Environmental factors and coral community composition associated with coral diseases in the Northern Florida Keys and Bahamas’ Exuma Chain, Part II  (Year 2 of 2) Project Number: CMRC-03-PRJV-01-03C Principle Investigators: Richardson, L. L., and J. Voss Region(s): Lee Stocking Island Summary The increase in the number of coral diseases and the expansion of their ranges over the past 25 years pose serious threats to the health of coral reef ecosystems worldwide. Thus far, little is known about coral epidemiology or the conditions that promote coral infection. While some studies provide data on the distribution of these diseases, few studies have addressed the factors that may drive the distributions. Anthropogenic nutrient loading, increased sedimentation, and global climate change (including increased temperature) have been suggested in the literature as potential causes of the increase in coral disease incidence. This research specifically addressed 11 environmental factors (total nitrogen, nitrite, nitrate, ammonia, soluble phosphorus, total phosphorus, turbidity, salinity, depth, temperature, and sedimentation) and 4 coral community composition factors (species richness, species diversity, colony size, and density [colonies/ m2]) associated with coral disease incidence and prevalence on reefs near Lee Stocking Island in the Bahamas’ Exuma Chain. During June and July, 2002 Voss found 73 incidences of coral disease on colonies in reefs surrounding Lee Stocking Island. Comparisons of environmental factors and community composition between infected areas and healthy areas both near LSI and in the Florida Keys revealed that some of these factors likely influence disease prevalence and distribution (see 2002 Annual Project Summary for CMRC-02-PRJV-01-02A). In 2003 repeat surveys of these reefs will not only build upon the 2002 data but also determine if previously infected colonies are more likely to experience a recurrence of infection. This research will provide direct regional comparisons of coral disease along with the environmental factors and community composition associated with infections. Because the number and distribution of coral diseases continue to increase, this project is vital for understanding the role of disease in reef ecosystems and developing viable strategies for coral reef management near LSI, in the Florida Keys, and throughout the wider Caribbean. Situation and Need Over the past two and a half decades the number of coral diseases and the resulting degradation of coral reef ecosystems have increased dramatically (Epstein et al. 1998, Goreau et al. 1998, Hayes and Goreau 1998, Richardson 1998, Harvell et al. 1999, Porter et al. 2001). In addition, the range of coral diseases has expanded from initially observed outbreaks in the Florida Keys (Dustan 1977) and Caribbean (Antonius 1973, Gladfelter et al. 1977) to a worldwide distribution (Richardson and Aronson 2002). Although the specific long-term effects of coral diseases on reef ecosystems are poorly understood, coral diseases is known in at least one case to have caused dramatic, lasting shift in the community structure of a Belizean reef (Aronson and Precht 1997, 2000). Coral reefs Caribbean-wide may also be susceptible to such alterations. Therefore knowledge of the causes and resulting distributions of coral diseases is fundamental in determining their potential impact on coral communities. To date approximately thirty coral diseases have been observed worldwide. However, of these only six have been well characterized: the scleractinian (stony coral) diseases black band, white band, white plague, white pox, and tissue lysis by Vibrio corallyticus, and the fungal gorgonian disease aspergillosis. The pathogen for bacterial bleaching, Vibrio shiloi, has also been identified but no tissue death has been documented (Kushamro et al. 1996). During surveys near LSI in 2002 Voss observed incidences of black band and white plague and the newly emerging dark spots syndrome. These diseases will be the focus of the surveys conducted in 2003 and are briefly discussed below. Black band disease (BBD), first identified in 1973 by Antonius, has been the most intensely studied of the coral diseases. BBD functions as a microbial consortium (Carlton and Richardson 1995) consisting of the cyanobacterium, Phormidium corallyticum, the sulfide-oxidizing bacterium Beggiatoa, sulfate-reducing bacteria including Desulfovibrio spp., and uncharacterized gram-negative bacteria (Richardson 1996, Richardson et al. 1997). Black band is to date the most widely distributed of the coral diseases. This disease is found throughout the Caribbean primarily on massive boulder-shaped sceleractians and has been observed on at least 16 hard corals (Green and Bruckner 2000) and two octocoral species (Feingold 1988). The distribution of BBD may be correlated with human influence. Initial outbreaks of BBD have been recorded near sewage outflows or other areas with increased pollution (Antonius 1988, Bruckner and Bruckner 1997, Goreau et al. 1998). Water samples taken near colonies infected with BBD showed significantly higher nutrient levels than areas near healthy colonies (Bruckner and Bruckner 1997, Kuta 2000). Given this correlation, the anthropogenic eutrophication of specific areas through pollution may result in the increased virulence of BBD. Seventeen incidences of black band were observed on reefs near LSI in 2002 infecting Siderastrea siderea, Montastrea annularis, and Colpophyllia natans. First described by Dustan (1977), the early outbreaks of white plague (now referred to as type I) were not studied on a regional basis and little is known about the disease’s etiology. In 1995 a disease similar to the initial plague outbreak was identified as plague type II and fully characterized (Richardson et al. 1998a,b). The pathogenic bacterium represents a novel bacterial genus and species, Aurantimonas coralacida (Denner et al. 2002). The initial outbreaks of white plague (type I and II) were centered in the reefs of the Florida Keys, but more recent studies indicate that the range of type II has greatly expanded to a Caribbean-wide distribution (Borger 2001, Weil et al. 2002, Voss and Richardson in prep). Furthermore, the number of coral species infected by type II is also on the rise. Where as Richardson and others (1998a,b) observed plague type II on 17 coral species, Weil and his colleagues have identified 32 scleractinian species susceptible to type II infections (Weil et al. 2002). Eighteen incidences of white plague II were observed on colonies of M. annularis, M. cavernosa, Diplora labyrinthiformis, S. siderea, and Dichocoenia stokesi during 2002 near LSI. Dark spots disease, first observed in 1990, is characterized by dark pigmented, roughly circular areas of depressed tissue on colonies of S. siderea, Stephanocoenia intersepta, M. annularis, M. faveolata, M. franksi, and M. cavenosa (Garzon-Ferreira and Gil 1998, Borger 2001, Gil-Agudelo and Garzon-Ferreira 2001). Gil-Agudelo and Garzon-Ferreira (2001) reported a Caribbean-wide prevalence of 16.4% among all species, while local species-specific prevalence can be as high as 56% for S. siderea (Cervino et al. 2001). Thus far no pathogen has been identified for dark spots but tissue loss has been documented at rates of 3.99 cm/month (Cervino et al. 2001). Because dark spots disease affects three of the most important Caribbean reef-building species, S. siderea, M. annularis, and M. cavernosa, it has the potential to be a substantial negative impact on the ecological processes and productivity of reefs throughout this region. In 2002 dark spots were recorded exclusively on 38 colonies of S. siderea near LSI. Objectives Anthropogenic eutrophication, sedimentation, and direct diver or boat contact have been suggested as potential factors that increase disease susceptibility and incidence. It is therefore hypothesized that coral disease prevalence will be higher near human population centers as compared to pristine areas. Furthermore, it is hypothesized that nutrient and sedimentation levels will be greater on diseased reefs than on those without infections. Coral diseases are most active during the warmer months of the year (June-September). Global climate change and increasing water temperatures may therefore be contributing to the increase in disease incidences. It is hypothesized that temperatures will be higher on diseased reefs as compared to healthy reef sites. Initial data collected in 2002 did not support this hypothesis. Further investigation of temperature during the summer of 2003 may provide more evidence on the validity of hypothesis. Coral colonies with greater surface area are in contact with a greater volume of water, and thus their exposure to pathogens in the water column may be increased. Larger colonies are therefore hypothesized to have greater disease prevalence than smaller colonies. Observations by Borger (2001) support this hypothesis as does the data Voss collected in 2002. Loss of large coral species may result in long-term deleterious effects on reef communities. At the community level, infectious diseases are more likely to spread among more densely aggregated reefs. Thus more areas with greater colonies per square meter are hypothesized to exhibit increased disease prevalence. However, coral diversity and richness may counteract this model, increasing the possibility of disease resistant species. Based on the 2002 data, significant differences in diversity and richness are not expected at the intraregional level between diseased and healthy sites. Finally, colonies that were infected in 2002 may harbor reservoir populations of pathogens that result in repeat infections the following year as the warmer temperatures return. In this case disease prevalence among previously infected would be greater than that of the rest of the community. However, previously infected colonies that are not completely denuded my acquire resistance to the pathogens. As a result, the prevalence of infection among previously diseased corals may be lower than the prevalence of infection among colonies that did experience prior infection. The alternative hypotheses and their associated null hypotheses are stated explicitly here: Ho1: Disease prevalence is not correlated with proximity to anthropogenic impact. Ha1: Disease prevalence is greater in regions near human population centers. Ho2: Nutrient concentrations and sedimentation do not differ in the FL Keys and LSI. Ha2: Nutrient concentrations and sedimentation are higher in the FL Keys than LSI. Ho3: Intraregionally, nutrient concentrations and sedimentation do not differ between diseased and healthy (uninfected) sites. Ha3: Intraregionally, nutrient concentrations and sedimentation are greater on diseased sites than on healthy sites. Ho4: Temperature does not differ between diseased and healthy sites. Ha4: Temperature is greater on diseased sites in comparison to healthy sites. Ho5: Colonize size does not correlate to disease prevalence. Ha5: Colonize size correlates positively with disease prevalence. Ho6: Coral density, richness, and diversity do not differ between diseased and healthy sites. Ha6: Coral density, richness, and diversity on diseased sites are not equal to healthy sites. Ho7: Previously infected and uninfected colonies are equally susceptible to infection. Ha7: Previously infected and uninfected colonies demonstrate unequal susceptibility to infection. To test these hypotheses reefs in the northern Florida Keys and LSI that were surveyed in 2002 will again be examined in 2003. The specific objectives of the 2003 study are as follows: 1. Conduct repeated 10 m radial surveys on LSI reefs to record disease incidents, temperature, salinity, and coral community data (colony size, density, richness, diversity). 2. Examine tagged colonies that were diseased in 2002 for signs of repeat infection. 3. Collect and freeze water samples from the surveys for nutrient analysis (total nitrogen, nitrite, nitrate, ammonia, soluble phosphorus, total phosphorus, turbidity) at SERC/FIU. 4. Deploy PVC sediment traps to collected and measure sedimentation rates. 5. Collect and freeze disease samples for future molecular analyses. 6. Tagged newly infected colonies for future monitoring.   SEMI-ANNUAL REPORT OBJECTIVES: 1. Conduct repeated 10 m radial surveys on LSI reefs to record disease incidence and prevalence, temperature, salinity, and coral community data (colony size, density, richness, diversity). 2. Examine tagged colonies that were diseased in 2002 for signs of recurring infection. 3. Collect and freeze water samples from the surveys for nutrient analysis (total nitrogen, nitrite, nitrate, ammonia, soluble phosphorus, total phosphorus, turbidity) at SERC/FIU. 4. Deploy PVC sediment traps to collected and measure sedimentation rates. 5. Collect and freeze disease samples for future molecular analyses. 6. Tagged newly infected colonies for future monitoring. METHODS: Approximately sixty 10m radial transect on reefs at Big Point, Goby Spot, Horseshoe, North Norman’s, North Perry, Rainbow Gardens, South Perry, Square Rock, Tug and Barge, and White Horse (all also surveyed in 2002) were surveyed between June 20 and July 24, 2003 for the presence of coral diseases using methods described by Edmunds (1991). For each transects every scleractinian colony was identified to species and measured (longest axis) to determine average colony size, colony density, species richness, and species diversity (Shannon-Weaver index). For infected colonies, disease type, band width, and percent tissue loss were recorded. Disease prevalence will be calculated as the proportion of infected colonies to total colonies in each transect. A sample of the disease tissue was taken using sterile 5 ml plastic syringes, transferred aseptically to cryovials in the laboratory on LSI, and frozen at -20oC for future molecular analyses. The infected colonies were tagged and 2-4 digital photographs were taken to monitor disease band progression and disease recurrence in future surveys. Four 60ml water samples were collected from each transect using sterilized plastic syringes. Two of these were passed through GF/F filters while the other two will remain unfiltered. All have been transferred to 60ml sample bottles and frozen at -20oC for storage and transport to South Florida. At FIU the thawed filtered samples will be analyzed for total nitrogen, nitrate, nitrite, ammonium, and soluble phosphate by FIU’s Southeast Environmental Research Center (SERC). The unfiltered samples will be thawed and analyzed for total phosphorus and turbidity. Salinity, temperature, and depth will be recorded in situ using digital instruments. PVC pipe sediment traps (5 x 30cm) secured to a steel stake at each survey site were used to collect sediment for a minimum of one week. The sediments were collected and dried at 60oC until a constant dry weight was recorded. Statistical comparisons between diseased and healthy regions, and between the Exumas and Florida Keys, will be made using nonparametric Mann-Whitney U-tests. Multivariate multiple regression and principle components analysis will be used to create a model to predict disease prevalence among different species on the reef in various environmental conditions and community assemblages. PRELIMINARY RESULTS: Our surveys in 2003 indicate that coral disease incidence and prevalence have increased on reefs near Lee Stocking Island since June-July, 2002. Black band disease was most abundant at Horseshoe, and present at North Perry, South Perry, Whitehorse, G-spot, and Rainbow. Siderastrea siderea and Colpophyllia natans were the primarily affected species. Recurrence of black band infection was observed on 13 of the 17 corals that were infected in 2002. In addition a cessation of black band was observed on 7 colonies during the first week of July, which appears be correlated to a drop in temperature during that period. Samples were taken at the healthy tissue, bare skeleton interface. Analysis of these samples will determine if the pathogens were still present in a dormant, non-pathogenic form. White plague incidence was highest at South Perry, and present at North Perry, Horseshoe, Whitehorse, and G-Spot. The primarily affected species were Montastraea annularis, S. siderea, and Dichocoenia stokesi. No recurrence of white plague was observed on colonies that were infected with plague in 2002. One particularly rapid plague outbreak was observed at G-Spot. Within 4 days 5 D. stokesi colonies were infected within a 5 meter radius. Two of the colonies were completely denuded within 3 days and the other three had lost at least 40% of their tissue at our last observation. White band disease was not observed on LSI reefs in 2002. In 2003, however, white band infections were found on Acropora cervicornis colonies at both Bock Wall and North Norman’s. Fortunately, new, uninfected A. cervicornis colonies were observed at Horseshoe, South Perry, and North Perry. Dark spots has been the only disease to show a decline in incidence over the past year, most notably at Whitehorse. Only 17 S. siderea colonies were infected in 2003, and compared to 38 in 2002. ANNUAL REPORT OBJECTIVES: 1. Conduct repeated 10 m radial surveys on LSI reefs to record disease incidence and prevalence, temperature, salinity, and coral community data (colony size, density, richness, diversity). 2. Examine tagged colonies that were diseased in 2002 for signs of recurring infection. 3. Collect and freeze water samples from the surveys for nutrient analysis (total nitrogen, nitrite, nitrate, ammonia, soluble phosphorus, total phosphorus, turbidity) at SERC/FIU. 4. Deploy PVC sediment traps to collected and measure sedimentation rates. 5. Collect and freeze disease samples for future molecular analyses. 6. Tagged newly infected colonies for future monitoring. METHODS: Thirty 10m radiusdiameter radial sites on reefs at Big Point, Goby Spot, Horseshoe, North Norman’s, North Perry, Rainbow Gardens, South Perry, Square Rock, Tug and Barge, and White Horse (all also surveyed in 2002) were surveyed between June 20 and July 24, 2003 for the presence of coral diseases using methods described by Edmunds (1991). For each site every scleractinian coral colony was identified to species and measured (longest axis) to determine average colony size, colony density, species richness, and species diversity (Shannon-Weaver index). For infected colonies, disease type, band width, and percent tissue loss were recorded. Disease prevalence will be calculated as the proportion of infected colonies to total colonies in each transect. A sample of the disease tissue was taken using sterile 5 ml plastic syringes, transferred aseptically to cryovials in the laboratory on LSI, and frozen at -20oC for future molecular analyses. The infected colonies were tagged and 2-4 digital photographs were taken to monitor disease band progression and disease recurrence in future surveys. Previously infected and tagged colonies (2002) were specifically inspected for signs of disease. Four 60ml water samples were collected from each transect using sterilized plastic syringes. Two of these were passed through GF/F filters while the other two remained unfiltered. All were transferred to 60ml sample bottles, frozen at -20oC for storage, and transported to FIUSouth Florida. At FIU the thawed filtered samples were analyzed for total nitrogen, nitrate, nitrite, ammonium, and soluble phosphate by FIU’s Southeast Environmental Research Center (SERC). The unfiltered samples will be thawed and analyzed for total phosphorus and turbidity. Salinity, temperature, and depth were recorded in situ using digital instruments. PVC pipe sediment traps (5 x 30cm) secured to a steel stake at each survey site were used to collect sediment for a minimum of one week. The sediments were collected and dried at 60oC until a constant dry weight was recorded. RESULTS: Our surveys in 2003 indicate that total coral disease incidence and prevalence have not increased on reefs near Lee Stocking Island since June-July, 2002. However, within diseases, changes have occurred (see below). White plague prevalence was not significantly different between years. Incidence in 2003 was highest at South Perry, and present at North Perry, Horseshoe, Whitehorse, and G-Spot. The primarily affected species were Montastraea annularis, S. siderea, and Dichocoenia stokesi. No recurrence of white plague was observed on colonies that were infected with plague in 2002. One particularly rapid plague outbreak was observed at G-Spot. Within 4 days 5 D. stokesi colonies were infected within a 5 meter radius. Two of the colonies were completely denuded within 3 days and the other three had lost at least 40% of their tissue at our last observation. White band disease was not observed on LSI reefs in 2002. In 2003, however, white band infections were found on Acropora cervicornis colonies at both Bock Wall and North Norman’s. Fortunately, new, uninfected A. cervicornis colonies were observed at Horseshoe, South Perry, and North Perry. Dark spots has been the only disease to show a significant decline in prevalence and incidence over the past year, most notably at Whitehorse. Only 19 colonies were infected in 2003, and compared to 38 in 2002. ADDITIONAL PERSONNEL (Students, Other scientists, technicians, etc.): Travis Thyberg, FIU Masters Student PUBLISHED ABSTRACTS OF PAPERS PRESENTED BASED ON 2003 WORK: Voss, JV and LL Richardson. 2003. Environmental Factors and Coral Community Composition Associated with Coral Diseases in The Northern Florida Keys and Bahamas’ Exuma Chain. 31st Meeting of the Association of Marine Laboratories of the Caribbean, Port of Spain, Trinidad. Abstracts, p. 103. Mills, DK, JD Mayorga, ER Remily and LL Richardson. 2003 Development of a Species- SpecificMolecular Probe for the White Plague Type II Pathogen. . 31st Meeting of the Association of Marine Laboratories of the Caribbean, Port of Spain, Trinidad. Abstracts, p. 8. Voss, JV and LL Richardson. 2003. Environmental Factors and Coral Community Composition Associated with Coral Diseases in The Northern Florida Keys and Bahamas’ Exum Chain. and 88th Annual Meeting of Ecological Society of America, Savannah, GA. Poster. Abtracts, p. 346XXX. Mills, DK, JD Mayorga, ER Remily and LL Richardson. Development of a Species-Specific Molecular Probe for the White Plague Type II Pathogen. . 31st Meeting of the Association of Marine Laboratories of the Caribbean, Port of Spain, Trinidad. Abstracts, p. 8. Voss, JV and LL Richardson. 2004. The role of coral diseases in coral population and community structure. Florida International Symposium Biology Symposium, Miami, FL. Presentation. Abstracts, p. 22.XXX Mills, DK, JD Voss, and LL Richardson. 2004. Amplicon Length Heterogeneity - a Tool to Investigate Coral Microbial Communities. 29th Annual Eastern Fish Health Workshop, Atlantic Beach, NC. Presentation. (Abstract accepted) Richardson, LL, ER Remily and DK Mills. 2004. Species Specific Molecular Probe Investigations of “White” Diseases of Corals. . 29th Annual Eastern Fish Health Workshop, Atlantic Beach, NC. (Abstract accepted) MANUSCRIPTS AND PUBLICATIONS: Voss, JV and LL Richardson. In review. Environmental Factors and Coral Community Composition Associated with Coral Diseases in The Northern Florida Keys and Bahamas’ Exuma Chain. Submitted to Coral Reefs (in revision based on reviewers recommendations). Richardson, LL, D Mills, ER Remily, JD Voss. In review. Development and Ffield Aapplication of a Mmolecular Pprobe for the Pprimary Ppathogen of the Ccoral Ddisease Wwhite Pplague Ttype II. Submitted to Revista de Biologia Tropical. (in review) Voss, JV and LL Richardson. 2004. The role of coral diseases in coral population and community structure. Florida International Symposium Biology Symposium, Miami, FL. Abstracts, p. 22. Mills, DK, JD Mayorga, ER Remily and LL Richardson. 2003. Development of a Species-Specific Molecular Probe for the White Plague Type II Pathogen. . 31st Meeting of the Association of Marine Laboratories of the Caribbean, Port of Spain, Trinidad. Abstracts, p. 8. Richardson, LL, ER Remily and DK Mills. 2004. Species Specific Molecular Probe Investigations of “White” Diseases of Corals. 29th Annual Eastern Fish Health Workshop, Atlantic Beach, NC. Abstracts p. 43. Voss, JV and LL Richardson. 2003. Environmental Factors and Coral Community Composition Associated with Coral Diseases in The Northern Florida Keys and Bahamas’ Exuma Chain. 88th Annual Meeting of Ecological Society of America, Savannah, GA. Abstracts, p. 346. Mills, DK, JD Voss, and LL Richardson. 2004. Amplicon Length Heterogeneity - a Tool to Investigate Coral Microbial Communities. 29th Annual Eastern Fish Health Workshop, Atlantic Beach, NC. Abstracts p. 45. Voss, JV and LL Richardson. 2003. Environmental Factors and Coral Community Composition Associated with Coral Diseases in The Northern Florida Keys and Bahamas’ Exuma Chain. 31st Meeting of the Association of Marine Laboratories of the Caribbean, Port of Spain, Trinidad. Abstracts, p. 103. Richardson LL, Voss JD. 2005. Changes in a coral population on reefs of the northern Florida Keys following a coral disease epizootic. Mar. Ecol. Prog. Ser. 297:147-56. Richardson LL, Mills DK, Remily ER, Voss JD. 2005. Development and field application of a molecular probe for the primary pathogen of the coral disease white plague type II. Int. J. Trop. Biol. 53(1):1-10. Voss JD, Mills DK, Richardson LL. 2005. Black band disease dynamics, drivers, and variation in the associated pathogenic microbial community. June 13-17, 2005. Curacao. 32nd Scientific Meeting of the AMLC.

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Updated: May 28, 2004