4% pr^ll United States
Environmental Protection
#m Agency
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
1 United 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 forTropical 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
6TetraTech, 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.
-------
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 overtime. 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 ofthe 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 ofthe 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) ofthe area sampled; 15 ± 9% (662 ha) ofthe 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% ofthe colonies were diseased, with white pox affecting 41.4% ofthe monitored species. White pox and
aspergillosis were the most abundant diseases observed at sites, where greaterthan 20% ofthe 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 ofthe 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 ofthe 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.
-------
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 ComponentAnalysis 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 forthe study during the 1998-2000 surveys B-1
C. Pie charts presenting the percent species and disease composition
foreach geographic region for 1998-2000 surveys C-1
D. Tables presenting percent species and disease composition foreach
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 foursurveys 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 Aspergillosis 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 Aspergillosis 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
LR02 Loggerhead Reef2
LR03 Loggerhead Reef3 PR01
LR04 Loggerhead Reef4 PR02
LR05 Loggerhead Reef 5
LR06 Loggerhead Reef6 SR01
LR07 Loggerhead Reef 7 SR02
WH01 White Shoals 1 AR01
WH02 White Shoals 2 AR02
BK01 Bird Key Reef 1 MR01
BK03 Bird Key Reef 3 MR02
BK04 Bird Key Reef 4
BK05 Bird Key Reef 5 NG01
BK06 Bird Key Reef 6 NG02
BK07 Bird Key Reef 7 NG03
BK08 Bird Key Reef 8 NG04
BK09 Bird Key Reef 9 NG05
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
Elkhorn Reef 1
Pacific Reef 1
Pacific Reef 2
Sombrero Reef 1
Sombrero Reef 2
Alligator Reef 1
Alligator Reef 2
Molasses Reef 1
Molasses Reef 2
New Grounds 1
New Grounds 2
New Grounds 3
New Grounds 4
New Grounds 5
-------
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
Pontes 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 PeterW. Andersonwas 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 etal. 2003, Hughes etal. 2003, Wilkinson 1998,2000,2002). The rate and intensity of destruction for
coral reef habitats are greaterthan previously documented in modern orgeological records (Aronson and Precht
1997a, b, Hughes 1994, Hughes and Tanner2000, Pandolfi etal. 2003, Hughes etal. 2003). It is widely accepted
among the scientific community that pristine reefs no longer exist anywhere on earth (Pandolfi etal. 2003). Some
scientists are forewarning of ecological extinction for region-wide coral reefs in this century if current trends
persist (Gardner etal. 2003, Hughes etal. 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 year2030. A meta-analysis of263 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 (Gardneretal. 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 overtime. 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 (Gardneretal. 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 etal. 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 overthe 8-year
study.
Lower Keys coral coverage declined from 12% to 6% overthe same period.
1
-------
14%
In
0>
a 12%
o
0
g 1°%
3
u 8%
>i
| 6%
U)
a? 4%
3 2%
£
0%
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, Gladfelteret 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 etal. 2002, Porter and Meier 1992, Richardson etal. 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 etal. 1999a).
Diseased orseverely bleached corals often show little or no recovery and can be replaced by turf algae (Aronson
and Precht 1999, McClanahan etal.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-mentto 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 ofwhite-band
coral disease (Aronson and Precht 1997a, b, Bythell and Sheppard 1993, Gladfelter 1982, Gladfelteret al. 1977,
Miller et al. 2002), and more recently in the Florida Keys by white pox disease (Patterson etal. 2002) (Fig 2).
These losses have been so great that NOAA recently listed A. palmata and A. cervicornis as "threatened"
throughout theirgeographical range (Bruckner2003, Acropora Biol. Rev. Panel 2005). Anotherstudy 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.
t.trtu
7.4S
7>%
T.9S
TJi
i i i i i
199B 1M7 199& 1999 20£H> 2001 2002 2D03 2004
2
-------
1496
1997 "HA
V#6f
1994
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.
Year
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 Nino) 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 waterquality. Although it is clearthat new diseases are emerging
at an accelerated rate, cause and effect relationships are not well-established. Coral health and diseases have
not been critically orthoroughly characterized, and few baseline studies have been conducted to understand their
frequency and distribution.
-------
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 Biscayneto the DryTortugas,
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 (FMR11998). 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) ofthe area had between 0.4-
2.2% ofthe colonies affected by coral disease. In 28 ± 15% (1236 ha) ofthe area, 2-4% ofthe colonies were
affected by disease. Finally, 24 ±4% (1060 ha) ofthe 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
-------
I I Not Present
~ Present
85%+9
Figure 3. Distribution or areal extent forthe 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.
15%+9
50 "
40 J
$30
£ 20 ¦¦
10 <¦
0
j 2200
2000
1600
1300
1400 id
1200 |
¦¦ 1000 1
{ 800 1
600
400
200
0
>0-2
>2-1
>4-E >5-13
96 Colonies Diseased
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. Asurvey planned for early summer 2000 was not supported
by ship operations.
5
-------
Pulaski Shoals |1|
While ShoRls (Z|
*-=* Birr! Key
Reds p|
Lrjugtrliead
Ree*s (7)
r *
New Grounds |S|
Elfchorn Reef
r # (1)
irysforl R«*f (3|
IMdIshrbr R«1 |I|
* Allij*lof(2ji
f SnmhrnrD Koy (2\
Sand Kay >15)
Rock K«v 43)
E. Dry Rocks (3|
* Looa Key f3)
* * £, SBiWbo Reer j3j
W S-anibD Reef (A|
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.
n REEFS
! i ANO
W
IT
A
C-SV TORTUGAS
ifj/
NEiV GROUNDS
AO MILES
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 forthe 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 OSVAnderson 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 (FMR11998). 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 forthe 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 forthe 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 greaterthan 10cm in diameterwere 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 = 314.16.1 m*
\
Subsurface
Float
Figure 7b. Adiagram of the
radial arc used in the transect
method. AKevlar™ line is
marked in 2m increments and
rotated around a fixed pivot rod.
The radius of the arc is 10m.
Originally each 2m increment
was assessed.
Figure 7c. The radial arc transect
method was modified when it was
determined that only the outer 8-10m
segment or 113.1m2 was necessary to
estimate the parameters.
Radial Belt Transect Method
r = 8-10m; A= 113.1m2 ^
/
Subsurface
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 etal. 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 Wndows (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% ofthe colonies were diseased at a single sampling
period, including six sites during the summer 1998 sampling period (Table 1). Five ofthese six sites occurred
on reefs near Key West and in the Lower Keys, with white pox affecting the majority ofthe 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
%
Diseased*
Primary
Disease
% Primary Other Imp.
Diseases Diseases
Dry Tortugas
BK04
1999
Spring
28.336
PX
27.50
WB
Dry Tortugas
BK05
1999
Spring
27.378
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 ofthe 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. A1.7% 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
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
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 forthese 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 underthe 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.
RK03
3K01
5*02
SK06
WSD4
LK03
ER.Q1
Figure 8. Absolute number of colonies of Acropora palmata at sites showing
the greatest loss from spring 1998 to summer 2000.
12
-------
WH02
RK01
BK05
LR03
Figure 9. Absolute number of colonies of Aeropora cervicornis at sites showing the greatest
loss from spring 1998 to summer 2000.
35 30
31 ^ "I
10
WS04 \ M 13 10 16 10
WH01 Ml 10 n 15
1 13 12
SKQ1
WS03
r
cgs
¦
LK01 ^ ^ ^
LR03 ^ & /
"i 120
100
so
i
€0
e
o
40
o
£
20
0
1BK01 ^
Figure 10. Absolute number of colonies of Montastraea annularis complex at sites showing
the greatest loss from spring 1998 to summer 2000.
13
-------
! 1 Jj 111
# ' "RK01
^ ¦ BK01
^ 91 VP
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 theirdisease 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 forthe foursurvey 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
Variance
PC1 + PC2
Variance
PC1+PC2+PC3+PC4+PC5
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
Component
Survey
PC1
PC2
PC3
PC4
PC5
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 Pontes 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 ofthe diseases did not correspond to specific geographical regions, reef types, or water depths.
The distribution of each primary disease was mapped overtime 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 DryTortugas, 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 overthe course of the study were Acropora paimata, 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.
Ourstudy 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 ourstudies included the reeftypes and locations chosen. The CRMP included inshore patch reefs and
hard bottom habitats in the FKNMS, whereas ourstudy 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.
Ourstudies 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 clearspatial
correlations between disease distributions and geographical regions, reeftypes, 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 importantto 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 stressordistributions that cannot be evaluated
using other approaches. Associations between coral health metrics and stressordistributions 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.
References
Acropora Biological Review Team. 2005. Atlantic Acropora Status Review Document. Report to National
Marine Fisheries Service. Southeast Regional Office. March 3,2005.155p +App.
Aeby, G. and D.L. Santavy. (in press). The role of reef fish in the transmission dynamics of black-band disease
in the Florida Keys. MEPS.
Antonius, A. 1981. The "band" diseases in coral reefs. In: E.D. Gomez, C.E. Birkell and R.W. Buddemeier,
R.E. Johannes, J.A. Marsh, and R.T. Tsuda (eds), Proc. 4th Inter. Coral Reef Symp. 2: 7-14.
Antonius, A. 1985. Coral diseases in the Indo-Pacific: A first record. P.S.Z.N.I. Mar. Ecol. 6:197-218.
Antonius, A. 1988. Distribution and dynamics of coral diseases in the Eastern Red Sea. In: J.H. Choat, D.
Barnes, M.A. Borowitzka, J.C. Coll, P.J. Davies, P. Flood, B.G. Hatcher, D. Hopley, P.A. Hutchings, D.
Kinzey, G.R. Orme, M. Pichon, PF. Sale, P. Sammarco, C.C. Wallace, C. Wilkinson, E. Wolanski, and O.
Bellwood (eds), Proc. 6th Inter. Coral Reef Symp. 2:293-299.
Aronson, R.B. and W.F. Precht. 1997a. Degradation ofstaghorn coral populations in Belize: A novel event. Ann.
Meet. Soc. Integrat. Comp. Biol. Boston, Mass. (Jan. 3-7, 1998), Am. Zool. 37:12A.
Aronson, R.B. and W.F. Precht. 1997b. Stasis, biological disturbance, and community structure of a Holocene
coral reef. Paleobiology 23:326-346.
Aronson, R.B.. and W.F. Precht. 1999. Herbivory and algal dynamics on the coral reef at Discovery Bay,
Jamaica. Limnol. Oceanogr. 45:251-255.
Beaver, C.R., W.C. Jaap, J.W. Porter, J. Wheaton, M. Callahan, J. Kidney, S. Kupfner, C. Torres, S.H. Wade,
and D. Johnson. 2004. EPA/NOAA Coral Reef Evaluation and Monitoring Project, 2003 Executive Sum-
mary. Report of Florida Fish and Wldlife Conservation Commission. 3pp.
Bruckner, A.W., and R.J. Bruckner. 1997. Outbreak of coral disease in Puerto Rico. Coral Reefs 16:260.
Bruckner, A.W., R.J. Bruckner and E.H. Wlliams. 1997. Spread ofa black-band disease epizootic through the
reef system in St. Ann's Bay, Jamaica. Bull. Mar. Sci. 61:919-928.
17
-------
Bruckner, A.W. 2000. Black-band disease (BBD) ofscleractinian corals: Occurrence, impacts, and mitigation.
University of Puerto Rico, Mayaguez. PhD Dissert. 286pp.
Bruckner, A.W. 2003. Proceedings of the Caribbean Acropora Workshop. NOAATech. Memo. NMFS-OPR-
24A.
Bythell, J. and C. Sheppard. 1993. Mass Mortality of Caribbean Shallow Corals. Mar. Poll. Bull. 6: 296-297.
Cheney, D. P. 1975. Hard tissue tumors in scleractinian corals. Adv. Exp. Med. Biol. 64:77-87.
Clarke, K.R. and R.N. Gorley. 2001. PRIMER v5: User manual/tutorial. PRIMER-E, Plymouth, UK, 91 pp.
Dustan, P. 1977. Vitality of reef coral populations off Key Largo, Florida: Recruitment and mortality. Environ.
Geol. 2:51-58.
Dustan, PA. and J. Halas. 1987. Changes in reef-coral communities of Carysfort Reef, Key Largo, Florida:
1974-1982. Coral Reefs 6:91 -106.
Dustan, P. 1999. Coral Reefs Under Stress: Sources of Mortality in the Florida Keys. Natural Resources
Forum, 23:147-155.
Florida Fish and Wildlife Conservation Commission (FFWCC). 2005. Coral Reef Evaluation and Monitoring
Project, 2004 CREMP Executive Summary, May 2005. Report Fish and Wldlife Research Institute. 12 pp.
Florida Marine Research Institute (FMRI). 1998. Benthic Habitats of the Florida Keys. FMRI Technical Report
TR-4. St. Pete, FL 53 pp. CD-ROM.
Gardner, T.A., I.M. Cote, J.A. Gill, and A. Grant. 2003. Long-Term Region-Wde Declines in Caribbean Cor-
als. Sci. 301: 958-960.
Garzon-Ferreira, J. and D. L. Gil, 1998. Another unknown Caribbean coral phenomenon? Reef Encounters
24:10.
Gladfelter, W.B., E.H. Gladfelter, R.K. Monahan, J.C. Ogden, and R.F. Dill. 1977. Environmental studies of
Buck Island Reef National Monument, St. Croix U.S. Virgin Islands. Spec. Rept. Nat. Park. Ser. US Dept.
Int. 137pp.
Gladfelter, W.B. 1982. White band disease in Acropora palmata: implications for the structure and growth of
shallow coral reefs. Bull. Mar. Sci. 32:639-643.
Goreau T.J., J. Cervino, M. Goreau, R. Hayes, M. Hayes, L. Richardson, G. Smith, K. DeMeyer, I. Nagelkerken,
J. Garzon-Ferrera, and others. 1998. Rapid spread of diseases in Caribbean coral reefs. Rev. Biol. Trap. 46,
Suppl. 5:157-171.
Harvell C.D., K. Kim, J.M. Burkholder, R.R. Colwell, PR. Epstein, D.J. Grimes, E.E. Hofmann, E.K. Lipp,
A.D.M.E. Osterhaus, R.M. Overstreet, J.W. Porter, G.W. Smith, and G.R. Vasta. 1999. Emerging Marine
Diseases-Climate Links and Anthropogenic Factors. Science 285:1505-1510.
Holden, C. 1996. Coral disease hot spot in the Florida Keys. Science 274:2017.
Hughes, T.P 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Sci-
ence 265:1547-1551.
Hughes, T.P. and J.E. Tanner. 2000. Recruitment failure, life histories, and long-term decline of Caribbean
corals. Ecol. 81:2250-2263.
Hughes, T.P.,A.H. Baird, D.R. Bellwood, M. Card, S.R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Gulberg,
J.B.C. Jackson, J. Kleypas, P. Marshall, M. Nystrom, S.R. Palumbi, J.M. Pandolfi, B. Rosen, and J.
Roughgarden. 2003. Climate Change, Human Impacts, and the Resilience of Coral Reefs. Science 301:929-
933.
Jaap, W.C., J.W. Porter, J. Wheaton, K. Hackett, M. Lybolt, M. Callahan, C.Tsokos, G. Yanev, and P. Dustan.
2000. Coral Reef Monitoring Project Executive Summary. EPA Science Advisory Panel, Key Colony Beach,
Dec. 5-6, 2000. FMRI.
Jaap, W.C., J.W. Porter, J. Wheaton, K. Hackett, M. Lybolt, M. Callahan, C. Tsokos, G. Yanev, and P. Dustan
2001. Coral Reef Monitoring Project Updated Executive Summary 1996-2000. Steer. Comm. Meet. Aug.
1, 2001. FMRI Tech. Rep., St. Pete., FL.
Johnson, R.A. and D.W. Wchern. 1983. Applied Multivariate Statistical Analysis. Prentice-Hall, Inc. Englewood
Cliffs, NJ. 594pp.
Kuta, K.G. and L.L. Richardson. 1996. Abundance and distribution of black band disease on coral reefs in the
northern Florida Keys. Coral Reefs 15:219-224.
18
-------
Loya, Y., G. Bull, and M. Pichon. 1984. Tumorformations in scleractinian corals. Helgol Meeresunters. 37:99-
112.
McCarty, H. B. and E.C. Peters. 1998. The Coral Disease Page©, http://ourworld.compuserve.com/homepages/
mccartyandpeters/co raldis.htm.
McClanahan, T.R. and N.A. Muthiga. 1998. An ecological shift in a remote coral atoll of Belize over 25 years.
Environ. Conserv. 25:122-130.
McClanahan T.R., R.B Aronson, W.F. Precht and N.A. Muthiga. 1999. Fleshy algae dominate remote coral
reefs of Belize. Coral Reefs 18:61-62.
McClanahan, T.R., B.A. Cokos and E. Sala. 2002. Algal growth and species composition under experimen-
tal control of herbivory, phosphorus and coral abundance in Glovers Reef, Belize. Mar. Poll. Bull. 4:441-
451.
Miller, M.W., I.B. Baums, D.E. Williams, and A.M. Szmant. 2002. Status of candidate coral, Acropora palmata,
and its snail predator in the upper Florida Keys National Marine Sanctuary: 1998-2001. NOAA Technical
Memorandum, NMFS-SEFSC-479, 27.
Mueller, E., D.L. Santavy, and E.C. Peters. 1998. Survey and quality assurance protocols for the assessment
of coral disease distribution. Inter. Soc. for Reef Studies, Perpignan, France, 1-4 Sept., 1998. Abst.
Europ. Meet.
Nagelkerken, I., K. Buchan, G.W. Smith, K. Bonair, P. Bush, J. Garzon-Ferreira, L. Botero, P. Gayle, C.D.
Harvell, C. Heberer, K. Kim, C. Petrovic, L. Pors and P. Yoshioka. 1997a. Widespread disease in Carib-
bean sea fans: I. Spreading and general characteristics. Proc. 8th Inter. Coral Reef Symp. 1:679-682.
Nagelkerken, I., K. Buchan, G.W. Smith, K. Bonair, P. Bush, J. Garzon-Ferreira, L. Botero, P. Gayle, C.D.
Harvell, C. Heberer, K. Kim, C. Petrovic, L. Pors and P. Yoshioka. 1997b. Widespread disease in Caribbean
sea fans: II. Patterns of infection and tissue loss. MEPS 160:255-263.
Pandolfi, J.M., R.H. Bradbury, E. Sala, T.P. Hughes, K.A. Bjorndal, R.G. Cooke, D. McArdle, L. McClenahan,
M.J.H. Newman, G Paredes, and R.R. Warner. 2003. Global Trajectories of the Long-Term Decline of
Coral Reef Ecosystems. Sci. 301:955-958.
Patterson, K.L., J.W. Porter, K.B. Ritchie, S.W. Poison, 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.
Peters, E.C., J.J. Oprandy and P.P. Yevich. 1983. Possible causal agent of "white band disease" in Caribbean
acroporid corals. J. Inv. Path. 41:394-396.
Peters E.C. 1984. Asurvey of cellular reactions to environmental stress and disease in Caribbean scleractinian
corals. Helgol Meeresunters 37:113-137.
Peters, E.C., J.C. Halas and H.B. McCarty. 1986. Calicoblastic neoplasms in Acropora palmata, with a review
of reports on anomalies of growth and form in corals. J. Natl. Cancer Inst. 76:895-912.
Peters E.C. 1992a. Diseases of other invertebrate phyla: Porifera, Cnidaria, Ctenophora, Annelida, Echinoder-
mata. In: Couch J.A. Fournie J.W. (eds) Pathobiology of Marine and Estuarine Organisms Boca Raton, FL:
CRC Press. Pp 388-444.
Peters, E.C. 1992b. The role of environmental stress in the development of coral diseases and micro-parasite
infestations. Amer. Zool. 32:960.
Porter, J.W. and O.W. Meier. 1992. Quantification of loss and change in Floridian reef coral populations. Amer.
Zool. 32: 625-640.
Porter, J.W., S.K. Lewis, and K.G. Porter. 1999. The effect of multiple stressors on the Florida Keys coral reef
ecosystem: A landscape hypothesis and a physiological test. Limnol. Oceanogr., 44 (3, part 2): 941-949.
Porter, J.W. and J. Tougas. 2001. Reef Ecosystems: Threats to their biodiversity. Encyclopedia of Biodiversity.
Volume 5: 73-95. Academic Press.
Porter, J.W., V. Kosmynin, K.L. Patterson, W.C. Jaap, J.L. Weaton, K. Hackett, M. Lybolt, C.P Tsokos, G.
Yanev, D.M. Marcinek, J. Dotten, D. Eaken, M. Patterson, O.W. Meier, M. Brill, and P. Dustan. 2002.
Detection of coral reef change by the Florida Keys coral reef monitoring project. In: J.W. Porter and K.G.
Porter (eds). The Everglades of Florida Bay, and Coral Reefs of the Florida Keys An Ecosystem Sourcebook
27: 749-769. CRC Press.
Richardson, L.L. 1993. Red band disease: a new cyanobacterial infestation of corals. Amer. Acad, of Under.
Sci. 13:153-160.
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. Trap. 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. Trap. 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.
Rutzler, 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.
Rutzler, 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 Bias 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 Bias, 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.ora.
Wlkinson, 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.
Wlkinson, C.R. 2000. Status of coral reefs of the world: 2000. Australian Institute of Marine Science. Townsville,
Australia. 363pp.
Wlkinson, 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
Loggerhead Reef2
LR02
10-15
24° 37.799'
82° 56.172'
Loggerhead Reef 3
LR03
~6
24° 38.0877'
82° 55.3679'
Loggerhead Reef4
LR04
~8-11
24° 38.107'
82° 54.980'
Loggerhead Reef 5
LR05
10
24° 39.031'
82° 54.899'
Loggerhead Reef6
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
24° 38.532'
82° 53.807'
White Shoals 2
WH02
15-16
24° 38.518'
82° 53.812'
Bird Key Reef 1
BK01
33
24° 36.703'
82° 52.239'
Bird Key Reef 3
BK03
19
24° 37.204'
82° 52.004'
Bird Key Reef 4
BK04
8
24° 37.237'
82° 52.042'
Bird Key Reef 5
BK05
8
24° 37.236'
82° 52.039'
Bird Key Reef 6
BK06
10
24° 37.868'
82° 52.706'
Bird Key Reef 7
BK07
10
24° 37.865'
82° 52.706'
Bird Key Reef 8
BK08
10
24° 37.225'
82° 52.146'
Bird Key Reef 9
BK09
10
24° 37.216'
82° 52.146'
Pulaski Shoals 1
PS01
27
24° 41.645'
82° 46.293'
Sand Key 1
SK01
20
24°27.141'
81°52.591'
Sand Key 2
SK02
11
24°27.1190'
81°52.650'
Sand Key 3
SK03
29-35
24° 27.087'
81°52.799'
Sand Key 4
SK04
30-35
24° 27.087'
81°52.799'
Sand Key 5
SK05
4
24°27.18'
81°52.718'
Rock Key 1
RK01
30-37
24027.211'
81°51.602'
Rock Key 2
RK02
15-19
24° 27.298'
81°51.582'
Rock Key 3
RK03
4
24° 27.353'
81°51.526'
Eastern Dry Rocks 1
ED01
8-18
24° 27.575'
81°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
24° 28.8577'
81°43.0774'
Western Sambo 3
WS03
24-30
24° 28.776'
81°42.861'
Western Sambo 4
WS04
9
24° 28.799'
81°42.968'
Western Sambo 5
WS05
4
24° 28.842'
81° 43.069'
Eastern Sambo 1
ES01
25
24°29.513'
81°39.674'
Eastern Sambo 2
ES02
15-20
24°29.552'
81°39.687'
Eastern Sambo 3
ES03
10
24° 29.532'
81°39.919'
Looe Key 1
LK01
45
24° 32.543'
81°24.877'
Looe Key 2
LK02
10-25
24° 32.747'
81°24.349'
Looe Key 3
LK03
4
24° 32.819'
81°24.361'
Sombrero Reef 1
SR01
23-25
24° 37.550'
81°06.508'
Sombrero Reef 2
SR02
9-23
24° 37.573'
81°06.568'
Alligator Reef 1
AR01
25
24° 50.788'
80° 37.248'
Alligator Reef 2
AR02
15-20
24° 50.762'
80° 37.286'
Molasses Reef 1
MR01
55-75
25° 01.057'
80° 21.840'
Molasses Reef 2
MR02
12-22
25° 01.104'
80° 22.062'
Carysfort Reef 1
CR01
15-22
25° 13.461'
80° 12.493'
Carysfort Reef 2
CR02
15-25
25° 13.318'
80° 12.607'
Carysfort Reef 3
CR03
5-8
25° 13.496'
80° 12.562'
Elkhorn Reef 1
ER01
10
25°21.807'
80° 09.925'
Pacific Reef 1
PR01
45
25°21.735'
80° 08.370'
Pacific Reef 2
PR02
15-22
25° 22.225'
80° 08.387'
DryTortugas
Key West
Lower Keys
Middle Keys
Upper Keys
Biscayne
National Park
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 Name
Disease
Abbreviation
Species Affected in Tropical Western Atlantic
References
Aspergillosis
Black-Band Disease
Dark Spot Disease
Hyperplasia
Patchy Necrosis/
White Pox
Red-Band Disease
White Plague I
White Plague II
White Band Disease 1
AS
BB
DS
HP
PX
RB
WP1*
WP2
WB1
White Band Disease 2 WB2*
Yellow Blotch Disease YB
* Did not find in any of our surveys.
Gorgonia spp.
Diploria strigosa, D. labyrinthiformis,
Colpophyllia natans, Montastraea
cavernosa, M. annularis, M. franksi, M.
faveolata, Siderastrea siderea,
Gorgonia spp.
C. natans, M. annularis (species complex),
S. siderea, Stephanocoenia intersepta
D. strigosa, Dichocoenia stokesii
Acropora palmata
Gorgonia spp., C. natans
C. natans, Mycetophyllia ferox
D. stokesii, Agaricia agaricites, A. larmarki,
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
A. cervicornis, A. palmata, A. prolifera
A. cervicornis
M. faveolata, M. annularis
Nagelkerken et al.1997a,b; Smith et al. 1996
Antonius 1981; Rutzler et al. 1983; Rutzler &
Santavy 1983
Garzon-Ferreira & Gil 1998
Cheney 1975; Loya et al. 1984; Peters et al.
1986
Bruckner & Bruckner 1997; Patterson et al.
2002
Rutzler & Santavy 1983; Richardson 1993
Dustan 1977
Richardson et al.1998a, b
Gladfelter 1982; Peters 1984, Peters et al.
1983
Richie & Smith 1998
Santavy et al. 1999a
-------
Appendix C
Pie charts presenting the percent species and disease composition
for each geographic region for 1998-2000 surveys.
C-1
-------
ifl u'l O < O u. -J g; 5 V.
UQQP OEEEEEw««
is*************
1?
a ^ |
« % S
# s* 3*
¦ ¦ ¦
O e B z > z s
5£o532li:Jia=sin
BS«l£2SSESww«
O - Q
a S
C-2
-------
Dry Tortugas
Percent Disease
35.51%
Spring 1998 Summer 1998
% Healthy
1% BB
/ rS % PX WB /164V.
/ ¦% RM 96 0™' / > 22%
4.49% -— ^0 58D«n d. qw* ^^MM-34/p
\ —GM% %WP 4'93/\ -0.07%
^ —0.64% % WP YB \
0
1
CO
% OTH '0.60%
YO.37%
x0.
Spring 1999 Summer 2000
% Healthy 2&%
% AS /r 025%
!/ o.:
1 yns
I % DS / Jp1,17%
4.51% -J-08% %px 4&1% -0-10%
\ rP-56% - yyg
/0.15% RR J^Q.35%
/ f0.05% "%BB new / y- 0.05%
9549% / X0,21% ¦%IDS A / ^-1,17%
1.93%
•™ ^ X ^82#
5 VQ.05%
% YB
% Healthy
% AS
¦ %BB
¦ % DS
%WB
%WP
% W5 YB
% OTH
% Healthy
¦ % AS
¦ % BB
%CS
¦ % DS
¦ % HP
¦ % PX
% px^m
¦ % RB
% WB
% WP
-------
New Grounds
1.7G%'
2.79%
fl.,20%
Spring 1
1 06%
10.39%
O.M%
31 %%
Q SS%
Percent Species
52 55V.
¦%
CfOAT
%
dlab
%
DSTO
%
DSTR
m%
GOR
%
MAM IV
%
MCAV
¦%
MFER
%
MLAM
¦ %
SBOU
%
SMIC
¦%
SSID
Summer 1998
S,1.4% 0L3TK
3,19%-v4'^
D.32%-\ \
123%-
24.56%-
CI 32%-
0.97%
258%
11.15%
4163%
Summer 2000
¦ %
CNAT
%
DLflB
%
DSTO
%
DSTR
9%
GOR
%
W AN Pi
%
MCAV
¦%
MFER
%
MLAM
%
seou
%
SMIC
SSID
# 73%'
6.
26%-y
.3.4SVV
n H\%-^
1H
J
1 62 /-Df.70%
¦ I 39%
¦1D67%
¦IS.72%
I % CN AT
% dl te.
% DSTO
% DSTR
I % GOR
% MCAV
I % M PER
I % SBOU
% SMI C
I % SSID
-------
New Grounds
Percent Disease
Spring 1998
Summer 1998
99.02%
D.98%
«
9&ar%
0.9B%
% Healthy
1% HP
1.13%:
0
1
cn
/0.16%
% Healthy
Y 0.32%
%fiS
1-0.32%
¦ % HP
-0.32%
¦ % RW
%WFYB
Summer 2000
99.54% /
n ^ % Haalthiy
0,46% I -0.4$%
\ %WB
-------
0
1
CD
Spring 1998
0 17%
I a
Q.2«%
9.44%
25.07%
1,21%
Spring 1999
20.93%
a 10%
18,03%
<162%
1.76%
D.83%
21%"^
121%-f
9,04%
2,30%
0.73%
29.64%
Key West
Percent Species
24.85%
0.94%
0.94%
1389%
¦ % ACER
*%APAL
¦ %CNAT
% DLAB
%DSTO
% D5TR
¦ % GOft
%MANN
%MCAV
% M DAN
¦ %MFER
%ML AM
¦ %SBOU
%SM»C
¦ %55Ei
¦ % ACER
¦ % APAL
¦ % GNAT
% DLAB
% DSTO
% DSTR
¦ % GQR
% MAAIN
% MCAV
% MDAN
¦ % MFER
¦ % SBOU
% SMIC
¦ % SKID
Summer 1998
1.35%
19,76%
&G7%
0.54%-
0 1S%
1.17%—;
0.39%
C'.36%
fl.OJ'.D
3.07%
11.36%
0.99ft-,
26,$0%
Summer 2000
2.43%
ria.fi 3%r 0.30%
Q 3fl%-
Q. 20%-
23.36%
0.70%
0.20%
0.60%'
O.SD',y,
— 1.71%
1.21%
29.71%
i % «;er
l%0PAL
1% CNAT
% DLA3
% DSTQ
% DSTR
1% GOR
% M ANN
% MCAV
% MDAN
1 % MFER
% MUV.l
% SBOU
% SMIC
I %S SID
) % ACER
1% APAL
I % CNAT
% DLAB
% D$TO
% DSTR
)% GOR
% MANN
% MCAV
% MDAN
I % MFER
% ML AM
% SBOU
% S MIC
I % S 5ID
-------
Key West
Percent Disease
Spring I<>98
94.09%
/
5.91%
0
1
0.66%
06%
0.06%
-2.62%
0.11%.
0,72%
0.99%
0,50%
% Healthy
% AS
%DS
l%HP
%FX WB
l%RM
%WB
%WP YB
%OTH
Summer IWS
07.20%
1.53%
0.36%
1.71%
1Z80%
>3.79%
¦^1.17%
VQ.09%
V2.9S%
V 1.08%
0,09%
% Healthy
% AS
I % 68
% DS
%PX WB
I % RB
I % RM
% WP
% WP YB
%OTH
Spring 1999
93.16%
6.&4%
/ 2.07%
-"0.73%
^1.07%
-0,52%
-1.24%
^0.31%
X0,10%
% Healthy
% AS
% DS
%PX
% WB
%WP
% YB
% OTH
Summer 2000
94 66%
/0.30%
A151%
5.34%
0.60%
D.10%
m
x^O.20%
- \\£
\X0J
*¦1.5
30%
81%
.51%
% Healthy
% AS
1% BB
% DS
1% HP
% PX WB
1% RB
% WB
% OTH
-------
Spring 1998
4.19%
23.36%
0
1
00
0 2G%
4.7114
1.14%
3.66%
X
0.79%^f^
I.DSTi
13 61 4
1 B.D6%
26.96%
Lower Keys
Percent Species
I % CN AT
%DIJ56
%DSTO
% DSTR
l%GOR
% MANN
%MCAV
% MOAN
1%MFER
%5BQU
% SMIC
l%SS©
19.66%
0.65%
0S5%-\\
0.85%—
0.43%
5 S : i
1*K? V
Summer 1998
13.54%
20.09%
1.31%
2.21%
0.22%
0.44%
o&a%-s^
b,A4%-^
~ 2.87%
7 2&%
11.26%
Spring 1999
13.56%
3.421'.
1.71%
5.56%
5.98%
24.79%
¦%
L
¦%
CNAT
¦ %.
DL^B
%
DSTO
%
DSTR
m%
GOR
%
M4NN
%
MCAV
%
MDAN
¦%.
MFER
MLAM
¦%
SflOJ
¦%
SSID
30.02%
I % APAL
I % ON AT
%PLAE
% DSTO
% DS TR
I %GOR
% MWJN
% MCAV
% MDAfvS
I % MFER
% S BCHU
% S MIC
I % 5 SID
-------
Lower Keys
Percent Disease
Spring 1998
Fall 1998
93.19%
6.61%
0
1
CD
2.65%
1,05%
1.57%
1.57%
% Healthy
% AS
I % BB
%DS
%WPYB
TB.81%
21.19%
/9.4S%
[ 152%
/9.71%
<-0,22%
^ 0.44%
%Hearthy
% AS
%DS
%PXWB
%WP
%WP YB
Spring 1999
I % Healthy
93.59% "%BB
, 2.56% B % DS
^0,43% Plf
\ ^-0.43%
\ ^1.71% I % RB
% WP
-------
5 S s
O IE
. I55Sigi>Q
9Sd88S3£Sli^8£8
5fl
4>
"O
t/s
"3
a»
a
c«
c
q>
o
S*
Q>
£ 9
e
e
5^
s
8
¦
DC
z
§
1
i
X
ai
1
3
o
o
Q
O
V
a
¦J.
_
c
5
M
O
e
2
?
E
E
«
W
cm
*
a?
if
3?
s*
a*
¦
¦
¦
SfpK^SjoiiQ
JiflcflOUtQgtfj
:7i p C v I J ti uo u"j
Lfc
C-10
-------
Middle Keys
Percent Disease
Spring 1998
Summer 1998
96.64%
BS.16%
3.36%.
-3.36%
% Healthy
% AS
/ "0.81%
184% "0,61%
\ -0.61%
% Healthy
% AS
% DS
% WP YB
O
Spring 1999
97.54%
2,46%\^
•0.52%
¦1.64%
% Healthy
% DS
% WP
-------
Spring 1*198
1.3m
1.63%~\ I 1,36%
i6.oe%
t.91%
2.1B%'
0
1
l-O
127%
0.54%
5.93%
64.58%
Upper Keys
Percent Species
¦%flp^t
¦ % CNAT
% DLffl
1.9«4-\
% DSTO
Q49%"0
%DSTft
\
¦ %GOft
Z4S%—
%mann
i
% WCAV
% MDAN
%seou
% SMIC
¦ % SSID
16.6™
Summer 1998
1.23%
Ui% J
1.23%
u 25%
Spring 1999
1.92%-
1.15%
1 35%
1.35%
23.46%
D.3fl%
3.65%
4.23%
0 19%-v\
QlSS%-^
0 19%"
61.35%
I % APAL
%DLAB
% DSTQ
% DSTR
I % GQR
% MAMM
% MCAV
% WDAN
% MFER
% MLAM
%5BOU
% SMIC
I % SSID
55,20%
I % APAL
I %CWAT
%DLm
%DSTO
%DSTR
I % GQR
%MANN
% W CAV
%MDAN
%SMiC
I % SSID
-------
Upper Keys
Percent Disease
S prin« 1998
Summer 1998
35,93%
14.17%
0
1
CO
"I '.44%
/0.54%
~\~0.27%
X1J
.91%
% Healttiy
% AS
% PXWB
1% RB
% WP YB
90.20%
9.80%
/5.BB%
r 1.95%
0.74%
0.49%
0.74%
\
% Heatthy
% AS
%. OS
% PX WB
% WP YB
% OTH
Spring 1999 %Hoa.thy
%AS
\ '-0.19%
\ n>O.30%
\H:
\-n ¦
%DS
%PX
a, / ^QM%
95.77% / |^1 J5% ¦ % RB
4.23%^ C%3\%y? % WB
%WP
1a/ VPL
38%
¦0,19% % OTH
-------
Biscayne National Park
i iij
Spring 1998
t2£3%
0.74% /
H70f£
1 .iJFl'L
- -in ,v
0
1
Ji.
7Q.SB%
Percent Species
Summer 19*>8
0.C5V, 9-1,2%
,%APAL
% DLAB ^ X\,
* DSTO
I^GOR
% M ANN
14 MCAV
%5BOU
% 5 MIC
I*.', sat)
Spring 1999
14.33%
D.33%
D.98S
¦J W%
69 71V.-
0,3fl%
IV.APAL
% DLAB
14 D5TO
% DSTR
114 GOR
V. MCAV
14 50 OU
% swe
I % S-SID
6 gS',
O.SS^.4
a.89%
1 mvi
0.39%
1.1
a
1% APfi-
% DSTO
114 G OR
% MANN
% MCAV
14 SBOU
14 SMIC
114 SSID
87 20%
-------
Biscayne National Park
Percent Disease
Spring 1998
Summer 1998
SI. 23%
8.77%
0
1
cn
^4.91%
^yQ.35%
^2.61%
,—0.35%
~~ 0.35%
% Healthy
% AS
%DS
%PX
%WB
% WP YB
96.09%
351%
/1.9W,
yO.33%
-0.33%
0-0.65%
*-o.6w;
% Healthy
% AS
% DS
% PX WB
%W
% WP Y B
Spring 1999
99.40%
/ % Healthy
0.60% ( —0.60% a/ ftC
\ % AS
-------
-------
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
DryTortugas
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
-------
rn
i
hJ
Zk
PS01
LRU 7
WH01
WH02
2?
LRU 6
BK06
I overhead „ m BK07
LR04
LR02 "*¦ /_•yy
# BK05
LR01 BK04
¦ « fl #
BK03
BK01
4 Miles
Hospital Ki'\
I I Reef
I I I.and
Figure 1: Base Map of Dry Tortugas snrvey sites. Each site sampled is denoted as black circle (^)) with the site code.
-------
Spring 1998
Summer 1998
&
BK06
BK07
S
BK05
BK03
-------
Spring 1998
Summer 1998
BK06
BK07
0
BK05
BK03
Spring 1999
&
WHO 2
BK06
-S4
BK07
*
BK05
BK03
3&
S3
BK01
BK06
BK07
S
BK05
BK03
38?
^ftO
Summer 2000
WH02
BK06
BK07
BK05
BK03
as
to
Figure 3: Survey sites in Dry Tortugas that had Dark Spots Disease present by survey periods. Each site with disease has (9).
-------
Spring 1998
Summer 1998
r-KPi
TO
usr
"^7 «M1
)*£X
Lfi"
Ljga • • BHOJ
fli *^£*
i mi
mm
SOT
v-00 3NPi
. "CI" i
'-/e-v.
Spring 1999 ^,- -
< ' V >-*' fcj
^aSSfcr
LAM
*
I.RO» BRQB
LRU • * DKDT
LW *^LW A WH
LRM -m;j
BKD1
BgDl *
®ss
G \/
G^XjVT?
J0L ,
LW ««,
L^C *W^a
MM) 3- BKCit
LAM # + HKD7
Vv flr.
i» - i*
X .sr U*
<*" > i£>
H «L^1F
fBOl
J .
LgT
Summer 2000
r
FOk
iv-'V^F ,
I n»
LKE-i r_.KOC
. • •»'
LjJ,
aw.SF
Iwrafe'Sy "jsp
¦KQ1
$&W
k5^^* a _jq ^ry
b'ipr« 4- Survey sites in Dry Tortugss that had While Pox Disease present by survey periods, Each sile with diseuse ha* ( i
-------
Spring 1998
Summer 1998
m
i
CD
BK06
BK07
s
BK05
BK03
Ss
Spring 1999
WH02
BK06
BK07
BK05
BK03
BK01
01
BK06
BK07
,0
BK05
BK03
Summer 2000
PS01
z?
BK06
BK07
BK05
BK03
Figure 5: Survey sites in Dry Tortugas that had White Band Disease present by survey periods. Each site with disease has (®).
-------
Spring 1998
Summer 1998
m
i
BK06
BK07
s
BK05
BK03
Ss
Spring 1999
WH02
BK06
BK07
*
BK05
BK03
BK01
01
BK06
BK07
BK05
BK03
Summer 2000
z?
BK06
BK07
BK05
BK03
Figure 6: Survey sites in Dry Tortugas that had White Plague Type II Disease present by survey periods. Each site with disease has (•).
-------
N
Key West
A
O *4
f
WS02
RK01
Reef
I I Land
4 Miles
Figure 7: Base Map of Key West survey sites. Each site sampled is denoted as black circle (4B0 with the site code.
-------
Spring 1998
SK05 RKftJ E£2£*
SK*SK04jRKIJ2»^D3
a a a * Ful>4
•••• RKQ1
WSD2 WSflg
WS04
SKttl SK&3
WS03
Summer 1998
¦ "
WS02 WS05
HWSD4
5K05 REQ3. fcS£''»
# * ED03
J8® ''
WS02
Spring 1999
C®3s
SR05 RKD3
® AESLffn JEtKpji
l
SK* SK« f™'
.if
WSC2 '«VS1K
• •
»WS04.
Summer 2000
ws&a
WSD2 *"VSfl5
WSfU
SK05 RKQ3
WSD3
SK«2 SK045 ^
mmm • EDM
~••• RK01
SK01 SKW
Figure 8; Survey sites in Key West thai had Aspergillus is presem by survey periods. Each site with disease Has 4^1.
-------
m
i
O
Spring 1998
WS02
ED04
Summer 1998
SK01 SK03
RK01
WS02
ED04
RK01
SK03
Spring 1999
T'VIl
b.
Summer 2000
WS02
ED04
WS02
RK01
SK01 SK03
SK01 SK03
RK01
ED04
Figure 9: Survey sites in Key West that had Dark Spots diseases present by survey periods. Each site with disease has (9).
-------
Spring 1998
WS02
ED04
SK01 SK03
RK01
Summer 1998
WS02
ED04
RK01
Spring 1999
T'VIl
b.
Summer 2000
WS02
ED04
WS02
RK01
SK01 SK03
ED04
SK01 SK03
RK01
Figure 10: Survey sites in Key West that had White Pox disease present by survey periods. Each site with disease has ( ).
-------
Spring 1998
SK01 SK03
RK01
WS02
ED04
Summer 1998
WS02
ED04
RK01
Spring 1999
Summer 2000
WS02
ED04
WS02
RK01
SK01 SK03
SK01 SK03
RK01
ED04
Figure 11: Survey sites in Key West that had White Band disease present by survey periods. Each site with disease has ( ).
-------
Spring 1998
WS02
ED04
SK01 SK03
RK01
Summer 1998
WS02
ED04
RK01
Spring 1999
WS02
SK01 SK03
RK01
ED04
Summer 2000
WS02
SK01 SK03
RK01
ED04
Figure 12: Survey sites in Key West that had White Plague Type II disease present by survey periods. Each site with disease has ( ).
-------
-------
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. Nail, 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. Poison, E. Mueller, E.C. Peters, D.L. Santavy, and G.W.
Smith. 2002. The etiology of White Pox, a lethal disease ofthe 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. Wltse. 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. Porterand 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. Oliverand 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 ofthe 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
-------
*» E PA
ited States
if iron mental Protection
ency
ce of
Research and Development
Washington DC 20480
Official Business
Penalty for Private Use
$300
EPA/600/R-05/146
May 2006
www.epa.gov
I
------- |