Coral Disease Handbook
Guidelines for Assessment,
Monitoring & Management
1
Editors: Laurie J. Raymundo, Courtney S. Couch and C. Drew Harvell
Contributing authors: Laurie J. Raymundo1, Courtney S. Couch2, Andrew W. Bruckner3, C. Drew Harvell4,
Thierry M. Work5, Ernesto Weil6, Cheryl M. Woodley7, Eric Jordan-Dahlgren8, Bette L. Willis9, Yui Sato9, Greta S. Aeby10.
Cover photos: (top) Lyle Vail, Lizard Island Research Station (A facility of the Australian Museum), (bottom) Ernesto Weil,
University of Puerto Rico.
1University of Guam, 2Cornell University, 3NOAA Coral Reef Conservation Program, 4Cornell University, 5USGS-National Wildlife Health Center,
6University of Puerto Rico, 7NOAA Center for Coastal Environmental Health and Biomolecular Research, 8Universidad Nacional Autónoma
de México, 9James Cook University, 10Hawaii Institute of Marine Biology.
The Coral Reef Targeted Research & Capacity Building for Management (CRTR) Program is a leading
international coral reef research initiative that provides a coordinated approach to credible, factual
and scientifically-proven knowledge for improved coral reef management.
The CRTR Program is a partnership between the Global Environment Facility, the World Bank, The University
of Queensland (Australia), the United States National Oceanic and Atmospheric Administration (NOAA) and
approximately 50 research institutes and other third-parties around the world.
Coral Reef Targeted Research and Capacity Building for Management Program, c/- Centre for Marine
Studies, Gerhmann Building, The University of Queensland, St Lucia, Qld 4072, Australia
Tel: +61 7 3346 9942 Fax: +61 7 3346 9987 Email: info@gefcoral.org Internet: www.gefcoral.org
ISBN: 978-1-9213-17-01-9
Product code: CRTR 001/2008
Editorial design and production: Currie Communications, Melbourne, Australia, June 2008.
© Coral Reef Targeted Research and Capacity Building for Management Program, 2008.
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
1
Contents
2
1. The Objectives and Scope of This Manual
7
2. A Decision Tree for Describing Coral Lesions in the Field
17
3. Confirming Field Assessments and Measuring Disease Impacts
33
3
4. Assessment and Monitoring Protocols
47
5. Detecting and Assessing Outbreaks
65
4
6. Management Issues and Actions
75
References
85
Acknowledgements
95
5
Appendices
99
Glossary and acronyms
Regional contact list of coral disease experts
Supplementary disease and compromised health photographs
Data sheets currently used for assessment and monitoring
Supplementary disease descriptions
6
Authors
121
3
4
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Foreword
Our research careers began in Discovery Bay, Jamaica, in the mid 1970s, where we both studied the
behavior of coral reef organisms, rather than the corals themselves. At that time, living coral covered
70 percent of the bottom, and no one worried about the long term persistence of the reefs, even
though the reefs were clearly impacted by people via severe overfishing. Quite simply, we took the
reefs for granted.
That sunny confidence turned out to be total y unfounded. In 1980, Hurricane Al en, a category
five storm, struck and turned much of the reef into a rubble ground. However, reefs routinely get hit
by hurricanes and typhoons, so they should have recovered. But in 1982 the sea urchin Diadema
antillarum was decimated by an as yet unidentified pathogen, and losing this last remaining major
grazer contributed to the overgrowth of corals by seaweeds throughout the region. By 1995, coral
cover stood at less than 10 percent.
But the loss of grazers was not the only thing happening to these reefs. A more subtle and gradual
but no less important killer was also taking its toll the white band disease of the branching staghorn
and elkhorn corals. These two species used to be so common that as students we were taught about
the "Acropora cervicornis zone" and the "Acropora palmata zone". Now both species are listed as
endangered under the Endangered Species Act, having lost over 90 percent of their numbers in the
ensuing decades. Like the elms and chestnuts of US forests, they have largely vanished due to disease.
And they are not alone white plague, yel ow band, black band, and many others have since been
documented as major reef killers, not only in the Caribbean but in the Pacific as well. For most of these
diseases we still do not know the causative agent nor the extent to which pollution and increased
sea surface temperatures may be contributing to disease outbreaks or affecting the ability of corals to
recover from infections. Yet progress is being made, and simply reliably recognizing and documenting
these syndromes and their patterns of infection are important first steps in addressing this problem.
This handbook makes it much easier to do just that. Designed for managers, it outlines procedures
for describing signs, measuring disease impacts, monitoring disease outbreaks, assessing causes, and
managing reefs to minimize losses due to disease. As the authors note, information and expertise on
coral disease are inadequate relative to the scale of the problem. This handbook helps managers not
only to document and manage disease on the reefs they are responsible for, but also al ows them to
contribute to our scientific understanding of this grave threat.
Nancy Knowlton
Marea Hatziolos
Sant Chair in Marine Science
Environment Department
National Museum of Natural History
The World Bank
Smithsonian Institution
5 5
6
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
1
Chapter 1
The Objectives and Scope of This Manual
In this chapter you will find:
A general introduction to infectious diseases in corals
what they are, why they are a growing problem, and
what is currently understood about them.
A look at the current global patterns and
hotspots in regard to coral reef diseases.
A summary of the impact of ocean warming and
poor water quality on coral reef diseases.
7
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
The Objectives and Scope of This Manual
L. Raymundo and C. D. Harvell
1.1 The state of coral reefs and the purpose of this manual
Coral reefs are the most diverse and among the most productive ecosystems on earth. Mil ions of
people directly rely on the harvest derived from coral reefs as their major source of protein and income.
In addition, the revenue coral reefs earn from tourism, recreation, education and research is of major
importance to their local and national economies. And final y, current research in such areas as natural
products chemistry suggest that coral reefs support an unknown number of organisms that may prove to
be of major benefit in the treatment of critical human diseases. Yet, in spite of their obvious importance,
reefs continue to be impacted by "the big four" human activities that threaten their sustainability:
climate change, land- and marine-based pol ution, habitat degradation and over-fishing.
Many of these impacts have obvious and immediate effects, such as smothering or fragmentation of
coral to the point of total mortality. However, some effects, such as those from chemical pol utants,
waste or excess nutrients, are more insidious, and their impacts may be more difficult to understand
and quantify. One phenomenon which has recently gained the attention of coral reef scientists and
managers is disease. Diseases affecting corals, particularly in the Caribbean, have increased in both
frequency and severity within the last three decades and caused major community shifts on Caribbean
reefs. Yet we are only beginning to understand enough about drivers of disease outbreaks to consider
management actions.
While diseases affecting corals have increased since the 1970's, there are few individuals throughout
the world trained to recognize diseases on coral reefs. In addition, there are many areas where there
is absolutely no information regarding the status of coral health and disease.
Written for coral reef managers, this manual aims to fil the knowledge gap by bringing together
what is currently known about coral diseases, how they are studied, and what options are available
for managing them. We first present some general concepts about disease to put this manual and its
scope in perspective. We then present the most current descriptions of known coral diseases, with
information to assist in their field identification. Subsequent chapters are devoted to confirming field
identifications, quantifying impacts of disease to coral communities, assessing disease on reefs, and
setting up monitoring programs. We then provide information as to what is currently understood
regarding disease outbreaks and how to track and study them. We end with guidelines on management
practices and suggestions for where to obtain further information and direction.
Included in the appendices are categories of additional information which we hope will be useful.
Underlined terms throughout the text indicate words listed in the glossary in Appendix 1.
1.2 What is disease?
Diseases are a natural aspect of populations, and are one mechanism by which population numbers
are kept in check. For the purposes of this manual, we wil use the term disease to mean "any
impairment to health resulting in physiological dysfunction". Disease involves an interaction between
a host, an agent, and the environment. The focus of this manual is infectious biotic diseases; those
that are caused by a microbial agent, such as a bacterium, fungus, virus, or protist, that can be spread
between host organisms and negatively impact the host's health. Other forms of disease that impact
corals may be considered abiotic diseases; they do not involve a microbial agent but impair health,
nonetheless. Examples may be those caused directly by environmental agents such as temperature
stress, sedimentation, toxic chemicals, nutrient imbalance and UV radiation. In addition, noninfectious
biotic diseases are not transmitted between organisms, though they may be caused by a microbial
agent. For example, certain microbes secrete a toxin which damages the host animal or plant.
A good example of this is botulism; toxins released by the bacterium Clostridium botulinum cause a
8
non-infectious but deleterious disease in organisms that consume it.
1.3 Why study infectious diseases of corals?
1
Pathogenic microorganisms, having very short reproductive cycles, evolve more rapidly than
multicellular organisms. They are also continually transported to new environments in the oceans by
runoff, shipping vessels, aquaculture, and changing ocean currents. Therefore, we can expect that
new diseases will continue to emerge. Recent examples of emergent infectious diseases on land that
are threats to humans and wildlife include AIDS, bird flu, and SARS. Under specific conditions, disease
levels may exceed a population's ability to cope, resulting in rapid and widespread mortality.
A disease is considered an outbreak
when the rate at which new hosts
become
infected
increases.
Technical y, an outbreak is defined
as R >1. R is the ratio of new
0
0
infections to existing infections (see
Chapter 5 and Appendix 1).
Over the past three decades, coral
reefs worldwide have experienced
major changes in structure and
function due to both anthropogenic
and natural impacts (15-18). Virtually
all of the most pervasive threats
impacting coral reef ecosystems,
including land-based and marine
pol ution, overfishing, global climate
change, and ocean acidification,
Figure 1.1 Reef in Hanalei Bay, Kauai, Hawaii, which has experienced have been suggested as synergists
extreme sediment stress, resulting in reduced coral coverage and the or facilitators of infectious disease
proliferation of the zooanthids. Photo: G.S. Aeby
(Figure 1.1). Infectious disease in
corals has increased in frequency
and distribution since the early 1970's when a white band disease outbreak took a heavy tol on
Caribbean acroporids. There has since been an exponential increase in numbers of reported diseases,
host species and locations with disease observations. This rate of change is not normal, and has
resulted in significant loss of coral cover.
Currently, the study of coral disease
is in its infancy and those who
devote their time and expertise to it
are virtual y "learning as they go
along". However, through the
experience of others who study and
manage diseases in wildlife, farmed
and cultured animals and plants,
and even human populations, we
can adapt methodologies and
strategies to coral diseases that
have been successful in other
medical arenas.
Figure 1.2 Students being trained in coral disease assessment methods in the
Zaragosa Marine Protected Area, Central Philippines. Photo: L. Raymundo
9
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
This manual aims to address an urgent need: to update coral reef managers regarding our current
understanding of the basic ecology of coral diseases. This will help improve monitoring efforts and
aid in proper recognition of coral diseases and related issues of coral health (Figure 1.2). Although it
is important to remember that detailed laboratory investigation remains essential for proper disease
diagnosis and a complete understanding of the impacts to the coral host, we also hope that this
manual will help increase the number of individuals able to provide information on the state of health
of the world's reefs. By studying disease and establishing baselines prior to a crisis, we can arm
ourselves with a better knowledge of appropriate management options for a given situation.
1.4 The emergence of coral disease
Damage to coral by abiotic and biotic factors acting alone or in synergy have led to a global reduction
in coral cover (6,18,22-24). To date, the most infectious syndromes of coral for which a causative
agent has been isolated involve bacteria (26). In addition to the loss of coral tissue, disease can cause
significant changes in reproduction rates, growth rates, community structure, species diversity and
abundance of reef-associated organisms (28,29). While an unprecedented increase in coral disease
has been well-documented in the Caribbean over the last decade (11,25,30-32), and some argue
that climate warming has driven part of the increase in damaging outbreaks (Causey, pers. comm.),
much less is known about the status of disease throughout the Indo-Pacific (26). However, preliminary
surveys in Australia (33), the Philippines (34), Palau (35), Northwestern Hawai an Islands (36), American
Samoa (37), the central Pacific (38), and East Africa (39,40), have revealed significant and damaging
new diseases in all locations surveyed. Many of these are suspected or confirmed as infectious.
What has prompted this emergence
of coral disease? Current research
suggests that humans may not
only be introducing new pathogens
into the oceans though aquaculture,
runoff, human sewage, and ballast
water, but may also be exacerbating
existing opportunistic infections
due to stressors such as poor water
quality and climate warming
(16,41). Climate warming is now
established as an important factor
in some current outbreaks
(23,32,42). Some experts, such
as Bil y Causey (Superintendent,
Florida Keys National Marine
Sanctuary), argue that stressful
Figure 1.3 Coral bleaching within the Basdiot Marine Protected Area,
warming events may have driven
Philippines, summer 2006. Photo: K. Rosell
even more outbreaks than we have
detected to date (Causey, pers.
comm.). Because reef-building corals have a narrow range of thermal tolerance (between 18°C and
30°C), they are extremely susceptible to temperature stress. It is well known that corals "bleach" (lose
their symbiotic zooxanthellae) at high temperatures (Figure 1.3). The coral bleaching observed
worldwide fol owing the 1998 El Niño was the most massive and devastating recorded up to that
point (43), only to be exceeded by another bleaching event in Australia in 2002. The latter part of 2005
brought widespread bleaching to the Caribbean, caused by the largest warm thermal anomaly in 100
years (Eakin, pers. comm.). The Caribbean thermal anomaly of 2005 was immediately fol owed by
outbreaks of white plague, yel ow band disease (42) and white patch disease (32).
10
Our working hypothesis is that, in some cases, the death of coral during hot thermal anomalies is
exacerbated by opportunistic infectious pathogens whose virulence is enhanced by increased
1
temperatures. Changing environmental conditions could also influence disease by altering host-
pathogen interactions. Increased temperatures could affect basic biological and physiological
properties of corals, particularly their ability to fight infection, thus influencing the balance between
potential pathogen and host (44). In addition, the pathogens themselves could become more virulent
at higher temperatures (45). This is particularly challenging to study because of the complexity of
the coral holobiont. The animal itself consists of the coral polyp, the unicel ular algae (zooxanthel ae)
with which it co-exists in a mutualistic relationship, and a bacterial community existing within the
surface mucous layer (SML), the coral tissue itself and its skeleton. This is very similar to the human
holobiont that has its own unique and critical gastrointestinal mucosal microbiota which produces
essential vitamins and amino acids not otherwise available to the human host. The coral SML contains
a complex microbial community that responds to changes in the environment in ways that we are just
now beginning to appreciate (46,47). The normal microbial flora within the mucus layer may protect
the coral against pathogen invasion, and disturbances in this normal flora could lead to disease (48).
The massive introduction of non-indigenous pathogens, which may occur with aquaculture and bal ast
water release, could also disturb the microbial community (16).
1.5 What is our current state of knowledge?
The current, and rather urgent, focus of research is the biology of microorganisms that can be
pathogenic to corals. We are working diligently to develop new molecular and biomedical tools to
identify specific agents and their origins, and determine the role of these agents in causing disease
in corals. In Figure 1.4, we present five diseases with documented causal agents. The process by
which causation is verified is explained in detail in Chapter 3. Undoubtedly as we learn more, we
wil continue to find that certain diseases may be caused by more than one microorganism, though
whether this may be a matter of location, seasonality or other environmental parameters is unknown.
For instance, the species comprising the microbial consortium associated with black band disease
appears to vary with different geographic locations (49). Similarly, there is evidence that Caribbean
yellow band disease (YBD) is caused by a consortium of bacteria (50). Because of inherent difficulties in
the process, proving causation may be based on relatively few corals or disease events. For example,
the demonstration of causation for both white plague type II and white patch disease are based
on tests of relatively few corals, each from a single location or outbreak event. Our vision is that
coral disease managers wil eventual y be equipped with molecular diagnostics to reliably verify the
identity of a given infectious micro-organism. Thus the process of continuing to verify these agents is
important (51).
11
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
White plague II
White band II
White pox*
Aspergillosis
Bacterial bleaching
Diploria
Acropora
Acropora
Gorgonia
Oculina
labyrinthiformis
cervicornis
palmata
ventalina
patagonica
Aurantimonas
Vibrio carchariae
Serratia marcescens1 Aspergillus sydowii2 Vibrio coral i lyticus
coralicida
(bacterium)
(bacterium)
(fungus)
(shown) and
(bacterium)
V.shiloi (bacterium)
Figure 1.4 The five coral diseases for which Koch's postulates have been fulfilled, showing disease, host coral and microbial
pathogen. The classic way to prove a microorganism causes disease is to satisfy Koch's postulates. A microorganism must be
isolated from a diseased individual. That "isolate" is then used to infect a healthy individual. The same disease must develop,
and the same organism must be isolated from the new infection. This classic method is a tough chal enge in the face of
unculturable marine microorganisms and polymicrobial syndromes, requiring molecular approaches.
* Original y named white pox, but field signs for this disease are now termed "white patch disease"; this name wil be used in
this book.
1 source: http://commtechlab.msu.edu/sites/dlc-me/zoo/microbes/serratia.html
2 source: http://www.cdc.gov/ncidod/dbmd/mdb/images/aspergillos.JPG
Harvell et al. (26). Photos by: A. Bruckner and E. Weil.
The last decade has been a time of intense research into causative agents of coral disease. Though
we still lack evidence showing the origin of any coral disease, the role of specific pathogens in causing
various diseases, their pathogenesis, and agent-host interactions, significant progress is being made in all
of these areas. Some infectious agents that cause disease in marine animals, such as that of aspergil osis
of octocorals (Figure 1.5) and toxoplasmosis in sea otters, are thought to originate on land.
Others, such as viruses inadvertently introduced from
shrimp or abalone farms to wild populations (McCal um,
pers. comm.), originate in aquaculture farms (16). Tracking
the origins of pathogenic agents might reveal sources that
can be control ed before being introduced into the ocean.
For example, Serratia marcescens is a ubiquitous bacterium
introduced into coastal waters via sewage that may be the
cause of white patch, a disease that affects Acropora
palmata (52). There is a very real risk, therefore, that human
activities may inadvertently introduce environmental
stressors and potential pathogens to marine communities,
and wil continue to do so unless our understanding of
Figure 1.5 Caribbean sea fan Gorgonia ventalina
with multiple aspergillotic lesions. Photo: E.Weil
such dynamics improves.
1.6 What are the global patterns and where are the hotspots?
The Caribbean has been referred to as a "hot spot" for disease because of a rapid emergence of new,
extremely virulent diseases, increased frequency of epizootic events, and rapid spread of emerging
diseases among new species and regions. At least 82 percent of coral species in the Caribbean are
host to at least one disease (21).
In the Pacific, the threat of coral diseases has been regarded as minor, due to the large distances
12
between reefs and island nations, fewer potential sources of pathogens, a paucity of epizootiological
studies and few recorded outbreaks. However, there were relatively few comprehensive detailed
studies of coral disease in the Pacific prior to 2000, and most available information came from a handful
1
of locations and researchers. As efforts increase to document coral diseases from more locations
within the Pacific, the lists of species affected by disease, locations where diseases are reported, and
prevalence of those diseases, are steadily increasing. It is now apparent that certain sites in the
Pacific show a rather high prevalence of disease, and reports of outbreaks that kill a large number
of colonies in a relatively short time suggest that the threat of disease impacts can no longer be
considered minor.
1.7 What do we know about environmental drivers and stress?
An understanding of the influence that the environment plays in disease outbreaks could guide the
development of useful management strategies (Figure 1.6). In this section, we summarize what is
known about the relationship between particular environmental drivers and disease outbreaks.
As with most aspects of the management of infectious disease in a marine setting, it is a work in
progress and it is critical to keep in mind that al infectious syndromes are different and may respond
in different ways to environmental change. However, identifying the factors that control the most
important infectious syndromes is a key management strategy.
Environment
i.e. changing water
temperature
Normal environment
Compromised environment
Increased pathogen range
and virulence
Host immuno-competent
Host immuno-suppressed
Adequate melanization
Decreased melanization
and ameobocyte activity
and amoebocyte activity
Pathogen
Normal resistance
Lowered resistance
Healthy Host
Immuno-suppressed host
Melanization
Amoebocytes
Figure 1.6 A schematic model showing the effect of an environmental impact changing temperature on a gorgonian
coral infected by fungus. The healthy octocoral on the left is immuno-competent and is thus able to mount a normal immune
response (melanization and amoebocyte activity). The diseased and dying octocoral on the right shows decreased melanization
and suppressed amoebocyte activity, and is thus susceptible to attack by microorganisms. Modified from Mydlarz et al. (53).
Photos by: C Couch and E. Weil.
13
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Temperature
Outbreaks of some diseases are enhanced by ocean warming anomalies. An increase in disease
fol owing warming events may occur because corals are less able to fight disease while under
temperature stress, or because pathogens are more virulent at higher temperatures. In three known
cases where the pathogen can be cultured separately (Aspergil us sydowi , Vibrio shiloi and Vibrio
coralliilyticus), pathogen growth and/or virulence increased with rising temperature, up to an optimal
temperature (45,54-57).
Seasonal patterns in disease prevalence in the northeastern Caribbean provide further support for
a link between warming ocean waters and disease outbreaks. Recurrent outbreaks of two virulent
and damaging diseases, white plague and yel ow band, have developed during seasons of highest
water temperatures for the past four years on Puerto Rican reefs (Weil unpubl. data; Hernández-
Delgado unpubl. data) and in the US Virgin Islands (42,58). Immediately following the peak of the
2005 bleaching event, the most devastating recorded in the North-eastern Caribbean, outbreaks of
white plague, yel ow band and white patch (32) were even more extensive in these areas and some
outbreaks continued through 2007.
On the Great Barrier Reef, coral disease prevalence increased from winter to summer in al major
families of coral (33). Prevalence increased fifteen-fold in acroporids, twelve-fold in favi ds and
doubled in pocil oporids in summer surveys. In addition, prevalence of three coral diseases increased
significantly in summer surveys, with skeletal eroding band increasing more than two-fold, black band
and other cyanobacterial infections more than three-fold, and white syndrome more than 50-fold.
Further work to document a link with temperature was carried out using disease prevalence surveys
spanning 500 km of a latitudinal gradient along the Great Barrier Reef. In 1998, the Australian Institute
of Marine Science's Long-Term Monitoring Program began to systematical y monitor white syndrome
(WS), which affects more than 15 coral species, including dominant plating acroporids. Divers
conducted annual coral disease surveys on 47 reefs from 1998 to 2004 to quantify the number of
cases of WS. Using a weekly four km data set of temperature values derived from the NOAA AVHRR
Pathfinder (a radiation-detection imager that can determine sea surface temperature), a significant
relationship was detected between the frequency of warm temperature anomalies and the incidence
of white syndrome, indicating a relationship between temperature and disease. Interestingly, this
relationship also depended on a high degree of coral cover, as would be expected for transmission
of an infectious agent between hosts (23).
Links between outbreaks or increasing prevalence and warm temperature have thus been detected
for black band disease, aspergillosis, yellow band disease, white patch disease and white syndrome.
The list will likely grow as the data set expands. We still need to understand the mechanism operating
in each syndrome: can we distinguish whether increased disease transmission during ocean warming
is caused by compromised host immunity or the expansion of geographic range of microorganisms?
Understanding these dynamics should aid in developing management strategies during periods of
stressful temperatures.
Water Quality
As human populations continue to increase, nutrients, terrigenous silt, pol utants and even pathogens
themselves can be released into nearshore benthic communities (59). While the link between
anthropogenic stress and disease susceptibility is currently poorly understood, one hypothesis is
that coral disease is facilitated by a decrease in water quality, particularly due to eutrophication and
sedimentation. It is an urgent management priority to understand the link between water quality and
infectious coral disease, because this is a local factor we can have some hope of managing.
14
Although corals are able to grow in high-nutrient water (60), recent evidence suggests a synergistic
effect between elevated nutrients and disease. High nutrients (N, P) were associated with accelerated
1
disease signs in both yel ow band disease- and aspergil osis-infected corals in field manipulations
(61), and in black band disease (62), although high nutrients alone were not associated with increased
tissue loss in healthy corals. This is consistent with the findings of Kuntz et al. (63) who observed rapid
tissue shedding in healthy corals exposed to elevated carbon sources, but little effect on corals of
elevated N and P. Thus, corals seem to thrive under high nutrient conditions, but the combination of
an active infection and elevated nutrients increases the disease progression rates of some syndromes.
It is unclear whether this effect is due to an impact on host resistance or a positive effect on pathogen
growth or virulence.
Sedimentation offers yet another
chal enge
to
host
disease
resistance. The impacts of
terrigenous sedimentation on
nearshore communities are visible
and well-documented; corals
inhabiting silted reefs often
possess large patches of dead,
exposed skeleton bordered by
apparently receding margins of
healthy tissue (Figure 1.7). While
coral tissue mortality was previously
assumed to be the result of direct
smothering, microbial agents may
also contribute. Early work by
Hodgson (64) identified silt-
associated bacteria as a possible
Figure 1.7 Tissue loss in a massive Porites in Palau caused by silt deposition.
cause for necrosis in sediment-
Photo: A. Croquer
damaged corals, as antibiotic-
treated water reduced the amount
of tissue damage in experimental y-silted corals. More recently, opportunistic terrestrial pathogens
(the soil fungus Aspergillus sydowii and the human enterobacterium Serratia marcescens) have been
demonstrated as causal agents for two diseases currently impacting dominant corals in the Caribbean
(52,65). Thus, terrigenous silt may not only cause physical stress for shallow, benthic organisms such
as corals, but may also act as a pathogen reservoir.
This evidence suggests that anthropogenic stressors are linked with disease severity in complex ways.
It is important to establish and quantify such linkages, as these factors may be possible to mitigate
via improved reef management and land-use practices. The challenge lies in demonstrating these
linkages in the complex system of diverse stressors acting upon the coral holobiont.
15
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Box 1.1
Coral Reef Targeted Research: The Coral Disease Working Group
A Global Environment Facility/ World Bank initiative, the Coral Reef Targeted Research and
Capacity Building for Management Program created six working groups to address the current
alarming rate of reef decline by improving gaps in our knowledge of coral reef management
(see www.gefcoral.org). As the Coral Disease Working Group for this project, the goals of our
program are to fil critical information gaps about infectious coral reef disease, build capacity
to study and monitor disease internationally, and help develop solutions for managing and
conserving reef ecosystems. The cooperative research efforts are guided by our international
team of microbiologists, ecologists and physiologists towards these ends. Working out of four
Centers of Excellence, our research priorities include:
· assessing the global prevalence of coral disease;
· investigating the environmental drivers of disease;
· identifying the pathogens that cause disease; and
· understanding the coral's ability to resist disease.
We are also testing specific hypotheses about climate and anthropogenic changes that threaten
coral reef sustainability. By building the capacity to manage these ecosystems, we hope to
enhance reef resilience and recovery, worldwide.
16
Chapter 2
A Decision Tree for Describing
Coral Lesions in the Field
2
In this chapter you will find:
A standardized procedure that will enable you to describe
lesions in corals that encompasses the range of variation
in colony morphology and geographic location.
Guidance for organizing and collecting data, particularly if
you encounter a lesion that is unfamiliar or undescribed.
Descriptions and photos of commonly encountered lesions in
the Western Atlantic, Indo-Pacific, Red Sea and East Africa.
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
A Decision Tree for
Describing Coral Lesions in the Field
L. Raymundo, T. Work, A. Bruckner and B. Willis
2.1. Introduction
Disease is the absence of health and is usually manifested by the presence of a lesion (a morphologic
abnormality). Three important points should be kept in mind when reading this chapter:
1. Diseases can have many causes; some of these are infectious (such as bacteria, parasites,
or viruses) and others are not (such as genetically-based or toxicant-induced disorders).
2. The typical sign of a diseased coral is a lesion; a manifestation of disease that may not provide any
clue regarding causation.
3. Some lesions in corals may have known causes that are not attributable to disease, though they
result in the coral's health being compromised. For example, fish bites and crown-of-thorns starfish
feeding scars should be characterized as predation; lesions associated with breakages may be
caused by storms or anchor damage and should be characterized as disturbance; and lesions
caused by aggressive interactions between corals or between corals and other sessile organisms
should be characterized as competition. Al can lead to tears and breaks in the tissue and partial
mortality, and can stress the host coral. In suspected disease cases, it is often impossible to
determine the cause of the lesion (and, therefore, the cause of the disease) without additional
laboratory or experimental efforts (as discussed in Chapter 3).
Given the diversity of coral morphologies and the potential for environmental stressors to influence
the progression of a disease, lesions may take on gross morphologies that differ between species
or that vary temporally or spatially. The rapid growth of literature on coral diseases in the past few
decades, in the absence of a standardized approach to describing lesions in corals, has resulted
in a proliferation of disease names and confusion among researchers. The need for a standardized
approach to describing lesions in corals is clear and urgent.
In this chapter we present a scheme that will allow you to describe lesions in corals in a manner that
can be interpreted by others regardless of colony morphology or geographic location. This scheme
also permits you to determine whether or not a lesion has a cause that can be readily determined
with a high degree of confidence after a rapid assessment of the scene (i.e. predation, competition
such as algal overgrowth, invertebrate gal s). There are two compel ing reasons for including lesions
of known cause in your surveys:
1. Certain organisms that interact with corals may be vectors of disease or create potential entry
wounds for infectious agents. Recording observations of such associations can lead to greater
understanding of how a particular disease is spread, and thus is vital y important.
2. Documentation of such interactions indirectly provides information on ecosystem health.
For example, a great number of lesions caused by smothering from silt may suggest that the reef is
affected by land-based sedimentation. Reef managers could make use of this information to work
with land managers and local legislators to improve land use practices because of a documented
effect on coral health.
18
2.2 A decision tree for field-based assessments
of diseases and compromised states of health
Presented here is a decision tree that outlines the steps needed to properly describe lesions in corals,
applicable to reefs worldwide (Figure 2.1). It also provides a method for organizing information and
offers a list of the types of data that are useful to collect if you encounter a lesion that is unfamiliar,
or if a cause cannot be determined after an investigation of the scene. In such cases, it is critical
to systematical y describe what you see using the attached decision tree as a guide. Remember
you wil not be able to diagnose the cause of such lesions in the field without additional laboratory
work. Chapter 3 provides information on sample col ection should you wish to submit specimens to a
laboratory for analyses to prove causation.
2
After the decision tree, in sections 2.3 and 2.4, you wil find descriptions of commonly encountered
lesions in the Western Atlantic and Indo-Pacific/East Africa/Red Sea respectively. These examples can
be used to identify the diseases currently known for each region (additional information on these can
be found in Appendix 6). Note that for each disease, a description of the lesion (compiled using the
decision tree as a guide) is provided as an example.
For diseases that may be new or emerging, Figure 2.1 provides a guide for describing the lesions
observed. In all cases, it is absolutely essential to identify and record the host affected to genus (and
species, if possible). Some diseases affect very few coral species while others appear to affect a wide
range of hosts. Such information is invaluable in assessing impacts of a disease on a reef community,
and is also important when evaluating the potential causes of disease in the laboratory.
Using the decision tree
1. Follow steps from 1 to 4 to identify and properly describe lesions in corals.
2. Use steps 4a
4e to describe a lesion of unknown cause and determine whether it can be
classified as any of the diseases described in section 2.3 (Western Atlantic) or 2.4 (Indo-Pacific,
East Africa and Red Sea).
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
1. Lesion Present
2. Host affected
3. Scene investigation: known cause?
4a. Lesion type
3a. No record:
3b. Yes record:
Tissue loss (refer to 4b 4e)
Fish bites/skeletal damage
Growth anomaly (refer to 4b, 4c, 4e)
Gastropod bites
Tissue discoloration (refer to 4b, 4e)
Galls, tube formers
Overlying pigmented material
Algal abrasion/overgrowth
(refer to 4b 4e)
COTS predation
4b. Lesion pattern
Sediment damage
Focal
Multifocal
Diffuse
4c. Rate of progression
Rapid
Moderate Not progressing
(= acute)
(= subacute)
(= chronic)
4e. Lesion Color
4d. Lesion margin (=band):
Color:
Thickness:
Shape: linear,
Border:
describe
measure
annular, irregular
discrete, diffuse
Figure 2.1 A global y-relevant decision tree used to identify known causes of lesions and describe lesions of
unknown cause. Al lesions denoted as white represent bare, exposed skeleton; green symbolizes secondary
algal colonization of bare skeleton. Other colors represent examples of commonly-encountered lesions or
20
legion margins characteristic of specific diseases.
1. Lesion Present
2. Host affected
3. Scene investigation: known cause?
2.3 Field assessments of Western Atlantic
diseases and compromised health states
1. Tissue loss: known predation by fish
and invertebrates resulting in compromised health
4a. Lesion type
3a. No record:
3b. Yes record:
Fish bites
· Predominant corallivorous fishes including parrotfish, butterflyfish, filefish, pufferfish, triggerfish,
and damselfish families.
Tissue loss (refer to 4b 4e)
Fish bites/skeletal damage
· Corallivores may be in the surrounding area, but often are not observed feeding on coral.
Growth anomaly (refer to 4b, 4c, 4e)
Gastropod bites
2
· Most predators create distinctive scars characterized by removal of tissue and underlying skeleton.
Butterflyfish delicately extract tissue from individual polyps without abrading the skeleton these
Tissue discoloration (refer to 4b, 4e)
Galls, tube formers
lesions are often only visible with a hand lens.
Overlying pigmented material
Algal abrasion/overgrowth
Below we describe the most common examples of fish predation encountered on western
(refer to 4b 4e)
Atlantic reefs.
COTS predation
Parrotfish (focused biting)
4b. Lesion pattern
Sediment damage
· Diffuse patterns of tissue loss associated with scrapes or gouges (i.e.
bite marks) by Sparisoma viride (stoplight parrotfish) that remove
corallites and underlying skeleton.
· Lesions are large (2-50cm wide), and may be focal, multifocal or
diffuse. Lesions often expand rapidly over one to five days, beginning
at a focal point at the colony margin or within the colony surface and
Focal
Multifocal
Diffuse
radiating out.
4c. Rate of progression
· Sparisoma viride graze predominantly on Montastraea annularis,
Montastraea faveolata, Colpophyllia natans and Porites astreoides,
and on 18 other species.
· In brain corals (C. natans and Diploria strigosa), fish remove tissue in
a radiating band starting at one end of the colony. Look for predators
Rapid
Moderate Not progressing
in the area.
(= acute)
(= subacute)
(= chronic)
Spot biting
4e. Lesion Color
· Multifocal, paired lesions associated with removal of corallites,
resulting from bite marks of parrotfish, pufferfish and other fishes.
· The size and shape of lesions may form a pattern consistent with the
upper and lower jaw of the predator.
4d. Lesion margin (=band):
· Various species leave numerous bite marks on individual colonies.
· Scars include recent lesions lacking tissue and lesions in various
stages of regeneration, as evidenced by pale tissue covering
the injury.
Damselfish
· Multifocal wel -circumscribed, circular, less than 1cm in diameter, acute to
subacute (most species) or dif use (brain corals) associated with tissue loss
Color:
Thickness:
Shape: linear,
Border:
describe
measure
annular, irregular
discrete, diffuse
and removal of corallites by Stegastes planifrons.
· Lesions general y expand outwards, as older lesions are colonized
by algae.
Figure 2.1 A global y-relevant decision tree used to identify known causes of lesions and describe lesions of
unknown cause. Al lesions denoted as white represent bare, exposed skeleton; green symbolizes secondary
algal colonization of bare skeleton. Other colors represent examples of commonly-encountered lesions or
legion margins characteristic of specific diseases.
21
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
· In Acropora, coral growth over time may create chimney-like structures
encircling the algae. In brain corals, bites fol ow ridges (previously
misdiagnosed as "ridge mortality disease") lesions progressively
expand outwards, but tissue remains in grooves until overgrown by
algae. In M. annularis species complex (shown) and Siderastrea siderea,
fish bite at individual polyps in a mosaic pattern.
· Look for predators in the area.
Hermodice carunculata (fireworm or bristle worm)
· Diffuse acute tissue loss beginning from branch tips or colony
projections, revealing intact underlying bare skeleton.
· The amphinomid polychaete H. carunculata feeds on less than 10
species of scleractinians, milleporids, anemones and gorgonians.
· Usually active only at night, but sometimes seen during the day.
Gastropod predation
· Coralliophila is the only major genus that is predatory on Western
Atlantic corals:
· Focal to multifocal, smal , ovoid acute tissue loss. With heavy
infestations, a scal oped pattern of shel scars may extend from the
base or margin of the colony and radiate up and out.
· Two species commonly feed on corals. C. abbreviata (see arrow)
feed on scleractinian and hydrozoan corals, while C. caribaea prefers
gorgonians and zoanthids.
· Smal individuals are relatively immobile and may cluster at colony
margins.
· Snails may retreat to the base of the colony during the day.
· Look for predators on colony or at base.
2. Tissue loss: abiotic and biotic diseases
2a. Pigmented band diseases:
the presence of a distinct narrow band of pigmented tissue
Black band disease
· Black or dark reddish-brown linear, diffuse or annular bands of acute
to subacute tissue loss with a 1mm to 5cm wide margin, less than
1mm thick.
· Band is composed of black-red filamentous organisms peppered with
white filaments, separating healthy tissue and white, bare skeleton.
· Band radiates outwards from the colony margin or a focal site
of injury.
22
· In moderate (subacute) infections, denuded skeleton is colonized by
filamentous algae and other epibionts.
· May be more than one disease front per colony which may merge
over time. Affects 22 scleractinian corals, one hydrozoan coral and
four octocorals.
Red band disease
· Diffuse to circular band of red or dark reddish-brown filamentous
organisms lacking white filaments, 1mm to 5cm wide.
· Rapid to moderate (acute to subacute) tissue loss reveals intact, bare
2
to algae-covered skeleton.
· Band is linear to annular to irregular, radiating outwards from the
colony margin or a focal site of injury.
· Common on octocorals, also affects Agaricids, Meandrina and
Mycetophyllia and other less common scleractinians (see Appendix 4).
Caribbean ciliate infection
· Observed infecting coral in two distinct patterns: a diffuse black or
grey band, several mm to 2cm thick, separating healthy tissue from
bare skeleton or a diffuse scattered patch.
· Both bands and patches have a "salt-and-pepper" speckled
appearance caused by the presence of ciliates.
· Patches may be associated with colonizing algae on bare skeleton
2b. Focal or multifocal tissue loss without distinct microbial band
Ulcerative white spots
· Multifocal wel -circumscribed, distinct white discoloration or acute
tissue loss revealing intact bare skeleton.
· Lesions are less than 1cm in diameter with discrete margin and may
either contain bleached tissue or be devoid of tissue.
· Lesions may coalesce and become colonized by algae, or heal
and disappear.
White patch disease
· Diffuse focal or multifocal lesions, 1-80cm in diameter with a sharply
circumscribed leading edge of tissue loss.
· Lesions may radiate out over time and coalesce (see arrow), or
(in Acropora) heal and resheet once mortality stops.
· Frequently, tissue remnants are visible adjacent to the leading edge.
· Coral ites may be eroded, but underlying skeleton is intact.
· Formerly called white pox and patchy necrosis in Acropora palmata,
but similar signs reported in other massive and plating corals.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
2c. Annular or linear tissue loss without distinct pigmented band
White band disease
· Disease front characterized by linear, discrete band of acute tissue
loss, 2-10cm wide, which may circumscribe the branch.
· Band separates healthy tissue from exposed skeleton colonized
by epibionts.
· Disease progresses rapidly (mm-cm/day) from colony base or
branch bifurcation.
· Tissue adjacent to exposed skeleton may be bleached; snails and
fireworm predators may colonize the disease front.
· Only observed in Acropora.
White plague
· Lesions are focal or multifocal-to-coalescing, with a linear or annular
margin, depending on colony morphology.
· A discrete band of bare skeleton separates live tissue from
algal-colonized skeleton.
· Tissue adjacent to exposed skeleton may be bleached.
· Linear tissue loss begins at the base or margin of a colony, or emanates
from an algal/sediment interface within the colony, and advances
1mm to > 10cm/day.
· Closely resembles white band disease, but affects more than 40 spp.
of non-acroporid massive and plating corals.
2d. Tissue loss without distinct pigmented band
Caribbean white syndromes
· Diffuse patterns of tissue loss with no distinctive pigmented mat or
band at the interface, i.e. tissue loss that is not characteristic of either
white band or white plague.
· In acroporids, this can include diseases that start within the colony
and not at the base, and spread in irregular patterns.
3. Discoloration
Dark spots disease
· Focal to multifocal lesions with annular to irregular margins, purple to
brown in color and 1cm to more than 45cm in diameter.
· Dark spots may expand over time, coalesce, and form diffuse to
annular bands adjacent to or surrounding exposed skeleton.
· Affected tissue may be associated with a depression of the coral
surface and may seasonal y disappear.
· Underlying skeleton may retain dark pigmentation when tissue is gone.
24
· Primarily affects Stephanocoenia, Montastraea and Siderastrea.
Yellow band disease
· Focal, multifocal, diffuse lesions with annular to linear margins of pale
yel ow, bordered by healthy tissue.
· Lesions progress mm to cm per month.
· The leading edge of the band remains pale yellow or lemon colored,
while tissue previously affected gradual y darkens prior to ful tissue
loss; acute tissue loss is rare.
· Primarily affects Montastraea.
Pigmentation response
2
· Multifocal or diffuse areas of white, purple, yellow, brownish or blue
colored tissue discoloration.
· Tissue may appear unhealthy, swol en, and/or peeling away at
the edges.
· Pigmentation may form lines, bumps, spots, patches, bands or
irregular shapes.
· Considered a response of the coral host to a variety of stressors
(i.e. unidentified pathogens, competition, predation, boring fauna,
abrasion, etc.), suggesting that organism health is compromised.
· Common on corals such as Porites, Siderastrea, and Montastraea
and octocorals such as Gorgonia, Pseudoplexaura, Plexaura,
Briareum, and Erythropodium.
Aspergillosis
· Diffuse lesion(s) of various sizes and shapes distributed throughout
the sea fan blade and branch network, resulting in loss of tissue
and/or skeleton.
· Tissue surrounding the lesion often becomes dark purple
(pigmentation response). Affected colonies may also produce
purple nodules or galls near the lesion, which can encapsulate
fungus, algae or other epibionts in an attempt to confine
the infection.
· Lesions recently produced by predation (flamingo tongue, fireworms)
usually do not show purple coloration but instead the dark brown
skeletal matrix, devoid of tissue, is clearly seen.
· Some of these lesions along the branches eventually produce
purpled edges.
· Lesions from continuous contact with other octocorals, corals,
hydrocorals and/or the substrate usually show the pigmentation
response at the point of contact.
· Only affects octocorals, most commonly Gorgonia, Pseudop-
terogorgia, Plexaura, Plexaurella.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Ulcerative white spots
· Described above under Tissue Loss.
· Also involves loss of pigmentation, as lesions may contain bleached
tissue at certain stages, so it is cross-referenced here.
Bleaching
· Focal, multifocal-to-coalescing, or diffuse areas of tissue discoloration.
· Loss or reduction in the number of endosymbiotic algae (zooxanthel ae)
from coral tissue.
· Tissue is present, but with reduced or absent pigmentation.
· Bleaching can affect the entire colony, upper surfaces, the base, or
discrete patches.
· Bleached tissue may be associated with irregular patterns of tissue loss.
4. Growth anomalies
Galls
· Focal to multifocal skeletal deformation with presence of organism
(crab, barnacle, etc.).
· Deformations caused by skeletal deposition around the resident
invertebrate result in uncharacteristic patterns. Resulting lesions may
be focal or multifocal, circular to irregularly shaped mass of thickened
coenosteum (see arrow), elevating polyps 2-4mm above the surface
of the colony or fan.
· Also reported as tumor-like growth, tumor, algal tumor, algal gal ,
gorgonin pearl, and nodules on gorgonians.
Growth anomalies of unknown cause
· Focal or multifocal, annular to diffuse lesion consisting of abnormal y
arranged skeletal elements (coral ites, ridges, val eys), which are visibly
larger or smal er than those of adjacent healthy tissue.
· They may protrude above the colony surface, and may or may not be
covered by intact tissue.
· Pigmentation may be normal, lighter (suggesting loss of zooxanthellae),
or completely absent (suggesting an absence of zooxanthellae).
· In some types, corallites may be completely absent, and the growth
anomaly resembles a white plaque over the colony surface. In other
types, coral ites may be highly disorganized and tissue may die in
irregular patches and bare skeleton may be colonized by epibionts.
· Also includes conditions referred to as gigantism, accelerated growth,
tumors, and chaotic polyp development.
26
2.4 Field assessments of Indo-Pacific, East African
and Red Sea diseases and compromised health states
1. Tissue loss: known predation or
stress resulting in compromised health
Fish bites
· Look for predators in survey area (though they may actively feed at night) and distinctive scars
on coral skeleton.
· These examples are not exclusive and other fish predators may leave different scars.
2
· Look for gouging, scraping, or other regular patterns of tissue loss, often clustered on
colony surface.
Below we describe common examples of fish predation encountered in the Indo-Pacific, East Africa
and Red Sea regions.
Parrotfish
· Diffuse patterns of tissue loss associated with scrapes or gouges
(i.e. bite marks or scars) that expose bare skeleton.
· Recent lesions are white and typically have discrete borders.
· Older lesions may be healing or partially or wholly colonized by algae,
the latter indicating that tissue loss is not progressing.
· Scars may be focused along exposed ridges of coral.
· Parrotfish are usual y in the vicinity and feed by day.
Pufferfish
· Multifocal, linear to oblong paired areas of distinct tissue loss with
mild erosion of bare skeleton (see arrows).
· Pufferfish may be in vicinity, but may not be observed feeding.
· Less damaging to skeleton than parrotfish bites, and may also be
concentrated along exposed colony ridges.
Damselfish
· Diffuse patterns of tissue loss producing lesions that may be linear,
annular or irregular in shape.
· Lesions are colonized by algae that are farmed by damselfish visible
in the area.
· Most frequently observed in branching Acropora thickets.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Acanthaster planci (Crown-of-Thorns starfish; COTS)
· Diffuse morphous area of tissue loss revealing intact, bare skeleton.
· Lesion margin may be scal oped (see arrow) on plating, massive or
tabular colonies.
· Lesion border is general y discrete and may have visible strings of
tissue and mucus.
· Feeding usual y occurs from colony edge (plating massive, tabular
forms) or base (branching forms), exposing large areas of white
skeleton consistent with rapid tissue loss.
· COTS are in vicinity either feeding or under colony by day.
Tube formers
· Focal to multifocal, circular to amorphous areas of tissue loss with
erosion of skeleton and annular thin band of white or pink tissue
accompanied by presence of boring polychaetes (tube worms
see arrow), gastropods (vermetids), or barnacles.
· Feeding structures and gil s protrude from the coral surface. Common
on massive Porites.
· Also observed in the western Atlantic.
Gastropod predation
The fol owing two genera are major predators of Indo-Pacific corals (limpets and other mol uscs are
also known corallivores):
Drupella
· Diffuse areas of tissue loss extending from branch bases or colony
edges, revealing bare, intact skeleton (see arrow).
· Lesion has a discrete border, and strings of mucous and tissue may
be visible.
· Rate of tissue loss typically slower than for A. planci predation, though
during outbreaks, numbers per colony may be in the hundreds.
· Drupella in vicinity hiding at colony base by day, often clustered,
or feeding by night. Empty shel s also indicate presence.
Coralliophilia
· Focal to multifocal areas of tissue loss revealing bare eroded skeleton
and occasional raised thin pink annular band (pigmented coral tissue
encircling lesion).
· Shel s are relatively immobile and firmly attached to colony surface;
may be heavily fouled and more visible on massive corals.
· May be clustered in colony crevices and show strong preference for
massive and branching Porites.
28
· Old feeding scars may be present (see arrow).
Sediment damage
· Diffuse amorphous area of tissue loss revealing skeleton covered by
sediment.
· Water is typically highly turbid and sediment visible on benthic
surfaces. When it accumulates on live coral, it leaves dead, fouled
skeleton underneath.
· Also observed in the western Atlantic.
Algal overgrowth
2
· Colonization and overgrowth of living coral tissue by algae
(various species).
· With heavy overgrowth, underlying coral tissue usual y dies, leaving
bare skeleton.
· Abrasion may cause a pigmentation response (see below under
Discoloration), but this is not always present.
· Also observed in the western Atlantic.
2. Tissue loss: abiotic and biotic diseases
This refers to lesions that do not have any of the discrete patterns of tissue loss or skeletal damage
consistent with predation or compromised health states described above.
2a. Pigmented band diseases:
presence of a distinct narrow band of pigmented material
Black band disease
· Black or dark reddish-brown linear or diffuse annular bands at the
interface between live coral tissue and exposed skeleton (see arrow).
· Band comprises black-red filamentous organisms (cyanobacteria)
peppered with white filaments which can only be seen
microscopical y.
· Band radiates outwards from the colony margin or a site of injury
on massive, plating or foliose corals, or circumscribes branches on
branching corals.
· In moderately progressing infections, denuded skeleton is colonized
by filamentous algae and other epibionts.
· May be more than one disease band per colony which may merge
over time.
· Affects at least 40 species of corals, particularly Acropora species.
· Also observed in the western Atlantic.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Skeletal eroding band
· Black or dark green "salt-and-pepper", speckled, diffuse band.
· May form either a discrete, dark band several mm to cm wide at
interface between healthy tissue and recently exposed skeleton
(1o infection; photo) or a diffuse, scattered patch on exposed skeleton
(2o infection fol owing predation or other tissue loss).
· Speckled appearance caused by boring ciliates which erode skeleton.
· Common in Acropora and Pocillopora.
Brown band
· Brown, linear or annular band at the interface between live tissue and
exposed skeleton, though a thin white band between brown band
and healthy tissue is sometimes also present.
· Lesion border is typical y discrete.
· Tissue loss may be rapid and begins from branch base but may
spread to adjacent branches at contact points.
· Band consists of mobile ciliates, which may contain zooxanthel ae
from consumed tissue (visible under microscope; gives band its
brown color).
· Observed most commonly on branching Acropora.
2b. Tissue loss without distinct band
Ulcerative white spots
· Multifocal patterns of tissue loss exposing intact, bare white
skeleton.
· Lesions are smal (<1cm diameter), regularly ovoid, with
discrete margins and may either contain bleached tissue
or be devoid of tissue.
· Heavy infections may result in lesion coalescence (see arrow) fol owed
by algal colonization.
· Most common on Porites; also on Montipora, favi ds, and the octocoral
Heliopora.
· Also present in western Atlantic.
White syndromes
· Diffuse areas of tissue loss exposing bare, intact skeleton.
· No band apparent between healthy tissue and bare skeleton;
lesion border may be discrete or diffuse, but not pigmented.
· Rate of tissue loss moderate to rapid.
· Lesions behind active disease fronts are white, grading to brown
distal y as skeleton becomes fouled. Can resemble bleaching,
but close inspection reveals absence of tissue.
· Host range wide, affecting at least 15 genera.
30
Atramentous necrosis
· Multifocal to irregular pattern of tissue loss exposing bare, white
skeleton subsequently colonized by a distinctive grayish-black, fouling
community.
· Lesions typically start as small bleached spots followed by tissue
loss and coalescence of adjacent lesions.
· Bare skeleton may be covered by a thin white film, under which
a black sulfurous deposit may accumulate, giving the lesion a
grayish appearance.
2
· Chronic infections result in colonization by epibionts which obscure
typical signs of disease.
· Montipora are most susceptible, but it has also been observed on
Acropora, Echinopora, Turbinaria and Merulina.
3. Tissue discoloration
Pigmentation response
· Multifocal or diffuse areas of pink, purple or blue brightly colored
tissue discoloration.
· Tissue on coral ite wal s may appear swol en or thickened.
Pigmentation may form lines, bumps, spots, patches or
irregular shapes.
· Considered a response of the coral host to a variety of stressors
(i.e. competition, boring fauna, algal abrasion see arrow), suggesting
that coral health is compromised.
· Common on Porites, which displays bright pink or purple
pigmentation.
Trematodiasis
· Multifocal, distinct pink to white, small (1-2mm) areas of
tissue swel ing.
· Swelling is a response to presence of an encysted parasitic trematode
(flatworm) visible under microscope if tissue is sampled.
· Only observed on massive Porites.
Unusual bleaching patterns
· Diffuse focal, or multifocal-to-coalescing amorphous areas of white
tissue with a discrete margin.
· Loss or reduction in the number of endosymbiotic algae
(zooxanthel ae) from coral tissue. Note that tissue is present,
but with reduced or absent pigmentation.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
· Distinguished from thermal bleaching which typical y affects upper or
entire surfaces of corals. Unusual bleaching patterns include white
stripes or patches often with discrete borders.
· The degree of bleaching can vary from pale to white, and indicates
compromised health.
4. Growth anomalies
Galls
· Focal to multifocal skeletal deformation associated with the presence
of an organism (i.e. crab, barnacle, etc.).
· Deformations caused by skeletal deposition around the resident
invertebrate in uncharacteristic patterns. Resulting lesions may be
focal or multifocal, circular to irregularly shaped masses of thickened
coenosteum (see arrow), elevating polyps several mm above the
surface of the colony.
· Also present in the western Atlantic.
Growth anomalies of unknown cause
· Focal or multifocal, circular to diffusely shaped lesions consisting of
abnormal y arranged skeletal elements (coral ites, ridges, val eys),
which are larger or smal er than those of adjacent healthy tissue.
· They may protrude above the colony surface, and may or may not
be covered by intact normal-appearing tissue.
· Pigmentation may be normal, lighter (suggesting loss of
zooxanthellae), or completely absent (suggesting absence of
zooxanthel ae). In some coral ites it may be completely absent,
and the growth anomaly resembles a white plaque over the colony
surface. In other types, coral ites may be highly disorganized and
tissue may die in irregular patches and bare skeleton may be
colonized by epibionts.
· Also includes conditions referred to as: gigantism, accelerated
growth, tumor, neoplasia, hyperplasia, chaotic polyp development.
· Also present in the western Atlantic.
32
Chapter 3
Confirming Field Assessments and
Measuring Disease Impacts
In this chapter you will find:
Key questions to ask when disease is detected: geographic
extent, host range, seasonality, and case fatality rate.
Basic methods for describing lesions in
corals and confirming field assessmnts.
3
A summary of current practices used to determine
the causes of unknown lesions in corals.
Information on how to collect, handle and preserve specimens
for histology, microbiology and molecular assays and general
considerations such as safety, permits and labelling.
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Confirming Field Assessments
and Measuring Disease Impacts
T. Work, C. Woodley and L. Raymundo
3.1 Monitoring changes over time
Three questions are of paramount importance to resource managers when disease is detected in an
animal population:
1. How widespread is the disease (geographic extent)?
2. Is the disease spreading and if so, how fast (geographic spread)?
3. Is the disease kil ing animals (case fatality rate)?
To answer these questions, the state of disease in the ecosystem must be monitored over time.
Deciding how frequently to monitor is dictated primarily by the behavior of the disease in the field.
For example, diseases that appear to be spreading rapidly will need more frequent monitoring than
those that are spreading slowly or appear static. It is important during this phase of monitoring to
liaise with appropriate experts who can help determine the cause of disease (refer to Appendix 2).
This will, at a minimum, necessitate collection of samples for laboratory investigations (see Section
3.4 of this chapter). Chapter 4 provides guidance in developing a monitoring program to help you
address impacts of disease on coral communities.
1. Geographic extent
To determine the regional extent of a disease requires that you know the location of populations at
risk of disease; those most likely to be affected by the disease. Criteria that should be considered
when deciding which areas to survey for extent of disease include, but are not limited to, percent
coral cover, species richness, proximity to the original site of disease detection, susceptibility of the
population, and accessibility of the site. Depending on how the disease is behaving, some criteria may
take priority over others. If the disease affects multiple genera of corals, those reefs with the highest
coral cover would be prioritized for supplementary surveys (Figure 3.1.A). If the disease only affects
a single genus, reefs with high cover of that particular genus would be prioritized for supplementary
surveys (Figure 3.1.B). If field evidence suggests the disease may be infectious (i.e. a lesion is observed
spreading over time from a diseased coral to adjacent colonies), priority would be given to surveying
adjacent reefs or those down-current (Figure 3.1.C). The extent of disease can be tracked spatially
using commonly available geographic information systems software (GIS) tools.
3
2
3
1
Island
Island
Island
1
2
1
2
A
B
C
Figure 3.1 Hypothetical island with fringing reefs (grey areas), prevailing ocean currents (blue arrow), and reef with disease (red
dot). Numbers indicate order of priority for survey sites. A) If disease appears to affect al corals, then surveys to assess extent
are targeted for those reefs with highest coral cover. B) If disease affects only one particular genus, then surveys to assess
extent are targeted to those reefs that have highest cover of that genus (blue areas). C) If disease appears infectious, surveys
are targeted to adjacent reefs down and up stream of the diseased reef.
34
When assessing the geographic extent of disease, managers should address the fol owing questions
(listed under the headings "Hosts", "Place" and "Time"). The answers may provide clues to laboratory
diagnosticians on potential causes of disease.
Hosts
· Does disease primarily affect a particular group or genus of corals?
Some diseases, particularly those caused by infectious agents, are very host-specific. On the other
hand, if multiple hosts are affected, this may indicate a non-specific cause of disease (i.e. elevated
temperature, poisoning, etc.).
· Does disease primarily affect a particular size
class of coral?
Certain diseases affect older colonies more
than younger ones and vice versa.
· Does disease appear to be spreading
between adjacent colonies?
Evidence of this is strongly suggestive of
a communicable agent (Figure 3.2). Note
that this needs to be confirmed through
additional laboratory investigations.
3
Figure 3.2 White syndrome spreading to adjacent colonies of
Pachyseris in Palau. Photo: L. Raymundo
Place
· Do corals affected by the disease have a particular spatial distribution?
For example, perhaps colonies that are shaded are more prone to disease. Perhaps disease appears
to affect colonies predominantly on the reef flat but those on the reef crest or slope are unaffected.
Perhaps there is a depth or water circulation gradient associated with disease occurrence.
· Have there been recent changes in the environment?
Answering this could partly explain why disease suddenly occurs at a particular location.
For example, have there been recent changes in land use patterns adjacent to the reef (chemical
spil s, construction, excessive terrestrial runoff) or unusual environmental events (hurricanes,
temperature anomalies, fresh water influxes)? It is important to col aborate with local agencies
and other managers who are responsible for monitoring environmental characteristics such
as rainfal , water temperature, turbidity and salinity (see Chapter 4 for details). Keeping track of
such data, along with changes in disease prevalence or incidence, can often reveal patterns
which may be exacerbating or inhibiting the impact of the disease.
Time
· Does disease occur more frequently during certain times of the year?
Some diseases have a seasonal component. Determining whether a temporal component exists
could provide clues to potential causes of disease, and will help to predict future impacts.
35
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
2. Geographic spread
Visual surveys of geographic extent over time can give an indication of how fast a disease is spreading.
However, it is usual y more desirable to quantify the spread of disease in a population, particularly
when one is comparing multiple regions or sites. One practical way to do this is to measure the
incidence of disease. Unlike prevalence, which is a static measure (of disease), incidence measures
the number of new cases of disease over a defined time period and thus can be a useful indicator of
whether or not disease is spreading. Increasing incidence suggests a spreading disease. By its very
nature, incidence (of disease) can never be greater than prevalence (see Box 3.1). See Chapter 4 for
calculations of disease prevalence, incidence and other parameters.
3. Case fatality rate
This is measured as the percent of colonies
having a disease that actual y die from that
disease. Managers should be more concerned
with diseases that have a high case fatality rate
(see Box 3.1). To get a measure of case fatality
rate, it is necessary to mark colonies affected
with disease and to measure the number of
colonies with disease that die after a set time
period. Various methods exist to mark coral
colonies (i.e. masonry nails, flagging tape,
plastic or stainless steel tags), but we have
found that commercial y available cattle ear
tags affixed to colonies with cable ties wil last
for at least one year, even in highly turbulent
Figure 3.3 Cattle ear tag (see arrow) used to mark and code
conditions (Figure 3.3).
a coral colony. Photo: T. Work
One last note on corals
Corals are colonial animals that fragment as a means of asexual reproduction. They can also partial y
die and later grow new tissue over this dead skeleton; both processes can slow growth of the colony
as a whole and reduce colony size. The age of a colony may, therefore, be difficult to estimate from
colony size. While it can be assumed that large colonies of a given species are old, small colonies
are not necessarily younger; they could have experienced fragmentation or partial mortality or other
factors which have resulted in slow growth rate. While measuring coral colony sizes is reasonably
straightforward, it is important to remember that estimating age from size should not be attempted.
Another factor which can be chal enging when assessing disease in a coral community is colony
boundaries. With extensive monospecific stands, it may be difficult to determine where one colony
ends and another begins, particularly when colonies are in physical contact. When faced with this
situation, look for subtle changes in coloration; often different colonies wil appear as slightly different
shades. Also, look for the borders where the colonies abut each other; if a stand or thicket is composed
of different colonies (rather than a single one), then these colony margins wil not fuse, but wil remain
separate, and may be differential y pigmented or show signs of competition.
36
Box 3.1
Examples of prevalence and incidence measures in a chronic disease.
White circles are live coral colonies; green circles are diseased colonies documented during the previous
time period (prevalence), red circles are new cases of disease (incidence), and black circles are dead colonies
(mortality).
Time 1
Time 2
Time 3
Time 4
Time
Total cases
New cases
Population
Prevalence
Incidence
1
5
100
0.05
2
8
3
100
0.08
0.03
3
14
6
100
0.14
0.06
4
24
10
100
0.24
0.1
Example 1: Incidence is much lower over time than prevalence, but increases steadily. This indicates the
3
spread of disease in the population.
Time 1
Time 2
Time 3
Time 4
Time
Total cases
New cases
Population
Prevalence
Incidence
1
5
100
0.05
2
8
3
100
0.08
0.03
3
14
5
100
0.14
0.05
4
26
2
100
0.16
0.02
Example 2: Incidence initial y rises, reflecting increasing new cases. Incidence then decreases, reflecting
a decline in new cases. Prevalence continues to increase the entire time.
Time 1
Time 2
Time 3
Time 4
Time
Total cases
New cases
Population
Prevalence
Incidence
1
5
100
0.05
2
12
11
96
0.12
0.11
3
22
21
85
0.25
0.25
4
35
33
66
0.53
0.5
Example 3: An acute lethal disease spreading quickly through a coral population. Incidence tracks
prevalence much more closely. The case fatality rate at times 2,3 and 4 would be 80% (4/5), 90% (10/11),
and 90% (19/21), respectively. This is very high.
37
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
3.2 Basic methods for confirming
field assessments and describing disease states
3.2.1 Recognizing disease in the field
This discussion builds on the information presented in Chapter 2, and is meant to provide you with
more decision-making power. The most critical aspect of recognizing disease states in corals is to
"know your animal". While this recommendation may seem trite, recognizing what comprises "normal
variation" in morphologic appearance of a coral is a critical first step to understanding the role that
disease plays in a reef ecosystem. For example, some coral species have different morphologies or
color schemes depending on their geographic location or reef zone. White discoloration is common
in the growing tips of some coral species where tissues have yet to be colonized by zooxanthel ae,
and this could be misinterpreted as partial bleaching (Box 3.2).
For the field biologist, diseases in corals are manifested as a change in morphology (via a lesion).
When encountering a diseased coral, two important points should be kept foremost in mind:
1. Disease is a continuum between health and death, and this continuum is reflected by changes
in morphology as disease progresses. Thus, when observing a lesion on a coral, remember that
this lesion could be in the early, middle, or late stages of the disease. Establishing this requires
diseased colonies to be marked and monitored over time (see Section 3.1, Case Fatality Rate, for
methods). Marking colonies with lesions and documenting the progression of the lesion over time
can provide invaluable data for understanding how a disease impacts host colonies, how fast it kil s
tissue, and whether or not colonies can recover or halt the spread of disease.
2. The causes of most coral diseases are unknown, and except for certain cases (see Section 3.3),
you wil not be able to determine the cause of a lesion without further laboratory investigations.
Given these two limitations, the first step to
describing a coral disease is to formulate a
good morphologic description of the lesion.
Doing this is critical for two reasons. First, it
forces you to focus on the evidence (i.e. the
lesion) and not the potential cause of the lesion.
Second, a good morphologic description of
the lesion provides the best tangible objective
data regarding that disease (pending further
laboratory work). These objective data can then
be used to communicate facts about this
disease to others in a standardized manner,
thereby al owing for accurate comparisons of
disease among geographic regions. The
Figure 3.4 A colony of Porites cylindrica exhibiting subacute
decision tree in Chapter 2 (Figure 2.1) of this
tissue loss from white syndrome. Photo: L. Raymundo
manual will help you do this.
3.2.2 Describing a lesion in a hard coral
Hard corals are relatively simple animals that consist of a thin layer of tissue overlying a calcium
carbonate skeleton. Accordingly, a lesion in corals will manifest in three ways:
1. Tissue loss
Tissue is missing, revealing underlying skeleton (Figure 3.4). In such lesions, close attention should
be paid to the skeleton as this may give clues to the progression or potential cause of the disease.
For example, a defined area of bare, intact white skeleton bordered by tissue indicates that tissue
loss was recent and relatively rapid (acute). In contrast, a progression from healthy tissue to a band
of bare, white, intact skeleton to algae-covered skeleton would suggest an advancing front of
tissue loss (subacute). If tissue loss is acute, note whether the skeleton is intact or eroded; acute
38
tissue loss with skeletal erosion suggests trauma (i.e. fish bite, anchor damage, etc.), and a visual
assessment of the immediate area may provide further clues as to the origin of that trauma. When
observing white skeleton on a coral, it is helpful to look closely to make sure no tissue is overlying
the area; magnifying lenses are helpful for this. Failure to do so may confuse tissue loss with white
discoloration (bleaching).
2. Discoloration
This is a deviation from the "normal" color of tissues. The discoloration most familiar to many
biologists is white discoloration (bleaching) due to loss of zooxanthellae from tissues. However,
other types exist and it is important to reiterate
here that many coral species show broad ranges
in normal coloration. This must be considered
when diagnosing a potential disease state
(Figure 3.5). When describing the discoloration
of corals, it is important to stick with basic colors
(i.e. white, purple, pink, brown, etc.) and avoid
obscure terms.
3
Figure 3.5 Tissue discolouration caused by dark spots
disease on Stephanocoenia. Photo: E. Weil
3. Growth anomaly
This is an abnormal configuration of the coral skeleton. Typical growth anomalies form as nodular
or cauliflower-shaped growths of the coral skeleton. These often lack, or have reduced numbers
of, polyps and are discolored white or are distinctly
paler in color than surrounding healthy tissue. Other
coral ilte structural irregularities may also be present,
but require a microscope to see (Figure 3.6).
The three basic types of lesions described above
are not mutual y exclusive and can occur singly or
in various combinations. A final step to describing
a coral lesion is to note the distribution of that
lesion on the colony. A lesion can be focal (a single
occurrence on the colony), multifocal (several
scattered or clumped occurrences), or diffuse
(encompassing more than 25 percent of the colony
surface Figure 3.7). Additional terms and details
Figure 3.6 Growth anomalies on Goniastrea edwardsi.
Photo: D. Burdick
to systematically describe lesions in corals are
available in Chapter 2.
Figure 3.7 Lesion types: (A) focal lesion of a growth anomaly. Photo: D. Burdick; (B) multifocal lesions of trematodiasis.
Photo: G. Aeby; (C) diffuse lesion of white syndrome. Photo: L. Raymundo
39
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
3.3 Determining causes of lesions: How to collect, handle
and preserve specimens for histology, microbiology and
molecular assays
3.3.1 The challenge of determining causation
The goal of this chapter is to provide a summary of current practices employed to determine causation of
unknown lesions in corals. As we discussed in Chapter 2, determining the cause of lesions from predation
or certain environmental impacts may be relatively straightforward if the evidence is present and visible in
the immediate environment of the reef. Therefore, an initial assessment of the immediate area surrounding
the coral is essential for such diagnoses. For example, a coral displaying `multifocal acute tissue loss with
skeleton erosion in a consistent pattern (i.e. linear, el iptical), and with coral ivorous fish nearby inducing
similar lesions' should be diagnosed as fish bite (predation). Similarly, `focal acute tissue loss and erosion
of skeleton bordered by a thin band of pink discoloration with presence of snails' could be attributed to
snail predation. Other animals may also be visible within the coral skeleton. For example, barnacles will
encrust in coral skeleton and be bordered by a thin margin of white discolored tissue, but wil be visible in
the center of the lesion upon close scrutiny.
In most cases, however, determining the actual cause of a coral lesion is not possible without
additional laboratory investigations, particularly if involvement of a microbial agent is suspected. While
we recognize a ful -on investigation into causation may be beyond the capacity of many managers
reading this book, we feel that it is appropriate to provide background information that outlines what
can be done, should this course of action be deemed appropriate. Even if it is not within the capacity
of a field station, local laboratory, or managing organization to take on such work, we believe it is
important to convey the complex nature of investigating coral disease and determining causation. To
this end, we offer information on current approaches to assessing and testing for causation. Briefly, this
usually involves characterizing the lesion at tissue and cellular levels (histopathology). If an infectious
agent is suspected as a cause of the lesion, additional samples may be needed for microbiology (see
Section 3.4 for sampling protocols). In the end, disease investigations in corals are best done through
a partnership between coral biologists and disease diagnosticians familiar with appropriate laboratory
methods (Figure 3.8).
Determining a specific cause of a
disease is, of course, of paramount
importance and is a major goal in
al disease characterization efforts.
However, it is a chal enging and
lengthy process. If an infectious
agent is suspected, one way to
address this is by employing a
step-by-step process to prove
what is known as Koch's Postulates
(66). The first step in this process
requires col ecting diseased and
healthy tissue samples and
describing the morphology of the
lesion at the gross and cel ular
level which, in some cases, may
reveal the presence of a potential
causative agent. Various approp-
Figure 3.8. Col aboration with local scientists to assist with microbiological
analyses is important. Here students are processing samples from coral mucus. riate laboratory tools are used to
Photo: T. Lewis
culture, isolate and identify
suspected causative agents. These
putative pathogens are then introduced to healthy host tissue under controlled experimental conditions
and the response of the host tissue is observed. If lesions develop, the tissue is sampled to re-isolate
the introduced microbe. If it is re-isolated from the diseased lesion, then it can be classified as a causal
40
agent for the disease.
Koch's Postulates have been proved for only a handful of coral diseases to date (see Chapter 1, Figure
1.4), principal y due to the limitations of this method. Black band disease, for instance, is the most
comprehensively studied disease, but is caused by a microbial consortium dominated by cyanobacteria,
Beggiatoa and Desulfovibrio, which col ectively have harmful effects on coral tissue and contribute to
its death (67,68). Using Koch's Postulates to prove causation is not an appropriate method in this case,
as more than one agent is involved. In addition, certain diseases may be caused by microbial agents that
are not culturable, and so cannot be tested using this method. This is one reason why the histological,
microbial, and molecular characterization for most diseases remains very incomplete and why alternative
methods are currently being developed. Below, we provide some guidelines for col ecting and handling
specimens to assist in this characterization. It should be stressed that such work requires col aboration
between those in the field (i.e. ecologists and reef managers) and laboratory scientists (i.e. histologists,
microbiologists, toxicologists, molecular and cellular biologists). Please refer to Appendix 2 for a list of
experts in the field who can be contacted should you be interested in pursuing this route. Arrangements
should be made prior to sampling and specimen preparation, so the scientist or laboratory receiving
specimens can be prepared to process them.
Specimens are samples containing material from a
disease site, col ected for laboratory analyses.
Relevant samples include coral tissue (fragments
from diseased and healthy tissue of the same colony,
as wel as from an unaffected reference colony), coral
3
surface mucus and water (col ected using a sterile
syringe), and sediment (col ected with a sterile tube),
as wel as other flora or fauna associated with the
diseased corals (Figure 3.9). Available historical or
Figure 3.9. Diver col ecting coral mucus with a syringe background information surrounding the problem
from the surface of a Siderastrea siderea colony. such as that discussed in Section 3.1, along with
Photo: B. Seymour
photo documentation, wil assist in the diagnostic
process and should be included with the samples (69,70). The specimens must be handled in a
manner that preserves the individual sample's identity, prevents cross-contamination and avoids
damage to the sample. The preservation method used will be dictated by the intended analysis
(i.e. histology, microbiology, toxicology, virology).
3.3.2 General considerations
Permits
Permits for col ection and/or transport are required for most studies involving coral disease, regardless of
the jurisdiction. The number and type of permits required vary from one location to another. Managers
are often in charge of issuing permits, and thus play a crucial role. It is often the manager who must set
restrictions on sample size, type and number, and who may be instrumental in establishing procedures
for biocontainment, quarantine, or reef closures. Therefore it is essential that col ection permit requests
include a clear rationale for the type and number of samples being requested.
Safety
The primary consideration when col ecting diseased tissue of any kind is personal safety and
infection control for both human and coral. Here are general considerations for minimizing risk of
spreading disease:
· When multiple sites are to be visited, ALWAYS visit the healthy (or apparently healthy) sites before
entering an area with known disease, to prevent potential spread of infectious agents. Similarly, when
sampling within a diseased site, first sample the apparently unaffected (healthy) individuals, followed
by portions of a diseased colony that appear unaffected (healthy) and sample the diseased portion
(lesions) of the colony last.
· Each col ected sample should be placed into a separate label ed container; live or frozen tissues
should be transported in double containment to prevent any possible contamination back to the
ocean at new sites.
41
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
· Divers should consider themselves and their equipment as potential vectors of disease between
locations. If sampling from multiple reefs, ensure that between sites you quickly rinse SCUBA gear
and other equipment in five percent bleach solution (or other suitable disinfectant solution) then
rinse in fresh water.
3.3.3 Specimen documentation
Labelling
Label col ection containers prior to sampling. A smal tag of waterproof paper with information written
in pencil can be placed in the container (bag/jar/tube) and allows you to change or add information
after sampling. Label syringes for mucus collection prior to the dive as well. Basic label information
should include the following:
· collection site
· coral genus and species (if known)
· location on coral where sample was collected (reference tissue from healthy colony, unaffected
portion of diseased colony, diseased tissue margin, disease mat)
· date
· initials of sampler
Photographing
Photographing lesions provides a record of color, location and appearance. Both actual size and
macro shots should be taken before and after removal of tissue biopsies; include a scale of some sort
in each picture (ruler, dive knife, coin, etc). Make sure to document where and when the photo was
taken. Photos of the general reef site are useful additional documentation.
3.3.4 Sampling
For Histology
Histological analyses characterize the microscopic morphology of tissue and may help guide further
investigations (71). Typically, samples are viewed with a light microscope for general tissue organization.
Histological data can reveal cellular changes that occur in tissues under normal, stressed or diseased
conditions, and whether foreign organisms (i.e. bacteria, fungi, parasites) are present (Figure 3.10).
A
B
Figure 3.10 Histological samples of sea fan coral Gorgonia ventalina. (A) tissue from a healthy coral. (B) tissue from a lesion of
a coral with Aspergillosis; the fungus has spread throughout the skeleton of this coral. This analysis can be useful for confirming
field assessment. Photo: C. Couch
42
Sampling for histology is straightforward, but involves handling potential y hazardous chemicals, so the
sampler needs to be aware of proper procedures. In general, a tissue sample is taken and placed in a
suitable fixative or preservative. If the analysis is solely for morphology, then 10 percent seawater-buffered
formalin is sufficient. However, if immunological or DNA-based staining or preparation for electron
microscopy is needed, additional fixatives and procedures are necessary. These preparations should be
done under supervision by personnel from the laboratory where the samples will be sent for analysis.
Histological coral samples can be removed in a number of ways. The most simple is removing a small
fragment of the coral using a hammer and chisel, coring devices (i.e. leather punch, pneumatic dril ,
hand drill), rongeurs, wire cutters, or garden clippers. Light microscopy usually requires approximately
two cm2 of apparently healthy tissue taken several centimeters from the diseased tissue and another
sample that includes the disease margin (i.e. bare skeleton and intact, diseased tissue). The samples
should be placed in label ed plastic bags with fresh seawater until returning to the boat. It is important
to completely immerse the sample in fixative as soon after collection as possible (the recommended
ratio of fixative to sample is 10:1), noting the time interval between collection and fixation; cellular
changes can begin as soon as a sample is removed from the coral.
For microbiological analyses
Microbiological analyses are important diagnostic tools if an infectious agent is suspected as a cause
of disease. Two approaches are currently used to isolate and identify possible microbes involved
in disease: culture-dependent methods and culture-independent (DNA-based) techniques. Culture-
3
dependent techniques (Figure 3.11A) are used to isolate, grow and identify microbes such as bacteria
or fungi from lesions, tissue, mucus or surrounding water or sediment. While these methods are useful,
they are only able to identify a small fraction of the total microbial community, as many such organisms
are not culturable. Therefore, culture-independent methods (Figure 3.11B) have been developed that
use DNA or RNA present in the samples to examine the diversity of microbial communities in samples
or in specific molecular tests (such as polymerase chain reaction assays). Samples are usually taken from
healthy and/or diseased coral tissue and coral mucus, to look for shifts in these communities between
hosts, healthy versus diseased tissue, species, seasons, geographic location or environments.
The viability of bacteria and their community structure within samples change rapidly and unpredictably
after sampling, thus it is critical that samples be processed rapidly. There are two main approaches:
a) sampling specimens for preservation (i.e. DNA extraction, protein analysis,
anthropogenic chemical analysis); and
b) sampling specimens that require rapid processing (i.e. live bacterial culture).
A
B
Figure 3.11 Examples of approaches to investigating a potential infectious cause of coral disease.
A) culture-dependent techniques to isolate and identify microorganisms. The plates shown represent
two different culture media (TCBS and GASW) at two concentrations (10µl and 100µl). B) culture-
independent technique wherein the DNA or RNA of various microorganisms in a sample can be used to
identify the number of different organisms present. Photos: C. Woodley
43
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Field work often does not al ow for quick processing, so documenting time intervals between sample
col ection and processing is essential. Samples for culturing live bacteria must be processed within
12 to 24 hours. Although culture-dependent methods are not difficult they do require trained
individuals to conduct the procedures. Local hospitals or diagnostic laboratories may be able to assist
managers with sampling, plating and culturing techniques. Culture plates should then be sent to a
marine microbiologist for further analysis. Some samples, particularly those for international shipments,
may require additional permits or documentation for export and/or import, so the col ector should be
aware of relevant policies and regulations.
Sampling for culture-independent analyses is straightforward but time-sensitive, so while specialized
training is not required, attention to detail and proper labelling are essential. As this procedure
requires specialized equipment, such work should be undertaken as a col aborative effort between
field ecologists and a microbiology laboratory.
Biochemical and molecular analyses
Molecular analyses address the formation, structure, and function of macromolecules such as lipids,
metabolites, nucleic acids and proteins. Several such analyses have been adapted to coral and can be
used to define a cel 's physiological condition or health status (Figure 3.12; 70). The sampling
protocol for these analyses is identical
to those for col ecting tissue biopsies
for histology or culture independent
analyses, but requires equipment
which may not be available. Please
consult experts for detailed information.
Figure 3.12 ELISA assay for measuring cel ular diagnostic parameters.
Photo: Haereticus Environmental Laboratory
Specimen shipment
Prior to any sample col ection, arrangements must be made with the receiving laboratory(ies) for
shipment and analyses. Shipping documentation must be considered, particularly with international
shipments, and proper authorization obtained. A key consideration is the protection of sample
integrity during shipping. This involves:
· preventing cross-contamination;
· preventing decomposition;
· preventing leakage;
· preserving individual specimen identity; and
· proper labeling (69).
Attention to these wil ensure safe delivery and avoid fines (which can be considerable, depending on
the infraction). Further regulations and permits (i.e. CITES) may be required depending on the type of
sample being collected and shipped, as well as the country of origin and the destination.
44
Box 3.2
Coral disease nomenclature: a current challenge
Much confusion has resulted from the many reports of new diseases over the last ten years.
Several of the names presented in the literature have been assigned on the basis of a few
or single observations, and they lack photographic documentation, detail on gross signs, or
evidence of coral tissue destruction. Other conditions were presumed to have been caused by
a pathogen, but later shown to result from predation or competition. Different researchers have
also used terminology interchangeably to describe similar signs, such as the various names
given to the white syndromes. There is also a growing number of diseases identified in the
Caribbean that have been subdivided (i.e. "Type I" and "Type II"), based on rates or patterns
of disease spread or species affected. It can be extremely difficult to verify which "type" of
3
disease is present based on single observations, as initial signs of infection may look different
from later stages and rates of spread cannot be determined without monitoring. Furthermore,
certain diagnostic features, such as the presence of a bleached front of tissue that advances
ahead of the dying tissue, are not readily visible or may be absent depending on the time of
observation. For example Caribbean white plague type I and II (6) and white band type I and
II (8) differ in rate of progression, a characteristic which is only discernible via monitoring. Dark
spot type I and II, dark band syndrome, purple band syndrome and tissue necrosis (11) all
basically refer to the same suite of disease signs, as do white pox, patchy necrosis and necrotic
patch syndrome (13). The proliferation of names presents difficulties when evaluating host
ranges and geographic distribution of coral diseases and can lead to incorrect assumptions
about causative agents.
This confusion and lack of coordination has resulted in an increased effort to consolidate
information, build consensus regarding nomenclature, and develop the science of coral
disease research in a coordinated fashion. Such efforts are vastly improving our current state
of knowledge and should continue to do so in the future. Properly describing lesions and
disease signs and developing new histological and molecular diagnostic tests is crucial to this
effort. It is hoped that the information in this book will further assist in the development of a
coordinated approach.
45
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
46
Chapter 4
Assessment and Monitoring Protocols
In this chapter you will find:
Objectives and methods for rapid
assessment and long-term monitoring.
Designing a valid and reliable sampling protocol.
Quantifying coral disease prevalence,
incidence and mortality rate.
Guidelines for measuring basic environmental
variables which may impact disease dynamics.
4
47
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Assessment and Monitoring Protocols
E. Weil, E. Jordán-Dahlgren, A. Bruckner and L. Raymundo
4.1 Rapid assessment versus monitoring
goals and objectives of each
Most protocols used to assess coral reef ecosystems involve characterizing coral cover, species
diversity, fish community structure, water quality, and human activities, with an emphasis on detecting
change. While this approach may provide a detailed picture of reef condition at the time of the survey,
and how the reef has changed between survey periods, it may fail to identify factors responsible for
the changes observed, or predict future trends under varying management scenarios. Alternatively,
surveys focusing only on a specific threat to a community, such as disease or bleaching, may provide
detailed diagnostic information and rigorous data on prevalence, incidence, and impacts, but may miss
additional information on reef condition that is critical to understanding the impacts of the threat.
The ideal approach to studying
coral diseases and their impacts,
given sufficient funding and
qualified personnel, is a well-
designed,
integrated,
multi-
component survey. Such a survey
would
provide
population,
community and/or ecosystem-
level data on benthic organisms,
fishes, water quality, environmental
parameters and the human
dimension, along with disease
components at different spatial
and temporal scales (Figure 4.1).
This approach al ows assessment
of coral reef community structure
and function, temporal changes,
and potential links between
assessed parameters that might
Figure 4.1 An integrated approach to obtain quantitative data on a reef be responsible for observed
community can provide a more complete picture of a reef's health status than changes in reef condition. It is
a survey examining only disease states. Here, divers take detailed data on the
coral population. Photo: B. Willis
important to understand that
significant correlations between
disease prevalence and environmental and/or biological factors do not prove causality. It simply
suggests associations between the variables considered.
Due to the potential for high coral mortality from disease, estimating the magnitude of disease
impacts should be a fundamental management goal. There are two main approaches in current use:
rapid assessments and monitoring.
1. Rapid assessments These characterize the reef area(s) surveyed at the moment of the assessment;
a single point in time. This usually estimates relatively static (state) variables about a population or
a community and is useful for comparing multiple sites or different time periods.
48
2. Monitoring This detects changes over time within the same reef area(s). The aim of such surveys
is to estimate changing (process) variables. For both approaches, a protocol that answers specific
questions must be designed. For instance, initial questions for a protocol that seeks to describe a
general reef condition would include:
· Are there coral diseases present on the reef? If so, which ones?
· What species are affected?
· Are there reefs, reef zones or reef areas apparently more affected than others?
In this case, a relatively simple sampling effort using qualitative or semi-quantitative rapid assessments
could provide the answers (see Table 4.1 for surveying techniques). On the other hand, monitoring
would address the questions of changes over time something rapid assessments cannot do.
Therefore monitoring should be the approach considered in any short or long-term management
program for Marine Protected Areas and other areas of high conservation value.
Table 4.1 Descriptions of commonly-used surveying techniques. Descriptions taken from Edmunds (1), Porter & Meier (5),
Antonius (7), Kuta & Richardson (9), English et al. (10), Bruckner & Bruckner (12), AGRRA (14), Jaap et al. (19), Santavy et al. (20),
Bruckner (21), Weil et al. (25), Feingold (27).
Survey
Description
Advantage
Disadvantage
Manta Tows
A diver/snorkeler is
Al ows rapid coverage
Detailed diagnostic or
towed behind a small
of large areas. Provides
quantitative data not
boat at a slow and
estimates of coral
possible. Dependent
constant speed for a
cover, dominant coral
on high water quality.
fixed time interval.
types, broad mortality
May only be useful to
estimates.
estimate mortality
cause if very visible
(i.e. COTS, BBD).
Timed Swims
Diver swims for a fixed
Provides semi-
Not used for prevalence
4
time in a straight line
quantitative information
or incidence (no total
along a single depth
on abundance of disease colony count; survey
gradient. Al diseased
over large areas.
area only estimated).
corals in a 2m band
Disease count categories
noted: species, disease
used: rare (1-3 cases),
type, lesion number.
moderate (4-12 cases),
frequent (13-25 cases),
abundant (26-50 cases),
epidemic (51-100 cases),
catastrophic (>100 cases)
Circular areas
Infected and healthy
Provides quantitative
Cannot be used on a reef
colonies of al species
data on prevalence and
slope because multiple
counted within a circular
incidence of diseases.
zones may be included
area (10m radius; 314
If size measurements
in a single sampling
Pivot
10 Subsurface m2). A stake pounded
are included, population site. Does not provide
Float
into substrate is used
structure can be
information on coral
Rod
to define the pivotal
estimated. Best on
cover unless combined
center of the circle;
flat reef substrates, in
with other measures.
a 10m transect tape is
studies of single diseases Impractical in areas with
held by diver as she/he
(BBD, YBD).
high cover and density.
swims around the stake,
keeping the tape taut.
49
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Survey
Description
Advantage
Disadvantage
Radial belt transect
Sampling circular areas in Counts the total number Assessment of multiple
concentric belts (or arcs)
of infected and healthy
permanent sites may be
around a pivot point. The colonies of each species
time consuming.
area sampled is either a
within the outer 8-10m of
Pivot
Subsurface
contiguous circle (radial
a circle (314m2 plot) and
3 6 8 10 Float
sampling) or a series of
identifies al diseases.
Rod
rings (radial belt transect)
around the pivot point.
Belt transects
All corals within a
Can provide detailed data Requires multiple
predefined area (i.e.
on prevalence based on a transects in each zone.
2x20m) are counted
whole colony assessment, With high diversity, high
and disease presence
population dynamics, and cover and abundant
recorded. 1m or 2m PVC health status. Long term
smal corals, individual
stick is used to define a
monitoring of tagged
transects may require
quadrat along a transect. colonies can provide data multiple dives to
May include more
on colony fate (recovered/ complete.
measurements such as
dead/stasis, etc.).
colony size, coral cover,
and percent mortality.
Line intercept transects
Can provide detailed data Al ows rapid assessment Requires multiple
on prevalence based on a of coral community
transects throughout
whole colony assessment, structure, condition, and each zone to quantify
population dynamics, and prevalence of disease
prevalence. Does not
health status. Long term
from a whole colony
provide a comparable
monitoring of tagged
perspective. Provides
assessment of area
colonies can provide data information on size
surveyed if corals vary
on colony fate (recovered/ structure, colony density, in size between sites.
dead/stasis, etc.).
coral cover.
Colony size based on
actual measurements (or
size classes) but percent
colony mortality is
estimated and may vary
between observers.
Point intercept transects Requires multiple
Provides information on
Prevalence may be
transects in each zone.
cover of various benthic
incorrectly assessed
With high diversity,
organisms including
because relatively small
high cover and
coral as wel as substrate overal area is examined
abundant smal corals,
types. Faster to use than along each transect.
individual transects may
Line intercept, if multiple Does not provide
require multiple dives
survey sites are needed;
detailed information on
to complete.
allows rapid assessments. colony abundance (large
colonies may be counted
twice) or size structure.
Chain transects
Biotic and abiotic
Provides rapid
Assesses a very narrow
components identified
information on reef
band of reef. Diseases
directly under each
rugosity, species diversity and other factors may be
link in chain. Rugosity
and cover.
missed unless the chain
estimated by determining
lands on the diseased
ratio of the length of
portion of a colony.
chain laid fol owing
bottom contours to the
straight-line distance
between start and end
points of the transect.
50
Survey
Description
Advantage
Disadvantage
Quadrats
Quadrats of various sizes Provides quantitative
With exception of
(0.5m2, 1m2) are placed
information on
large quadrats
haphazardly, randomly,
cover of coral and
(i.e. 100x250m), poorly
or at specific intervals
other organisms
estimates disease
along transects.
and substrates, and
prevalence, abundance,
Percent cover of all
qualitative data on types size or condition of
species and substrate
of disease present.
corals; does not capture
types within quadrat area
disease on the portion of
determined by counting
a coral that fal s outside
number of quadrat
the quadrat. Does not
subunits occupied by
work wel for large
each category.
thicket-forming corals.
Photo-quadrats
Quadrats of varying
Accurate assessment
Requires considerable
sizes (<1m2) are
of cover and changes
lab work to analyze
photographed using high in cover (when using
images. May fail to
resolution digital cameras permanent quads).
detect diseases and small
and video.
Less bottom time; data
colonies. Does not work
are analyzed in the lab,
wel for large branching
using image analysis
corals that form thickets.
software, such as NIH's
Resolution too low to
free Image J software®.
identify many corals
to species.
Validity and reliability
4
The importance of proper sampling design cannot be underestimated, particularly if the data are
going to be applied to management. A good assessment must be both valid and reliable. Validity
refers to how effectively the assessment reflects what we want it to measure, recognizing that we can
only survey a smal portion of the entire reef. Adequate sample representation is, therefore, a crucial
component. Reliability pertains to how efficiently a method measures specified parameters over the
entire set of sampling conditions likely to be encountered, and should incorporate valid replicability.
Sample representation and replication ensure that statistical power is optimized, a given situation is
properly characterized, and meaningful comparisons can be made in space and time.
Standardized sampling protocols
Many current surveys use a standardized sampling protocol. This facilitates regional comparisons
but sometimes sacrifices a detailed characterization of the complexity of local reef environments.
Therefore, it is important to consider what the objectives of an assessment or monitoring scheme
are. If the data are to be used local y to address management issues, then it is important to take
into account the complexity of the local reefs. However, if the data are to be deposited into a larger
database for regional or global comparisons, then a standardized protocol applied across sites is
necessary. With the general deterioration of reef communities at local and regional levels, it is clear
that the best approach combines the two.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
4.2 Coral disease rapid assessment and monitoring protocols
Validity and reliability of all types of quantitative assessments require satisfying a fundamental condition:
an adequate estimation of the natural variation of the chosen parameters (disease prevalence, coral
cover, etc.). Imposed upon this critical point is the very real consideration of time, resources and
personnel limitations. The fol owing recommendations are provided to help address these issues.
What are the goals of the sampling?
What questions are to be addressed and at what spatial and temporal scales? Rapid regional
assessments can reveal large-scale processes such as the expansion rate of a particular disease from
an infection `hot spot' to nearby reefs, and serve as an early warning system to identify and track
disease outbreaks. Monitoring targeted to address very specific questions can provide data on the
status of a particular disease or coral species, seasonality, incidence and effects of diseases at a local
scale, and the role of localized stressors on disease processes and impacts. Monitoring individual
colonies wil result in the documentation of patterns of spread, rates of tissue destruction, impact of
diseases at a colony or population level, and the fate of affected colonies.
How many sites?
Reefs can general y be divided into distinct zones, created by strong environmental gradients acting
on the benthic community. The back reef, reef flat, reef crest, fore reef or slope are the standard zones,
though these can be highly modified by bathymetry and coral growth, and may even be absent.
Further, depth can change drastically within a zone and provide even more complexity. Here, we
define "site" as a zone or habitat of distinct structure within a reef.
For descriptive or rapid assessment surveys, logistics and time constraints may make it necessary to
limit sampling to a single zone within a reef (such as the reef crest). In such cases, the same habitat
or zone should be surveyed at each location. If great variation exists in community structure within a
depth range or zone (due to high relief, spur and groove formations, etc.), there may be more than one
"habitat" present and further within-zone stratification wil be required. For space/time comparisons,
at least three replicate sampling units per zone/habitat (linear transect, radial arc, etc.; see Table 4.1)
are recommended, as differences between sampling units can only be examined in comparison to
variation within sampling units.
What sampling technique and sampling unit?
Consider objectives, logistics, time, and resources, and refer to Table 4.1 for the most commonly used
sampling techniques. Select the technique that best suits the local conditions while addressing the
objectives of the sampling. The same sampling technique should be used in all areas. The sampling
unit is defined by the question(s) asked, which should consider appropriate spatial and temporal
scales. For example, if the question refers to colony properties, the sample unit wil be each colony
and the technique may involve censusing al colonies within a defined area. If the question refers to
populations or communities, then the sampling unit will be an area or length of reef that is surveyed.
Belt transects, circular areas, and quadrats are examples of area sample units, while line, chain and
point intercept transects are examples of linear sampling units. Sampling units should be replicated
within each site; this is discussed in the section below on sampling unit number.
What sampling unit size?
This depends on the size and type of spatial distribution of the coral colonies and, in practice, on
logistical constraints. A community with large colonies requires larger sampling areas than one
dominated by smaller ones. Area-based sampling units (quadrats, belt transects, etc.) bias count data,
due to the effect of including or excluding colonies that extend beyond the edges of the sampling unit
(i.e. the "edge effect"). The larger the colony size in relation to the size of the sampling unit, the larger
this effect, as a greater proportion of colonies wil be excluded. To minimize the edge effect, Green
(72) recommends that the ratio of colony size to unit sample size should be very smal : a sample area
should be 20 times larger than the mean colony size. Zvuloni et al. (73) propose a mid-point criterion:
if more than 50 percent of the colony lies within the sampling unit, the colony should be counted. If
a reef community contains many single-species stands (i.e. Acropora thickets), then a smaller size is
52
convenient (see Green 72, for details). Again, within a single monitoring program, the same sample
unit size should be used in al reefs. This may require some compromise as reef communities are
unlikely to be the same, but it is an important point if data are to be compared across reefs.
How many sampling units per zone/site?
Replication is mandatory because without it, there is no way to estimate variance of the measured
parameters. For a preliminary sampling effort, three sampling units per site may be enough, provided
the site is relatively homogeneous. If resources permit, six sampling units are sufficient in most
instances. The number of replicates should be constant for al areas compared, i.e. six belt transects of
20m² (10mx2m) in each of three habitats or depth intervals (deep reef, intermediate depth and shal ow
reef). This amount of replication (18 total sampling units) adequately samples the different habitats
and the reef as a whole, provided the sampling units are adequately distributed. However, this takes
a large amount of time and may not be logistical y possible. In such cases, it may be necessary to
sample at two depths, and to cut the number of sampling units to three per depth.
How should the sampling sites and units be spatially distributed?
Sampling sites and units should be randomly distributed within the reef zone/site area if possible
(Figure 4.2). If the sampling units are not independent of each other and are somehow influenced by
the researcher's own decision-making process, then a major violation of statistical principles has been
made and the results wil be invalid. Therefore, spatial randomization must be worked out beforehand.
The best way to do this is by fol owing these steps:
1. If a benthic map is
available that shows the
different reef zones or
habitats, roughly define
the spatial extent you are
interested in sampling
using
geographical
coordinates.
4
2. Within that area, overlay a
square grid. The squares
should be slightly larger
than the area of the
sampling unit to avoid
overlap.
3. Then assign a number
to each square, and
randomly select which
numbered squares will
Figure 4.2 A schematic map showing placement of quadrats along a series of transects.
be sampled. (There are
The quadrats to be surveyed were randomly selected prior to surveying.
several free random
number
generating
programs
available
on the Internet.)
4. Upon arrival at the reef, find the squares to be surveyed using a GPS. Finding the predetermined
squares using GPS at the site is chal enging, and wil not be possible if you do not have access to a
boat. If this approach is not possible, then it is common practice to locate the general reef habitats
once at the site, and to place replicate sampling units equidistant from each other while keeping
depth constant within a habitat or zone. This can be done by deciding on a predetermined number
of fin kicks to swim underwater between transects.
By making an arbitrary decision regarding placement of transects before conducting the surveys,
you will avoid observer bias.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Permanent or re-randomized sampling units for monitoring?
Different monitoring programs use different strategies. The decision to establish and resurvey
permanent sites or randomly select new sites to survey each time may or may not be within the
manager's control. However, when a manager is able to make this decision, the pros and cons of the
two approaches are outlined below.
Permanently fixed sampling units
Permanent sampling units minimize variability due to sampling error, which increases data reliability.
The main challenge lies in taking the care to establish well-marked permanent units. If this is not
done, then searching for underwater markers and re-deploying sampling units can eat up valuable
bottom time underwater. There are steps that can be taken however, to make relocation relatively
straightforward (see Box 4.1). Furthermore, accuracy in relocating permanent sites increases over
time as observers become more familiar with the site. Final y, permanent sites al ow estimation of
disease incidence and impacts over time using many fewer sites. This approach may provide specific
information for a particular reef or zone but much more time is required to discern patterns over
multiple reef systems.
Re-randomization of sampling units
Re-randomization of sampling units for each survey of the same reef site may result in more
comprehensive data on prevalence over an entire reef system than is possible with fixed transects, as
a greater reef area is surveyed over time. However, variance is likely to be higher due to micro-habitat
differences and sampling error, and a larger number of sampling units wil be required to achieve the
same statistical power. Furthermore, the number of random sites needed to measure change wil be
much greater because you are not looking at the same corals each time.
The optimal approach, given sufficient personnel and funding, is to establish permanent sites in
representative habitats/depths and supplement these with a larger number of random sites that are
examined using a rapid assessment technique.
What sampling frequency?
It is preferable to sample quarterly or more often to avoid missing disease outbreaks and capture
any seasonal component that might be impacting the reef. Diseases often affect individual hosts
for a relatively short time, with new infections appearing on surrounding corals at frequent intervals.
Infrequent sampling makes it difficult, if not impossible, to accurately assess the duration of individual
infections and their role in coral mortality. Further, targeted samplings during a certain time of year
may incorrectly estimate the importance of disease in structuring coral communities. Coral mortality
may be caused by numerous factors in addition to disease, which may not be recorded if samplings
are conducted infrequently. Because outbreaks caused by rapidly-progressing diseases may die
out in a short period of time, it is advisable to conduct rapid assessments frequently and be ready
to conduct quantitative surveys if such an event occurs (see Chapter 5, for details on characterizing
an outbreak).
When are controls necessary?
In scientific research, a "control" is the treatment whereby al parameters are exactly the same as
for the experimental manipulation except for the one parameter that is being tested. This al ows a
comparison of the effect of the parameter. In ecological monitoring, control sites may be necessary
if the objective is to examine the effect of an impact on some aspect of the reef community. In this
case, a control site is one unaffected by the impact and against which impacted reefs are compared.
For example, if the objective of a monitoring program is to quantify the effects of a sewage outfall
on disease prevalence, it is necessary to identify a minimum of three replicate sites predicted to be
affected by sewage. The same number of sites remote from the outfal , but of similar structure, must
be selected as un-impacted controls against which to compare the effect of sewage.
54
Why is preliminary sampling advisable?
Prior to beginning a major rapid assessment or monitoring effort, it may be necessary to conduct
preliminary pilot assessments. Such assessments are useful in estimating the amount of variation in
the parameters being monitored (i.e. live coral cover, prevalence, etc.), so appropriate decisions can
be made regarding replication and sampling technique. Preliminary sampling also has an additional,
rather practical benefit most potential problems can be identified early. These include problems
relating to sampling design decisions (sites, stratification, type, number and size of sampling units,
taxonomic level desired, disease types or signs) and field logistics. Therefore, the final sampling design
will be based on direct, practical knowledge of the area, rather than on untested assumptions.
4.3 Designing a monitoring program
A comprehensive coral disease monitoring program should apply principles of epidemiology and
risk analysis to coral health assessments. This will help identify predictors (i.e. risk factors) for changes
in coral and ecosystem health (such as warm temperatures or increased nutrient loads); quantify the
strength of those associations; and focus diagnostic efforts towards identifying etiology (see Chapter
3). Standardized disease monitoring programs can be supplemented with the fol owing:
a. detailed disease assessments (see Appendix 4 for sample data sheets);
b. additional population information (i.e. abundances, size classes, species diversity, and health status);
c. quantification of species which may indicate potential health risks to corals, or improvement in reef
health as a consequence of management (i.e. macroalgae, herbivores, coral predators); and
d. measures of water quality (i.e. sedimentation, nutrient input, bacterial load). Often, water quality
monitoring may be undertaken by a different local agency or individual, so collaborative agreements
between coral disease and water quality monitoring agencies or individuals may result in reduced
cost and effort.
Monitoring should be proactive; it can help predict the likelihood of events such as a disease outbreak,
4
responsive changes in community structure, and recovery rates. A combination of rapid random
assessments and long-term monitoring of permanent sites provides the most comprehensive picture
of the impacts of disease on an area.
4.4 Characterizing long-term disease effects on population
dynamics, community structure and ecosystem function
Monitoring permanent sites (in addition to random surveys) results in data on the rate of occurrence of
new infections and disease impacts at different scales (colonies, species, populations, communities).
Long-term monitoring of individual y tagged colonies affected by disease can also provide detailed
information on the spatial and temporal dynamics of particular diseases. Such information
might include:
· the rate of spread of infection within a colony;
· amount and patterns of mortality sustained from an infection;
· change in the number of lesions over time;
· change in lesion spatial distribution;
· lesion dynamics (position of lesions on colony, temporal scale);
· duration of infection;
· host colony fate (recovery, progression, stasis, mortality, re-infection); and
· environmental correlates.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
A monitoring program implemented for coral diseases at the population/community level should
address the following:
· types of diseases/syndromes, host range, and variation in disease dynamics between species;
· prevalence and incidence of diseases (population or species level), duration of an outbreak,
consequences to host species, and variability at various spatial and temporal scales;
· local, regional and global distribution of diseases;
· physico-chemical parameters (depth, water clarity, temperature, nutrient load, etc.), biological
factors (predators, algal abundance, bacterial load, etc.), and anthropogenic impacts (pollution,
runoff, sedimentation, etc.) associated with either chronic or acute disease events;
· long-term effects of disease on coral reef community structure and function at local and regional
scales; and
· potential reservoirs and vectors of disease.
4.5 Establishing and relocating permanent monitoring sites
Working with permanent sampling units can be chal enging to begin with, as it involves finding an
original marker position after time has lapsed, doing so in changing environmental conditions, finding
markers that are covered with overgrowth, and working with different personnel. However, it is important
to do these things properly so the time spent setting up permanent sites does not go to waste.
Once sites are selected and the survey method defined using the guidelines in Section 4.2, a list of
materials must be produced (see Table 4.2). This list should include everything needed for:
a) marking and finding the sites;
b) marking and finding the permanent sampling units; and
c) col ecting data.
Many of these materials should be available during every survey because re-bars, tags, flagging tape,
buoys, etc. can disappear between surveys and require replacement.
When establishing permanent sites, researchers should attempt to minimize human interaction on
the reef and deploy permanent stakes and tags in as discriminate a manner as possible. For example,
re-bars and masonry nails should never be inserted into live coral and all floats, cable ties, tags and
other materials should be secured such that they do not abrade corals or other sessile invertebrates.
A procedure for establishing permanent transects is described below. This method requires insertion
of multiple re-bars per transect. Other approaches, such as those for radial or circular sites, require a
single permanent rebar (and submerged buoy or float to facilitate relocation of the site) and equipment
for subdividing the site into measurable units, which are temporarily deployed only when assessments
are underway. After the study is completed, the markers should be removed.
56
Table 4.2. Recommended materials list for setting up a permanent survey area within a reef
Site ID materials
Marking materials
Data collection materials
Differential GPS
1/2 m long 5/8' re-bar stakes
UW disease ID cards
Depth gauge
Heavy hammer or mallet
UW coral species ID cards
Mooring buoy
Large plastic numbered tags
Slateboards
Rope
Cable ties (different lengths)
Plastified UW paper
UW digital camera
Small floaters/buoys
Transect tapes
Temperature loggers*
Monofilament for tying
Mechanical pencils
Submerged buoy(s)**
Clipper and dive knife
Underwater notebooks
Masonry nails
Magnifying lens
Marine epoxy or Z-spar®
Plastic caliper or ruler
Plastic bags+
Hammer, chisel, wire cutters
*HOBO® temperature loggers are easy to deploy and can remain at a station for up to five years.**At some sites, it may be
necessary to deploy marker buoys underwater. A GPS unit can be used from the surface to mark the site of a submerged
buoy. +Plastic bags are used to store diseased tissue sampled using a hammer and chisel or wire cutters, if a microscope is
necessary to verify field determination.
Establishing a permanent monitoring site using a transect
Refer to Box 4.1 at the end of this chapter for advice on how
to relocate sites in successive visits. For the regional assessment
and monitoring of diseases in the Caribbean, for example, the
design included five 10mx2m (20m²) belt transects in each of
three depth intervals (habitats) per reef (n=15 per reef, with a
total surveyed area of 300m²), three reefs in each country, and
three countries per major geographic region (Weil, pers. comm.)
4
Below is a step-by-step procedure for establishing a permanent
monitoring site using a transect:
1. If the sampling design includes depth intervals or multiple
reef habitats, start with the deepest habitat first. Once a pre-
survey swim of the site has revealed the optimum general
area for monitoring, hammer in the first tagged re-bar and
deploy the transect tape, keeping depth relatively constant
(Figure 4.3). At the end of the predetermined transect
Figure 4.3 A rebar stake used to position
a transect line. Photo: C. Caballes
length, hammer in the end re-bar. Re-bar stakes may require
additional epoxy, cable ties, or other means of stabilization;
they must be completely immobilized and secured to the
bottom. The first re-bar of each transect should already have
the tag number and/or buoy attached so you do not waste
time underwater. Use plastic tags with large numbers (such
as livestock tags; see Figure 3.3).
2. Hammer in masonry nails every 5m along the tape, avoiding
living tissue. These will allow placement of the tape over
the same line every time. If there is surge or currents, the
tape is wound around the nails to prevent bending and
displacement. In reefs with high topographic relief or on
transects more than 10m long, nails may not be visible;
re-bar stakes can be used in their place at 5-10m distances
Figure 4.4 Laying a transect line along a
along the transect length. The transect tape should be laid
permanently monitored site. The line must be
along this line tautly, to prevent displacement by surge or
laid taut, so that the area monitored remains
the same over time. Photo: C. Caballes
current (Figure 4.4).
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
3. Tie flagging tape or a submerged buoy onto the beginning
and end re-bars of the transect (Figure 4.5). An additional
buoy/floater can be tied to the midway transect marker
(nail or re-bar). This wil facilitate finding the transect in
future surveys.
4. To place the next belt transect haphazardly, use a
pre-established method such as moving 1m to the right or
left of your previous transect and swimming 10 fin kicks.
Then, hammer in the first re-bar of the second transect.
Repeat this procedure with al transects at al depths.
If quadrats are used along the transect, their position
should be randomized (see Figure 4.2) and recorded.
Rebar stakes or nails can be used as reference points to
position the quadrat in exactly the same position each time
(Figure 4.5).
Figure 4.5 Flagging tape tied to the end of
a re-bar stake provides a visual marker for
relocating a transect. Photo: E. Weil
4.6 Calculating prevalence,
incidence, and gross disease characteristics
Data collection
Data from any sample unit that surveys a defined area (belts, quadrats, circles) may be applied to the
calculations detailed below. Using the selected sample unit, al colonies larger than 5cm in diameter
(or whatever criterion is selected) are counted, identified to whatever taxonomic unit is decided upon
(species, genus, morphological type, etc.), and examined for presence of disease or compromised
health, using categories outlined in Chapter 2. These data are entered on a data sheet (see Appendix
5 for examples in current use). How precise a taxonomic identification is needed depends on the
questions, surveyors and geographic area. In the Caribbean, there are only ~62 zooxanthellate coral
species, so col ecting data at the species level is possible. In the Indo-Pacific, more than 700 species
have been recorded, so data are normally collected at the genus level, and segregated by morphology
(branching, massive, encrusting, etc.). Additional data on colony size and percent mortality can provide
useful information on population dynamics, community structure and impacts of disease and other
stressors. For example, in the western Atlantic many researchers measure the height and diameter of
colonies and record the percent of the colony surface with recently denuded skeleton and older, algal
colonized skeleton.
Disease prevalence
Disease prevalence is the proportion of diseased colonies to the total measured population of
colonies. It can be calculated for individual populations, species or genera, or for the coral community
as a whole, as wel as for each particular disease/syndrome, similar group of diseases or for al diseases
lumped together. What is calculated depends on the questions asked.
Prevalence (P) = (# diseased colonies/total # of colonies) x 100
A prevalence value is estimated for each area-sample unit. An average prevalence value with standard
deviation can then be calculated for habitats, zones or reefs (depending on the stratification and the
questions) using the sample unit prevalence value.
58
Disease incidence
Disease incidence is the number of new infections appearing in the population within a period of
time. This is a very important record of the progress of a particular disease in a particular species,
population or community; it characterizes the epizootic temporal dynamics. To estimate the incidence
of a particular disease, all infected colonies found during the first survey should be tagged and/or
mapped within each sampling area. This is particularly important if the disease is short-lived or seasonal
(such as black band disease or white plague). During subsequent surveys of the same sampling units,
newly infected colonies are then identified, counted, tagged and mapped. Dead colonies should be
counted and caution must be taken to make sure colonies are not counted twice. For example, if a
colony is infected during time T , and is dead at time T , it is only added to incidence calculations
2
4
at time T . Records of dead colonies should be noted separately, as mortality rate. However, if the
2
colony was healthy (and, therefore, unmapped and untagged) during a previous survey (i.e. time T ),
2
but dead by the next survey period (i.e. time T ) then it should be counted in both incidence and
3
mortality calculations at time T (but only if cause of death can be verified as the disease in question).
3
It should also be tagged and mapped so that it is not recounted in later surveys. Average incidence is
calculated for the site as a whole after incidence values are calculated for each sampling unit for the
habitat and/or reef in question. See Chapter 5 for how to use incidence observations to calculate rate
of outbreak.
Incidence (I) = number of new infections within a time period, T
Mortality
Often, the aspect of most concern is mortality rate, as this can have profound consequences on the
structure of a reef community. Mortality rate can be calculated as follows:
M = number of colonies dying per census area per unit time
total number of colonies within census area
4
However, if the dynamics of a particular disease are of interest, such as how this disease is affecting
a particular species, or how severe it is, then the case fatality rate (Chapter 3, Section 3.1) may be
of interest. The case fatality rate measures the mortality rate of those susceptible and affected by a
particular disease:
CF = number of colonies dying of a disease per census area per unit time
total number of colonies with the disease per census area per unit time
These calculations can be used on individual coral species, or on the coral population as a whole.
Another aspect that may be of interest is partial mortality. Corals, as colonial animals, can "partially
die", i.e. they may lose a certain portion of their tissue, but the remaining tissue may be healthy and
capable of regrowth. Therefore, it may be of value to monitor partial mortality as a percentage of the
colony which dies as a result of a disease. One can then monitor whether or not the tissue regrows and
recovers after partial mortality has apparently stopped, whether partial mortality continues to progress
to ful colony mortality, or whether the disease appears to come to a halt, but with no apparent
tissue regrowth over bare skeleton. In these cases, it is necessary to develop a way of determining
the percent of the colony surface area affected. For branching and foliose morphologies, the total
number of branches, as wel as dead and dying ones, can be counted and a `percent of colony
affected' calculated. For massive, plating and encrusting forms, the percent of affected surface area
can be calculated from photographs, (see "using photographs" below), or lesion and colony diameter
can be measured by hand using a transect tape or calipers. If hand measurements are to be used it is
customary to take a measurement at the widest diameter and then one perpendicular to the widest.
The mean can then be calculated from these two, and the `percent of colony affected' calculated as
the ratio of lesion size to colony size.
59
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Disease characteristics at the colony level
If colonies are tagged in order to monitor disease characteristics at the colony level over time,
representatives of both diseased and healthy colonies must be tagged within or near the sampling
unit. If the disease is affecting multiple species, then
replicate colonies of each species should be monitored.
Logistics and time resources should be considered when
deciding how many replicates to tag, although five healthy
and five diseased colonies per species would be a
minimum number. The information obtained through this
process (such as that listed in Section 4.4) is useful for
characterizing the etiology of particular diseases. These
diagnostic characteristics help define the etiology, such as
daily, weekly, monthly or seasonal changes in lesion or
band appearance. Al information should be col ected in a
template sheet already formatted for this purpose to
reduce the amount of underwater time needed, and to
standardize data col ection.
Figure 4.6 A masonry nail (see arrow) hammered into
dead skeleton can provide a useful reference point
and scale for monitoring disease progression in an Using photographs
active lesion. Here a massive Porites colony exhibits Photographs of diseased colonies are important sources of
signs of white syndrome. Photo: L. Raymundo
information. When taking photos for later analysis, always
place an appropriate scale bar in each photo; a plastic ruler
is the easiest to use. In addition, in massive and encrusting
morphologies, a masonry nail can be hammered into the
colony at the immediate edge of the advancing front when
the colony is initial y tagged (hammer into dead skeleton,
not into live tissue; Figure 4.6).
In subsequent visits, the distance from the nail to the
new disease front is measured with a ruler. In many cases,
especial y in massive corals, you need a minimum of two
nails per colony for common diseases that advance in a
linear or annular manner as the distance from one nail
to the disease front will vary depending on where you
take the measurement. For branching colonies, a colored
cable tie can be used to mark the original position of the
Figure 4.7 A branch of Acropora with white disease front (again, place the cable tie at the edge of
syndrome. The green cable tie marked the original dead skeleton, not on live tissue) and the distance from
position of the band when it was first observed and
was used to measure disease progression. Photo: the cable tie to the new disease front can be measured
L. Raymundo
in future surveys (Figure 4.7). Average linear advance rate
can be calculated per week or month as follows:
Linear progression rate = distance from nail/cable tie to new disease front
length of time of census (days/weeks/months)
Individual colony time-series photographs, those taken at the same angle and distance during
successive monitoring visits, are powerful visual tools for examining the rate of advance of the disease
front and host colony fate (Figure 4.8). These can greatly reduce bottom time, providing exactly the
same position is used each time. However, you do need to factor in the time needed to process
each photo in the lab. Photographs can be analyzed using image analysis software, which wil al ow
accurate measurements to be taken of lesion size dynamics (increase/decrease) over time. Software
packages provide instructions on how photographs should be taken. The National Institutes of Health
(NIH) provides a free image analysis software package, ImageJ, which can be downloaded from
their website: www.nih.gov. Another suggested package is CPCe, produced by Nova Southeastern
University in Florida, which also provides a method for assessing cover using a series of random
60
points. It can be found on their website: www.nova.edu/ncri/research/a10.html
Figure 4.8 Five-day progression of a white syndrome infection on a tagged colony of Lobophyllia.
Flagging tape tied to a nail provided both a visual reference and a scale bar to use a image
analysis of the rate of tissue loss. Photo: K.Rosell
4.7 Studying links with environmental drivers
In Chapter 1, we discussed environmental degradation on global, regional and local scales
and its links (potential and realized) with stress to coral communities. Because of this link, the
importance of monitoring water quality concurrently with benthic monitoring has been recognized.
Suggestions for how to do this are outlined below. However, logistical and cost issues may preclude
a comprehensive plan.
Included in this section are guidelines for measuring some of the basic environmental variables which
may have potential impacts on disease dynamics. Managers are encouraged to find out what water
quality parameters are regularly monitored by other agencies in their area, and to develop collaborative
arrangements so such data can be shared. Correlations between changes in environmental parameters
and disease prevalence or incidence, or in the severity or rate of disease progression, can be tested
with simple statistical tools, and by graphing a certain disease parameter against the environmental
parameter in question (Figure 4.9).
4
Sea water temperature
At present, the only regional/global environmental variable of concern that can be easily monitored
is sea water temperature, but it is an important one for diseases as well as bleaching events. An
efficient way of monitoring sea water temperature is by means of submersible continuous recorders
such as Tidbits (HOBO®) water temperature loggers. These loggers can be preprogrammed
to record data at fixed intervals
for a prolonged period of time.
10
Earlier models require calibration
before and after use with a clinical
evalence 8
thermometer, as they can be
inaccurate by up to 3ºC. However,
6
new versions (U22-001 units) can
be deployed deeper (to 30m) and
4
programmed to record data for up
otal Disease Pr
to five years. Data can be
downloaded and re-launched
2
underwater with a shuttle unit, and
Mean T
so can be immediately redeployed.
0
24
26
28
30
32
Mean Water Temperature, oC
Figure 4.9 Hypothetical data set showing a strong relationship between increasing
sea temperatures and total disease prevalence. Simple graphs, such as this one,
can il ustrate the strength of a relationship between a measured environmental
parameter and disease.
61
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Two units per sampling site are recommended; one deployed at shallow and one at deep depth limits
of the monitored habitat or zone. If a strong environmental gradient exists among sampling sites, more
may be needed. Temperature data can be summarized and plotted against disease prevalence data
so evidence of co-variation between disease prevalence and seasonal changes of specific diseases or
disease outbreaks can be detected.
Silt and sedimentation
Sedimentation is problematic in many
coastal regions of the world where
land use practices are poorly regulated
and terrigenous soil and silt are
deposited into nearshore communities
via rivers and runoff (Figure 4.10).
The sedimentation rate reflects the
processes of deposition/delivery and
resuspension of silt. It can be measured
by setting replicate sediment traps
in sampling areas and col ecting and
replacing the traps on a weekly or
monthly basis (Figure 4.11). Sediments
are processed in the lab fol owing
standard protocols (rinsing, air- or oven-
drying, weighing) and sedimentation
rates per unit time (day/week/month)
Figure 4.10 Chronic highly turbid conditions from silt deposition and are estimated. Sediment composition
resuspension can stress corals and other nearshore benthic organisms.
Photo: L. Raymundo
(i.e. the proportion of calcium carbonate
to terrigenous materials) and granule
size composition can also be determined. Such analyses can provide useful information regarding the
sources of silt, its long-term impacts to benthic community health and structure, seasonality variations
in silt delivery, and covariation with disease prevalence and bleaching events.
If sediment traps and laboratory equipment for sediment
analysis are unavailable, a less sophisticated method of
estimating water clarity can be used. A Secchi disc provides
qualitative estimations of clarity/turbidity, though it is not useful
in shal ow, clear water. A Secchi disc is a 30-cm diameter
fiberglass, metal or wooden disc, painted white (Figure 4.12).
(Note that those used for freshwater lakes are usual y painted in
black and white alternating quadrants.) It is lowered over the
side of a boat attached to a weighted rope, and sunk until it is
no longer visible. The length of rope deployed is then measured,
the disc is pul ed up until it is visible again and then lowered
again until it disappears. The water depth at which the disc
disappeared is used as an estimate of the depth of light
attenuation. These measurements are rather qualitative and are
therefore only used relative to other such measurements (i.e.
when irradiance, cloud and wave conditions are similar).
Nonetheless, they can provide an easy and inexpensive way to
Figure 4.11 A sediment trap can be a compare variability of water turbidity between sites and seasons.
deployed to quantify the amount of silt and To standardize Secchi disc readings, always have the same
other particulate matter settling onto a reef.
Photo: E.Weil
person take the measurements, lower the disc on the shaded
side of the boat, and always take measurements on sunny days,
between 10am and 2pm, and at the same position at each site.
62
Other water quality parameters
Additional water quality parameters that may indicate environmental stress on corals include pH,
nutrient load, and bacterial load. These, however, are more difficult to measure continuously if
there are no funds for instrumentation and laboratory analyses. Managers are encouraged to link
with laboratories, local environmental regulatory agencies, and even hospital laboratories, if it is
perceived that any of these factors may be an important management issue that requires attention
and monitoring.
Rainfall and river discharge
It has been verified that two diseases in the Caribbean,
aspergil osis and white patch disease, are caused by
ubiquitous terrestrial opportunistic pathogens (a soil fungus
and a human intestinal bacterium, respectively) (52,65).
While a definitive source of these pathogens has not been
identified, it is a strong possibility that human activities
were instrumental in either delivering these pathogens to
nearshore reef environments or increasing their concentration
in these environments.
In addition to being a source of potential pathogens in
coastal waters, river discharge and non-point runoff are the
main sources of terrestrial-based anthropogenic stressors
such as fertilizers, pesticides, silt, sewage, and heavy
metals from roads. Rainfal varies seasonal y and alters river
discharge, affecting salinity and pol utant loads in coastal
receiving waters. Therefore, data on rainfal patterns may
Figure 4.12 A Secchi disc is a useful and provide a proxy for seasonal shifts in the delivery of fresh
inexpensive tool for qualitatively comparing water and pol utants onto reef communities. Often, rainfal is
water turbidity between sites, providing it is used
in a standardized manner.
monitored by a local weather bureau which may also monitor
river discharge. Such data are usual y easy accessed, and
4
may reveal links with seasonal changes and the prevalence of specific diseases. Where covariation is
observed, further investigation is warranted to determine what stressors or pathogens may be linked with
the disease impacts.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Box 4.1
Relocating difficult sites
We wil address one difficult, but not uncommon, case here: setting up a sampling area which
meets all criteria of the survey plan, and then relocating it in future survey trips when there are
no convenient external spatial references (coastal reference marking, visible mooring buoys) or
when conditions are difficult (strong winds, deep sampling sites, limited underwater visibility).
Before leaving the dock, tag al re-bars (or long masonry nails) and organize them in groups
for marking each transect. When the reef site has been selected after preliminary survey
dives, its waypoint (i.e. geographic coordinates) should be recorded in the GPS unit and in
a field notebook, along with al reference information to the site (bearing direction from the
dock, distance from shore, any shore positioning markings, etc.). After al transects have been
established, construct a map of the survey area with the relative location of transects and any
major bottom features that can help relocate the sampling area (Figure 4.13). Bearings should
be taken with a high precision UW compass, and distances between markers estimated to help
divers find the transects in subsequent trips.
Placing a mooring buoy to mark the sampling site is the quickest way to relocate the site
and ensure anchor damage is prevented. But when this is not possible, a sub-surface buoy
can be used. To avoid problems of limited visibility or to compensate for a less-than-accurate
GPS re-positioning, another sampling site waypoint can be obtained to mark the position of a
very distinct and large bottom feature within the sampling area. This feature should be clearly
identifiable from some distance and will be the bottom spatial reference point, marked in the
sampling area map and photographed for future use.
Obviously, the most practical way to relocate a site is with a GPS unit (Figure 4.14). However,
the usefulness of this approach is dependent on the familiarity of the user with its limitations.
Care should be taken to obtain the correct first GPS position, making sure that there are no
drifting effects. To avoid this, mark the waypoint with a small anchored buoy with very little
rope slack. Relocating the waypoint also requires counteracting any drifting effects, so use the
same principle when returning to the site.
Figure 4.13 A map of transect locations at Las Pelotas in
Figure 4.14 A map of a series of transects on the Yucatan
Puerto Rico. Additional underwater structures and data
Peninsula, Mexico. Transects were located by GPS for ease
loggers were included for reference, to assist in relocating
in relocation.
transects during subsequent visits.
64
Chapter 5
Detecting and Assessing Outbreaks
In this chapter you will find:
How to define a disease outbreak
in a coral community.
An overview of early warning signs
of coral disease outbreaks.
Approaches for determining the extent
and impact of a disease outbreak.
5
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Detecting and Assessing Outbreaks
C.D. Harvell, C. Woodley, L. Raymundo and Y. Sato
5.1 When is a situation an "outbreak"?
An infectious disease outbreak is defined as a situation whereby the rate at which new hosts become
infected increases. In other words, it is an unexpected increase in disease or mortality where it does
not normally occur, or is at a frequency greater than previously observed. In Figure 5.1, we provide an
example of outbreak dynamics for human diseases. As demonstrated in this graph, once the infected
host population reaches a critical size, the number of new cases increases exponentially. As
more individuals within a population
are exposed to the disease, the
Establishment
Exponential
Endemicity
Growth
number of new cases eventual y
declines, either through host recovery
and immunity or death. The disease
Removal of
then becomes a long-term aspect of
Susceptibles
the population dynamics, becoming
endemic and either reaching
equilibrium with few occasional cases,
or undergoing periodic outbreaks.
Figure 5.2 shows an actual outbreak
Equilibrium or
Rate of New Infections
Recurrent Epizootics
of Bubonic Plague in Sydney in 1903.
The epidemic fol owed this general
pattern, becoming endemic afterwards
until it was eradicated.
Time
Figure 5.1
For coral, the situation is different;
General example of dynamics of an infectious disease outbreak
in a human population. An outbreak begins with random events that infect corals are a highly diverse assemblage
a small number of hosts. New cases occur exponentially after the infected of immobile, colonial animals that
population reaches a critical number. The outbreak dies out when the can only come into contact with
susceptible population declines either through death or increased immunity.
Redrawn from Anderson et al. (4).
other such animals via growth. The
surrounding water in which they grow
provides a means of contact with
potential vectors of disease such as
fish. In addition, portions of a colony
may die in response to disease, while
other parts may remain disease-free,
providing an avenue for recovery or
eventual re-infection. Therefore, we
need to modify approaches applied
to humans and other vertebrates
to manage coral diseases. For
instance, in corals, we may also
apply the concept of an outbreak
to a disease that suddenly affects
a species previously thought to be
resistant, or when there are signs of
disease which do not correspond
with any described in the literature
Figure 5.2 Disease dynamics of Bubonic Plague in Sydney, Australia, 1903. (i.e. a potential y new or emerging
Modified from Keeling & Gilligan (3).
disease). To develop a table similar to
that of Table 5.1 for a coral disease
would require catching the outbreak
66
in its early stage, marking al diseased
colonies in a defined area of reef, and monitoring the accumulation of new cases through time. This
brings to the forefront the importance of long-term monitoring and regular random assessments, as
it is during such activities that the early stages of outbreaks may be noticed. If a disease outbreak is
observed early, then as much information as possible can be gleaned from the event, and a number
of management options can be undertaken. Refer to Chapter 6 for detailed information on strategies
and options for managing coral disease.
Technically, an outbreak is defined as an R value greater than one (4). R is the "average number
0
0
of secondary infections produced when one infected individual is introduced into a population
of susceptible hosts". An estimation of R can be calculated if enough information about disease
0
transmission is known: (the number of contacts per unit time) x (transmission probability per contact) x
(duration of infectiousness). A more direct approach of estimating R from field data as the normalized
0
accumulation of new cases (i.e. newly infected colonies) over time may be more attainable.
Because corals are sessile, it is more possible to directly estimate R in field populations than for
0
most animals.
R = (NT - NT ) / NT
0
2
1
1
Where
NT1 = the number of cases at time T1
NT2 = the number of cases at time T2
A disease will increase in a population with R > 1; i.e. a diseased individual wil more than replace
0
itself. A disease will decline with R < 1, and is considered endemic when R = 1.
0
0
Table 5.1 presents some established R values for certain wildlife diseases.
0
Table 5.1 Examples for estimation of the basic reproductive rate (R ) for various pathogens in wildlife species (modified from
0
Real and Biek 74).
Pathogen
Host species
Scientific name
R
0
Rabies virus
Spotted hyena
Crocuta crocuta
1.9
Phocine distemper virus
Harbor seal
Phoca vitula
2.8
Mycobacterium bovis
Feral ferret
Mustela furo
0.181.20
Mycobacterium bovis
Eurasian badger
Meles meles
1.2
Classical swine fever virus
Wild boar
Sus scrofa
1.12.1
5
Both R and incidence can be estimated from field populations of marked corals (see example of
0
incidence calculation in Chapter 3). The fol owing example is provided for Black Band Disease of
Montipora near Orpheus Island, Australia. Three 10mx10m quadrats were established in the vicinity,
each encompassing 10-30 diseased colonies. Within the quadrats, al diseased colonies were marked.
Quadrats were subsequently censused monthly for two years, and water temperature was recorded
simultaneously. Monthly census intervals were considered sufficient as BBD does not spread very
rapidly. In 2006 and 2007, outbreaks coincided with rising summer temperatures from November
through to March, and declined in the cooler months of April through to August (Figure 5.3).
R was calculated as the average per capita increase in colonies with BBD (Table 5.2). An R < 1 in
0
0
February 2006 indicated that BBD cases were declining; an R > 1 in December 2006 and January
0
2007 showed an increase in disease within the susceptible population. The extremely high R value
0
of 7.5 in December 2006 indicated the outbreak could become epidemic if temperatures remained
high. However, by the following month, temperatures had begun to cool and a corresponding decline
in the number of new cases was observed.
67
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Mean new cases/7days
2.5
2
1.5
1
0.5
0
22- 2- 22- 22- 18- 15- 21- 26- 14- 2- 6- 5- 17- 18- 22- 22- 28-
Jan Feb Feb Mar Apr Jun Aug Sep Nov Jan Mar May Jun Aug Oct Dec Jan
Figure 5.3 The mean number of new cases of black band disease (incidence) affecting Montipora species on the Great Barrier
Reef, Australia. Data are shown only for months when sampling took place. Values taken from three quadrats monitored over
a two-year period. This pattern closely fol ows a seasonal temperature trend and also il ustrates the disease dynamics typical
of an outbreak. Data printed with permission from Sato et al. (2).
Table 5.2 Estimations of R from the change in the number of cases observed during monthly censuses of a black band disease
0
outbreak on the Great Barrier Reef. Mean recovery, change in case number and new cases were calculated as the difference
between the sampling months presented (i.e. Jan-Feb, Oct-Dec, Dec-Jan). Mean change in case number reflects both recovery
and new infections. Mean calculated from three 100m2 quadrats. Data printed with permission from Sato et al. (2).
Census month
Jan 06
Feb 06
Oct 06
Dec 06
Jan 07
Mean # BBD cases seen
14.00
16.33
0.67
5.67
15.67
Mean recovery
0.67
0.00
1.67
Mean change in # BBD cases 2.33
5.00
10.00
Mean new cases seen
3.00
5.00
11.67
R
0.21
7.50
2.06
0
Outbreaks are usually short-lived, and should be treated with some urgency so as much information
as possible can be collected while it is available. Chronic diseases can have equally devastating effects
on populations and communities, particularly due to their potential effect on fitness. Yet because they
are less strikingly visible, it is often more difficult to garner support for an investigation. Nevertheless,
it is important to develop sound protocols for investigating and monitoring both transient outbreaks
and chronic low-level disease, as both wil factor as mechanisms of community change and indications
of impacts to reef health.
68
5.2 Early warning systems for coral disease epizootics
Diagnostic tools for coral disease outbreaks lag behind those developed for bleaching events (For
detailed guidelines see Marshall and Schuttenberg 75). Though global efforts to fill the knowledge
gaps have resulted in great progress, we do not yet have the ability to accurately detect pending
disease outbreaks before they happen. However, there are predictive tools available which are
currently being tested for applicability to disease outbreak investigations. For example, regular
monitoring of water quality parameters and environmental factors, as discussed in Chapter 4, can
indicate potential stressful conditions for corals. Increased stress can affect resistance and increase
susceptibility to existing pathogens. Over time, we expect to discern links between a change in a
specific parameter and a change in the prevalence of one or more diseases. Therefore, monitoring
environmental parameters may help to develop an early warning system for certain diseases.
The complex interactions among stressors, and their effects on corals and reef ecosystems, are generally
poorly understood, making it difficult to assign a specific cause to local or regional declines in coral
health. Persistent high levels of stress can cause sudden whole-colony mortality and disease may or
may not be implicated as a direct cause of death. In contrast, chronic low levels of stress are likely to
result in non-acute, sub-lethal effects on corals, which can have measurable (but not necessarily visible)
effects on growth, reproduction or survival. Furthermore, chronic stress can reduce a coral's ability to
resist disease, making a community of stressed corals vulnerable to an outbreak. Identification and
mitigation of these stressors (i.e. toxicants, pollutants, sediment, nutrients, temperature) at an early
stage of detection may enable the prevention of a disease outbreak.
Compromised health may manifest itself through shifts in coral physiology which may not be visibly
detectable when surveying corals in the field. In the absence of acute mortality, biological indictors
or biomarkers are being developed and tested to identify delayed or sublethal effects of exposure
to stressors in coral. Biomarkers are substances that can be detected, sampled and measured to help
characterize specific changes in health or physiological state. Antibodies, which can be sampled from
vertebrate blood, are examples of biomarkers that can be used to detect exposure to a particular
pathogen. Coral biomarkers can potentially detect cellular physiological changes in a coral before the
coral develops visible signs of il health such as tissue loss or partial mortality. This developing science
is referred to as cellular diagnostics (70). Biomarkers from coral are being sought that can:
1. indicate exposure to a stressor or pathogen;
2. pinpoint an effect of stress or disease on coral physiology; or
3. show susceptibility to the stressor or pathogen.
As with human diagnostic assays, information about particular cel functions can be used to
diagnose various disease states as a result of exposure to a specific stressor(s), and provide
an indication of overall health in the coral. As this technology improves, it is hoped that simple,
"user-friendly" diagnostic tools can be developed which test for levels of stress in corals and which
5
might suggest increased susceptibility to disease before an outbreak occurs.
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
5.3 Techniques to quantify the extent and impact of an outbreak
When almost nothing is known about a disease (as is the case for most coral diseases) or at the
time when a new or emergent disease is discovered, outbreak investigations are vital. An organized,
systematic approach helps determine the extent and impact of the event, the causative agent(s), each
agent's reservoir or source, and transmission routes between hosts. It can also identify knowledge
gaps, help formulate hypotheses for further study, focus research goals, and help identify control or
management strategies. When the cause of an outbreak is known (i.e. when we have identified the
pathogen causing the disease which is rapidly increasing in a population), but the source (reservoir) or
route of transmission remains unknown, much investigative work is still required (as was the case with
Vibrio shiloi, the causative agent of one type of bacterial bleaching). In this case, investigations can
focus on filling the knowledge gaps with regard to the ecology of the disease to better guide future
control and management efforts.
Managers often have the most accurate and up-to-date information critical for an outbreak investigation.
Their knowledge and historical information on local reefs are invaluable when it comes to informing
the investigative process and determining the impact of a disease outbreak. The first objective in this
situation is to create a "definition" of the disease. This includes identifying features that distinguish
this particular disease from others and provides a route to understanding how and why the outbreak
is occurring (76). The questions a manager can begin asking are:
· `who' is affected? (What species?);
· `where' is the outbreak located? (Including descriptions of surrounding environmental factors and
investigating other possible outbreak sites);
· `when' is the event occurring? (Seasonal trends, the rate of movement through a population and
rate of lesion progression on individual colonies);
· `what' features do the clinical and pathology analyses provide toward identifying a causative agent?
(Protocol for this process is described in Chapter 3); and
· `why' or `how' did this occur? (This is the pathogenesis but can also include environmental factors
which might have triggered the event, such as a sudden change in temperature or rainfal , or a toxin
spill).
The initial information provided by the manager is critical to developing the case history and any
subsequent investigation and laboratory work. Assistance in determining if an outbreak is occurring
and how to respond to it can be obtained by contacting the Coral Disease and Health Consortium
(CDHC) via email at cdhc.coral@noaa.gov, Dr. Andy Bruckner or Dr. Cheryl Woodley at NOAA (or see
Appendix 2 for a list of regional experts associated with the CRTR Coral Disease Working Group).
Managers who regularly monitor or assess disease wil know what the characteristic prevalence levels
are for a given area for each disease that has been documented and observed in that area. If a
situation of concern is observed in the course of monitoring or rapid assessments, certain steps can
be taken immediately. The most obvious situation is a much higher number of infected colonies than
is normal y observed for a given disease. Although we usual y speak of an outbreak as referring to a
single disease, this may not necessarily be the case. An outbreak in Palau in January 2005 involved
multiple coral species and both white syndrome and black band disease, though the host range
of the two diseases differed (35). An even more complicated case occurred during a Florida Keys
2003 outbreak, where a disease looked visibly identical in three acroporid host species. Extensive
histological and molecular analyses, however, ruled them to be completely different pathologies (77).
Below are a few simple steps that can be taken when documenting an outbreak:
1. Make an initial description of the affected site, which should include the fol owing information:
benthic composition (see Chapter 4 for methods), depth range, reef zone/habitat, dominant
benthic species, water clarity, current direction and relative strength, proximity to potential sources
of stress such as river mouths, coastal construction zones, cities, and any additional information
available that might shed light on why the outbreak is occurring at that place and time. Even if this
information is qualitative, it can still be useful.
70
2. Identify and describe the characteristics of the lesions of the disease(s) you are observing, using
the decision tree presented in Chapter 2. Photo-document lesions in all species affected. Make
a presumptive field diagnosis of the suspected disease(s) you are dealing with; are you seeing a
disease previously described and/or documented from the affected site? Or do the signs of disease
you are observing not correspond with any previous description? This situation may represent a
new or emerging disease in the area.
3. Develop a host range list a list of all taxa
apparently affected by each disease you
are seeing (Figure 5.4). Make sure to note
any colonies affected by more than one
lesion type per colony. In addition, note all
other taxa within the affected area which
are not infected; resistance to a particular
disease is equal y important information. It
is most helpful to identify to species
wherever possible; at the very least, corals
should be identified to genus.
4. Tag colonies for regular monitoring of
disease progression. If possible, tag
replicate colonies of each species affected
for each disease observed. Attach tags to
dead portions of the colony, or to nearby
substrate, using flagging tape. Photograph
al tagged colonies, being careful to
Figure 5.4. Top view of white syndrome outbreak spreading
among at least 5 species in the genera Lobophyllia, Mycedium,
place a scale bar or ruler in each picture.
Merulina, Fungia, Favia in Palau. Photo: B. Willis
Photographs should attempt to include
the entire lesion; depending on the size
of the colony and the lesion, it may useful
to take both a close-up picture, and a
whole-colony picture (see Appendix 3 for
additional photos).
5. Using a systematic search swim pattern,
(snorkeling or manta tows may be possible
if the area is shallow), determine the
physical boundary of the affected reef area.
Mark the perimeter at regular intervals
using flagging tape tied to corals or other
underwater structures (Figure 5.5). Marking
5
the boundary wil al ow you to determine the
rate at which the affected area is spreading
Figure 5.5 Flagging tape tied to a dead portion of a
colony or the substrate is an effective temporary means
spatially in future visits to the site. Quantify
of marking an outbreak area boundary so that spread
this area by measuring maximum width and
beyond an initial observation point can be tracked over
width perpendicular to maximum using a
time. Photo: K. Rosell
transect tape, and determine depth range.
6. Contact a laboratory with which you have a col aborative agreement, and make arrangements
for sample analysis. Collect samples for microbial and histological analysis using the procedures
outlined in Chapter 3. If you do not have a col aborative agreement with a laboratory, but feel this
situation is urgent and requires resources beyond your capacity, contact the CDHC via email at
cdhc.coral@noaa.gov.
7. Col ect al environmental data available for this site, either from your own agency or others. This
might include water temperature, rainfal , current wave height and tide patterns, sedimentation,
and/or bacterial load.
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A Coral Disease Handbook:
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8. Soon after you complete steps 1 to 5, perform rapid surveys (manta tows are particularly good
for this) at increasing distances from the outbreak site, to look for sites of secondary outbreaks.
Remember: do not go straight to "clean" sites from the outbreak site. Separate trips should be
planned for these surveys, using equipment which has undergone the sterilization procedures
outlined in Chapter 3. It is vital that those investigating a disease outbreak avoid spreading the
disease to unaffected sites.
9. Set up a monitoring schedule to
revisit the principle outbreak site at
regular intervals. If mortality is
occurring rapidly, then it is advisable
to resurvey at weekly or biweekly
intervals, depending on your
resources. When you revisit the site,
photograph al tagged colonies,
measure the linear progression of
the disease front and note the health
status of the colony (progressing,
stasis, recovering, dead; Figure 5.6).
Also look for new infections,
either as additional lesions on
previously-affected colonies or
as new hosts. Over time, look for
evidence of recovery, either from
tissue resheeting over dead skeleton
or through the recruitment of new
colonies (Figure 5.7). Final y, at
Figure 5.6 Remeasuring a black band disease front on Montipora sp. during
periodic intervals, repeat step 8, to
a two year-long monitoring effort of a BBD outbreak on the Great Barrier
make sure that secondary sites of
Reef. The ruler in the photo provided a scale bar for both image analysis
infection are not developing.
and measures of linear progression. Photo: Y. Sato.
And, final y, how is this information to be used? Data gleaned from a comprehensive documentation
of an outbreak and subsequent monitoring is likely to include identification of susceptible and
resistant species, species-specific mortality rates, species-specific recovery rates from tissue regrowth/
resheeting, community recovery via recruitment, and responses of other reef biota such as macroalgae
or sponges. Al of these data can be used to examine changes in reef community structure as a
consequence of the outbreak and coral mortality. Chapter 6 addresses specific management options,
where this information may be applied.
72
3.5
BL
3.0
2.5
2.0
WP
YBD
BL
1.5
1.0
5
0.5
Linear tissue mortality (cm/mth) 0.0
SU-01 W1-02 SU-02 WI-03 SU-03 W1-04 SU-04 W1-05 SU-05 W1-06 SU-06
Season
Figure 5.7 Time series photographs of one Montastrea faveolata colony with yel ow band disease (YBD) in Puerto Rico monitored
from 2004 to 2006. Several YBD lesions developed in June 2004, which expanded outwards during the fol wing months.
In February 2005, this colony also became infected with white plague (WP). In September 2005, all of the remaining living
tissue bleached (see white area). After the bleaching event most of the colony became infected with YBD and by August 2006,
the entire colony was dead. The graph shows the rate of this colony's tissue loss from summer 2001 to summer 2006, and the
coinciding bleaching events (BL) and disease outbreaks. Photo: E. Weil
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A Coral Disease Handbook:
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74
Chapter 6
Management Issues and Actions
In this chapter you will find:
A summary of the most current and comprehensive
coral disease databases.
Where to go for further assistance and advice.
A look at management options for coral disease
general thoughts, what has been tried and
current research efforts.
6
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Management Issues and Actions
L. Raymundo, C. D. Harvell, A. Bruckner and C. Woodley
6.1 Management issues and challenges
The management of marine
disease is a new frontier.
Traditional management tools
for human and wildlife disease
control include quarantine,
cul ing,
vaccinating
and
education (Figure 6.1). However,
only quarantine and education
are currently viable options for
dealing with coral diseases and
examples where they have been
applied are rare. We must
consider certain fundamental
differences between marine and
terrestrial systems when looking
Figure 6.1 Disease management for humans and wildlife involves quarantine,
vaccination, cul ing, and education, most of which are not currently viable options at options for managing coral
for marine diseases. www.cdc.gov; www.dailygalaxy.com, www.rabies-vaccination.
disease. Ocean water supports
com; www.leolabs.com
a rich and diverse microbial
community. How many of those
microbes are pathogenic, or potential y so, remains unknown. Because ocean water supports such a
vast microbial community, marine systems are considerably more "open" and connected to each
other than terrestrial systems. Additional y, our incomplete knowledge of corals, their diseases, their
resistance capabilities and the influence of environmental stressors on their health, pose additional
challenges to developing workable management options.
However, the impacts that diseases are having on coral populations highlight an urgent need to develop
management options concurrently with scientific investigation of diseases. Although the science is
still in its infancy, there are practical steps that reef managers can take to manage coral disease. The
current perception that coral diseases are "unmanageable" is untrue and managers are in the unique
position of being able to develop and test options for controlling disease spread. However, these
tests should be conducted with careful planning: any potential management tool should be tested via
a properly designed experiment and, most importantly, results should be reported. The authors of this
manual are available as contact persons for advice on this (their contact details are listed in Appendix
2). Below we present some areas which could guide coral disease management.
6.2 Global disease databases: options for managing information
Resource management must be based on sound science. In turn, scientific information must be
interpreted and communicated effectively so it facilitates meaningful management decisions. As a
growing field of science and an urgent management issue, coral disease is the focus of a world-wide
research effort which is generating an enormous amount of information. Due to the global implications
of disease impacts and the pressing need to standardize al aspects of disease investigation, data
generation and management are two very important features contributing to this effort.
There are a number of databases, accessible to the public via the internet, which contain various types
of information on coral diseases. Such databases are integral to synthesizing information from diverse
sources and rely heavily on the addition of accurate information as it becomes available. A repository
for global information which is accessible, accurate, and helpful is key to developing and testing
76
management options. Below is a brief description of the most current and comprehensive of these.
The Global Coral Disease Database
The Global Coral Disease Database (GCDD), available at http://www.unep-wcmc.org/GIS/coraldis/
index.cfm, is the most comprehensive compilation of coral disease information. It was developed
by the U.S. National Oceanic and Atmospheric Administration's (NOAA) Coral Reef Conservation
Program in conjunction with the United Nations Environmental Program's (UNEP) World Conservation
Monitoring Centre (WCMC). It is a web-accessible GIS database that compiles records of disease
observations and tracks their spread over time, by geo-referencing disease locations and plotting
their occurrences onto WCMC coral reef distribution maps. The GCDD includes an online mapping
tool (a prototype IMAPS tool) that enables users to search and plot data by disease name, year,
or country, with zoom capabilities and a full information sheet for each line of data. It also has the
option to separate reports into novice and expert data. For each disease, information can be obtained
regarding: its global and regional occurrence and abundance, affected locations (i.e. country, reef,
latitude and longitude) and species, and any available site-specific data on prevalence, incidence, and
extent of mortality, by querying the database or using the mapping tool.
The database is linked to WCMC's Protected Areas and Coral Species databases, and contains coral
disease identification tools and a photographic key to western Atlantic diseases. Al in situ observations
on prevalence, host range, global geographic distribution, and mortality for coral diseases are
compiled for the period 1972-2006 from peer-reviewed journal articles, technical reports, regional
monitoring data from Atlantic and Gulf Rapid Reef Assessment surveys, CARICOMP surveys, Global
Reef Check monitoring efforts, and reports submitted by researchers. These datasets reflect wider
spatial coverage of disease surveys, repeat surveys, and increases in the types of diseases and species
affected over the last few years. The GCDD currently contains over 8000 records of disease, and
includes reports of over 40 coral diseases from the western Atlantic, 28 from the Indo-Pacific and five
from the Red Sea. Contact Dr. Andy Bruckner, Andy.Bruckner@noaa.gov for more information, or to
submit information on coral diseases.
6.3 Where to go for assistance and advice
It is important to be aware that there is a network of dedicated and qualified scientists and managers
who can be contacted for assistance, information, and advice. In many remote locations, managers
often juggle numerous projects and responsibilities with few resources, and may even be forced to
take on responsibilities for which they have no formal training. One objective of this book is to provide
assistance to individuals who may be working in relative isolation. Another objective is to expand the
current network of individuals working in the field of coral disease and coral reef management, and
to assist managers who could benefit from additional expert support in obtaining the advice and
information they need. Further, we wish to convey the importance of communicating research and
management experiences in the field of coral diseases, either through publication or presentation at
symposia. There are many geographic locations for which there is no information currently available
on the status of coral diseases; this is particularly true for much of the Indo-Pacific and East Africa. By
linking managers and scientists with other managers and scientists, information can be exchanged
and productive collaborations can be forged. Below, we present two organizations whose members
can be contacted for information and can answer specific questions beyond the scope of this book.
The Coral Reef Targeted Research Program, Coral Disease Working Group
The Coral Disease Working Group (CDWG) as described in Chapter 1 (Box 1.1) is one of six working
groups of the Global Environment Facility and World Bank's Coral Reef Targeted Research (CRTR)
program, launched in 2005. The CDWG maintains collaborations in support of coral disease research
6
at each of the CRTR's four regional Centers of Excellence: the Marine Science Institute/Bolinao Marine
Laboratory of the University of the Philippines, Philippines; University of Dar Es Salaam, Institute
of Marine Science, Zanzibar, Tanzania; University of Queensland Heron Island Research Station,
Queensland, Australia; and Unidad Académica Puerto Morelos, Instituto de Ciencias del Mar y
Limnología, Universidad Nacional Autónoma de México (National Autonomous University of Mexico,
Institute of Marine Sciences and Limnology, Puerto Morelos, Mexico). All Centers of Excellence have
the capability to conduct field assessments of local infectious coral syndromes and can provide
77
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
information on sample collection and where to send samples. The CRTR website can be found at www.
gefcoral.org. This site describes current research efforts in coral reef ecology, and provides additional
contact information. Contact information for individual members of the Coral Disease Working Group
of the CRTR can be found in Appendix 2.
The Coral Disease and Health Consortium
The Coral Disease and Health Consortium (CDHC) was created in 2003 as a cooperative effort linking
representatives from U.S. agencies involved in coral reef management. Partners include the U.S.
NOAA, the U.S. Environmental Protection Agency (EPA), the U.S. Department of Interior (primarily,
National Park Service and Geological Survey), U.S. Coral Reef Task Force agencies, not-for-profit
organizations and academia, both national and international. Currently, the group is involved in health
assessments; outbreak responses within the U.S. and associated territories; research and development
for diagnostics and pathology; an International Registry for Coral Pathology; and capacity building
efforts that include training, technology transfer, and strategic research planning. For a downloadable
copy of the statement of purpose of the CDHC, refer to: www.coralreef.gov/library/pdf/FInal%20
CDHC%20plan.pdf. You may contact the CDHC directly at this email address: cdhc.coral@noaa.
gov, or either Dr. Andy Bruckner or Dr. Cheryl Woodley at NOAA. Please see Appendix 2 for their
contact information.
6.3 Management options in the face of incomplete knowledge
6.3.1. Some general thoughts and options
Management strategies for coral disease must develop as a result of careful and rigorous testing and
reporting of results. As we stated earlier, the traditional methods of cul ing and vaccination for disease
control currently have limited application for coral disease management. However, certain aspects of
coral life history may lend themselves to disease control if they are incorporated into a management
strategy: corals, unlike most other wildlife species of concern, are immobile; once a diseased colony
has been located, it will remain in that location and can be counted and revisited (and potentially
treated, if viable methods are developed). Furthermore, corals have the potential to regrow over dead
skeleton by resheeting. In these ways, corals function more like plants. Keeping these characteristics
in mind may help managers to "think outside the box" and develop management strategies unique
for corals and other sessile, benthic organisms. Experiences from the agriculture and plant disease
literature may provide guidance to management of coral diseases.
As mentioned previously, proving the cause of a disease is a difficult, lengthy process, beyond the
scope of most managers and their laboratories or field stations. However, one does not need to
know the causal agent of a disease to take management steps. A first important step is to develop a
working knowledge of the diseases and compromised health states present in a given management
area (i.e. to know what is normal y present, and at what levels, in the coral community). It is only by
understanding what represents `baseline' conditions that one is able to assess what represents above-
normal disease levels and their potential for increased mortality.
Building on this idea, long-term monitoring data sets should be viewed as valuable tools for local
management agencies. Responses to natural phenomena such as seasonally warm sea surface
temperatures or periodic coral ivore outbreaks can be observed both in the long-term and in a
larger geographic context to identify sites that show greater or lesser resilience to such impacts. It is
now considered good policy to identify particularly vulnerable sites (as wel as those that show high
resilience and resistance) for increased protection and management (78). Such data sets can also
be used to bring about policy change (such as guidelines for coastal development) and to assess
the impacts of events such as ship groundings and chemical spills. In many jurisdictions, there may
not be a legal framework in place to force the perpetrators of such events to remediate damage.
A comprehensive data set which quantifies "before and after" impacts can be used as a basis for
developing laws and regulations to guide remediation.
78
This, then, is another important manage-
ment tool: by controlling the input of
anthropogenic stressors on reefs, we can
optimize conditions favorable for reef
health and coral growth. Ultimately, this
might be the most powerful and successful
management strategy, one with multiple
positive consequences on al coastal
ecosystems, and one whereby local
management agencies can exert some
control. Demonstrated links between coral
disease and specific anthropogenic inputs
can be used as political leverage to improve
water quality, particularly in those local
economies dependent on diving tourism
Figure 6.2 Intensive aquaculture, such as this fish pen, can and reef health. To date, it appears that
deliver high concentrations of organic nutrients, antibiotics and many infectious syndromes of corals are
pesticides to coastal ecosystems, with unknown impacts to health. caused by opportunistic bacteria, with
Photo: L. Raymundo
many representatives of the genus Vibrio.
Vibrio spp. are among the most common bacteria in the ocean (79), and members of this genus are
also responsible for certain important water-borne human diseases such as cholera (Vibrio cholerae;
80). Similarly, the ciliate infections, such as brown band disease (BrB), skeletal eroding band (SEB) and
Caribbean ciliate infection (CCI) are likely to be opportunistic. For these infections, the best
management option is to control or reduce the stress in the environment, thereby improving the
corals' chance of resisting or recovering from infections (Figure 6.2).
6.3.2. What has been tried?
There is evidence to suggest corals that survive a bleaching episode may later succumb to an
opportunistic infection, as their resistance is lowered by the stress of bleaching (42,81). In such cases,
imposing a quarantine on a reef acutely impacted by either
bleaching or disease may be a viable option. The reef can
be closed to human activity by prohibiting diving and
snorkel ing for a period of time. This was successful y
undertaken in Florida in 2003 during a disease outbreak.
A Florida Keys reef was closed to al human activity except
approved research and investigation for 60 days (B.
Causey, pers. comm. and Federal Registrar 82). This
management approach has a number of potential y
positive consequences. First, when dealing with an
outbreak of an apparently unknown disease, the possible
risk to humans is very real; closing access can prevent an
impact on human health. Second, not only can divers
break and abrade corals, they can also potential y transmit
pathogens between reefs via contaminated gear. Many
dive operations take large numbers of divers to several
reefs in a single day, which could greatly facilitate the
spread of infection between reefs via dive gear. Closing a
reef can isolate an infection and limit its damage.
Figure 6.3 Applying putty to a yellow band disease
6
front slowed the progress of disease. Photo: A.
Bruckner
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A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
More direct management actions to alleviate infections may be possible in the case of a few pathogens.
For example, there has been some success in controlling the spread of black band disease (BBD)
during warming anomalies by aspirating the band using large syringes or pumps. Clay or underwater
epoxy putty can then be placed directly over the band. These methods were first developed by Harold
Hudson in 1986, and since then have been adapted by other scientists (Causey, pers. comm.). If clay
is used, al cyanobacterial filaments must be removed; it does not persist long and, the filaments will
eventually emerge from within the clay (83). Putty is harder to work with as it does not adhere as well.
However, it is more permanent and effectively halts any cyanobacterial growth left in underlying coral
skeleton after aspiration. This has also been successful y attempted with yel ow band disease, white
plague and white band disease. Preliminary results showed that band progression was slowed, and
in more than 60 percent of cases, the disease was arrested (Bruckner, pers. comm.; Figure 6.3). If this
approach is to be attempted, it should be done with great care to avoid spreading cyanobacteria and
other microorganisms comprising a diseased band to surrounding corals.
Another practice that has been attempted is shading highly susceptible reefs during bleaching events.
It necessitates deploying shade cloth that eliminates approximately 60 percent of incoming irradiance
and requires 10 to 12 days to take effect. However, shading corals for this length of time may also
exacerbate bleaching, so this practice is not recommended.
Final y, experiments have shown that black band disease can be eliminated and the rate of appearance
of new infections can be reduced through re-introduction of herbivorous urchins Diadema antil arum
into habitats where they were formal y abundant (83). Through grazing behavior, these urchins reduce
the potential for algal competition with corals, thereby reducing the likelihood of injuries that may
facilitate an invasion by pathogens, and directly removing the substrate that cyanobacterial filaments
require for attachment.
While antibiotics are successful in treating systemic infections of humans and wildlife, it is not
recommended to apply antibiotics in open marine ecosystems, and especial y to corals. The coral
holobiont is an extremely complex consortium involving beneficial surface bacteria and indiscriminate
use of antibiotics without proper understanding of this complexity may do more harm than good.
One final point: currently, the "treatment" of coral diseases in the traditional sense is not considered
feasible for eliminating disease during an outbreak. It is costly and time consuming, and infections
tend to be in varying states of progression at any given point in time. However it may be a viable
approach to save certain high-value colonies, such as massive reef building corals, or rare species that
are viewed as particularly important.
6.3.3 Current research efforts
One experimental program underway at the University of Tel Aviv involves phage therapy of corals.
Bacteriophages are viruses that kil bacteria and many are extremely specific in the bacteria they kil .
This program involves the isolation of specific phages
that prey on bacteria pathogenic to corals. In test
cases, the bacteria treated were Vibrio coralliilyticus
and Thalosomonas loyaeana. Scientists were able to
successful y isolate phages, introduce them to tanks
with infected corals and increase the survival rate of
the corals. However, transferring such a technology
to a reef system has serious logistical and ethical
issues, and to date, this has not been attempted.
Another potential y important area of research is
the identification and removal of vector organisms.
Figure 6.4 A population explosion of the gastropod Vectors can transmit pathogens between hosts by
corallivore Drupella cornus. This population kil ed a contacting the hosts during predatory, commensal or
several hundred-year-old massive Porites colony, among competitive interactions. Recent research efforts have
many others, in the central Philippines. Note the white
patches of recently-kil ed tissue and the brown patches uncovered a number of links between host corals
covered with recruiting macroalgae. Little healthy tissue and organisms that transmit a pathogen. The marine
80
remains on this colony. Photo: L. Raymundo
corallivorous fireworm, Hermodice carunculata, for example, is thought to transmit Vibrio shiloi, which
causes bleaching (84). The green calcareous alga Halimeda opuntia can transmit the causal agent for
white plague, Aurantimonas coralicida, to host corals it brushes against (85). The Caribbean gastropod
Coralliophila abbreviata is a vector for a white syndrome that affects Acropora (86) and the three spot
damselfish (Stegastes planifrons) has been shown to transmit black band disease between colonies
via predation (87). However, we do not advocate the indiscriminate removal of al coral ivores, as
there is ample evidence from terrestrial systems of unpredictable consequences resulting from either
the addition or removal of species to and from ecosystems. That said, there are certain species that
cause an inordinate amount of destruction because their populations go through "boom and bust"
cycles. If it was established that any of these highly destructive corallivores, such as the Crown-of-
Thorns starfish (COTS), Acanthaster planci, or the gastropods Drupella spp. (Figure 6.4), transmitted
a pathogen, then removal of these predators could potential y control the spread of disease. Indeed,
in the case of COTS, removal efforts during outbreaks are regularly attempted. Caution must be
exercised, however, as there may be other impacts to the ecosystem of such practices. For example,
prior to a full understanding of COTS biology, it was a common practice for volunteer divers to cut
the starfish into pieces. Due to the regenerative powers of starfish, this acted as an asexual means of
reproduction and virtually created more starfish. When this practice was stopped, volunteers began
eviscerating the starfish and leaving them on the reef. However, trauma to the gut initiates spawning
in COTS, and so created the next generation of starfish. Today, it is understood that the most effective
means of controlling COTS during an outbreak is simple removal from the reef.
Final y, one cannot underestimate the
importance of education and public
awareness efforts (Figure 6.5). Managers
should make every effort to disseminate
to the public local y-relevant information
on coral diseases and their potential
impacts. Managers may also focus their
attention on target groups who interact
regularly with the reef: fishers, recreational
divers, and diving tourism operators and
their clients. In places where diving
tourism is a major source of revenue,
there may be hundreds of visitors to a
single reef each day. Poorly-trained dive
instructors and tourist dive guides can
wreak havoc on a reef by encouraging
Figure 6.5 Here, col ege students developed hands-on activities to
teach grade school students about the importance of coral reefs and physical contact with corals and other
the organisms that depend on them. Photo: B. Baldwin.
benthic organisms (Figure 6.6). However,
educating and involving such individuals
in conservation efforts can have productive results. Many dive operators would like to know how
they can adopt an eco-tourism approach to their operations, and many are enthusiastic about
participating in monitoring activities. Harnessing such enthusiasm will provide managers with
additional observers underwater, and the only efforts that are necessary are some initial training and
regular communication.
6
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A Coral Disease Handbook:
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6.4 Procedures and practices to promote better management
Details of some of these procedures have been outlined elsewhere in this book, but to apply them
specifical y in a management context, we summarize them here as wel .
1. Restrict translocation of corals to prevent movement of disease.
Corals are translocated local y, regional y, and global y for a variety of reasons (rehabilitation,
aquaculture, and the aquarium trade, to name a few). Such practices should only be al owed
if quarantine conditions are possible. No corals with visible signs of disease or compromised
states should be col ected and transported to other field locations, no matter what the purpose.
Transport to quarantine facilities should be under strict biocontainment conditions that prevent
release of diseased materials or water into the environment.
2. Provide guidance for proper handling and
containment regimes during coral disease experiments.
Chapter 3 of this book discussed such procedures in detail. Managers may be in a position to
create regulations and enforce rules locally, and it is hoped that the information provided in this
book will be used for this purpose. If additional guidance is necessary, please consult the list of
experts in Appendix 2.
3. Monitor proposed coral management and research activities,
as wel as rehabilitation or remediation activities, to minimize
or avoid ethical and legal problems with the potential spread of disease.
Again, managers are in a unique position to understand the ethical and legal issues involved
with the use and transport of coral, and the manipulation of coral reef communities. Ensuring the
proper procedural controls on these activities will help manage disease.
4. Promote the use of universal precaution
measures when dealing with diseases in the field.
The suggestions outlined in Chapter 3 and 4, such as working from uninfected to infected areas,
and sanitizing SCUBA gear and equipment when moving between reefs etc. can be worked into
a formal regulation and permitting procedure, to ensure compliance.
Figure 6.6 Many dive operations run by poorly-trained instructors encourage their clients
to touch and handle corals. The potential for abrasion and breakage, as wel as disease
spread, is very high with such practices. Photo: D. Burdick
82
5. Encourage ethical behavior and improved sanitary practices
among divers and other users of the marine environment.
As outlined above, disseminating this type of information to the public wil educate recreational
users in their role in this management process, and assist managers in promoting reef health.
6. Communicate and report disease outbreaks and interventions.
Communication of disease events and efforts to manage them, even if such efforts were
unsuccessful, is essential. Only through coordinated, collaborative effort will significant progress
be made. Such information can be communicated in many ways: disseminating technical reports,
publishing in the scientific literature, presenting talks or posters at scientific meetings, and
submitting data to the GCDD are the most efficient means available and will reach the largest
number of professionals.
6.5 A look to the future
This book is a first attempt to provide resource managers with a practical approach towards identifying,
assessing, quantifying and monitoring coral disease. We hope that it provides useful and practical
information and resolves some of the current issues relating to coral disease. However, we recognize
that given the extraordinarily rapid rate of accumulation of information, certain areas of this book may
become obsolete fairly quickly. It is our hope that future editions and other publications produced by
this working group wil provide updated information, as wel as answers to some of the more urgent
questions we are confronting now.
Given the current focus on research for management and with a concerted global effort to link managers
and scientists, we predict that future efforts will result in a much greater understanding of coral
disease. This understanding wil undoubtedly have a ripple effect, resulting in further comprehension
of related topics. So far, our initial efforts to understand coral disease have expanded our knowledge
in the areas of coral histopathology, microbial ecology, the coral holobiont, epidemiology and
veterinary medicine, to name a few related fields. In the future we expect managers wil be equipped
with improved histological and molecular diagnostic tools to identify causative agents. Improved
understanding of the genetic diversity of coral communities, and their resilience to absorb changes to
their environment may increasingly be used as criteria for selecting reefs in urgent need of protection
(i.e. Marine Protected Areas, sanctuaries, reserves).
6
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Guidelines for Assessment, Monitoring and Management
84
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111. Gil-Agudelo, D.L. and J. Garzon-Ferreira. (2001). Spatial and seasonal variation of
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112. Gochfeld, D.J., J.B. Olson, and M. Slattery. (2006). Colony versus population variation in
susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea.
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113. Croquer, A., C. Bastidas, and L. Lipscomb. (2006). Fol iculinid ciliates : a new threat to
Caribbean corals? Diseases of Aquatic Organisms 69 (1):75-78.
114. Loya, Y., G. Bul , and M. Pichon. (1984). Tumor formations in scleractinian corals.
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115. Peters, E.C., J.C. Halas, and H.B. McCarty. (1986). Calicoblastic neoplasms in
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116. Nagelkerken, I., K. Buchan, G.W. Smith, K. Bonair, P. Bush, J. Garzon-Ferreira, L. Botero,
P. Gayle, C.D. Harvel , 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.
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117. Nagelkerken, I., K. Buchan, G.W. Smith, K. Bonair, P. Bush, J. Garzon-Ferreira, L. Botero,
P. Gayle, C.D. Harvel , C. Heberer, K. Kim, C. Petrovic, L. Pors, and P. Yoshioka. (1997a).
Widespread disease in Caribbean sea fans. I. Spreading and general characteristics.
Proceedings of the Eighth International Coral Reef Symposium, Panama, 1:670-682.
118. Santavy, D. and E.C. Peters. (1997). Microbial pests: coral disease in the Western Atlantic.
Proceedings of the Eighth International Coral Reef Symposium, Panama, 1:607-612.
119. Richardson, L.L. (1992). Red band disease: a new cyanobacterial infestation of corals.
Proceedings of the American Academy of Underwater Sciences Tenth Annual Scientific
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120. Miller, I. (1996). Black band disease on the Great Barrier Reef. Coral Reefs 15 (1):58-58.
121. Antonius, A. (1987). Survey of Red Sea coral reef health I. Jeddah to Jizan.
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122. Chesher, R. (1985). Practical problems in coral reef utilization and management: A Tongan
case study. Proceeding of the Fifth International Coral Reef Symposium, Tahiti 213-218.
123. Glazebrook, J.S. and H.M. Streiner. (1994). Pathology associated with tumours and black band
disease in corals from Agincourt Reef. Joint Scientific Conference on Science, Management
and Sustainability of Marine Habitats in the 21st Century, Townsville, Australia
124. Littler, M.M. and D.S. Littler. (1996). Black band disease in the South Pacific.
Coral Reefs 15 (1):20.
125. Korrûbel, J.L. and B. Riegl. (1998). A new coral disease from the Arabian Gulf.
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126. Jordan, I.E. and M.J. Samways. (2001). Recent changes in coral assemblages of a
South African coral reef, with recommendations for long-term monitoring.
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127. Dinsdale, E.A. (2002). Abundance of black-band disease on corals from one location
on the Great Barrier Reef: a comparison with abundance in the Caribbean region.
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128. Kaczmarsky, L. (2006). Coral disease dynamics in the central Philippines.
Diseases of Aquatic Organisms 69 (1):9-21.
129. Dalton, S.J. and S.D.A. Smith. (2006). Coral disease dynamics at a subtropical location,
Solitary Islands Marine Park, eastern Australia. Coral Reefs 25 (1):37-45.
130. Burdick, D., V. Brown, J. Asher, M. Gawel, L. Goldman, A. Hal , T. Leberer, J. Kenyon,
E. Lundlad, J. McIlwain, J. Mil er, D. Minton, M. Nadon, N. Pioppi, L. Raymundo, B. Richards,
R. Schroeder, P. Schupp, E. Smith, and B. Zgliczynski. (2008). The State of the Coral Reef
Ecosystems of Guam. J. Waddell (ed). The State of the Coral Reef Ecosystems of the United
States and Pacific Freely Associated States: 2008, NOAA Technical Memorandum NOS
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131. Raymundo, L.J.H., C.D. Harvell, and T.L. Reynolds. (2003). Porites ulcerative white spot
disease: description, prevalence, and host range of a new coral disease affecting
Indo-Pacific reefs. Diseases of Aquatic Organisms 56 (2):95-104.
132. Rosenberg, E. (2002). The Oculina patagonica-Vibrio shiloi model system of coral bleaching.
Prepared for Workshop Coral Health and Disease: Developing a National Research Plan Coral
Health and Disease Consortium, Charleston, South Carolina, January 22-25, 2002.
133. Jones, R.J., J. Bowyer, O. Hoegh-Guldberg, and L.L. Blackal . (2004). Dynamics of a
temperature-related coral disease outbreak. Marine Ecology-Progress Series 281:63-77.
134. Cheney, D.P. (1975). Hard tissue tumors of scleractinian corals.
Advances in Experimental Medicine and Biology 64:77-87.
135. Coles, S.L. and D.G. Seapy. (1998). Ultra-violet absorbing compounds and tumorous
growths on acroporid corals from Bandar Khayran, Gulf of Oman, Indian Ocean.
Coral Reefs 17:195-198
136. Yamashiro, H., M. Yamamoto, and R. van Woesik. (2000). Tumor formation on the
coral Montipora informis. Diseases of Aquatic Organisms 41 (3):211-217.
137. Kaczmarsky, L.T., M. Draud, and E.H. Wil iams. (2005). Is there a relationship between
proximity to sewage effluent and the prevalence of coral disease. Caribbean Journal
of Science 41 (1):124-137.
138. Aeby, G.S. (1991). Behavioural and ecological relationship of a parasite and
its hosts within a coral reef system. Pacific Science 45:262-269.
139. Antonius, A. (1999). Halofolliculina corallasia, a new coral-kil ing ciliate on Indo-Pacific reefs.
Coral Reefs 18 (3):300.
140. Winkler, R., A. Antonius, and A.D. Renegar. (2004). The skeleton eroding band disease
on coral reefs of Aqaba, Red Sea. PSZNI: Marine Ecology 25 (2):129-144.
141. Riegl, B. and A. Antonius. (2003). Halofolliculina skeleton eroding band (SEB): a coral
disease with fossilization potential? Coral Reefs 22 (1):48.
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94
Acknowledgements
95
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
96
Acknowledgements
In 2007, at the CRTR's Coral Disease Working Group annual workshop at the Bolinao Marine
Laboratory in the Philippines, the idea of a coral disease handbook tailored for reef managers
was first discussed. From July 2007, the group collaborated with the Coral Disease & Health
Consortium (CDHC) so that additional commonly used field and laboratory methods could
be incorporated into the handbook, along with a larger network of disease experts.
We are grateful to Esther Peters for her helpful feedback on nomenclature discussions and to
Dave Burdick, Billy Causey and Paul Marshall, who reviewed this book as potential users and
also provided valuable feedback. We would also thank the CRTR Program's Synthesis Panel
a partnership between the Global Environment Facility, the World Bank, the University of
Queensland, and NOAA for their support and funding to make this publication possible.
We are indebted to the entire staff of Currie Communication for their inspiring creativity,
fantastic care with detail and many long nights. Most of all, we thank Andy Hooten for the
good idea to write this manual, and support and advice along the way.
Photograph credits
We thank the following people for use of images for this handbook: Greta Aeby, Brad
Baldwin, Roger Beeden, Andy Bruckner, Dave Burdick, Ciemon Caballes, Courtney Couch,
Aldo Croquer, Teresa Lewis, Cathie Page, Laurie Raymundo, Kathryn Rosell, Yui Sato, Peter
Schupp, Brett Seymour, Lyle Vail, Lizard Island Research Station (A facility of the Australian
Museum), Ernesto Weil, Bette Willis and Thierry Work.
acknowledgements 97
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Guidelines for Assessment, Monitoring and Management
98
Appendices
In the appendices you will find:
Glossary and acronyms.
Regional contact list of coral disease experts.
Supplementary disease and compromised health photographs.
Data sheets currently used for assessment and monitoring.
Supplementary disease descriptions.
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Guidelines for Assessment, Monitoring and Management
100
Appendix 1:
Glossary and acronyms
Glossary
(Terms defined in the glossary are bold in the text)
Acute disease A disease that has a relatively rapid onset (i.e. influenza or food borne-diarrhea; 88).
Agent A factor capable of producing an effect (i.e. a cause of disease; 88).
Biomarker a substance that indicates the status or condition of a specific biological property (70).
Case history A chronological record of significant events and observations made during a
disease investigation.
Chronic disease (infection) A disease or infection that has a relatively slow onset (i.e. cancer; 88).
Coenosteum Skeleton deposited outside and between the corallite walls of the polyps of a
colonial scleractinian (71).
Corallite The calcium carbonate skeleton deposited by and around a single polyp (89).
Corallivore An animal that eats live coral tissue; certain parrot fish, gastropods such as
Drupella and Cyphoma, fireworms, and the starfish Acanthaster planci (90).
Diagnosis The determination of the nature of a disease (88).
Disease Any impairment that interferes with or modifies the performance of normal function,
including responses to environmental factors such as nutrition, toxicants, and climate; or infectious
agents, congenital defects, or combinations of these factors (91).
Endemic Present in a susceptible community at all times, but in low frequency (92).
Environment An area where agent and host interact to produce disease (93).
Emergent disease Any resurging disease that was previously at low levels in a population,
or a new disease in a population (94).
Epidemiology The study of the distribution and determinants of health-related states or events
in specified populations, and the application of this study to the control of health problems.
For non-human animals, the term epizootiology is used (92).
Epizootic Occurrence of disease at levels above what is expected in a population (88).
Applies to non-human animals.
Histology The study of tissues and cells on the microscopic level (95).
Holobiont The animal-plant complex formed by interactions between a coral polyp,
its endosymbiotic algae (zooxanthellae), and its associated bacterial community (44).
Host An organism that harbors the agent causative of disease (93).
Host range The collection of species which are susceptible to a given pathogen.
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Immunity Non-susceptibility to infectious or toxic agents (96).
Incidence The number of new cases of disease over a specified time period in a population at risk
for developing the disease (92).
Infectious Capable of causing infection (88).
Lesion Morphologic changes that accompany disease; manifestation of disease (88).
Necrosis Cell death characterized by irreversible damage, the earliest of which occurs in
mitochondria (modified from Stedman 88).
Octocoral Corals with polyp tentacles and mesenteries in multiples of 8; includes soft corals,
sea fans, Heliopora, and sea pens (89).
Opportunistic infection Infection caused by existing microorganisms not normal y pathogenic (88).
For instance, this may occur if environmental conditions change, thereby stressing the host
and increasing its susceptibility to the microorganism.
Outbreak (see epizootic)
Pathogen Any disease-producing agent (96).
Prevalence The number of diseased colonies relative to the total number of colonies present
within a defined area of survey at a given point in time. Usual y expressed as a percent:
(no. disease cases/total no. colonies) *100 (modified from Gordis 92).
Progression Increasing in severity (96).
R "R naught"; the average number of secondary cases generated by one primary
0
case in a susceptible population (4).
Reservoir An alternate host or passive carrier of a disease-causing organism (96).
Resistance (see Immunity)
Scleractinian Polyps with mesenteries and tentacles in multiples of 6; true stony corals;
Acroporidae, Poritidae, Pocilloporidae, etc. (89).
Severity The percent of a colony affected by a disease (97).
Sign Any objective evidence of a disease perceptible to an observer (96).
Stress The sum of biological reactions to an adverse stimulus that disturbs an organism's
homeostasis (96).
Syndrome A set of signs or a series of events occurring together that often point to a single
disease or condition as the cause (Dept. of Oncology, University of Newcastle Upon Tyne).
Transmission A passage or transfer of a disease from one individual to another (96).
Vector An animal that transfers an infectious agent from one host to another (96).
Virulence The relative pathogenicity of a microorganism (95); how easily it causes damage
to host tissue.
102
General acronym list
AGRRA:
Atlantic and Gulf Rapid Reef Assessment Program
ARC:
Australian Research Council
CARICOMP: Caribbean Coastal Marine Productivity Program
CDHC:
Coral Disease & Health Consortium
CDWG:
CRTR Coral Disease Working Group
CRCP:
NOAA's Coral Reef Conservation Program
CRTR:
GEF's & World Bank Coral Reef Targeted Research Program
EPA:
US Environmental Protection Agency
GCDD:
Global Coral Disease Database
GEF:
Global Environment Facility
NCCOS:
National Centers for Coastal Ocean Science
NOAA:
US National Oceanic and Atmospheric Administration
NMFS:
NOAA's National Marine Fisheries Service
UNEP:
United Nations Environmental Program
USGS:
United States Geological Survey
WCMC:
World Conservation Monitoring Centre
Disease/health state acronyms
ASP:
Aspergillosis
BBD:
Black band disease
BrB:
Brown band disease
CCI:
Caribbean ciliate infection
COTS:
Crown-of-thorns starfish
DSD:
Dark spots disease
GA:
Growth anomaly
PR:
Pigmentation response
RBD:
Red band disease
SEB:
Skeletal eroding band
UWS:
Ulcerative white spots
WBD:
White band disease
WP:
White plague
WS:
White syndrome
YBD:
Yellow band disease
appendices103
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104
Appendix 2:
Regional contact list of coral disease experts
(For a full list of experts, see www.gefcoral.org)
Caribbean
Peters, Esther C. Ph.D. (CDHC)
Bruckner, Andrew W. Ph.D. (CDHC)
(coral histopathology, ecotoxicology)
(coral reef ecology, coral diseases,
Tetra Tech, Inc.
conservation)
10306 Eaton Place
National Marine Fisheries Service
Suite 340
Office of Habitat Conservation
Fairfax, Virginia 22030, USA
NOAA Coral Reef Conservation Program
esther.peters@verizon.net
1315 East-West Highway
Silver Springs, Maryland 20910 USA
Richardson, Laurie L. Ph.D. (CDHC)
Andy.bruckner@noaa.gov
(coral microbiology)
Florida International University
Gil-Agudelo, Diego L. Ph.D.
Dept of Biological Sciences
(coral microbiology)
11200 SW Eighth St
Instituto de Investigaciones Marinas y
University Park Campus
Costeras (INVEMAR)
Miami, Florida 33199, USA
PO Box 1016
richardl@FIU.edu
Cerro Punta de Betín,
Santa Marta, Magdalena, Colombia
Ritchie, Kim B. Ph.D.
diego.gil@invemar.org.co
(coral microbiology)
Center for Coral Reef Research
Harvell, C. Drew Ph.D. (CRTR: CDWG, Chair)
Mote Marine Laboratory
(coral immunology, environmental stress,
1600 Ken Thompson Parkway
ecology)
Sarasota, Florida 34236, USA
Department of Ecology and
ritchie@mote.org
Evolutionary Biology
Cornell University
Rohwer, Forest Ph.D.
Corson Hall
(microbiology, virology)
Ithaca, New York 14853, USA
Department of Biology & Center
cdh5@cornell.edu
for Microbial Sciences
San Diego State University
Jordan-Dahlgren, Eric Ph.D. (CRTR: CDWG)
San Diego, California 92182, USA
(coral reef ecology, coral disease)
forest@sunstroke.sdsu.edu
Instituto de Ciencias del Mar y Limnología
Universidad Nacional Autónoma de México,
Apartado Postal 1152
77500 Cancún, Quintana Roo, México
jordan@mar.icmyl.unam.mx
appendices105
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Santavy, Deborah Ph.D. (CDHC)
Jacobson, Dean M. Ph.D.
(coral microbiology, Florida Keys)
(marine ecology, coral disease, oceanography)
Gulf Ecology Division
College of the Marshall Islands
One Sabine Island Drive
PO Box 1258
Gulf Breeze, Florida 32561, USA
Majuro, MH 96960, Marshall Islands
santavy.debbie@epa.gov
atolldino@yahoo.com
Smith, Garriet W. Ph.D.
Raymundo, Laurie J. Ph.D. (CRTR: CDWG)
(CRTR: CDWG, Co-chair)
(reef ecology, coral disease ecology, MPAs)
(microbial ecology)
University of Guam Marine Lab
University of South Carolina at Aiken
UOG Station
Department of Biology and Geology
Mangilao, Guam 96923, USA
471 University Parkway
ljraymundo@gmail.com
Aiken, South Carolina 29801 USA
SmithRes@usca.edu
Rohwer, Forest Ph.D.
(microbiology, virology)
Weil, Ernesto Ph.D. (CRTR: CDWG)
See Caribbean regional list for contact information
(coral ecology, reproduction, disease ecology)
University of Puerto Rico
Vargas-Ángel, Bernardo Ph.D. (CDHC)
Department of Marine Science
(histopathology, reef ecology)
P.O. Box 908
Joint Institute for Marine and
Lajas, Puerto Rico
Atmospheric Research
eweil@caribe.net
University of Hawai'i at Manoa
1000 Pope Road, Marine Science Building 312
Woodley, Cheryl M. Ph.D. (CDHC, Chair)
Honolulu, HI 96822, USA
(microbiology, ecotoxicology)
Bernardo.VargasAngel@noaa.gov
DOC/NOAA/NOS/NCCOS
Center for Coastal Environmental
Willis, Bette L. Ph.D. (CRTR: CDWG)
Health and Biomolecular Research
(coral ecology, reproduction, disease ecology)
Hol ings Marine Laboratory
ARC Centre of Excellence for Coral Reef Studies
331 Fort Johnson Rd
School of Marine and Tropical Biology
Charleston, South Carolina 29412, USA
James Cook University
cheryl.woodley@noaa.gov
Townsville Queensland, 4811, Australia
Bette.Willis@jcu.edu.au
Indo-Pacific
Work, Thierry M. D.V.M. (CDHC)
Aeby, Greta S. Ph.D. (CDHC)
(wildlife disease, epizootiology, pathogenesis)
(coral reef ecology, coral disease ecology)
USGS-National Wildlife Health Center
Hawaii Institute of Marine Biology
Hawai Field Station
P.O. Box 1346
PO Box 50167
Kaneohe, Hawai 96822, USA
Honolulu, Hawaii 96850, USA
greta@hawaii.edu
thierry_work@usgs.gov
Azam, Farooq Ph.D. (CRTR: CDWG)
(microbial ecology, microbiology)
Scripps Institution of Oceanography
University of California at San Diego
9500 Gilman Dr. La Jol a,
California 92093, USA
fazam@ucsd.edu
106
Red Sea/East Africa
Mesoamerica Centre of Excellence
Kushmaro, Ariel Ph.D.
Chair: Roberto Iglesias-Prieto, Ph.D.
(coral microbiology)
Unidad Académica Puerto Morelos (UAPM)
Department of Biotechnology Engineering
Instituto de Ciencias del Mar y Limnología
Ben-Gurion University of the Negev
Universidad Nacional Autónoma de México
PO Box 653
Apartado Postal 1152
Be'er-Sheva 84105, Israel
Cancún 77500, QR
arielkus@bgumail.bgu.ac.il
México
Tel : +52 (998) 871 02 19
McClanahan, Timothy R. Ph.D.
iglesias@icmyl.unam.mx
(coral reef ecology, coral disease, MPAs)
Coral Reef Programs
South-East Asia Centre of Excellence
Wildlife Conservation Society
Kibaki Flats no. 12
Chair: Emeritus Professor Edgardo Gomez,
Ph.D.
Bamburi, Kenyatta Beach
The Marine Science Institute
P.O. Box 99470
University of the Philippines
Mombasa 80107, KENYA
Diliman, Quezon City
tmcclanahan@wcs.org
1101 Philippines
Tel: +63 2 435 7417
Rosenberg, Eugene Ph.D. (CRTR: CDWG)
edgomez@upmsi.ph
(microbial ecology)
Department of Molecular Microbiology and
Biotechnology
Tel Aviv University, Ramat Aviv 69978, Israel
eros@post.tau.ac.il
Coral Reef Targeted Research
Program Centres of Excellence
Australasia Centre of Excellence
Chair: Professor Ove Hoegh-Guldberg, Ph.D.
Australasia Centre of Excel ence
Centre for Marine Studies
Heron Island Research Station (HIRS)
The University of Queensland
Queensland 4072, Australia
Tel: +61 7 3346 9418
oveh@uq.edu.au
East Africa Centre of Excellence
Chair: Alfonse Dubi, Ph.D.
Institute of Marine Science
University of Dar Es Salaam
P.O. Box 668,
Zanzibar, Tanzania
Tel: +255 24 2230741/ 2232128
dubi@ims.udsm.ac.tz
appendices107
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108
Appendix 3
Indo-Pacific Coral Health Decision Tree
Tissue Loss Predation
1
1a. Predation (PRD) e.g. fish, snail, starfish feeding scars
Tissue Loss Non-Predation Coloured Band Diseases
2
2a. Skeletal Eroding Band (SEB)
2b. Black Band Disease (BBD)
2c. Brown Band Disease (BrB)
Tissue Loss Non-Predation No overlying band of coloured material
3
3a. Ulcerative White Spots (UWS) focal tissue loss
3b. White Syndromes (WS) irregular tissue loss
3c. Atramentous Necrosis (AtN) grey-black material overlies irregular area of tissue loss
Tissue Discolouration White
4
4a. Bleaching (BL) environmentally induced partial or whole colony bleaching
4b. Focal Bleaching (FBL) early stage of UWS or unexplained spots
4c. Non Focal Bleaching (NFBL) unusual bleaching patterns, e.g. patches, stripes
Tissue Discolouration Non White
5
5a. Pigmentation Response (PR) coral response to a challenge (not a disease)
5b. Trematodiasis (TR)
Growth Anomalies
6
6a. Explained Growth Anomalies
6b. Unexplained Growth Anomalies
Compromised Health
7
7a. Pigmentation Response (see 5a. above)
7b. Unusual Bleaching Patterns (see 4c. above)
7c. Competition Aggressive Overgrowth e.g. cyanobacteria,
Terpios and Cliona sponges, red filamentous algae
7d. Sediment Damage
7e. Flatworm Infestation
Diseases in Other Reef Organisms
8
8a. Examples for Crustose Coralline Algae & Gorgonians
appendices109
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Appendix 3
Caribbean Coral Health Decision Tree
Tissue Loss Predation
1. Fish Predation (FPR)
2. Invertebrate Predation (IPR)
Tissue Loss Non-Predation Colored Band Diseases
3. Black Band Disease (BBD)
4. Caribbean Ciliate Infection (CCI)
5. Aspergillosis (ASP)
6. Purple Spots (PS)
7. Red Band Disease (RBD)
Tissue Loss Caribbean White Syndromes
8. White Band Disease (WBD)
9. White Plague (WP)
10. White Patch Disease (WPA)
11. Caribbean White Syndromes (CWS)
Tissue Discoloration White
12. Bleaching (BL)
Tissue Discoloration Non White
13. Dark Spots Disease (DSD)
14. Caribbean Yellow Band Disease (CYBD)
Growth Anomalies
15. Growth Anomalies (GAN)
Compromised Health
16. Compromised Health in Hard Corals (CHC)
17. Compromised Health in Octocorals (CHO)
18. Competition Overgrowth (CO)
Diseases in Other Reef Organisms
19. Coralline White Band Syndrome (CWBS)
20. Other Reef Organisms Sponges
21. Other Reef Organisms Zoanthids & Hydrocorals
appendices
110
Appendix 3
Supplementary disease and compromised health state photographs
Western Atlantic
Fish bites
Black band disease
Porites astreoides
Montastraea annularis spot
Whole colony view of
Close up of black
spot biting
biting lesions lacking tissue
Siderastrea siderea with
cyanobacterial mat on
(on right) and lesions that
black band disease
Siderastrea siderea
have begun to heal (left)
Red band disease
Acropora cervicornis with
Stephanocoenia intercepta
Meandrina meandrites
Close up of cyanobacterial
chimney-like structures from
with a damselfish territory
with red band disease mat
mat on Agaricia sp.
damselfish bites
(predation), often confused
(arrow)
with white syndrome
Carribean ciliate infection
Yellow band disease
Whole colony view of
Close up of Diploria
Whole colony view of
Close up of Montastraea
Diploria labyrinthiformis with
labyrinthiformis with band
Montastraea faveolata with
annularis new yel ow
progressing band of ciliates
of ciliates to traveling to the
multiple yellow band lesions
band lesion
(arrow), dead skeleton
right over healthy tissue
overgrown by algae
appendices
Ciliates, Halofolliculina sp.
from CCI mag. 50X
111
A Coral Disease Handbook:
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White patch disease
White band disease
Acropora palmata with
Close up of white patch
Whole colony view of
Close up of progressing
multiple white patch lesions,
lesion on Acropora palmata
Acropora palmata with
front of white band in
including acute (upper left and
white band disease
Acropora palmata
lower right), subacute (upper
right) and an older, algal
colonized lesion (middle) that
has begun to heal
White plague
Dark spots disease
Whole colony view of
Close up of progressing
Siderastrea radians with dark
Close up of progression
Montastraea annularis with
front of white plague in
spots disease
front of dark spots in
white plague
Montastraea franksi
Siderastrea radians
Carribean white syndromes
Whole colony view of
Close up Montastraea
Montastraea cavernosa
franksi white syndrome
with multiple white
syndrome lesions
Indo-Pacific/East Africa/Red Sea
Fish bites
Gastropod predation
Porites sp. with numerous
Close up of Porites sp. with
Acropora sp. infested with
Close up Acropora sp. tissue
parrotfish bite scars
puffer fish bites, showing
Drupella cornus
removed by Drupel a cornus
concentrated along ridges
regular paired scrape marks
(white region)
112
Black band disease
Skeletal eroding band
Whole colony view of
Close up of Echinopora
Acropora sp. with speckled
Close up of Acropora
Coeloseris mayeri with black
lamellosa with black band
band of ciliates. Dead
intermedia with speckled
band disease. The entire
skeleton colonized by algae
band of ciliates
colony was dead one month
after this photo was taken
Black band disease front,
Ciliates, Halofol iculina
showing filamentous
corallasia (arrow) from
cyanobacteria adjacent to
Acropora sp. with skeletal
dead coral skeleton (white)
eroding band, mag. 32X
on Montipora sp., mag. 45X
Brown band disease
Acropora sp. with brown
Close up of the brown band
Acropora with brown band
band disease (arrow)
of ciliates (arrow)
disease infested with ciliates
on Acropora sp.
Ulcerative white spots
appendices
Whole colony view of Porites
Porites cylindrica showing
cylindrica with ulcerative
two active lesions; the one
white spots disease
on the left is completely
devoid of tissue; the lesion
on the right is bleaching,
mag. 35X
113
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
White Syndrome
Pachyseris speciosa with
Porites cylindrica with an
An active disease front of
white syndrome
early white syndrome lesion
white syndrome spreading
(arrow)
within Lobophyl ia
hemprichii
Pigmentation Response
Whole colony view of
Close up of Porites sp.
a massive Porites sp.
tissue swelling and
pigmentation response to
pigmentation response to
macroalgae abrasion
macroalgae abrasion
Trematodiasis
Whole colony view of Porites
Close up Porites compressa
Trematode cyst (~1mm)
compressa with numerous
showing active pink nodules
removed from a
trematodiasis lesions
from trematodiasis
trematodiasis lesion
on Porites compressa,
mag 40X
Growth Anomalies of a unknown cause
Massive Porites sp. with a
Massive Porites with a
Skeleton of Porites sp. with
growth anomaly
growth anomaly of a
growth anomaly, mag. 10X
different morphology.
This type appears as a
white to pink plaque
114
Appendix 4
Data sheets currently used for assessment and monitoring
Comments
owth
gr
S/A/T/M
Date:
Over
omised health states
edation
Pr S/W/P/D
Millepora.
Depth:
Disease
unicate,
%
Bleached
Sponge, Algae, T
owth:
P/M/W
Bleaching
gr
evalence and compr
Over
T
ransect:
Height
Size
Dia
otfish, Damselfish.
, disease pr
Recent
m, Parr
ewor
% Mortality Old
Snails, Fir
Site:
% Live
edation:
Pr
ements, mortality
n Atlantic data sheet template
Species
Pale, Mottled, White.
ester
der:
Recor
Bleaching:
W Colony measur
115
Appendix 4
Data sheets currently used for assessment and monitoring
SI
PR
Patchy bleach
Silt smothering/abrasion:
Date:
omised health states
SEB
ed filamentous)
(r
2RF
UWS
oalgae)
(macr
2Ma
T
ransect Position:
WS
evalence & compr
(cyanobacteria)
BrB
2Cy
Depth:
owth/abrasion:
BBD
gr
Disease pr
Algal over
T
ransect:
owth
Gr anomaly
(Fish)
1F
(COT)
)
1CT
Site:
T
otal Colony Count
(
Coralliophilia
)
1Co
tabular
ea
n/bushy
isopora
massive
ea
o
corymbose
branching
ea
ea
ea
eopora
submassive
rachy
ea
diner
(
Drupella
staghor
(genera)
(genera)
ubastr
ubipora
1Dr
bottlebrush/digitate
ea/Leptastr
(genera)
ea/Pseudosider
der:
opora/Astr
faviids
Mussids
opora
ogyra/Physogyra
edation:
Recor
Acr
Anacr
Montipora
Pocillopora
Stylophora/Seriatopora
Stylocoeniella/Madracis
Porites
Goniopora/Alveopora
Favia/Montastr
Favites/Echinopora
Platygyra/Goniastr
Cyphastr
Other
Fungids
Galaxea/Simplastr
Pectinia/Oxypora
Echinophyllia/Mycedium
Lobophyllia/Symphyllia
other
Hydnophora
Merulina
Paraclav/Scapophyllia
Pavona
Leptoseris/Coeloseris
Pachyseris/Gar
Psammocora/Coscinar
Siderastr
Euphyllia/Catal/T
Pler
T
urbinaria/T
Heliopora/T
Millepora Pr
Indo-Pacific data sheet template
116
Appendix 4
Data sheets currently used for assessment and monitoring
Date:
T6
T5
Depth:
T4
L
i
n
e
i
n
t
e
r
c
e
p
t
t
r
a
n
s
e
c
t
d
a
t
a
T3
T2
Site:
T1
tabular
ea
digitate
n/bushy
Isoporan
ea
corymbose
bottlebrush
ea
eids
eopora
gonians
staghor
rachyphyls
ubipora/Millepora
ea/Leptastr
branching
submassive
aviids
der:
opora/Astr
massive
ophyllids
oalgae/fleshy algae
opora
Recor
Acr
Montipora
Anacr
Pocillopora
Stylophora/Seriatopora
Porites
Porites
Porites
Goniopora/Alveopora
Favia/Favites/Montastr
Platygyra/Goniastr
Cyphastr
other F
Fungids
Oculinids/Pectinids
Mussids/Merulinids
Agariicid/Siderastr
Dendr
Caryophyls, T
Soft corals/Gor
Heliopora/T
macr
r
ock with turfing algae
sand/silt
r
ecently dead standing coral
rubble
other (sponges, ascidians)
Indo-Pacific data sheet template
117
A Coral Disease Handbook:
Appendix 4
Guidelines for Assessment, Monitoring and Management
Data sheets currently used for assessment and monitoring
e skeleton)
een filamentous algae)
Diagnosis/Comments
ent; bar
ecent; gr
Date:
onic
Timing:
Acute (curr
Subacute (r
Chr
(epibiont community)
Timing A/S/C
10-24%
<10%
25-49%
50-100%
e
Severity ml/md/s/x
Mild
eme
Sever
Extr
Severity:
Moderate
gin (S/I)
Mar
gin:
egular
Lesion Color
Mar
Smooth
(S)
Irr
(I)
Lesion Diam
apical
T
ransect:
Location B/M/A
medial
Location:
Distribution F/M/C/D/L
basal
Lesion #/col
Lesion characterization data sheet
i
a
m
o
l
d (cm)
linear
C
Site:
fuse
dif
coalescing
Species
Distribution:
multifocal
der:
118 Data sheet template
Recor
focal
118
Appendix 5
Supplementary disease descriptions
ence
Refer
(98)
(11,99,100)
(31,101)
(13,52)
(102-104)
(13,105-110)
(11,109,111,112)
(31,113)
(114,115)
(29,54,116,117)
(104,118,119)
S.
esent
spp.
and
e
ibrio
V
ed by
egates often pr
bacterium
essors
; may be a disease of
sp ciliate
Schizothrix mexicana
cescens
charia
ibrio
sydowii fungus
Oscillatoria
V
; second type dominated by two
onmental str
gillus
esumed cause
obial consortium of cyanobacteria,
obial consortium dominated by
Pr
ibrio char
Unkown; bacterial aggr
V
Aurantimonas coralicida
Serratia mar
Micr Beggiatoa & Desulfovibrio
Possibly zooxanthellae
Fungal origin; associated with
Halofolliculina
Unknown; genetic or trigger envir
Asper
Micr Cyanobacteria calcicola species of
ype II
om published literatur
ozoan, 6
eoides
spp. complex,
Dichocoenia,
. astr
+ 40 spp. of non-
ea, S. intersepta, A.
opora
ea. sider
spp. & 6 other octocorals
n Atlantic, fr
opora plating & massive corals
gonians
gonia
gonia, Colpophyllia, Agaricia,
Host range
White line disease, white death, white plague
A. cervicornis
Diploria stokesi Acr
A. palmata
24 scleractinian corals, 1 hydr gor
Montastraea. annularis other faviids ; Agaricia agaricites
M. annularis M. faveolata, M. cavernosa, Siderastr agaricites
>10 species including Montastraea, Acr
Diploria, Colpophyllia, Porites Montastraea, Agaricia, A. palmata; Dichocoenia, Madracis
Gor
Gor Mycetophyllia Stephanocoenia; T reported on D. stigosa, M. annularis, M. cavernosa S. radians, P
ester
owth,
osis
ome, dark bands
oding band (SEB)
ome; yellow band/blotch
ome, Ring disease, DSD type II,
Synonym
White line disease, white death, white plague
WBD type II
Plague type II, white plague type III, plague; white band disease, white line disease
White pox, patchy necr
Black line disease
Y
ellow blotch disease; ring bleaching, yellow pox disease; yellow band syndr
Dark spot disease, dark spot syndr Purple band syndr
Skeletal er
Hyperplasia, Neoplasia, tumors, Gigantism, accelerated gr chaotic polyp development, calicoblastic epithelioma
Sea fan disease
Red band disease type I, RBD type II
. Major diseases of the W
ome
gillosis (ASP)
T
able 1
owth anomalies (GA)
Syndr
White band disease (WBD)
WBD type II
White plague
White patch disease
Black band disease (BBD)
Y
ellow band disease (YBD)
Dark spots disease (DSD)
Caribbean ciliate infections (CCI)
Gr
Asper
Red band disease (RBD)
119
Appendix 5
Supplementary disease descriptions
ence
Refer
(33,120-128)
(33,34,129,130)
(34,128,130,131)
(132)
(133)
(39)
(138)
(33,130,139-141)
(125)
(33,130)
-
ess
ematode
onmental str
, a colonial
ciliates
educing bacteria and
. shiloi
; normally called Porites
ibrio
V
caria of a digenetic tr
otrich ciliate
esumed cause
obial consortium dominated by cy
Pr
ibrio corallyliticus, V
Micr anobacteria, sulfate-r sulfide-oxidizing bacteria
Unknown
Possibly a Ulcerative White Spot Disease
V
Unknown
Unknown; genetic or envir triggers. Also known as hyperplasia, neoplasia, tumors, calicoblastic epitheliomas
Unknown
Metacer (parasitic flatworm)
Halofolliculina corallasia heter
Associated with a cyanobacteria
Helicostoma nonatum
ea
and
16
ozoan
opora,
fected
ea,
, 1 hydr
Pocillopora
ea
Pocillopora,
culata
. lobata
equently af
T
urbinaria, Acr
ea
essa, P
,Faviidae,
most fr
ea
epora, Montipora, Platygyra,
opora & Pocillopora
opora
opora, Pocillopora, Pavona, Fungia,
eopora, Montipora, Echinopora, opora, Goniopora, Platygyra,
Acr
opora, Pocillopora, Echinopora,
Host species
19 genera, 49 species; Acr
Multiple spp. of Goniastr Porites, Pavona, Stylophora, Montipora
Porites; Echinopora, Goniastr Heliopora, Favia, Montipora
Oculina pategonica; Pocillopora
Montipora aequituber
Acr Madr Porites, Goniastr
Astr Acr massive Porites, Pocillopra, Goniastr Hydnophora, Cyphastr
Porites compr
21 genera of scleractinia; most common on
4 genera, 12 species of scleractinia
Acr spp.
e
dan,
anzania
dan, PNG,
onga, South Africa,
onesia, Marshall
eat Barrier Reef, Australia
ench Polynesia, New Caledonia,
Location
Australia, Egypt, Fiji, India, Jor Papua New Guinea, Philippines, Saudi Arabia, T CNMI, Palau
Egypt, Australia, Solitary Islands, Philippines, Guam
Philippines, Guam
Mediterranean, Israel, T
Gr
CNMI, Oman , Philippines, Guam, Australia, Hawaii, Palau, Enewatak, Fr Maldives, Micr Islands, Japan, China
East African Coast
Hawaii
Australia, Egypt, Jor Mauritius , Australia, Guam
United Arab Emirates, Arabian Gulf, Iran
Australia, Guam
Major diseases of Indo-Pacific, East African and Red Sea corals, from published literatur
osis
ome (WS)
ome
oding band (SEB)
ome
T
able 2.
owth Anomalies (GA)
own band disease (BrB)
Syndr
Black band disease (BBD)
White syndr
Ulcerative white spot disease (UWS)
Bacterial Bleaching
Atramentous necr
Gr
Fungal syndr
T
r
ematodiasis
Skeleton er
Y
ellow band disease
Br
120
Authors
Laurie Raymundo (CDWG)
Courtney Couch (CDWG)
Andy Bruckner (CDHC)
Drew Harvell (CDWG)
University of Guam
Cornell University
NOAA Coral Reef
Cornell University
Conservation Program
Ernesto Weil (CDWG)
Cheryl Woodley (CDHC)
Thierry Work (CDHC)
Eric Jordan-Dahlgren
University of Puerto Rico
NOAA Center for Coastal
USGS-National Wildlife
(CDWG)
Environmental Health and
Health Center
Universidad Nacional
Biomolecular Research
Autónoma de México
Bette Willis (CDWG)
Greta Aeby (CDHC)
Yui Sato
James Cook University
Hawaii Institute of
James Cook University
Marine Biology
authors
121
A Coral Disease Handbook:
Guidelines for Assessment, Monitoring and Management
Disclaimer The information contained in this publication is intended for general use, to assist public knowledge and discussion
and to help improve the sustainable management of coral reefs and associated ecosystems. It includes general statements
based on scientific research. Readers are advised and need to be aware that this information may be incomplete or unsuitable
for use in specific situations. Before taking any action or decision based on the information in this publication, readers should
seek expert professional, scientific and technical advice.
To the extent permitted by law, the Coral Reef Targeted Research & Capacity Building for Management Program and its
partners, (including its employees and consultants) and the authors do not assume liability of any kind whatsoever resulting
from any person's use or reliance upon the content of this publication.
NOAA Disclaimer This publication does not constitute an endorsement of any commercial product or intend to be an opinion
beyond scientific or other results obtained by the National Oceanic and Atmospheric Administration (NOAA). No reference
shal be made to NOAA, or this publication furnished by NOAA, to any advertising or sales promotion which would indicate or
imply that NOAA recommends or endorses any proprietary product mentioned herein, or which has as its purpose an interest
to cause the advertised product to be used or purchased because of this publication.
The Coral Disease Handbook: Guidelines for Assessment, Monitoring and Management
summarizes the relevant known science for managing coral disease. Produced by the Coral
Reef Targeted Research and Capacity Building for Management Program and its partners, it is
designed to be used in conjunction with the Underwater Cards for Assessing Coral Health on
Indo-Pacific Reefs and the Underwater Cards for Assessing Coral Health on Caribbean Reefs.
These tools wil help managers and field scientists identify and monitor infectious syndromes of
coral and take the next step of implementing new management approaches.
The handbook includes three chapters on identifying infectious syndromes and their impacts
in the field; a chapter on coral disease monitoring protocols; a chapter detailing methods
for detecting and assessing new outbreaks of disease; and a chapter on developing new
management options for coral disease. It emphasizes the synergies between infectious disease
and the rapidly changing facilitators of disease outbreaks, like global warming. These factors
make coral disease management a moving target requiring cooperation and knowledge
exchange between microbiologists, molecular biologists, ecologists and managers.This
handbook aims to integrate critical, current scientific information about coral disease to
support and strengthen coral reef management.
Coral disease outbreaks have continued to increase and take out the major reef-builders in the
Caribbean during the last two decades. White band hugely affected Acropora palmata in the
1970s and in the Keys we started having major impacts of black band in 1986. We are in the throes
of several destructive outbreaks in the wider Caribbean now. Both in terms of coral bleaching and
the residual outbreaks of coral diseases, I think the Pacific is lagging about 12 to 14 years behind
the Wider Caribbean. This manual fills a critical gap in moving us to the next level in developing
increasingly ambitious management approaches for coral disease.
Billy Causey, Director
Southeast Region, Office of National Marine Sanctuaries
Overal , it is a very impressive compilation, and is sure to be a significant contribution to progress
in the field. These types of "state-of-play reviews" are invaluable, in my opinion, for capturing the
state of knowledge, facilitating coordination and cooperation among researchers, and setting the
agenda for future work. There should be more of them.
Paul Marshall, Director
Climate Change, Great Barrier Reef Marine Park Authority
The CRTR Program is a partnership between the Global Environment Facility, the World Bank, The University of Queensland
(Australia), the United States National Oceanic and Atmospheric Administration (NOAA) and approximately 50 research
institutes and other third-parties around the world.