The Epizootiology of Coral Diseases in South Florida

Research and Development

EPA/600/R-05/146 May 2006

The Epizootiology of Coral Diseases in South Florida

by

Deborah L. Santavy1, Jed Campbell1, Robert L. Quarles1, James M. Patrick1, Linda M. Harwell1, Mel Parsons2 , Lauri MacLaughlin3 , John Halas3, Erich Mueller4, 5, Esther C. Peters4, 6, Jane Hawkridge4, 7

1United States Environmental Protection Agency National Health and Environmental Effects Research Laboratory Gulf Ecology Division 1 Sabine Island Drive Gulf Breeze, FL 32561

2United States Environmental Protection Agency, Region 4 Science and Ecosystems Support Division 980 College Station Road Athens, GA 30605

3NOAA, Florida Keys National Marine Sanctuary Upper Region, MM 95 Overseas Highway Key Largo, FL 33037

4Mote Marine Laboratory Center for Tropical Research 24244 Overseas Highway (US 1) Summerland Key, FL 33042

5Perry Institute for Marine Science 100 N. U.S. Highway 1, Suite 202 Jupiter, FL 33477

6Tetra Tech, Inc. 10306 Eaton Place, Suite 340 Fairfax, VA 22030

7Joint Nature Conservation Committee, Monkstone House, City Road Peterborough, United Kingdom PE1 1JY Notice

The U.S. Environmental Protection Agency (U.S. EPA), Office of Research and Development (ORD), National Health and Environmental Effect Research Laboratory (NHEERL), Gulf Ecology Division (GED), the U.S. Department of Commerce (U.S. DOC) National Oceanographic and Atmospheric Association (NOAA) National Marine Sanctuary Program Florida Keys National Marine Sanctuary (FKNMS), and the U.S. Department of Interior (DOI) National Park Service (NPS) Dry Tortugas National Park (DTNP) jointly conducted this program.

The report has undergone U.S. EPA’s peer and administrative reviews and has received approval for publication as a U.S. EPA document. Mention of trade names or commercial products does not constitute endorsement or recommendation for use. The recommendations expressed in this publication are solely those of the authors and do not necessarily reflect those of the sponsoring agencies.

The appropriate citation for this report is: Santavy, D.L., J. Campbell, R.L. Quarles, J.M. Patrick, L.M. Harwell, M. Parsons, L. MacLaughlin, J. Halas, E. Mueller, E.C. Peters and J. Hawkridge. 2006. The Epizootiology of Coral Diseases in South Florida. EPA/ 600/R-05/146. U.S. Environmental Protection Agency, Gulf Ecology Division, Gulf Breeze, Florida.

ii Abstract

The mortality of reef-building corals has increased at unprecedented rates during the past three decades. It is widely accepted among the scientific community that pristine reefs no longer exist anywhere on earth. Some scientists are forewarning of ecological extinction for region-wide coral reefs within this century if current trends persist. This report summarizes the condition of South Florida reefs by providing an overview of historical studies published in the scientific literature and a synopsis of collaborative field investigations by EPA, NOAA and Mote Marine Laboratory. The study’s objectives were to establish the current status of coral health and disease and detect changes over time. Four epizootiological surveys were conducted: (1) spring 1998, (2) summer 1998, (3) spring 1999, and (4) August 2000. We surveyed sites in the Upper, Middle and Lower Florida Keys, the New Grounds of the Florida Keys National Marine Sanctuary, Biscayne National Park, and Dry Tortugas National Park. All surveys were conducted using a radial arc transect method developed for the coral disease assessment. Only the 2m-wide segment, 8-10m from the center of the radial arc transect, was surveyed at each site (area surveyed = 113m2). Twenty-two species of scleractinian corals and gorgonian sea fans were inspected for 11 coral diseases described in the literature, plus two additional syndromes.

A probabilistic survey design in August 2000 generated areal estimates of the extent and intensity of coral disease in South Florida. At least one coral colony was affected by active disease at any single location in 85 ± 9% (95% confidence interval) of the area sampled; 15 ± 9% (662 ha) of the area sampled contained no coral disease. Coral disease was widely dispersed throughout South Florida reefs and was not confined to a particular region. Although disease was widespread, maximum disease prevalence at a site was 13%, representing 2.2 ± 4% (97 ha) of the sampling area. This study established a baseline so that future probabilistic surveys can examine changes and trends in coral condition.

Annual disease prevalence from 1998 through 2000 ranged from 0 to 43% among all the sites surveyed. No hot spots were found where a high level of disease was sustained at the same site for multiple survey periods. The highest disease prevalence was observed at Looe Key (LK03) back reef site in summer 1998, where 42.9% of the colonies were diseased, with white pox affecting 41.4% of the monitored species. White pox and aspergillosis were the most abundant diseases observed at sites, where greater than 20% of the colonies were diseased. The dominant diseases found among all the sites were white pox, aspergillosis, dark spots disease, white-band disease, and white plague. Species with significant declines over the course of the study were Acropora palmata, Acropora cervicornis, Montastraea annularis complex, and Colpophyllia natans.

This report compares spatial and temporal distribution of species composition and disease prevalence among regions, reef types, and between survey periods. The highest level of disease prevalence was recorded in 1998 and 1999, with lower or no disease prevalence observed in subsequent years. Overall, the greatest destruction of coral colonies occurred during the summer of 1998, when a period of high disease prevalence, massive bleaching, and a powerful hurricane passed over this area causing great destruction of the reefs. Non-parametric multivariate analyses did not reveal any logical spatial correlations between disease distribution and geographical regions, reef type, or water depth. Future research will evaluate geospatial relationships between stressors, including water quality, and trends in coral health on the Florida reef tract.

iii iv Contents

Abstract ...... iii Figures ...... vi Tables ...... vii Site Names and Codes ...... viii Acronyms and Abbreviations ...... ix Acknowledgements ...... x

Introduction ...... 1 Documented Declines in Coral Coverage...... 1

Diseases of Reef-Building Corals...... 3 Distribution and Frequency of Coral Diseases ...... 4

Epizootiological Assessment of Coral Disease ...... 5 Background ...... 5 Approach ...... 5 Sampling Selection ...... 7 Survey Methodology ...... 7 Statistical Analysis ...... 9

Results and Discussion ...... 10 Species Composition and Disease Prevalence ...... 11 Principal Component Analysis ...... 14 Spatial Distribution of Diseases ...... 16

Conclusions ...... 16 References ...... 17 Appendices

A. All sites sampled during surveys, including regions, site names, codes, latitude and longitudes, and depths ...... A-1 B. Coral diseases sampled for the study during the 1998-2000 surveys...... B-1 C. Pie charts presenting the percent species and disease composition for each geographic region for 1998-2000 surveys ...... C-1 D. Tables presenting percent species and disease composition for each geographic region for 1998-2000 ...... D-1 E. Base maps and survey site maps of five most common diseases at locations for Dry Tortugas and Key West Regions during four surveys ...... E-1 F. Reports, Publications and Presentations, products resulting from this research ...... F-1

v List of Figures

Figure Page

1. The mean percent coral cover in the FKNMS ...... 2 2. Decline of Acropora palmata in the FKNMS ...... 3 3. Areal extent for coral diseases in the Florida Keys...... 5 4. Frequency of coral diseases in the Florida Keys ...... 5 5. Map of the coral disease assessment sites ...... 6 6. Map of the coral disease assessment regions ...... 6 7a. Underwater surveyors using the radial arc transect method ...... 8 7b. A diagram of the radial arc used in the transect method ...... 8 7c. Modified radial arc transect method ...... 8 8. Acropora palmata at sites showing the greatest loss ...... 12 9. Acropora cervicornis at sites showing the greatest loss ...... 13 10. Montastraea annularis complex at sites showing the greatest loss ...... 14 11. Colpophyllia natans at sites displaying the greatest loss ...... 14 C-1. Dry Tortugas Percent Species ...... C-2 C-2. Dry Tortugas Percent Disease ...... C-3 C-3. New Grounds Percent Species ...... C-4 C-4. New Grounds Percent Disease ...... C-5 C-5. Key West Percent Species...... C-6 C-6. Key West Percent Disease...... C-7 C-7. Lower Keys Percent Species ...... C-8 C-8. Lower Keys Percent Disease ...... C-9 C-9. Middle Keys Percent Species ...... C-10 C-10. Middle Keys Percent Disease ...... C-11 C-11. Upper Keys Percent Species ...... C-12 C-12. Upper Keys Percent Disease ...... C-13 C-13. Biscayne National Park Percent Species ...... C-14 C-14. Biscayne National Park Percent Disease ...... C-15 E-1. Base Map of Dry Tortugas survey sites ...... E-2 E-2. Survey sites in Dry Tortugas with Aspergilliosis present ...... E-3 E-3. Survey sites in Dry Tortugas with Dark Spot Disease present ...... E-4 E-4. Survey sites in Dry Tortugas with White Pox Disease present ...... E-5 E-5. Survey sites in Dry Tortugas with White-Band Disease present ...... E-6 E-6. Survey sites in Dry Tortugas with White Plague Type II Disease present ...... E-7 E-7. Base map of Key West survey sites ...... E-8 E-8. Survey sites in Key West with Aspergilliosis present ...... E-9 E-9. Survey sites in Key West with Dark Spot Disease present ...... E-10 E-10. Survey sites in Key West with White Pox Disease present ...... E-11 E-11. Survey sites in Key West with White-Band Disease present ...... E-12 E-12. Survey sites in Key West with White Plague Type II Disease present ...... E-13

vi Tables

Table Page

1. Survey sites exhibiting over 20% disease prevalence ...... 10 2. Percent and total number of healthy and diseased colonies at each geographic region...... 11 3. Variance attributed to each principal component for disease prevalence ...... 15 4. Results of principal component analysis shown as factor (disease) contributions ...... 15

A-1. Sites sampled ...... A-2 B-1. Diseases observed in surveys detailing the signs ...... B-2 D-1. Percent healthy and diseased colonies at each geographic region ...... D-2 D-2. Percent of healthy and diseased colonies, at each site in the Dry Tortugas Region...... D-3 D-3. Percent of healthy and diseased colonies, at each site in the New Grounds Region...... D-4 D-4. Percent of healthy and diseased colonies, at each site in the Key West Region ...... D-5 D-5. Percent of healthy and diseased colonies, at each site in the Lower Keys Region ...... D-6 D-6. Percent of healthy and diseased colonies, at each site in the Middle Keys Region ...... D-7 D-7. Percent of healthy and diseased colonies, at each site in the Upper Keys Region ...... D-7 D-8. Percent of healthy and diseased colonies, at each site in the Biscayne National Park Region ...... D-8

vii Site Code Site Name Site Code Site Name LR01 Loggerhead Reef 1 ER01 Elkhorn Reef 1 LR02 Loggerhead Reef 2 LR03 Loggerhead Reef 3 PR01 Pacific Reef 1 LR04 Loggerhead Reef 4 PR02 Pacific Reef 2 LR05 Loggerhead Reef 5 LR06 Loggerhead Reef 6 SR01 Sombrero Reef 1 LR07 Loggerhead Reef 7 SR02 Sombrero Reef 2

WH01 White Shoals 1 AR01 Alligator Reef 1 WH02 White Shoals 2 AR02 Alligator Reef 2

BK01 Bird Key Reef 1 MR01 Molasses Reef 1 BK03 Bird Key Reef 3 MR02 Molasses Reef 2 BK04 Bird Key Reef 4 BK05 Bird Key Reef 5 NG01 New Grounds 1 BK06 Bird Key Reef 6 NG02 New Grounds 2 BK07 Bird Key Reef 7 NG03 New Grounds 3 BK08 Bird Key Reef 8 NG04 New Grounds 4 BK09 Bird Key Reef 9 NG05 New Grounds 5

PS01 Pulaski Shoals 1

SK01 Sand Key 1 SK02 Sand Key 2 SK03 Sand Key 3 SK04 Sand Key 4 SK05 Sand Key 5

RK01 Rock Key 1 RK02 Rock Key 2 RK03 Rock Key 3

ED01 Eastern Dry Rocks 1 ED03 Eastern Dry Rocks 3 ED04 Eastern Dry Rocks 4

WS02 Western Sambo 2 WS03 Western Sambo 3 WS04 Western Sambo 4 WS05 Western Sambo 5

ES01 Eastern Sambo 1 ES02 Eastern Sambo 2 ES03 Eastern Sambo 3

LK01 Looe Key 1 LK02 Looe Key 2 LK03 Looe Key 3 LK04 Looe Key 4

CR01 Carysfort Reef 1 CR02 Carysfort Reef 2 CR03 Carysfort Reef 3 viii Acronyms and Abbreviations

Code Disease Code Coral Species

AS aspergillosis AAGA Agaricia agaricites BB black-band disease ACER Acropora cervicornis CS coenosarc swelling disease APAL Acropora palmata DS dark spots disease APRO Acropora prolifera HP hyperplasia CNAT Colpophyllia natans PX white pox DCLI Diploria clivosa RB red-band disease DLAB Diploria labyrinthiformis RM ridge mortality disease DSTO Dichocoenia stokesii WB white-band disease DSTR Diploria strigosa WP white plague GOR Gorgonia spp. YB yellow-blotch disease MANN Montastraea annularis MCAV Montastraea cavernosa MDAN Mycetophyllia danaana MFAV Montastraea faveolata MFER Mycetophyllia ferox MFRA Montastraea franksii MLAM Mycetophyllia lamarckiana PAST Porites astreoides SBOU Solenastrea bournoni SMIC Stephanocoenia michelini SSID Siderastrea siderea

Others

BNP Biscayne National Park CREMP Coral Reef Evaluation and Monitoring Project CRMP Coral Reef Monitoring Project DTNP Dry Tortugas National Park EMAP Environmental Monitoring and Assessment Program FFWCC Florida Fish and Wildlife Conservation Commission FIU Florida International University FKNMS Florida Keys National Marine Sanctuary FMRI Florida Marine Research Institute GED Gulf Ecology Division PCA Principal Component Analysis ORD Office of Research and Development PRIMER Plymouth Routines in Multivariate Ecological Research QAP Quality Assurance Plan SAS Statistical Analysis System SCUBA Self-Contained Underwater Breathing Apparatus SERC Southeast Environmental Research Center SERP Southeast Environmental Research Program WQPP Water Quality Protection Program

ix Acknowledgements

This work was supported by the U.S. Environmental Protection Agency (U.S. EPA), Office of Research and Development, National Health and Environmental Research Laboratory, intramural research program of the Gulf Ecology Division (GED). Funding was provided to the National Oceanographic and Atmospheric Association (NOAA) through an Interagency Agreement with U.S. EPA GED (RW13937452) and to Mote Marine Laboratory from U.S. EPA Region 4. The research vessel OSV Peter W. Anderson was furnished by U.S. EPA, Office of Water, Office of Wetlands, Oceans, and Watersheds. We thank members of the field crew: E. Anderson (GED), K.B. Muir (Region 2), the captain and crew of the OSV Anderson, the Lower Keys Office of the Florida Keys National Marine Sanctuary (FKNMS), and the staff of the Dry Tortugas National Park. K. Smith (GED) provided logistical support at GED. W. Jaap & C. Anderson of Florida Marine Research Institute made information available from the FKNMS Coral Reef Monitoring Project for data analysis (EPA Award No. X994649-94). Preparation of all pie charts, tables, and maps was by M. Adkinson (formerly with GED). Thanks to S. Embry (GED) who provided technical support on graphics and Valerie Coseo (GED) for the manuscript preparation. This report is Contribution No. (1244), U.S. EPA, NHEERL, GED, 1 Sabine Island Dr., Gulf Breeze, FL 32561-5299.

x Introduction

The mortality of reef-building corals has increased globally to unprecedented levels during the past three decades (Gardner et al. 2003, Hughes et al. 2003, Wilkinson 1998, 2000, 2002). The rate and intensity of destruction for coral reef habitats are greater than previously documented in modern or geological records (Aronson and Precht 1997a, b, Hughes 1994, Hughes and Tanner 2000, Pandolfi et al. 2003, Hughes et al. 2003). It is widely accepted among the scientific community that pristine reefs no longer exist anywhere on earth (Pandolfi et al. 2003). Some scientists are forewarning of ecological extinction for region-wide coral reefs in this century if current trends persist (Gardner et al. 2003, Hughes et al. 2003). Wilkinson (2002) estimates that 11% of the world’s modern reefs of live coral are already destroyed, 16% are severely damaged, and approximately 60% might be gone by the year 2030. A meta-analysis of 263 sites from 65 separate studies reports a massive decline of corals across the entire Caribbean region, with 80% reduction in the average live coral coverage from 1971 to 2001 (Gardner et al. 2003). On average, coral declined by 50% throughout the Caribbean in the 1970s, and by 10% in the past decade (Gardner et al. 2003).

This report summarizes the condition of South Florida reefs by providing an overview of historical studies published in the scientific literature and a synopsis of a collaborative field investigation program by EPA, NOAA and Mote Marine Laboratory. The study objectives were to establish the current status of coral health and disease and detect changes over time. Four epizootiological surveys were conducted from 1998-2000 to assess sites in the Upper, Middle and Lower Florida Keys, the New Grounds, Biscayne National Park, and Dry Tortugas National Park.

Documented Declines in Coral Coverage

Two comprehensive studies, using different approaches, have established baselines and detected changes in live coral coverage in the Western Atlantic. The Coral Reef Monitoring Project (CRMP) is an assessment program which began in 1996 in the Florida Keys (Jaap et al. 2001), a time when the Florida Keys reefs were already considered a highly degraded environment (Pandolfi et al. 2003). The second study is a synthesis of 11 studies from 1975 to 2003 in the Florida Keys (Gardner et al. 2003). It finds that shallow-water reef corals in South Florida are in poor condition and continuing to decline, albeit at a slower rate in the late 1990s than in the 1970s (Gardner et al. 2003, Hughes et al. 2003, Pandolfi et al. 2003). Gardner et al. (2003) did not include the CRMP’s extensive data from the Florida Keys in their analysis (Jaap et al. 2000, Wheaton et al. 2001) because it would have skewed their results, due to its great spatial and temporal scales relative to the other studies contained in the meta- analysis.

The CRMP is a comprehensive coral assessment examining temporal and spatial trends of live coral coverage in the Florida Keys. It began in 1996 and is still supported by US EPA, Region 4 and NOAA (Jaap et al. 2000, Porter et al. 2002, Wheaton et al. 2001, Beaver et al., 2004, FFCWW, 2005 ). The study assesses the total percentage of live coral coverage at 160 permanent stations annually. It has documented a 44.5% decline in live coral coverage in the Florida Keys National Marine Sanctuary (FKNMS) from 1996-2004 (Beaver et al. 2003, FFWCC 2005, Jaap et al. 2000, 2001) (Fig. 1). Other significant results obtained from this study include the following:

1) From 1996 to 2004 • 79% of stations lost species; 14% gained species, and 6% were unchanged. • Mean percent stony coral cover decreased by 44.5% sanctuary-wide. 2) By region: • The greatest loss in coral cover occurred in the Dry Tortugas from 1999-2004—from 19% to less than 12%. • The Middle Keys experienced the least decline in coral coverage over the 8-year study. • Lower Keys coral coverage declined from 12% to 6% over the same period.

1 Figure 1. The mean percent coral cover in the FKNMS at 160 stations during 1996-2004. The overall decline represents 44.5% of the total measured from 1996 to 2004 (FFWCC, 2005).

This trend has prompted increased awareness and stimulated focused studies on coral disease, coral bleaching, and other potential stressors to understand what processes are causing the continuing deterioration of reefs in South Florida. Losses of coral, and thus reef habitat, from diseases have been observed throughout the Caribbean over the last three decades (Bruckner and Bruckner 1997, Bythell and Sheppard 1993, Gladfelter et al.1977, Goreau et al.1998, Peters 1992a, b, Rogers 1985). Increasing numbers of coral diseases have been reported from South Florida reefs during the same period (Antonius 1981, 1985, 1988, Dustan 1977, Dustan and Halas 1987, Holden 1996, Kuta & Richardson 1996, Patterson et al. 2002, Porter and Meier 1992, Richardson et al. 1998a, Santavy and Peters 1997, Santavy et al. 1999a, 2001, 2005, Aeby and Santavy, in press). Moreover, newly and previously described diseases affecting additional species of scleractinian corals and gorgonian sea fans have increased significantly on reefs across the Western Atlantic Province (Bruckner et al. 1997, Bythell and Sheppard 1993, Nagelkerken et al. 1997a, b, Patterson et al. 2002, Richardson et al. 1998b, Santavy and Peters 1997, Santavy et al. 1999a).

Diseased or severely bleached corals often show little or no recovery and can be replaced by turf algae (Aronson and Precht 1999, McClanahan et al.1999, McClanahan and Muthiga 1998, Shulman and Robertson 1997). Concomitant with the destruction of corals has been the reduction of herbivores, such as the die off of the sea urchin, Diademia, removal of large fish, and increased nutrient loads resulting from coastal development and modification. These events have precipitated an ecological shift from a coral reef environ-ment to one dominated by fleshy algae (Hughes 1994, McClanahan et al. 2002).

The Caribbean and Florida Keys reefs once were dominated by elkhorn (Acropora palmata) and staghorn corals (Acropora cervicornis). Massive declines of acroporid corals have been attributed to epizootics of white-band coral disease (Aronson and Precht 1997a, b, Bythell and Sheppard 1993, Gladfelter 1982, Gladfelter et al. 1977, Miller et al. 2002), and more recently in the Florida Keys by white pox disease (Patterson et al. 2002) (Fig 2). These losses have been so great that NOAA recently listed A. palmata and A. cervicornis as “threatened” throughout their geographical range (Bruckner 2003, Acropora Biol. Rev. Panel 2005). Another study has shown that the distribution of coral disease in the Keys increased significantly from 1996 to1998 (Jaap et al. 2000). Massive bleaching events in1998 were more widespread and affected more coral species than ever before (Wilkinson 1998, 2000). Many isolated and remote reefs in the Indian and Pacific Oceans had levels of coral mortality greater than ever documented in modern or geological history. The massive bleaching event was associated with an increase in global sea-surface temperature. Increased coral mortality caused by disease and bleaching has reduced the amount of live coral coverage along with the physical structure and architecture that provide habitat for many reef-associated organisms.

2 Figure 2. (A) Decline of Acropora palmata coverage from seven locations in the FKNMS; (B) and complete loss of A. palmata from Eastern Dry Rocks Reef near Key West from 1994 to 2000 (Patterson et al., 2002). Data presented as mean ± SD.

Diseases of Reef-Building Corals

Coral disease assessments conducted in the summer of 1998 by Gulf Ecology Division (GED) documented that up to 28% of the coral populations off Key West and the Lower Keys were affected by disease (Santavy et al. 2001). The most disconcerting observations suggest that corals are not recovering. In extreme cases, there has been complete deterioration of several keystone species, most notably Acropora palmata (Patterson et al. 2002). Substantial changes since the 1970s point convincingly to human activities, through their effects on climate and the environment, as major causes. These changes translate into multiple stressors that include physical (e.g., elevated temperatures, sedimentation, UV), chemical (e.g., pesticides, herbicides, nutrients, pharm- aceuticals in sewage, oil spills, industrial discharge) and biological factors (e.g., disease, bleaching and algal competition) (Dustan 1999, Porter et al. 1999, Porter and Tougas 2001). Anthropogenic effects can be exacerbated by climatic events (El Niño) which have been increasing in intensity and frequency. Corals are adapted to oligotrophic, relatively stable, uniform environments, and, therefore, they are sensitive and vulnerable to physical and chemical changes in water quality. Although it is clear that new diseases are emerging at an accelerated rate, cause and effect relationships are not well-established. Coral health and diseases have not been critically or thoroughly characterized, and few baseline studies have been conducted to understand their frequency and distribution.

3 Distribution and Frequency of Coral Diseases

Studies have proven that coral disease and bleaching are related to increases in mortality, but scientific evidence is insufficient to establish the ultimate causes. Managers would like predictive tools to determine when and where mortality events will occur. Most studies of coral disease have focused on a single disease affecting specific reefs in response to disease outbreak observations. Consequently, a scientifically defensible, broad-scale survey to determine the frequency and distribution of coral disease and bleaching in the Florida Keys is crucial to understanding the magnitude of the problem (Santavy et al. 2001, 2005). Such a study was conducted in August 2000 by GED, incorporating 60 sites from Key Biscayne to the Dry Tortugas, including sites in Biscayne National Park, Florida Keys National Marine Sanctuary (FKNMS), and the Dry Tortugas National Park. An EMAP-type probabilistic sampling protocol was used to select site locations (Summers et al.1995, Santavy et al. 2001).

The sampling design was employed to estimate the baseline condition of reef corals for the purpose of comparisons with future assessments. Comparisons with the 2000 baseline study could be used to grade the environmental condition of different areas as in the National Coastal Condition Report II (http://www.epa.gov/ owow/oceans/nccr/2005), using red for poor condition, yellow for degraded condition or green for good condition. The probability-based design produced unbiased estimates of the spatial extent of ecological condition with a quantifiable level of uncertainty which measured both the distribution and frequency of coral disease in the Florida Keys Tract. The assessment of coral disease distribution documented the presence or absence at each site. The frequency of disease was calculated from the percentage of the coral community diseased at each site. Distribution and frequency of three intensities of causal bleaching were also determined, but are not included in this report.

The actual area represented by the study was 41 km2 (4100 ha) of the South Florida Keys Tract. The reef areas of the Florida Keys (Upper, Middle, and Lower Keys, New Grounds, and Dry Tortugas) that contained hard coral bottom were demarcated on benthic habitat maps of the Florida Keys (FMRI 1998). Habitat boundaries were redefined by experts to include areas that were known to have living corals and to eliminate areas that contained only dead or geological reef structure (Wheaton et al. 1995, 1996). An EMAP-type sample survey design was developed to estimate the proportion of coral habitat area that had evidence of disease. The design was developed in three steps: (1) regional stratification, (2) overlay of a hexagonal grid on the sample frame, and (3) random selection of multiple sites within grid cells (Summers et al. 1995, Santavy et al. 2005).

The areal estimates generated by the survey results indicated the extent and intensity of coral disease in the sampled community. At least one coral colony was affected by an active disease in any single location at 85 ± 9% (95% confidence intervals) of the area sampled (Fig. 3). Coral disease was widely dispersed throughout all of South Florida and did not seem to be confined to a particular region. Although disease was widespread (high regional prevalence), the proportion of colonies affected by disease at any particular location (local prevalence) was relatively low. The highest local prevalence of coral disease in South Florida during August 2000 was 13%, representing 2.2 ± 4% (97 ha) of the sampling area (Fig. 4). Approximately 15 ± 9% (662 ha) of the area sampled contained no coral disease, whereas 31 ± 14% (1369 ha) of the area had between 0.4- 2.2% of the colonies affected by coral disease. In 28 ± 15% (1236 ha) of the area, 2-4% of the colonies were affected by disease. Finally, 24 ± 4% (1060 ha) of the area sampled had 4-9% frequency of coral disease. The baseline established in 2000 will be compared with future surveys to examine changes and trends in the spatial and temporal distribution and frequency of coral conditions in South Florida.

4 15%+ 9 Not Present

Present

85%+ 9 Figure 3. Distribution or areal extent for the presence of coral disease in the Florida Keys. Not Present represents the percent of area where no coral disease was found. Present represents the percent of area where coral disease was found.

Figure 4. Frequency of coral disease or percent area having 0-13% of colonies affected by coral diseases in the Florida Keys. Error bars represent 95% confidence levels.

Epizootiological Assessment of Coral Disease

Background

An epizootiological approach was designed by GED to compare coral disease among geographical regions in the Florida Keys Reef Tract, including reefs in Dry Tortugas, Key West, Lower Keys, Middle Keys, Upper Keys, and Biscayne National Park. The coral disease surveys were designed to assess changes, develop the epizootiology, and relate coral diseases to spatial patterns and temporal trends to detect ecological change. These data could be used with environmental information in predictive models intended to help managers conserve coral resources in the Sanctuary and national parks in South Florida.

Approach

Our study objective was to understand the health and document changes of reef-building corals by determin- ing the species composition, health status, and types of diseases at many sites throughout the Florida Keys Reef Tract. The sampling design surveyed up to 60 sites spanning reefs in the Dry Tortugas, New Grounds, Key West, Lower Keys, Middle Keys, Upper Keys and Biscayne National Park, once in the late spring-early summer and once in the late summer for 4-5 years (Figs. 5, 6). Because of uncontrollable circumstances, implementing the full sampling design was not possible after the study had begun. The survey for late sum- mer 1999 was cancelled because of a hurricane. A survey planned for early summer 2000 was not supported by ship operations. 5 Figure 5. Map of the coral disease assessment sites examined at least once during the four surveys considered in this study. Numbers in parentheses are number of sites at a particular reef.

Figure 6. Map of the coral disease assessment regions in which all the sites were contained in this study, including areas in Dry Tortugas National Park, New Grounds, Key West, Lower Keys, Middle Keys, Upper Keys and Biscayne National Park.

6 A stratified random sampling design was used as a pilot study in 1997 in the Lower Florida Keys. Data were used to optimize sampling and experimental design for subsequent surveys (May 1998, September 1998, June 1999, and August 2000). The pilot study, designed and implemented by US EPA Gulf Ecology Division, was confined to the Lower Keys, New Grounds, and the Dry Tortugas. In 1998, Mote Marine Laboratory was funded by EPA Region 4 to implement a parallel survey for the Upper and Middle Keys. The two studies were coordinated to allow an integrated assessment of the entire Florida Keys Reef Tract. There were sites in the Upper, Middle and Lower Keys of the FKNMS, Biscayne National Park, and Dry Tortugas National Park (Fig. 6). Collaborations were established, with participation by Region 4, Office of Water, and the Gulf Ecology Division for EPA, NOAA’s FKNMS, Mote Marine Laboratory’s Center for Tropical Research, and the Univer- sity of Georgia. The study was supported by the GED Aquatic Animal Health Team and the Global Climate Change Team. Ship time on the OSV Anderson was supported by the Office of Water for all research cruises in 1997-2000. Logistical and field support were provided by NOAA’s FKNMS and the Dry Tortugas National Park.

Sampling Selection

The procedure used to select sites is detailed elsewhere (Santavy, et al. 2001, 2005). Briefly, sites were chosen from areas that contained hard coral bottom demarcated within each geographic region using a prototype of the Florida Marine Research Institute Benthic Habitats Map of the Florida Keys (FMRI 1998). If the location had sufficient coral coverage (>5%), a permanent installation was made, and the site was sur- veyed. The sampling design included stations with different reef types in each region. Originally, the intention of the design was to sample all sites twice per year, first in late spring, a period believed to include the onset of coral disease activity, and second in late summer, believed to be the most active period for coral diseases. This design could not be implemented because of logistical impediments; therefore, the design was modi- fied. The sites selected for the survey are listed in Appendix A. The table includes for each site: region, site name, site code, latitude, longitude, and depth.

Survey Methodology

All surveys were conducted using a radial arc transect method developed for the coral disease surveys (Fig. 7a-c) (Santavy et al. 2001). Deeper reefs were surveyed with self-contained underwater breathing apparatus (SCUBA), and shallow-back reefs were surveyed by snorkeling. Three surveyors swam in a concentric circle directly over the survey line, recording the number of colonies of each coral species having a specific coral disease or bleaching state (Fig. 7a, b). The radial arc method was developed and validated in 1997 and 1998 and used to determine disease prevalence. Only the 2m wide segment 8-10m from the center of the radial arc (113m2) was required for accurately estimating disease frequency (Fig. 7c) (Mueller et al. 1998, Santavy et al. 1999b, 2001). Twenty-two species of scleractinian corals and gorgonian sea fans were surveyed in the coral disease assessment. At each station, only colonies greater than 10cm in diameter were counted, since smaller colonies could not be reliably identified to species. The following species were surveyed: Agaricia agaricites, Acropora cervicornis, Acropora palmata, Acropora prolifera, Colpophyllia natans, Dendrogyra cylindrus, Dichocoenia stokesii, Diploria clivosa, Diploria labyrinthiformis, Diploria strigosa, Gorgonia spp., Montastraea annularis, Montastraea faveolata, Montastraea franksi, Montastraea cavernosa, Mycetophyllia danaana, Mycetophyllia ferox, Mycetophyllia lamarckiana, Porites astreoides, Siderastrea siderea, Solenastrea bournoni, and Stephanocoenia michelini. Montastraea annularis, Montastraea faveolata, and Montastraea franksi, the three species of coral contained within the Montastraea annularis complex (Weil & Knowlton, 1994) were combined as a single taxon (M. annularis) for data analysis. Two gorgonian species, Gorgonia flabellum and Gorgonia ventalina, were combined as Gorgonia spp.

7 Figure 7a. Underwater surveyors assess species and disease of corals using the radial arc transect method. Divers with slates are recording data. The diver in the background is tending the line which rotates around a fixed pivot point.

Radial Belt Transect Method r = 10m; A = 314.16.1m2 Figure 7b. A diagram of the radial arc used in the transect method. A KevlarTM line is marked in 2m increments and rotated around a fixed pivot rod. Subsurface The radius of the arc is 10m. Float Originally each 2m increment was assessed.

Radial Belt Transect Method r = 8-10m; A = 113.1m2

Figure 7c. The radial arc transect method was modified when it was Pivot 8 10 determined that only the outer 8-10m Rod segment or 113.1m2 was necessary to Subsurface estimate the parameters. Float

8 All diseases were enumerated only for colonies containing active lesions; diseases were not enumerated if mortality had occurred recently and the cause of death was not apparent. Signs used to distinguish most coral diseases have been detailed elsewhere (McCarty and Peters 1998, Patterson et al. 2002, Santavy and Peters 1997, Santavy et al. 1999a, b, 2001) (Appendix B). Because patchy necrosis disease (Bruckner and Bruckner 1997) and white pox (Holden 1996, Patterson et al. 2002) might be the same disease, we used the term white pox to describe the lesions found on Acropora palmata colonies that could not be attributed to white-band disease or predation. We did not distinguish between white plague type 1 and 2 (Dustan 1977, Richardson et al. 1998a, b), but identified these conditions only as white plague. If two diseases were found on the same colony, we used a separate category indicating both diseases were present in order not to over estimate the occurrence of disease. We used a combination of signs defined in the literature to identify aspergillosis (Nagelkerken et al. 1997a, b, Smith et al. 1996). Eleven disease conditions described in the literature and two additional syndromes affecting scleractinian coral species and gorgonian sea fans were used in the assessment.

Statistical Analysis

The data were standardized by representing each species as a percentage of the total number of colonies at a single site for each survey, so that different sites with different numbers of coral colonies could be com- pared. Accordingly, percentages of healthy and diseased colonies and the percentage of each type of dis- ease were standardized for species composition. SAS® for Windows (SAS Institute, Cary NC, Version 8) and Microsoft® Excel 2000 were used to format and view the data and to examine relationships. Data were summarized, descriptive statistics were generated, and tests conducted to determine whether the assump- tions for employing parametric statistics were met.

Pie charts and tables are used to summarize the data for each geographical region by survey period. The results can be compared by survey periods in different venues in Appendices C-E. Each species and disease was represented by a unique color and can be compared side by side in pie charts in Appendix C. Tables with the percentages of healthy and diseased colonies and the percentages of different diseases for each geo- graphical region by survey period are summarized in Appendix D. Disease distributions among sites for each survey period are mapped in Appendix E.

Since the data did not comply with the basic assumptions for use of parametric statistics, nonparametric multivariate statistics were computed with PRIMER® (Plymouth Routines in Multivariate Ecological Research Version 5; Clarke and Gorley 2001). No data transformations were necessary. Ordination maps were gener- ated to examine relationships among the sites based on disease prevalence. Specifically, hierarchical cluster analysis and multiple dimensional scaling were used to describe the relationships for disease variables by explaining similarities among the different survey sites (Sneath and Sokal 1973). Principal components analysis (PCA) was used to extract composite variables (principal components) from the original data. The PCA was displayed in three-dimensional space and rotated using PRIMER 5®. The PCA, with an Euclidian distance metric, identified the percentages of variance contributed by different variables from the original data set. The relationships could be resolved more clearly from the data when they were analyzed by survey period. To reduce the complexity of the data set, the number of variables was reduced into a smaller set of independent, proxy variables that captured the variance of the original data set. The objective was to explain as much of the variance from the original data set as possible in a simpler fashion. The variables that contributed to the first five principal components were used as the proxy variables for each survey period. Three-dimensional ordination maps using the proxy variables were generated to examine relationships between the sites. Geo- graphic region, reef type, and depth were individually projected on each cluster on the ordination maps to look at spatial relationships. Each variable or specific disease was individually overlaid on the ordination map to visualize the distributional relationships with the clustering patterns.

9 Results and Discussion

The percentage of diseased coral colonies ranged from 0-43% among all the sites surveyed during the four sampling periods. No geographic location was consistently identified as a hot spot where a high level of disease was sustained for multiple survey periods. The greatest percentage of diseased colonies occurred at Looe Key (LK03) back reef site during the summer 1998, where 42.9% of all the colonies were diseased, with white pox affecting 41.4% of them. At 12 sites, over 20% of the colonies were diseased at a single sampling period, including six sites during the summer 1998 sampling period (Table 1). Five of these six sites occurred on reefs near Key West and in the Lower Keys, with white pox affecting the majority of the colonies in these two regions. The other site with a high prevalence of white pox was WH01, located in the Dry Tortugas. All of these disease events co-occurred with the single most severe and massive bleaching event recorded in modern history in the Florida Keys.

Table 1: Survey sites exhibiting over 20% disease prevalence during a single sampling period. Abbrevia- tions: PX = white pox; AS = aspergillosis; WB = white-band disease; DS = dark spots disease; and PX-WB = white pox and white-band disease co-occurring on the same colony.

Region Site Year Period % Primary % Primary Other Imp. Diseased* Disease Diseases Diseases

Dry Tortugas BK04 1999 Spring 28.33 6 PX 27.50 WB Dry Tortugas BK05 1999 Spring 27.37 8 PX 27.37 Dry Tortugas WH02 1998 Summer 22.86 10 AS 17.14 DS, WB Key West RK03 1998 Summer 27.27 9 PX 18.80 WB Key West SK02 1998 Summer 36.61 3 PX 16.94 WB, PX-WB Key West SK05 1998 Summer 27.78 7 PX 22.22 WB Lower Keys ES03 1998 Summer 31.91 5 PX 31.91 Lower Keys LK03 1998 Summer 42.86 1 PX 41.43 WB Middle Keys AR02 1998 Spring 22.22 11 AS 22.22 Upper Keys CR02 1998 Spring 20.00 12 AS 20.00 Upper Keys CR03 1998 Spring 32.29 4 AS 23.53 PX Upper Keys CR03 1999 Spring 40.00 2 PX 25.00 WB, DS

* Ranked order from highest to lowest percent of diseased colonies.

The remaining sites with greater than 20% disease were observed during the late spring surveys, principally in the Upper and Middle Keys regions. Carysfort back reef site (CR03) was affected by disease during spring surveys in 1998 (primarily aspergillosis, with a considerable amount of white pox) and 1999 (primarily white pox). In all cases, white pox or aspergillosis was the most abundant disease observed at sites with at least 20% diseased colonies. Eight of the 12 sites had colonies affected primarily by white pox, and the remaining four sites had colonies primarily affected by aspergillosis. In nearly all cases, the primary disease was either the only disease affecting corals or else affected at least half of all diseased corals at a site during one survey. Sand Key fore reef (SK02) was the only exception, where the sub-dominant disease was a combination of white pox and white-band disease affecting a single colony.

The disease trends we observed are supported by work reported by the Coral Reef Monitoring Project (CRMP) and Coral Reef Evaluation and Monitoring Project (CREMP) Groups (FFWCC, 2005). They have reported a general decline in the percentage of coral coverage during 1996-2004 from 11.9% to 6.6% in the FKNMS, with the greatest loss recorded from 1997-1999. A 1.7% decrease was recorded from 1997-1998 and a 2.2% decrease from 1998-1999 in overall coral coverage in the FKNMS. They also reported the greatest decline in mean number of species from 1998-1999, with the greatest drop occurring at Middle Keys reefs and the second greatest at Lower Keys reefs.

10 Species Composition and Disease Prevalence

All results for the total percentage of species composition and disease presence are presented in graphic and tabular form in Appendices C and D for every survey by geographical region. Pie charts for each survey period include a bar graph that breaks out the percent prevalence for each disease (Appendix C). Changes in species composition and disease prevalence can be viewed for all survey periods for easy comparisons. Tables denoting the percent of healthy and diseased colonies, the number of total colonies, and diseased colonies are presented in Appendix D.

At some sites, no diseased colonies were observed following a previous season of high levels of diseased corals (Table 2). This trend reflected the fact that a large number of colonies died between one survey period to the next (Figs. 7 and 8). This pattern was observed most frequently between the summer 1998 and spring 1999 survey periods. Most of the sites displaying high levels of disease occurred during the summer of 1998, a period of massive bleaching. After our survey, a powerful hurricane passed over this area causing great physical destruction of the reefs. The shallow back reefs in the storm’s path experienced severe damage.

Table 2: Percentage and total number of healthy and diseased colonies at each geographic region for all sampling periods by geographic regions.

% % # # Diseased Region Year Period Healthy Diseased Colonies Colonies Sites

Dry Tortugas 1998 Spring 95.51 4.49 1715 77 13 Summer 95.07 4.93 1340 66 13

1999 Spring 95.49 4.51 1950 88 17

2000 Summer 95.39 4.61 1973 91 16

New Grounds 1998 Spring 99.02 0.98 510 5 5 Summer 98.87 1.13 6 19 7 5 2000 Summer 99.54 0.46 431 2 3

Key West 1998 Spring 94.09 5.91 1811 107 12 Summer 87.20 12.80 1109 142 13 1999 Spring 93.16 6.84 965 66 14 2000 Summer 94.66 5.34 993 53 15

Lower Keys 1998 Spring 93.19 6.81 382 26 4 Summer 78.81 21.19 453 96 6 1999 Spring 93.59 6.41 234 15 6

Middle Keys 1998 Spring 96.64 3.36 149 5 4 Summer 98.16 1.84 163 3 5 1999 Spring 97.54 2.46 122 3 4

Upper Keys 1998 Spring 85.83 14.17 367 52 5 Summer 90.20 9.80 408 40 5 1999 Spring 95.77 4.23 520 22 5

Biscayne 1998 Spring 91.23 8.77 285 25 3 National Park Summer 95.51 3.91 307 12 3 1999 Summer 99.40 0.60 336 2 3

11 Significant declines in the number of colonies present were noted during the subsequent spring of 1999. Our results show continued declines in the number of colonies present from summer 1998 to spring 1999, and continuing to summer 2000 on Key West reefs (ED03, RK01, RK02, RK03, SK02, SK05) and Lower Keys reefs (ES03) (Appendix D, Tables D-4 and D-5).

Unprecedented declines of A. palmata and A. cervicornis occurred throughout the Keys during the study. White pox (Patterson et al. 2001), white-band disease, coral bleaching, and physical damage from Hurricane Georges (1998) were the primary factors responsible for these declines. Other confounding consequences of the hurricane included very high concentrations of suspended particulates resulting in very low visibility, large amounts of rain that reduced salinity, and large amounts of terrestrial materials from rainfall run-off. These events left the population levels of Acroporids throughout the Keys so reduced that some recommended protecting these species under the Endangered Species Act (Bruckner 2003). Acropora palmata was widely affected by white pox in summer 1998, with major declines at SK02, SK05, LK03, and ER01 stations in spring 1999 (Fig. 8). Diseases occurred simultaneously with a massive bleaching episode and hurricane damage. At some sites there were substantial declines in this species observed from spring 1998 to summer 1998, specifically at sites RK03, SK01, SK05, and WS04. These sites contained A. palmata affected by both white pox and white-band disease during the survey of spring 1998, with mortality evident in summer 1998. Interestingly, A. cervicornis experienced severe declines in three sites, RK01, BK05, and LR03 from spring 1998 to summer 1998 surveys (Fig. 9), although LR03 had new recruits coming back by summer 2000. Two other important massive species, M. annularis complex and C. natans declined considerably during summer 1998. The number of colonies of M. annularis complex substantially decreased at five sites (Fig. 10). At two sites, the number of C. natans colonies decreased by 46% and 83% (Fig.11). Large colonies (>100 years old) of both species at many sites were completely lost between spring 1998 and summer 2000.

Figure 8. Absolute number of colonies of Acropora palmata at sites showing the greatest loss from spring 1998 to summer 2000.

12 Figure 9. Absolute number of colonies of Acropora cervicornis at sites showing the greatest loss from spring 1998 to summer 2000.

Figure 10. Absolute number of colonies of Montastraea annularis complex at sites showing the greatest loss from spring 1998 to summer 2000.

13 Figure 11. Absolute number of colonies for Colpophyllia natans displaying the greatest loss from spring 1998 to summer 2000.

Principal Component Analysis:

In an effort to describe the spatial dependence and inherent variation of disease prevalence in the South Florida Tract, principal component ordination analysis was performed. An eigenvalue is extracted from the relationships between the different sites based on their disease prevalence, where the eigenvalue is equal to the variance along its corresponding axis, or principal component. The principal axis corresponding to the largest eigenvalue is the dimension that accounts for the greatest variance generated from the data and is known as principal component 1 or PC1. The principal component corresponding to the second greatest variance generated from the data is PC2, etc. Usually 3-5 principal axes will be responsible for most of the variance. Therefore, it simplifies the relationships among a large number of variables from many different sites if a lower number of variables account for a large portion of the variation of the original data set (Johnson and Wichern 1982, Sneath and Sokal 1973).

Principal components of the coral and sea fan diseases were computed separately for the four survey periods. Five composite variables were significant at the p<0.05 level. In spring 1998, five principal components (PC1 + PC2 + PC3 + PC4 + PC5) accounted for 97% of the variability, whereas the first two principal components (PC1 + PC2) accounted for 88% of the variability in disease distribution (Table 3). In summer 1998, five principal components accounted for 99% of the variability. In spring 1999 and summer 2000, the first five principal components accounted for 97% and 90% of the variability, respectively. The factor loadings or correlations between the original variables and principal components indicated five separate modes or variations in the data. For each survey, a single disease was highly correlated with each of the first three principal components (PC1, PC2, PC3) (Table 4). In summer 1998, PC1 was strongly correlated with the presence of white pox disease; PC2 was strongly correlated with the presence of aspergillosis; PC3 was correlated with the presence of dark spots disease; PC4 was correlated with the presence of white-band disease; and PC5 was highly correlated with the presence of white-plague disease (Table 4). In spring 1998, PC1 was negatively correlated with aspergillosis; PC2 was strongly correlated with the presence of white pox; PC3 was negatively correlated with white plague; PC4 was positively correlated with the presence of black- band disease; and PC5 was strongly correlated with yellow-blotch disease.

14 Table 3: The amount of variance attributed to each principal component for disease prevalence from spring 1998 through summer 2000 surveys.

Survey PC1 PC1 + PC2 PC1+PC2+PC3+PC4+PC5 Variance Variance Variance

Spring 1998 60% 88% 97% Summer 1998 71% 87% 99% Spring 1999 78% 85% 97% Summer 2000 52% 73% 90%

Table 4: Results of principal component analysis shown as factor (disease) contributions from the first five principal components. These primary diseases represent the greatest contributors to the differences among stations. Values in parentheses are the coefficients of the principal disease contributors. Disease abbreviations are: AS=aspergillosis; PX=white pox; WP=white plague; BB=black-band disease; YB=yellow-blotch disease; DS=dark-spots disease; WB=white-band disease; and OTH=other undescribed conditions.

Principal PC1 PC2 PC3 PC4 PC5 Component Survey

Spring 1998 AS (-0.977) PX (0.967) WP (-0.938) BB (0.959) YB (0.960) Summer 1998 PX (0.985) AS (0.987) DS (0.924) WB (0.893) WP (0.974) Spring 1999 PX (-0.992) DS (-0.851) WP (-0.892) AS (0.755) BB (-0.575) WB (-0.515) Summer 2000 PX (0.995) OTH (0.926) DS (-0.736) WB (0.775) YB (0.689) YB (-0.581) WB (0.477)

White pox was always positively correlated with PC1 in the summer sampling seasons, whereas in spring 1999, it was negatively correlated to PC1. In spring 1998, PC1 was negatively correlated with aspergillosis, but PC2 was strongly correlated with the presence of white pox. In almost all cases, the same diseases were strongly correlated with a principal component in the study. White pox, aspergillosis, dark spots disease, white plague disease, black-band disease, yellow-band disease, and yellow-blotch disease were strongly correlated in positive or less often negative manner with a principal component. Only in summer 2000 was another disease important in the factor loadings: PC2 was represented by other diseases. During this time, a condition affecting Porites astreoides was observed throughout the Keys. The condition manifested as a paling of the pigment and wasting of the tissue from the skeleton with mucus production. This condition has persisted in subsequent surveys, and now extends to the Dry Tortugas reefs.

The proxy variables chosen for each survey were the following: spring 1998— aspergillosis, white pox, white plague, black-band disease, and yellow-blotch disease; summer 1998—white pox, aspergillosis, dark-spots disease, white-band disease, and white plague; spring 1999—white pox, dark-spots disease, white plague, aspergillosis, black-band disease, white band; and summer 2000—white pox, other diseases, dark-spots, white-band disease, yellow band disease. The spatial distribution of the mean factor contributions or the distribution of the diseases did not correspond to specific geographical regions, reef types, or water depths. The distribution of each primary disease was mapped over time to compare the Dry Tortugas and Key West sites (Appendix E).

15 Spatial Distribution of Diseases

Aspergillosis was less prevalent in the spring surveys than in the summer surveys. In the Dry Tortugas, it was present at only one site in the springs of 1998 and 1999, both times at BK03. In the summer it was present at five sites in both 1998 and 2000, and was observed at three of the same sites both times. In the Key West sites, the association with season was not as strong. During the springs of 1998 and 1999, aspergillosis was present at two sites and three sites respectively. Aspergillosis was present at four and seven sites respec- tively during the summers of 1998 and 2000. At SK01 aspergillosis infected sea fans during all the surveys. Sea fans at RK02 were infected first in summer 1998 and remained so during subsequent surveys. In sum- mer 2000, most of the sites at Sand Key and Eastern Dry Rocks also had infected sea fans.

White pox distribution was more disparate in the Dry Tortugas during the surveys. In spring 1998, white pox was present at three sites, but no active disease was found at these or any sites in summer 1998. Two sites (BK04 and BK05) had white pox in spring 1999; the same sites were affected in summer 2000, along with one additional site (LR04) where white pox had not been reported previously.

Conclusions

The dominant diseases found among all sites were white pox, aspergillosis, dark spots disease, white-band disease, and white plague. The greatest disease prevalences observed during our study coincided with the two most severe bleaching events to occur in the Florida Keys. Prolonged periods of elevated temperatures inducing coral bleaching occurred in the late summer months of 1997 and 1998. Very high disease prevalences followed the next spring and summer of 1998. The final catastrophic insult occurred while many corals were bleaching in late summer 1998 as a major hurricane passed through the study area in late September. Many coral reefs were damaged by the consecutive events, causing extensive coral mortality, which was observed in our surveys as decreases in coral abundance. These factors most likely were responsible for the greatest decline in coral abundance reported during our spring survey in 1999. Species experiencing significant declines over the course of the study were Acropora palmata, Acropora cervicornis, Montastraea annularis complex, and Colpophyllia natans.

Our results were consistent with the trends reported by the CRMP from their coral monitoring project from 1996-2000 (Jaap et al. 2000, 2001, Wheaton et al. 2002, Beaver et al., 2004, FFWCC, 2005). The greatest decline in the number of colonies and coral coverage occurred in1998-1999, two years following the massive coral bleaching episode throughout the Dry Tortugas and FKNMS (FFWCC 2005). The CRMP study reported the greatest loss of stony corals from 1996 thru 1999, when a 37% reduction in stony coral coverage was observed in FKNMS (Jaap et al. 2001). During that time 64% of their stations showed a decrease in coral coverage, and 67% of their stations showed a decrease in species richness (Jaap et al. 2000, 2001). The overall trends reported by the two projects were similar, although our sampling design differed from the CRMP/CREMP. Our survey included Gorgonia spp. in our assessments, whereas CRMP classified them separately. The CRMP study included the hydrocoral Millepora complanata in their stony coral class, and we did not.

Our study found the least change in coral abundance and disease prevalence in the Middle Keys region, and conversely, the greatest change in coral abundance and highest disease prevalances in the Lower Keys/Key West region. The CRMP study found the least change during the same time period in Middle Keys with 48% of the stations decreasing in coral coverage and the greatest change in coral coverage in the Upper Keys (Beaver et al. 2004, FFWCC 2005). They found that 73% of the Upper Keys stations lost coral coverage, and 69% of the Lower Keys stations lost coral coverage. Another difference between the two studies was the division of regions: we segmented the Lower Keys stations into two regions, those proximal to Key West as the Key West region and those distal from Key West as the Lower Keys region. The differences between our results presumably were explained by the inherent differences in the two studies. Additional disparities

16 between our studies included the reef types and locations chosen. The CRMP included inshore patch reefs and hard bottom habitats in the FKNMS, whereas our study included primarily deep and shallow offshore reefs. Many inshore patch reefs were included in their Lower Keys assessments. In addition, the approaches and methodologies contrasted between the two studies. We measured coral abundance and disease prevalence, whereas the CRMP recorded coral coverage and absence or presence of three disease classes at each station. Our metric for assessing disease prevalence was percentage of affected corals; the CRMP used percentage of stations with disease presence.

Our studies recorded the highest disease prevalences in 1997-1999, after which disease prevalences and declines in coral abundance decreased to relatively low levels in 2000 and 2001. Since coral colony abundances decreased during this same period, we believe that many of the susceptible individuals had died, and the disease had fewer susceptible hosts. Interestingly, in 2002 there was a significant increase in coral disease but not to the levels recorded in 1998. We speculate that the host range of the diseases might have increased to include other coral species. Multivariate non-parametric analyses did not reveal any clear spatial correlations between disease distributions and geographical regions, reef types, or water depths. Additional annual assessments are needed to determine spatial and temporal trends.

Since our database spans only a few years, it is important that annual assessments continue in order to determine what relationships are important in disease prevalence and prediction. It is apparent that species composition is important to consider and must be incorporated into any model. Analyses based on GIS might be used to understand spatial associations between coral condition and global change and other stressors. This tool can determine associations between coral health and stressor distributions that cannot be evaluated using other approaches. Associations between coral health metrics and stressor distributions can provide critical information to guide survey efforts (e.g., specific reef areas to investigate) and sampling activities (e.g., areas to focus data collection, such as water quality sampling). Information on geospatial correlations between coral health metrics and stressors will provide reef managers with information necessary to make policy decisions to help protect and conserve coral reefs in this region.

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19 Richardson, L.L., W.M. Goldberg, K.G. Kuta, R.B. Aronson, G.W. Smith, K.B. Ritchie, J.C. Halas, J.S. Feingold and S.L. Miller. 1998a. Florida’s mystery coral-killer identified. Nature 392:557-558. Richardson, L.L., W.M. Goldberg, R.G. Carlton and J.C. Halas. 1998b. Coral disease outbreak in the Florida Keys: Plague type II. Rev. Biol. Trop. 46 Suppl 5:187-189. Ritchie, K.B. and G.W. Smith. 1998. Description of Type II White Band Disease in Acroporid Corals. Rev. Biol. Trop. 46, Suppl. 5:173-185. Rogers, C.S. 1985. Degradation of Caribbean and western Atlantic coral reefs and decline of associated fisheries. Proc 5th Int Coral Reef Symp. 6:491-496. Rützler, K. and D.L. Santavy, 1983. The black-band disease of Atlantic reef corals I. Description of the cyanophyte pathogen. P.S.Z.N.I. Mar. Ecol. 4:301-319. Rützler, K., D.L. Santavy and A. Antonius, 1983. The black-band disease of Atlantic reef corals III. Distribu- tion, ecology, and development. P.S.Z.N.I. Mar. Ecol. 4:329-358. Santavy, D.L. and E.C. Peters. 1997. Microbial pests: Coral disease research in the western Atlantic. In: H.A. Lessios and I.G. Macintyre (eds). Proc. 8th Intern. Coral Reef Symp. 1:607-612. Santavy, D.L., E.C. Peters, C. Quirolo, J.W. Porter, and C.N. Bianchi. 1999a. Yellow-blotch disease out- breaks on reefs of the San Blas Islands, Panama. Coral Reefs 19:97. Santavy, D.L., E. Mueller, E.C. Peters, J.W. Porter, V.D. Engle, and J.G. Campbell. 1999b. Quality assurance measures associated with coral reef monitoring. Inter. Conf. Sci. Aspects of Coral Reef Assess., Monitor- ing, and Restoration. Apr. 14-16, 1999, Fort Lauderdale, FL. pp. 170-171. Santavy, D.L., E. Mueller, E.C. Peters, L. MacLaughlin, J.W. Porter, K.L. Patterson and J. Campbell. 2001. Quantitative assessment of coral diseases in the Florida Keys: Strategy and Methodology. Hydrobiol. 460: 39-52. Santavy, D.L., J.K. Summers, V.D. Engle, and L.C. Harwell. 2005. The condition of the coral reefs in South Florida using coral disease and causal bleaching as an indicator. Environ. Monitor. Assess. 100: 129-152. Shulman, J.F., and D.R. Robertson. 1997. Changes in the coral reef of San Blas, Caribbean Panama: 1983 to 1990. Coral Reefs 15:231-236. Smith, G.W., L.D. Ives, I.A. Nagelkerken and K.B. Ritchie. 1996. Caribbean sea-fan mortalities. Nature 383: 487. Sneath, P.H.A. and R.R. Sokal. 1973. Numerical Taxonomy. W.H. Freeman and Co., San Francisco. 573pp. Summers, J.K., J.F. Paul and A. Robertson. 1995. Monitoring the ecological condition of estuaries in the United States. Tox. Envir. Chem. 49:93-108. Weil, E. and N. Knowlton. 1994. A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander,1786) and its two sibling species, M. faveolata (Ellis and Solander,1786) and M. franki (Gregory,1895). Bull. Mar. Sci. 55:151-175. Wheaton, J.L., W.C. Jaap, P. Dustan, and J. Porter. 1995. Coral Reef and Hardbottom Monitoring Project. FMRI. Wheaton, J.L., W.C. Jaap, P. Dustan, and J. Porter. 1996. Coral Reef and Hardbottom Monitoring Project. FMRI. Wheaton, J., W.C. Jaap, J.W. Porter, V. Kosminyn, K. Hackett, M. Lybolt, M.K. Callahan, J. Kidney, S. Kupfner, C. Tsokos, and G. Yanev. 2001. EPA/FKNMS Coral Reef Monitoring Project, Executive Summary 2001. In FKNMS Symposium: An Ecosystem Report Card. Wash., D.C. Available from:http://wwwfloridamarine.org. Wilkinson, C.R. 1998. Status of coral reefs of the world: 1998. Global Coral Reef Monitoring Network and Australian Institute of Marine Science. Townsville, Australia. 184pp. Wilkinson, C.R. 2000. Status of coral reefs of the world: 2000. Australian Institute of Marine Science. Townsville, Australia. 363pp. Wilkinson, C.R. 2002. Status of coral reefs of the world: 2002. Australian Institute of Marine Science. Townsville, Australia. 378pp.

20 APPENDICES

21 22 Appendix A

All sites sampled during surveys, including regions, site names, codes, latitude and longitudes, and depths.

A-1 Table A-1. Sites sampled. Region Site Name Site Code Depth (ft.) Latitude Longitude

Dry Tortugas Loggerhead Reef 2 LR02 10-15 24o 37.799' 82o 56.172' Loggerhead Reef 3 LR03 ~6 24° 38.0877' 82° 55.3679' Loggerhead Reef 4 LR04 ~8-11 24o 38.107' 82o 54.980' Loggerhead Reef 5 LR05 10 24° 39.031' 82° 54.899' Loggerhead Reef 6 LR06 7-10 24° 39.148' 82° 54.847' Loggerhead Reef 7 LR07 ~9 24° 39.276' 82° 54.786' White Shoals 1 WH01 20-35 24o 38.532' 82o 53.807' White Shoals 2 WH02 15-16 24o 38.518' 82o 53.812' Bird Key Reef 1 BK01 33 24o 36.703' 82o 52.239' Bird Key Reef 3 BK03 19 24o 37.204' 82o 52.004' Bird Key Reef 4 BK04 8 24o 37.237' 82o 52.042' Bird Key Reef 5 BK05 8 24o 37.236' 82o 52.039' Bird Key Reef 6 BK06 10 24o 37.868' 82o 52.706' Bird Key Reef 7 BK07 10 24o 37.865' 82o 52.706' Bird Key Reef 8 BK08 10 24o 37.225' 82o 52.146' Bird Key Reef 9 BK09 10 24o 37.216' 82o 52.146' Pulaski Shoals 1 PS01 27 24o 41.645' 82o 46.293' Key West Sand Key 1 SK01 20 24o 27.141' 81o 52.591' Sand Key 2 SK02 11 24o 27.1190' 81o 52.650' Sand Key 3 SK03 29-35 24o 27.087' 81o 52.799' Sand Key 4 SK04 30-35 24o 27.087' 81o 52.799' Sand Key 5 SK05 4 24o 27.18' 81o 52.718' Rock Key 1 RK01 30-37 24o 27.211' 81o 51.602' Rock Key 2 RK02 15-19 24o 27.298' 81o 51.582' Rock Key 3 RK03 4 24o 27.353' 81o 51.526' Eastern Dry Rocks 1 ED01 8-18 24o 27.575' 81o 50.755' Eastern Dry Rocks 3 ED03 4 24° 27.680' 81° 50.632' Eastern Dry Rocks 4 ED04 30 24° 27.728' 81° 50.338' Western Sambo 2 WS02 4 24o 28.8577' 81o 43.0774' Western Sambo 3 WS03 24-30 24o 28.776' 81o 42.861' Western Sambo 4 WS04 9 24o 28.799' 81o 42.968' Western Sambo 5 WS05 4 24° 28.842' 81° 43.069' Lower Keys Eastern Sambo 1 ES01 25 24o 29.513' 81o 39.674' Eastern Sambo 2 ES02 15-20 24o 29.552' 81o 39.687' Eastern Sambo 3 ES03 10 24o 29.532' 81o 39.919' Looe Key 1 LK01 45 24o 32.543' 81o 24.877' Looe Key 2 LK02 10-25 24o 32.747' 81o 24.349' Looe Key 3 LK03 4 24o 32.819' 81o 24.361' Middle Keys Sombrero Reef 1 SR01 23-25 24o 37.550' 81o 06.508' Sombrero Reef 2 SR02 9-23 24o 37.573' 81o 06.568' Alligator Reef 1 AR01 25 24o 50.788' 80o 37.248' Alligator Reef 2 AR02 15-20 24o 50.762' 80o 37.286' Upper Keys Molasses Reef 1 MR01 55-75 25o 01.057' 80o 21.840' Molasses Reef 2 MR02 12-22 25o 01.104' 80o 22.062' Carysfort Reef 1 CR01 15-22 25o 13.461' 80o 12.493' Carysfort Reef 2 CR02 15-25 25o 13.318' 80o 12.607' Carysfort Reef 3 CR03 5-8 25o 13.496' 80o 12.562' Biscayne Elkhorn Reef 1 ER01 10 25o 21.807' 80o 09.925' National Park Pacific Reef 1 PR01 45 25o 21.735' 80o 08.370' Pacific Reef 2 PR02 15-22 25o 22.225' 80o 08.387'

A-2 Appendix B

Coral diseases sampled for the study during the 1998-2000 surveys.

B-1 Table B-1: Diseases observed in surveys, with corresponding abbreviations and references detailing the signs used in assessing condition.

Disease Disease Name Abbreviation Species Affected in Tropical Western Atlantic References

Aspergillosis AS Gorgonia spp. Nagelkerken et al.1997a,b; Smith et al. 1996

Black-Band Disease BB Diploria strigosa, D. labyrinthiformis, Antonius 1981; Rützler et al.1983; Rützler & Colpophyllia natans, Montastraea Santavy 1983 cavernosa, M. annularis, M. franksi, M. faveolata, Siderastrea siderea, Gorgonia spp.

Dark Spot Disease DS C. natans, M. annularis (species complex), Garzón-Ferreira & Gil 1998 S. siderea, Stephanocoenia intersepta

Hyperplasia HP D. strigosa, Dichocoenia stokesii Cheney 1975; Loya et al.1984; Peters et al. 1986

Patchy Necrosis/ PX Acropora palmata Bruckner & Bruckner 1997; Patterson et al. White Pox 2002 B-2 Red-Band Disease RB Gorgonia spp., C. natans Rützler & Santavy 1983; Richardson 1993

White Plague I WP1* C. natans, Mycetophyllia ferox Dustan 1977

White Plague II WP2 D. stokesii, Agaricia agaricites, A. larmarki, Richardson et al.1998a, b C. natans, Dendrogyra cylindrus, D. labyrinthiformis, D. strigosa, Eusmilia fastigiata, Madracis decactis, M. mirabilis. Manicina areolata, Meandrina meandrites, M. annularis (species complex), M. cavernosa, S. siderea, Solenastrea bournoni Stephanocoenia michelinii, and hydrocoral Millepora alcicornis

White Band Disease 1 WB1 A. cervicornis, A. palmata, A. prolifera Gladfelter 1982; Peters 1984, Peters et al. 1983

White Band Disease 2 WB2* A. cervicornis Richie & Smith 1998

Yellow Blotch Disease YB M. faveolata, M. annularis Santavy et al. 1999a

* Did not find in any of our surveys. Appendix C

Pie charts presenting the percent species and disease composition for each geographic region for 1998-2000 surveys.

C-1 C-2 C-3 C-4 C-5 C-6 C-7 C-8 C-9 C-10 C-11 C-12 C-13 C-14 C-15

Appendix D

Tables presenting percent species and disease composition for each geographic region for 1998-2000.

D-1 Table D-1. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each geographic region for all sampling periods.

% % # # Diseased # Region Year Period Healthy Diseased Colonies Colonies Sites

Dry Tortugas 1998 Spring 95.51 4.49 1715 77 13 Summer 95.07 4.93 1340 66 13 1999 Spring 95.49 4.51 1950 88 17 2000 Summer 95.39 4.61 1973 91 16

New Grounds 1998 Spring 99.02 0.98 510 5 5 Summer 98.87 1.13 619 7 5 2000 Summer 99.54 0.46 431 2 3

Key West 1998 Spring 94.09 5.91 1811 107 12 Summer 87.20 12.80 1109 142 13

1999 Spring 93.16 6.84 965 66 14 2000 Summer 94.66 5.34 993 53 15

Lower Keys 1998 Spring 93.19 6.81 382 26 4 Summer 78.81 21.19 453 96 6 1999 Spring 93.59 6.41 234 15 6

Middle Keys 1998 Spring 96.64 3.36 149 5 4 Summer 98.16 1.84 163 3 5 1999 Spring 97.54 2.46 122 3 4

Upper Keys 1998 Spring 85.83 14.17 367 52 5 Summer 90.20 9.80 408 40 5 1999 Spring 95.77 4.23 520 22 5

Biscayne 1998 Spring 91.23 8.77 285 25 3 National Park Summer 95.51 3.91 307 12 3 1999 Summer 99.40 0.60 336 2 3

D-2 Table D-2. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the Dry Tortugas Region.

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

BK01 1998 Spring 90.64 9.36 203 19 Summer 96.60 3.40 235 8 1999 Spring 96.91 3.09 194 6 2000 Summer 97.94 2.06 243 5 BK03 1998 Spring 99.40 0.60 167 1 Summer 97.89 2.11 142 3 1999 Spring 98.98 1.02 491 5 2000 Summer 98.42 1.58 253 4 BK04 1998 Spring 85.71 14.29 133 19 Summer 95.83 4.17 120 5 1999 Spring 71.67 28.33 120 34 2000 Summer 85.89 14.11 163 23 BK05 1998 Spring 83.33 16.67 168 28 Summer 95.79 4.21 95 4 1999 Spring 72.63 27.37 95 26 2000 Summer 85.59 14.41 118 17 BK06 1998 Spring 99.12 0.88 114 1 Summer 100.00 0.00 41 0 1999 Spring 100.00 0.00 40 0 2000 Summer 100.00 0.00 63 0 BK07 1998 Spring 97.87 2.13 47 1 Summer 97.44 2.56 39 1 1999 Spring 100.00 0.00 95 0 2000 Summer 96.61 3.39 59 2 BK08 1999 Spring 96.67 3.33 90 3 2000 Summer 98.25 1.75 114 2 BK09 1999 Spring 98.70 1.30 77 1 LR01 1998 Spring 100.00 0.00 8 0 Summer 100.00 0.00 6 0 LR02 1998 Spring 97.50 2.50 40 1 Summer 98.51 1.49 67 1 1999 Spring 98.98 1.02 98 1 2000 Summer 98.61 1.39 72 1 LR03 1998 Spring 99.24 0.76 132 1 Summer 82.42 17.58 91 16 1999 Spring 95.61 4.39 114 5

D-3 Table D-2. Continued

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

LR03 2000 Summer 98.11 1.89 106 2 LR04 1998 Spring 100.00 0.00 399 0 Summer 97.75 2.25 311 7 1999 Spring 98.77 1.23 162 2 2000 Summer 94.02 5.98 351 21 LR05 1999 Spring 97.96 2.04 49 1 2000 Summer 100.00 0.00 66 0 LR06 1999 Spring 100.00 0.00 41 0 2000 Summer 100.00 0.00 33 0 LR07 1999 Spring 96.97 3.03 33 1 2000 Summer 93.51 6.49 77 5 PS01 1998 Spring 96.23 3.77 53 2 Summer 93.88 6.12 49 3 1999 Spring 98.26 1.74 115 2 2000 Summer 98.80 1.20 83 1 WH01 1998 Spring 98.79 1.21 165 2 Summer 97.30 2.70 74 2 1999 Spring 100.00 0.00 85 0 2000 Summer 95.05 4.95 101 5 WH02 1998 Spring 97.67 2.33 86 2 Summer 77.14 22.86 70 16 1999 Spring 98.04 1.96 51 1 2000 Summer 95.77 4.23 71 3

Table D-3. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the New Grounds Region.

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

NG01 1998 Spring 99.08 0.92 109 1 Summer 99.06 0.94 106 1 2000 Summer 99.28 0.72 139 1 NG02 1998 Spring 98.53 1.47 136 2 Summer 99.46 0.54 184 1 2000 Summer 100.00 0.00 171 0 NG03 1998 Spring 98.77 1.23 81 1 Summer 98.89 1.11 90 1 NG04 1998 Spring 98.59 1.41 71 1 Summer 97.64 2.36 127 3 2000 Summer 99.17 0.83 121 1 NG05 1998 Spring 100.00 0.00 113 0 Summer 99.11 0.89 112 1

D-4 Table D-4. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the Key West Region.

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

ED01 1998 Spring 98.18 1.82 55 1 Summer 98.11 1.89 53 1 1999 Spring 91.95 8.05 87 7 2000 Summer 95.35 4.65 43 2 ED03 1998 Summer 95.88 4.12 97 4 1999 Spring 95.08 4.92 61 3 2000 Summer 96.15 3.85 52 2 ED04 1999 Spring 96.88 3.13 64 2 2000 Summer 97.33 2.67 75 2 RK01 1998 Spring 96.51 3.49 258 9 Summer 96.04 3.96 101 4 1999 Spring 96.91 3.09 97 3 2000 Summer 100.00 0.00 75 0 RK02 1998 Spring 98.77 1.23 163 2 Summer 91.43 8.57 175 15 1999 Spring 95.24 4.76 126 6 2000 Summer 93.85 6.15 130 8 RK03 1998 Spring 95.24 4.76 21 1 Summer 72.73 27.77 11 3 1999 Spring 100.00 0.00 10 0 2000 Summer 100.00 0.00 9 0 SK01 1998 Spring 92.92 7.08 424 30 Summer 90.83 9.17 109 10 1999 Spring 87.23 12.77 141 18 2000 Summer 84.17 15.83 139 22 SK02 1998 Spring 88.46 11.54 286 33 Summer 63.39 36.61 183 67 1999 Spring 91.76 8.24 85 7 2000 Summer 94.85 5.15 97 5 SK03 1998 Spring 97.67 2.33 43 1 Summer 90.91 9.09 44 4 1999 Spring 97.44 2.56 39 1 2000 Summer 95.45 4.55 44 2 SK04 1998 Spring 92.68 7.32 41 3 Summer 88.14 11.86 59 7 1999 Spring 97.44 1.75 57 1

D-5 Table D-4. Continued % % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

SK04 2000 Summer 98.25 1.75 57 1 SK05 1998 Spring 96.43 3.57 84 3 Summer 72.22 27.78 36 10 1999 Spring 100.00 0.00 14 0 2000 Summer 100.00 0.00 3 0 WS02 1998 Spring 90.48 9.52 105 10 Summer 95.24 4.76 63 3 2000 Summer 100.00 0.00 67 0 WS03 1998 Spring 95.76 4.24 165 7 Summer 92.73 7.27 110 8 1999 Spring 94.34 5.66 53 3 2000 Summer 92.16 7.84 51 4 WS04 1998 Spring 95.78 4.22 166 7 Summer 91.18 8.82 68 6 1999 Spring 93.26 6.74 89 6 2000 Summer 95.45 4.55 44 2 WS05 1999 Spring 85.00 15.00 60 9 2000 Summer 97.20 2.80 107 3

Table D-5. Percentage of healthy and diseased colonies, and total number of colonies and dis- eased colonies at each site for all sampling periods in the Lower Keys Region. % % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

ES01 1998 Spring 97.83 2.17 46 1 Summer 95.12 4.88 41 2 1999 Spring 88.37 11.63 43 5 ES02 1998 Spring 86.11 13.89 36 5 Summer 86.00 14.00 50 7 1999 Spring 97.83 2.17 46 1 ES03 1998 Summer 68.09 31.91 47 15 1999 Spring 90.00 10.00 20 2 LK01 1998 Spring 93.12 6.88 218 15 Summer 80.90 19.10 178 34 LK02 1998 Spring 93.90 6.10 82 5 Summer 88.06 11.94 67 8 1999 Spring 94.44 5.56 72 4 LK03 1998 Summer 57.14 42.86 70 30 1999 Spring 87.50 12.50 16 2 LK04 1999 Spring 97.30 2.70 37 1

D-6 Table D-6. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the Middle Keys Region.

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

AR01 1998 Spring 100.00 0.00 22 0 Summer 96.67 3.33 30 1 1999 Spring 96.00 4.00 25 1 AR02 1998 Spring 77.78 22.22 18 4 Summer 96.00 4.00 25 1 1999 Spring 100.00 0.00 32 0 SR01 1998 Spring 100.00 0.00 56 0 Summer 100.00 0.00 47 0 1999 Spring 93.33 6.67 30 2 SR02 1998 Spring 98.11 1.89 53 1 Summer 97.44 2.56 39 1 1999 Spring 100.00 0.00 35 0

Table D-7. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the Upper Keys Region.

% % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

CR01 1998 Spring 87.84 12.16 74 9 Summer 89.86 10.14 69 7 1999 Spring 97.50 2.50 80 2 CR02 1998 Spring 80.00 20.00 115 23 Summer 87.18 12.82 117 15 1999 Spring 98.28 1.72 233 4 CR03 1998 Spring 64.71 35.29 17 6 Summer 85.00 15.00 20 3 1999 Spring 60.00 40.00 20 8 MR01 1998 Spring 93.62 6.38 47 3 Summer 90.57 9.43 53 5 1999 Spring 91.07 8.93 56 5 MR02 1998 Spring 90.35 9.65 114 11 Summer 93.29 6.71 149 10 1999 Spring 97.71 2.29 131 3

D-7 Table D-8. Percentage of healthy and diseased colonies, and total number of colonies and diseased colonies at each site for all sampling periods in the Biscayne National Park Region. % % # # Diseased Site Year Period Healthy Diseased Colonies Colonies

ER01 1998 Spring 80.88 19.12 68 13 Summer 94.19 5.81 86 5 1999 Spring 100.00 0.00 35 0 PR01 1998 Spring 95.45 4.55 22 1 Summer 83.33 16.67 18 3 1999 Spring 100.00 0.00 20 0 PR02 1998 Spring 94.36 5.64 195 11 Summer 98.03 1.97 203 4 1999 Spring 99.29 0.71 281 2

D-8 Appendix E

Base maps and survey site maps of five most common diseases at locations for Dry Tortugas and Key West Regions during four surveys.

E-1 PS01 BK03 BK05 4 Miles BK01 BK07 BK04 BK06 WH02 2 WH01 LR05 LR04 LR07 LR06 LR01 LR03 LR02 20 Figure 1: Base Map of Dry Tortugas survey sites. Each site sampled is denoted as black circle ( ) with the site code.

E-2 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 Summer 1998 Summer 2000 BK04 BK04 BK06 BK06 WH02 WH02 WH01 WH01 LR04 LR05 LR04 LR05 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 LR02 LR02 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 BK04 BK06 BK06 WH02 WH02 WH01 WH01 Spring 1998 Spring 1999 LR05 LR05 LR04 LR04 LR07 LR07 LR06 LR06 Figure 2: Survey sites in Dry Tortugas that had Aspergillios is present by survey periods. Each site with disease has ( ). LR01 LR01 LR03 LR03 LR02 LR02

E-3 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 Summer 1998 Summer 2000 BK04 BK04 BK06 BK06 WH02 WH02 WH01 WH01 LR04 LR05 LR04 LR05 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 LR02 LR02 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 BK04 BK06 BK06 WH02 WH02 WH01 WH01 Spring 1998 Spring 1999 LR05 LR05 LR04 LR04 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 Figure 3: Survey sites in Dry Tortugas that had Dark Spots Disease present by survey periods. Each site with disease has ( ). LR02 LR02

E-4 E-5 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 Summer 1998 Summer 2000 BK04 BK04 BK06 BK06 WH02 WH02 WH01 WH01 LR04 LR05 LR04 LR05 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 LR02 LR02 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 BK04 BK06 BK06 WH02 WH02 WH01 WH01 Spring 1998 Spring 1999 LR05 LR05 LR04 LR04 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 Figure 5: Survey sites in Dry Tortugas that had White Band Disease present by survey periods. Each site with disease has ( ). LR02 LR02

E-6 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 Summer 1998 Summer 2000 BK04 BK04 BK06 BK06 WH02 WH02 WH01 WH01 LR04 LR05 LR04 LR05 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 LR02 LR02 PS01 PS01 BK05 BK05 BK03 BK03 BK01 BK07 BK01 BK07 BK04 BK06 BK06 WH02 WH02 WH01 WH01 Spring 1998 Spring 1999 LR05 LR05 LR04 LR04 LR07 LR07 LR06 LR06 LR01 LR01 LR03 LR03 LR02 LR02 Figure 6: Survey sites in Dry Tortugas that had White Plague Type II Disease present by survey periods. Each site with disease has ( ).

E-7 Reef Land WS04 WS05 WS03 WS02 Key West 4 Miles ED03 ED04 2 ED02 RK02 RK01 RK03 SK04 SK03 SK05 SK02 SK01 20 Figure 7: Base Map of Key West survey sites. Each site sampled is denoted as black circle ( ) with the site code.

E-8 E-9 WS04 WS04 WS05 WS05 WS03 WS03 WS02 WS02 Summer 2000 Summer 1998 ED03 ED03 ED04 ED04 ED02 ED02 RK02 RK02 WS04 RK01 RK01 WS05 RK03 RK03 WS04 WS05 SK04 SK04 WS03 SK03 SK03 WS02 SK05 SK05 SK02 WS03 SK02 WS02 SK01 SK01 ED03 ED04 ED02 ED03 ED04 RK02 ED02 RK01 RK02 RK03 Spring 1998 Spring 1999 RK01 SK04 RK03 Figure 9: Survey sites in Key West that had Dark Spots diseases present by survey periods. Each site with disease has ( ). SK03 SK04 SK05 SK02 SK03 SK05 SK01 SK02 SK01

E-10 WS04 WS04 WS05 WS05 WS03 WS03 WS02 WS02 Summer 2000 Summer 1998 ED03 ED03 ED04 ED04 ED02 ED02 RK02 RK02 WS04 RK01 RK01 WS05 RK03 RK03 WS04 WS05 SK04 SK04 WS03 SK03 SK03 WS02 SK05 SK05 SK02 WS03 SK02 WS02 SK01 SK01 ED03 ED04 ED02 ED03 ED04 RK02 ED02 RK01 RK02 RK03 Spring 1998 Spring 1999 RK01 SK04 RK03 SK03 Figure 10: Survey sites in Key West that had White Pox disease present by survey periods. Each site with disease has ( ). SK04 SK05 SK02 SK03 SK05 SK01 SK02 SK01

E-11 WS04 WS04 WS05 WS05 WS03 WS03 WS02 WS02 Summer 2000 Summer 1998 ED03 ED03 ED04 ED04 ED02 ED02 RK02 RK02 WS04 RK01 RK01 WS05 RK03 RK03 WS04 WS05 SK04 SK04 WS03 SK03 SK03 WS02 SK05 SK05 SK02 WS03 SK02 WS02 SK01 SK01 ED03 ED04 ED02 ED03 ED04 RK02 ED02 RK01 RK02 RK03 Spring 1998 Spring 1999 RK01 SK04 RK03 SK03 Figure 11: Survey sites in Key West that had White Band disease present by survey periods. Each site with disease has ( ). SK04 SK05 SK02 SK03 SK05 SK01 SK02 SK01

E-12 WS04 WS04 WS05 WS05 WS03 WS03 WS02 WS02 Summer 2000 Summer 1998 ED03 ED03 ED04 ED04 ED02 ED02 RK02 RK02 WS04 RK01 RK01 WS05 RK03 RK03 WS04 WS05 SK04 SK04 WS03 SK03 SK03 WS02 SK05 SK05 SK02 WS03 SK02 WS02 SK01 SK01 ED03 ED04 ED02 ED03 ED04 RK02 ED02 RK01 RK02 RK03 Spring 1998 Spring 1999 RK01 SK04 RK03 SK03 SK04 SK05 SK02 SK03 Figure 12: Survey sites in Key West that had White Plague Type II disease present by survey periods. Each site with disease has ( ). SK05 SK01 SK02 SK01

E-13

Appendix F

Reports, Publications and Presentations, products resulting from this research.

F-1 Reports

EPA Internal Products:

2000: Report on a quantitative assessment of coral diseases in the Florida Keys. (GPRA-V) 2001: Report on the frequency and distribution of coral diseases in coral ecosystems in South Florida. (GPRA 8.1.2,V) 2003: Report relating water quality to distribution and frequency of coral diseases in South Florida. (GPRA 6.2.3, C) 2003: Report on the potential consequences of climate change for coral ecosystems. (GPRA 6.2.3) 2004: Effects of elevated temperature and ultraviolet radiation on corals. (GPRA 6.2.3) Banks, K., C. Beaver, J. Bohnsack, R.E. Dodge, D. Gilliam, W. Jaap, B. Keller, V.R. Leeworthy, T. Matthews, R. Ruiz-Carus, D. Santavy, & R. Spieler. 2005. Status of the Coral Reef Ecosystems of Florida. In: NOAA Report: State of the US Coral Reef Ecosystems, 2004. Ed.: Andrews, K., L. Nall, C.Jeffrey, & S. Pittman. NOAA publ. Fisher, W.S., J. West, J. and R. Zepp. 2003. Coral reef ecosystems, In: Rogers, C.E., S.H. Julius, and J.M. West (Eds.) Problem Formulation Report for the Assessment of the Consequences of Global Change for Aquatic Ecosystems, Internal Report, Global Change Research Program, Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC, 2003. Santavy, D.L., J. Campbell, R.L. Quarles, J.M. Patrick, L.M. Harwell, M. Parsons, L. MacLaughlin, J. Halas, E. Mueller, E.C. Peters and J. Hawkridge. 2006. The Epizootiology of Coral Diseases of South Florida. U.S. EPA Publ. 600/R-05/145.

Publications

Journal Articles:

Aeby, G.S. and D.L. Santavy. (In press). Factors affecting the susceptibility of the coral Montastraea faveolata to black-band disease. Mar. Ecol. Prog. Ser. Anderson, S., R. Zepp, J. Machula, D. Santavy, L. Hansen, G. Cherr and E. Mueller. 2001. Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. In: 5th Annual NHEERL Symposium: Indicator and Risk Assessment. Human and Ecol. Risk Assess 7:1271-1282. Santavy, D.L., E. Mueller, E.C. Peters, L. MacLaughlin , J.W. Porter, K.L. Patterson and J. Campbell. 2001 Quantitative assessment of coral diseases in the Florida Keys: Strategy and methodology. Hydrobiologia.460:39-52. Santavy, D.L., E. Mueller, L. MacLaughlin, E.C. Peters, R. Quarles, J. Campbell, J.W. Porter, K. Sutherland and M. Barron. (In prep). Temporal Changes of Coral Health from reefs near Key West and the Dry Tortugas Coral Reefs. Santavy, D.L., J.K. Summers, V.D. Engle, and L.C. Harwell. 2005. The condition of coral reefs in south Florida using coral disease and causal bleaching as an indicator. Environ. Monitoring and Assess. 100:129-152. Patterson, K.L., J.W. Porter, K.B. Ritchie, S.W. Polson, E. Mueller, E.C. Peters, D.L. Santavy, and G.W. Smith. 2002. The etiology of White Pox, a lethal disease of the Caribbean Elkhorn coral, Acropora palmata. PNAS 99:8725-8730.

Presentations

Presentations made at International Professional Meetings:

Anderson, S., R. Zepp, J. Machula, D. Santavy, L. Hansen, G. Cherr, and E. Mueller. 2000. Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. Abstracts of 9th International Coral Reef Symposium, Bali, Indonesia, 23-27 October 2000. Abstract E2, p. 372. (poster)

F-2 Barron, M.G., D.L. Santavy, L. MacLaughlin, E. Mueller, E. Peters, B. Quarles, and J. Campbell. 2004. Temporal trends in the health of South Florida coral reefs. Society for Environmental Toxicology and Chemistry, International meeting, Portland, OR. Fisher, W.S. Large-scale environmental influences on the health of coastal and marine organisms. Proceedings of the U.S.-Russia Bilateral Conference. (In press) Fisher, W.S., D.L. Santavy, W.P. Davis and L.A. Courtney. Regional monitoring of coral condition in the Florida Keys. Proceedings of Monitoring Science and Technology. (In press) Fisher, W.S., D.L. Santavy, J.E. Rogers and R.G. Zepp. 2004. Coral responses to global climate and land use changes. Society for Environmental Toxicology and Chemistry, International meeting, Portland, OR. Fisher, W.S. 2004. Coral reef monitoring and indicator evaluation. Healthy Mesoamerican Reef Initiative Workshop, Miami, FL. Fisher, W.S. and W. Wiltse. 2005. Assessing coral condition: rapid, effective survey approach for coral reef monitoring and development of biocriteria. 24th Pacific Island Environmental Conference, Guam. Mueller, E., D.L. Santavy and E.C. Peters. 1998. Survey and quality assurance protocols for the assessment of coral disease distribution. Abstracts of the European Meeting, International Society for Reef Studies, Perpignan, France, 1-4 Sept. 1998. Mueller, E., D.L. Santavy, E.C. Peters, J.C. Porter, and L. MacLaughlin. 2000. The Epizootiology of Coral Diseases in the Florida Keys. Abstracts of 9th International Coral Reef Symposium, Bali, Indonesia, 23-27 October 2000. Abstract E7, p. 283. (Oral Presentation) Patterson, K.L., D.L. Santavy, J.G. Campbell, J.W. Porter, L.G. MacLaughlin, E. Mueller, and E.C. Peters. 1997. Coral Diseases in the Western Florida Keys, New Grounds and the Dry Tortugas. Am. Zool. 37(5): 13A. (Abstract) Patterson, K.L., D.L. Santavy, J.G. Campbell, J.W. Porter, L.G. MacLaughlin, E. Mueller , E.C. Peters. 1998. Coral Diseases in the Western Florida Keys, New Grounds, and the Dry Tortugas. Society for Integrative and Comparative Biology Annual Meeting, 1998, Jan. 3-7, 1998, Boston Mass. (Section on Coral Reef and Environmental Change-Adaptation, Acclimation or Extinction) Peters, E.C., and D.L. Santavy. 2001. Diseases of Corals: Research Progress, Reef Prospects. In: American Fisheries Society 2001 Annual Meeting, August 19-23, Phoenix, AZ. Invited presentation for the symposium, “The Role of Parasites and Disease in Aquatic Ecosystems,” organized by J. Frank Morado, NOAA, NMFS, Seattle, WA, and Elizabeth W. Davidson, Arizona State University, Department of Zoology, Tempe, AZ. (Abstract, oral presentation by E.C. Peters). Santavy, D.L. and J.G. Campbell. 1998. The Role of Coral Diseases and Anthropogenic Stressors on Tropical Marine Coral Reefs. In: SETAC 19th Annual Meeting, The Natural Connection: Environmental Integrity and Human Health. 15 - 19 Nov. 1998, Charlotte, NC. Abst. # 470, p.103. Santavy, D.L., L. MacLaughlin, J.W. Porter, J.G. Campbell, R.L. Quarles, and M. Parsons. 1999. An Upwelling Event in the Dry Tortugas During May 1998. Inter. Conf. On Sci. Aspects of Coral Reef Assessment, Monitoring and Restoration. April 14-16, 1999. Fort Lauderdale, FL. NCRI, Book of Abstracts: 170. Santavy, D. L., E. Mueller, E.C. Peters, J.W. Porter, and V. Engle. 1999. Quality Assurance Measures Associated with Coral Reef Monitoring. Inter. Conf. On Sci. Aspects of Coral Reef Assessment, Monitoring and Restoration. April 14-16, 1999. Fort Lauderdale, FL. NCRI, Book of Abstracts:170-171. Santavy, D. L., E. Mueller, J.W. Porter, E.C. Peters, L. MacLaughlin, J.G. Campbell, M. Parsons and. L. Becker. 1999. The Distribution and Frequency of Coral Diseases in the Florida Keys and the Dry Tortugas. Inter. Conf. On Sci. Aspects of Coral Reef Assessment, Monitoring and Restoration. April 14-16, 1999. Fort Lauderdale, FL. NCRI, Book of Abstracts:171. Santavy, D.L., E. Mueller, E.C. Peters, J.W. Porter and L. MacLaughlin. 2000. The Incidence of Coral Disease in the Florida Keys and Dry Tortugas. In: Ed. R.C. Cipriano, Abstracts 25th Annual Eastern Fish Health Workshop. Plymouth, MA., April 10-14, 2000. (Invited oral presentation made by Santavy). Santavy, D.L., E. Mueller, J.M. Hawkridge, L. MacLaughlin, J.W. Porter, and E.C. Peters. 2001. The Prevalence of Ten Coral Diseases in the Florida Keys and Dry Tortugas. 30th Scientific Meeting of the Association of Marine Laboratories of the Caribbean. June 24-29, 2001, La Parguera, Puerto Rico. Univ. of PR. Santavy, D.L., C.M. Woodley, and W.H. Walker. 2001. Coral Disease and Health Consortium: Partners for Preservation. EMAP Symposium, Pensacola Beach, FL. April 2001. F-3 Santavy, D.L., J.W. Hawkridge, R.L. Quarles, E. Mueller, and L. MacLaughlin. 2002. The Relationship between Water Quality and the Prevalence of Diseased Corals in the Florida Keys. European Meeting of the International Coral Reef Society. Sept. 2002, Univ. of Plymouth, Plymouth, UK. Santavy, D.L., E. Mueller, L. MacLaughlin, R. Quarles, J. Campbell, and E.C. Peters. 2005. The Prevalence and Distribution of “White Coral Diseases” in South Florida from 1997-2004. [Submitted to ERF 2005. (Invited oral presentation)]. Woodley, C.M., D.L. Santavy, W.H. Walker, A.W. Bruckner, D.W. Howard and S.M. McLaughlin. 2001. Coral Health and Disease Consortium: Finding Solutions. Organized by M. Rocco, Eastern Fish Health Workshop; Shepherdstown, WV, 23-26 April 2001.

Presentations made to Government and State Programs:

Fisher, W.S., R. Zepp, S.L. Anderson, D.L. Santavy, L.M. Oliver and J.E. Rogers. 2002. Coral reef responses to global climate change. U.S. Environmental Protection Agency Science Forum, Washington D.C. Fisher, W.S. 2003. Effects of global change on coral reef ecosystems. Office of Wetlands, Oceans and Watersheds, Washington, D.C. Fisher, W.S. 2004. Coral Condition Pilot Project. Florida Keys National Marine Sanctuary, Sanctuary Advisory Committee, Marathon, FL. Fisher, W.S. 2004. EPA/NOAA coral condition survey. Florida Keys National Marine Sanctuary, Technical Advisory Committee, Marathon, FL. Fisher, W., W. Davis, J. Campbell, L. Courtney, P. Harris, B. Hemmer, J. Patrick, M. Parsons, B. Quarles, D. Santavy. 2004. Global change effects on coral reef condition. EPA Science Forum, Washington, D.C. (poster and abstract). Fisher, W.S. 2005. Coral condition monitoring. St. Croix, U.S. Virgin Islands. Fisher, W.S., R.G. Zepp, J.E. Rogers, J.M. West, D.L. Santavy and L.M. Oliver. 2005. Elevated temperature and ultraviolet light condition of reef-building corals. U.S. Environmental Protection Agency Science Forum, Washington, D.C. Santavy, D.L. 1999. Coral Bleaching in the Florida Keys during 1998. Invited presentation to workshop entitled Major Problems Causing Coral Reef Decline at 2nd Meeting of US Coral Reef Task Force, March 5-6, 1999, Maui, Hawaii. Santavy, D.L. and E. Mueller. 2000. Epizootiology of Coral Disease in South Florida. Invited presentation to Science and Management Advisory Panels of FKNMS and Water Quality Protection Program for Overview of Research and Monitoring Programs. U.S. EPA Region IV and NOAA, Dec. 5-6, 2000; Marathon, FL. Santavy, D.L. 2001. Coral Disease in the Caribbean, and how the Coral Disease and Health Consortium (CDHC) can help. Invited presentation to 7th U.S. Coral Reef Task Force, at National Geographic Society, in Wash., D.C., Dec. 5, 2001. Santavy, D.L. 2002. Overview of the Coral Disease and Health Consortium (CDHC). Invited presentation at Workshop to develop Framework and Implementation Plan for CDHC. NOAA, NOS, Charleston, SC, Jan. 21-25, 2002. Zepp, R.G., and W.S. Fisher. 2003. Global change and coral reefs of the Florida Keys Health and Ecological Impacts of Climate Change Seminar. Office of Air and Radiation/Office of Research and Development. National Center for Environmental Assessment, Washington, D.C. Zepp, R.G., J.M. West and W.S. Fisher. 2003. Assessing the consequences of global change for coral reef ecosystems. US EPA Global Change Research Program Seminar, National Center for Environmental Assessment, Washington, D.C.

F-4 EPA United States Environmental Protection Agency Office of Research and Development Washington DC 20460 Official Business Penalty for Private Use $300

EPA/600/R-05/146 May 2006 www.epa.gov