colonial macro borers (> 1 mm) was determined in dead and live coral fragments from these reefs. Based upon traditional indicators of degradation such as high particulate suspended matter and low live coral cover, the reefs at Ca?o Island are in better condition than those at Golfo Dulce. Reef degradation in Golfo Dulce is mainly due to high loads of terrestrial sediments as a consequence of watersheds deforestation. In this study, 36 coral boring species are reported for the eastern Pacific. At the family level, there is high endemism (10%) and greater affinity with the Indo-Pacific (34%), as compared with the eastern Atlantic and Mediterranean (29%) and western Atlantic and Caribbean (27%). The dominant non-colonial macro boring families at the study reefs are mytilid bivalves, eunicid polychaetes and aspidosiphonid sipunculans, with the bivalves considered the main internal bioeroders due to their greater body size and abundances. The level of mortality of the coral colonies and the general level of reef degradation influenced the composition of non-colonial macro-borers. Diversity and total macro-borer density, especially aspidosiphonid density, is higher in corals with greates dead than live cover. In the healthiest coral colonies (less than 50% of partial mortality), mytilids domination, macro-borer diversity and total density, is higher in Golfo Dulce, where reefs are more degraded. In the most affected coral colonies (more than 50% dead), macro-borers total density, especially aspidosiphonids density, is higher, of the healthiest reef of this study, Platanillo. Bivalve relative abundance increases and sipunculan relative abundance decreases with increasing site degradation. In conclusion bioeroder variables can also be used as reef health indicators.     

Relationship between Phylogeny and Immunity Suggests Older Caribbean Coral Lineages Are More Resistant to Disease

Diseases affect coral species fitness and contribute significantly to the deterioration of coral reefs. The increase in frequency and severity of disease outbreaks has made evaluating and determining coral resistance a priority. Phylogenetic patterns in immunity and disease can provide important insight to how corals may respond to current and future environmental and/or biologically induced diseases. The purpose of this study was to determine if immunity, number of diseases and disease prevalence show a phylogenetic signal among Caribbean corals. We characterized the constitutive levels of six distinct innate immune traits in 14 Caribbean coral species and tested for the presence of a phylogenetic signal on each trait. Results indicate that constitutive levels of some individual immune related processes (i.e. melanin concentration, peroxidase and inhibition of bacterial growth), as well as their combination show a phylogenetic signal. Additionally, both the number of diseases affecting each species and disease prevalence (as measures of disease burden) show a significant phylogenetic signal. The phylogenetic signal of immune related processes, combined with estimates of species divergence times, indicates that among the studied species, those belonging to older lineages tend to resist/fight infections better than more recently diverged coral lineages. This result, combined with the increasing stressful conditions on corals in the Caribbean, suggest that future reefs in the region will likely be dominated by older lineages while modern species may face local population declines and/or geographic extinction.     

Status and progress in coral reef disease research

Recent findings on the ecology, etiology and pathology of coral pathogens, host resistance mechanisms, previously unknown disease/syndromes and the global nature of coral reef diseases have increased our concern about the health and future of coral reef communities. Much of what has been discovered in the past 4 years is presented in this special issue. Among the significant findings, the role that various Vibrio species play in coral disease and health, the composition of the 'normal microbiota' of corals, and the possible role of viruses in the disease process are important additions to our knowledge. New information concerning disease resistance and vectors, variation in pathogen composition for both fungal diseases of gorgonians and black band disease across oceans, environmental effects on disease susceptibility and resistance, and temporal and spatial disease variations among different coral species is presented in a number of papers. While the Caribbean may still be the 'disease hot spot' for coral reefs, it is now clear that diseases of coral reef organisms have become a global threat to coral reefs and a major cause of reef deterioration.     

Genetic Susceptibility,Colony Size,and Water Temperature Drive White-Pox Disease on the Coral Acropora palmata

Outbreaks of coral diseases are one of the greatest threats to reef corals in the Caribbean, yet the mechanisms that lead to coral diseases are still largely unknown. Here we examined the spatial-temporal dynamics of white-pox disease on Acropora palmata coral colonies of known genotypes. We took a Bayesian approach, using Integrated Nested Laplace Approximation algorithms, to examine which covariates influenced the presence of white-pox disease over seven years. We showed that colony size, genetic susceptibility of the coral host, and high-water temperatures were the primary tested variables that were positively associated with the presence of white-pox disease on A. palmata colonies. Our study also showed that neither distance from previously diseased individuals, nor colony location, influenced the dynamics of white-pox disease. These results suggest that white-pox disease was most likely a consequence of anomalously high water temperatures that selectively compromised the oldest colonies and the most susceptible coral genotypes.     

Distribution and prevalence of coral diseases in the Veracruz Reef System, Southern Gulf of Mexico

Ten reefs of the Veracruz Reef System (VRS) were surveyed to evaluate the distribution and prevalence of diseases that affect stony corals. Total disease prevalence on corals in the VRS was 4.8%. Seven diseases affecting 6 coral genera (4 of which are the most abundant) were observed in 85.2% of the evaluated sites. As observed in other reefs of the Caribbean, dark spots disease had the highest prevalence (2.9%) and widest distribution. The incidence of disease showed a patchy distribution, with prevalence being significantly higher on the reef flats than on the windward and leeward sides.     

Scleractinian coral diseases in south Florida: incidence, species susceptibility, and mortality

There are limited quantitative data available documenting the natural, or non-epizootic, occurrence of scleractinian coral diseases over multiple years. Individual coral colonies exhibiting black band disease (BBD), white plague (WP), dark spots syndrome (DSS), and white band disease (WBD) were monitored 3 times per year on 5 south Florida reefs over a 2 yr period. Surveys included measurements of coral population composition, coral diversity, disease type, coral species affected, colony size, percent of colony affected, and the number of lesions or active infections per colony. Data on re-infections of the same colonies, multiple infections per colony, disease duration, disease-associated tissue mortality, and coral recruitment are also presented. A total of 674 coral colonies exhibiting coral diseases were tagged and monitored. DSS was the most common syndrome (n = 620 infected colonies), but BBD and WP infections caused the largest amount of coral tissue death. The only disease that exhibited a linear increase in incidence with elevated temperature was BBD. DSS and BBD were the most persistent conditions, and WP infections were comparatively short-lived, with obvious signs of disease typically disappearing after 2 to 3 mo. The only disease that caused total colony death as oppposed to partial mortality during the survey period was WBD. WP and DSS incidence was significantly positively correlated with the relative frequency of the species most commonly affected by each disease at each study site. Of the 61 colonies examined in the recruitment survey, only 5 scleractinian coral recruits were identified. The most commonly recorded colonizer of exposed coral skeleton was filamentous/turf algae, thus indicating the potential for a shift towards algal-dominated reef communities.     

Ecological Physiology of a Coral Pathogen and the Coral Reef Environment

Laboratory studies on the ecological physiology of a coral pathogen were carried out to investigate growth potential in terms of environmental factors that may control coral diseases on reefs. The disease chosen for this study, white plague type II, is considered to be one of the major diseases of Caribbean scleractinian corals, affecting a wide range of coral hosts and causing rapid and widespread tissue loss. It is caused by a single pathogen, the bacterium Aurantimonas coralicida. A series of laboratory experiments using a pure culture of the pathogen was carried out to examine the roles of temperature, pH, and O₂ concentration on growth rate. Results revealed optimal growth between 30 and 35°C, and between pH values of 6 and 8. There was a distinctive synergistic relationship between pH and temperature. Increasing temperature from 25 to 35°C expanded the range of pH tolerance from a minimum of 6.0 down to 5.0. O₂ concentration directly affected growth rate, which increased with increasing O₂. The combined effects of increasing O₂ and increasing temperature resulted in a synergistic effect of more rapid growth. These laboratory results are discussed in terms of the coral host and the range of the environmental factors that occur on coral reefs. We conclude that changing environmental conditions in the reef environment, in particular observed increases in water temperature, may be promoting coral diseases by allowing coral pathogens to expand their ecological niches. In the case of the white plague type II pathogen, elevated temperature would allow A. coralicida to colonize the low pH environment of the coral surface mucopolysaccharide layer as an initial stage of infection. The synergistic effect between temperature and oxygen concentration appeared to be less environmentally relevant for this coral pathogen.     

Three scleractinian coral diseases in Dominica, West Indies: distribution, infection patterns and contribution to coral tissue mortality

Coral diseases have been documented in many areas of the Caribbean, but studies in the eastern Caribbean region have been lacking. The prevalence, distribution patterns and contribution to the mortality of coral tissue by black band discase (BBD), white plague (WP) and dark spots disease (DSD) were examined at five reef sites along the west coast of Dominica. 185 of the 325 diseased colonies recorded between March and August 2000, in a survey area of 5884 m2, were WP. This disease contributed to 89% of the total 4.08 m2 of tissue mortality caused by diseases during the survey period. WP also affected the largest average tissue surface area (relative to colony size) per colony and exhibited the largest average tissue loss per infection when compared to BBD and DSD. The species most susceptible to WP and BBD in Dominica differed from most other described Caribbean locations with Siderastrea siderea being most susceptible. S. siderea was also the only species noted to be susceptible to DSD. Measurements of colony size revealed that each disease affected the larger colonies of some coral species. Comparisons between disease prevalence at each site and various physical parameters, including temperature, wave height, depth, and current patterns, did not exhibit significant correlations. The lack of a direct correlation between temperature and disease prevalence indicates that there are other seasonal factors contributing to the higher prevalence of diseases recorded during the summer months in Dominica. WP prevalence at each site was positively correlated to the relative species abundances of the species most susceptible to WP. This was the dominant factor in determining site-specific disease densities of this disease and may therefore be a valuable predictive and management tool. There were no correlations between BBD or DSD and the relative abundances of susceptible species. The spatial distribution patterns of WP, BBD and DSD were clustered, which is a distribution pattern that suggests an infectious disease.     

Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994–2014

We propose ‘the moving target hypothesis’ to describe the aetiology of a contemporary coral disease that differs from that of its historical disease state. Hitting the target with coral disease aetiology is a complex pursuit that requires understanding of host and environment, and may lack a single pathogen solution. White pox disease (WPX) affects the Caribbean coral Acropora palmata. Acroporid serratiosis is a form of WPX for which the bacterial pathogen (Serratia marcescens) has been established. We used long-term (1994–2014) photographic monitoring to evaluate historical and contemporary epizootiology and aetiology of WPX affecting A. palmata at eight reefs in the Florida Keys. Ranges of WPX prevalence over time (0–71.4%) were comparable for the duration of the 20-year study. Whole colony mortality and disease severity were high in historical (1994–2004), and low in contemporary (2008–2014), outbreaks of WPX. Acroporid serratiosis was diagnosed for some historical (1999, 2003) and contemporary (2012, 2013) outbreaks, but this form of WPX was not confirmed for all WPX cases. Our results serve as a context for considering aetiology as a moving target for WPX and other coral diseases for which pathogens are established and/or candidate pathogens are identified. Coral aetiology investigations completed to date suggest that changes in pathogen, host and/or environment alter the disease state and complicate diagnosis.     

Coral diseases near Lee Stocking Island, Bahamas: patterns and potential drivers

The number of coral diseases, coral species they infect, number of reported cases, and range over which these diseases are distributed have all increased dramatically in the past 3 decades, posing a serious threat to coral reef ecosystems worldwide. While some published studies provide data on the distribution of coral diseases at local and regional levels, few studies have addressed the factors that may drive these distributions. We recorded coral disease occurrence, prevalence, and severity along with temperature, sedimentation, and coral population data (species abundance and colony size) over 2 consecutive summers on reefs near Lee Stocking Island (LSI) in the Bahamas' Exuma Chain. In 2002 a total of 11092 coral colonies (all species present) were examined within a survey area of 9420 m2, and 13 973 colonies within 10 362 m2 in 2003. Similar to other reports, relatively large, framework species including Siderastrea siderea, Colpophyllia natans, and Montastraea annularis, along with the smaller Dichocoenia stokesi, were the species most susceptible to coral disease. Recurring infections were observed on individual colonies from 2002 to 2003, and were more likely for black band disease (BBD) than for either white plague (WP) or dark spots syndrome (DS). In 2002, WP and DS demonstrated clumped distributions, while BBD was randomly distributed. However, in 2003 BBD and WP were clumped. This is the first study, to our knowledge, that quantitatively documents coral disease dynamics on reefs surrounding LSI.     

Extinction rate, historical population structure and ecological role of the Caribbean monk seal

The productivity and biomass of pristine coral reef ecosystems is poorly understood, particularly in the Caribbean where communities have been impacted by overfishing and multiple other stressors over centuries. Using historical data on the spatial distribution and abundance of the extinct Caribbean monk seal (Monachus tropicalis), this study reconstructs the population size, structure and ecological role of this once common predator within coral reef communities, and provides evidence that historical reefs supported biomasses of fishes and invertebrates up to six times greater than those found on typical modern Caribbean reefs. An estimated 233,000-338,000 monk seals were distributed among 13 colonies across the Caribbean. The biomass of reef fishes and invertebrates required to support historical seal populations was 732-1018 gm(-2) of reefs, which exceeds that found on any Caribbean reef today and is comparable with those measured in remote Pacific reefs. Quantitative estimates of historically dense monk seal colonies and their consumption rates on pristine reefs provide concrete data on the magnitude of decline in animal biomass on Caribbean coral reefs. Realistic reconstruction of these past ecosystems is critical to understanding the profound and long-lasting effect of human hunting on the functioning of coral reef ecosystems.     

Within-colony variation in inducibility of coral disease resistance

The abiotic environment influences a variety of ecological processes, including the emergence, transmission, and distribution of disease. In the oceans, increased temperatures associated with climate change are hypothesized to decrease host resistance and/or increase pathogen growth, virulence, or infectivity. Colonial organisms, such as corals, could face a unique challenge with respect to temperature and disease stress: heterogeneous within-colony distribution of constitutive and temperature-induced resistance to infection. This could facilitate disease if warming temperatures promote pathogen growth while decreasing resistance of some areas of the coral colony. Here, an experiment was used to test the hypothesis that temperature-induced disease resistance is heterogeneous within colonies of the sea fan coral, Gorgonia ventalina. Resistance, measured as activity of antifungal metabolites, increased (approx. 30%) with temperature only in young edge tissue, not in older center tissue, consistent with patterns of infection in older, larger sea fan colonies on Caribbean reefs.     

Low natural repopulation of marginal coral communities under the influence of upwelling

The study of coral repopulation in marginal communities may provide a useful analog for understanding the dynamics of coral reefs subjected to deleterious environmental changes. Repopulation of scleractinian reef corals may strongly impact the community structure on tropical reefs; however, the extent of this process on coral communities influenced by upwelling is unknown, especially in the Caribbean. In this study, the potential for natural repopulation of coral communities subjected to wind-driven upwelling was evaluated at three sites on the island of Cubagua, Venezuela. Coral spawning behavior was recorded and both larval settlement and juvenile abundance were estimated. Upwelling did not appear to affect coral spawning behavior, since at this locality spawning occurred at dates and times similar to those reported for well-developed reefs in the Caribbean. Also, juveniles produced by brooding corals were six times more abundant than those of broadcasting species, similar to patterns on other Caribbean reefs that are not under the influence of upwelling. By contrast, mean larval settlement (4 settlers m⁻²) and juvenile abundance (0.1 juveniles m⁻²) in Cubagua were both lower than those elsewhere in the Caribbean and on Pacific reefs. Thus, the potential for repopulation of these marginal communities seems lower than for well-developed coral reefs in other regions. These results suggest that more fully developed coral reefs also may have reduced repopulation potential, as they become influenced by suboptimal environmental conditions. Handling editor: I. Nagelkerken     

The urgent need for robust coral disease diagnostics

Coral disease has emerged over recent decades as a significant threat to coral reef ecosystems, with declines in coral cover and diversity of Caribbean reefs providing an example of the potential impacts of disease at regional scales. If similar trends are to be mitigated or avoided on reefs worldwide, a deeper understanding of the factors underlying the origin and spread of coral diseases and the steps that can be taken to prevent, control, or reduce their impacts is required. In recent years, an increased focus on coral microbiology and the application of classic culture techniques and emerging molecular technologies has revealed several coral pathogens that could serve as targets for novel coral disease diagnostic tools. The ability to detect and quantify microbial agents identified as indicators of coral disease will aid in the elucidation of disease causation and facilitate coral disease detection and diagnosis, pathogen monitoring in individuals and ecosystems, and identification of pathogen sources, vectors, and reservoirs. This information will advance the field of coral disease research and contribute knowledge necessary for effective coral reef management. This paper establishes the need for sensitive and specific molecular-based coral pathogen detection, outlines the emerging technologies that could serve as the basis of a new generation of coral disease diagnostic assays, and addresses the unique challenges inherent to the application of these techniques to environmentally derived coral samples.     

Development and field application of a molecular probe for the primary pathogen of the coral disease white plague type II

One of the current problems in the field of coral disease research is that of tracking coral pathogens in the natural environment. A promising method to do this is by use of pathogen-specific molecular probes. However, this approach has been little used to date. We constructed, and validated in the laboratory, a fluorochrome-labeled molecular probe specific to Aurantimonas coralicida, the bacterial pathogen of the Caribbean coral disease white plague type II (WPIl). We then used the probe to test field samples of diseased coral tissue for the presence of this pathogen. Probe design was based on a unique subset (25 nucleotides) of the complete l6S rRNA gene sequence derived from a pure culture of the pathogen. The pathogen-specific probe was labeled with the fluorochrome GreenStar* FITC (fluorescein isothiocyanate, GeneDetect Ltd, New Zealand). As a control, we used the universal eubacterial probe EUB 338, labeled with a different fluorochrome (TRITC, tetra-methylrhodamine isothiocyanate). Both probes were applied to laboratory samples of pure cultures of bacteria, and field samples collected from the surface of the disease line of corals exhibiting signs of white plague (types I and II), healthy controls, and corals with an uncharacterized disease ("patchy necrosis"). All samples were analyzed using fluorescence in situ hybridization (FISH). We have determined that the probe is specific to our laboratory culture of the coral pathogen, and does not react with other bacterial species (the eubacterial probe does). The WPII pathogen was detected in association with diseased coral samples collected from coral colonies on reefs of the Bahamas (n= 9 samples) exhibiting signs of both WPI and WPII. Diseased (and healthy) tissue samples (n- 4) from corals exhibiting signs of "patchy necrosis" were also assayed. In this case the results were negative, indicating that the same pathogen is not involved in the two diseases. Incorporation and use of pathogen-specific probes can significantly expand our knowledge of the etiology of coral diseases.