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172
Oceanogr
O
ap
ceanogr hy
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c
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l. 20, No. 1
o
t
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n
,

---

a c r o s s t h e g l o b e , we are witnessing the decline of coral reef ecosystems. One relatively
new factor contributing to this decline is the outbreak of destructive infectious diseases, especial-
ly on Caribbean reefs. As the Coral Disease Working Group of the Coral Reef Targeted Research
Program, our research focuses on four priorities: (1) assessing the global prevalence of coral
disease, (2) investigating the environmental drivers of disease, (3) identifying the pathogens
that cause disease, and (4) evaluating the coral's ability to resist disease. Monitoring has revealed
new coral-disease syndromes at each of four Global Environmental Fund Centers of Excellence:
the Caribbean, the Philippines, Australia, and East Africa. Over the last 20 years, drastic
balaNce BetWeeN
(> 50 percent) loss of coral cover has occurred on the Yucatán Peninsula, even in pristine areas.
Global surveys have revealed signifi cant levels of disease and disease outbreaks occurring not
only in the Caribbean "hotspots," but also in sites throughout the Pacifi c and Indian Oceans. By
monitoring coral disease, we will create a baseline and long-term data set that can be used to test
specifi c hypotheses about how climate and anthropogenic drivers, such as decreasing water qual-
ity, threaten coral reef sustainability. One such hypothesis is that high-temperature anomalies
drive outbreaks of disease by hindering the coral's ability to fi ght infection and by increasing the
pathogens' virulence. We observed recurrent outbreaks following the warm summer months of
two of the most damaging diseases in the Caribbean. In addition, we found that coral disease in
the Great Barrier Reef correlated with warm temperature anomalies. In the Caribbean and Med-
iterranean Seas, virulence of known coral pathogens and the normal coral fl ora changed during
high-temperature periods. Other stresses such as high nutrients and sedimentation may simi-
larly alter the balance between the coral and its resident microbial fl ora.
Oceanogr
O
ap
ceanogr hy
ap maracrh 2007
c
173

---

INtroductIoN
status of disease throughout the Indo-
2002. The fall of 2005 brought devastat-
Over the past few decades, coral reef
Pacific. However, preliminary surveys in
ing bleaching to the Caribbean, caused
communities around the world have
Australia (Willis et al., 2004), the Phil-
by the largest warm thermal anomaly in
been deteriorating due to a combina-
ippines (Raymundo et al., 2004), Palau
100 years (Mark Eakin, National Oceanic
tion of natural and anthropogenic fac-
(Cathie Page and others, James Cook
and Atmospheric Administration, pers.
tors (Harvell et al., 1999; Harvell, 2004;
University, pers. comm., December 2006),
comm., December 2006). The Caribbean
Hughes et al., 2003). Coral damage can
and East Africa (McClanahan et al., 2004;
thermal anomaly of 2005 was immediate-
be caused both by abiotic factors (e.g.,
Ernesto Weil, University of Puerto Rico,
ly followed by outbreaks of white plague
temperature stress, sedimentation, toxic
pers. comm., December 2006) revealed
and yellow blotch (Miller et al., 2006).
chemicals, nutrient imbalance, ultra-
significant and damaging new diseases in
Our working hypothesis is that, in
violet radiation) and biotic factors (e.g.,
all locations surveyed.
some cases, the death of coral during hot
predation, overgrowth of algae, infec-
What has prompted this emergence of
thermal anomalies is facilitated by op-
tious disease). These factors, acting alone
coral disease? Current research suggests
portunistic infectious pathogens whose
or in synergy, have led to a reduction in
that climate warming is an important
virulence is enhanced by increased tem-
coral cover (Green and Bruckner, 2000;
factor (Harvell et al., 2002; Selig et al.,
peratures. Changing environmental
Richardson and Aronson, 2002; Hughes
2006). Tropical reef-building corals are
conditions could also influence disease
et al., 2003). Infectious disease in coral,
generally found between the Tropic of
by altering host/pathogen interactions.
observed in the field as lesions or distinct
Cancer (23.5°N) and the Tropic of Cap-
Increased temperatures could affect basic
bands of tissue loss, can be caused by
ricorn (23.5°S). Because they have a nar-
biological and physiological properties
bacteria, viruses, protozoa, or fungi. In
row range of thermal tolerance (between
of corals, particularly their ability to fight
addition to the loss of coral tissue, disease
18° and 30°C), they are extremely sus-
infection, thus influencing the balance
can cause significant changes in repro-
ceptible to temperature stress. It is well
between potential pathogen and host
duction rates, growth rates, community
known that corals "bleach" (lose their
(Rosenberg and Ben-Haim, 2002). In ad-
structure, species diversity, and abun-
symbiotic zooxanthellae) at high, stress-
dition, the pathogens themselves could
dance of reef-associated organisms (Loya
ful temperatures. The coral bleaching
become more virulent at higher tempera-
et al., 2001). While an unprecedented in-
observed worldwide following the 1998
tures (Ben Haim et al., 2003a, 2003b).
crease in coral disease has been well doc-
El Niño was the most massive and devas-
This effect is particularly challenging to
umented in the Caribbean (Porter et al.,
tating recorded up to that point (Hoegh-
study because of the complexity of the
2001; Weil et al., 2002; Weil, 2004; Weil et
Guldberg, 1999), only to be exceeded by
coral holobiont--the coral polyp, which
al., 2006), much less is known about the
another bleaching event in Australia in
co-exists in a mutualistic relationship
with unicellular algae, zooxanthellae,
coral dIsease WorkINg group of the global eNVIroNmeNtal facIlIty
and a surface mucopolysaccharide layer
coral reef targeted research program. dreW harVell (cdh5@Cornel .edu)
(SML). The SML contains a complex
is Professor, Department of Ecology and Evolutionary Biology, Cornell University, Ithaca,
microbial community that responds to
NY, USA. erIc JordáN-dahlgreN is Researcher, Universidad Nacional Autónoma de
changes in the environment in ways that
México, Cancún, México. susaN merkel is Senior Lecturer, Department of Microbiol-
we are just now beginning to appreciate
ogy, Cornell University, Ithaca, NY, USA. eugeNe roseNberg is Professor, Department
(Azam and Worden, 2004; Klaus et al.,
of Microbiology, Tel Aviv University, Israel. laurIe raymuNdo is Coral Reef Ecologist,
2005). The normal microbial flora within
University of Guam Marine Laboratory, Mangiloa, Guam, USA. garrIet smIth is As-
the mucus layer may protect the coral
sociate Professor of Biology, University of South Carolina, Aiken, SC, USA. erNesto WeIl
against pathogen invasion; disturbances
is Professor, Department of Marine Sciences, University of Puerto Rico, Mayaguez, PR, USA.
in this normal flora could lead to disease
bette WIllIs is Professor, School of Marine Biology and Aquaculture, James Cook Univer-
(Ritchie, 2006). The massive introduction
sity, Townsville, Australia.
of non-indigenous pathogens, as is often
174
Oceanography Vol. 20, No. 1

---

North
North
Atlantic
Pacific
MESOAMERICA
Ocean
Ocean
PHILIPPINES
EAST AFRICA
Indian
Ocean
South
South
Pacfic
Atlantic
Ocean
Ocean
SOUTHERN
GREAT BARRIER
REEF
Centers of Excel ence
Existing Interconnectivity
Prospective Sites
Hypothetical Interconnectivity
figure 1. map showing the centers of excellence for the World bank/gef coral reef targeted research project.
seen with aquaculture and ballast-water
Research (CRTR) and Capacity Build-
ease. We are testing specific hypotheses
release, could also disturb the microbial
ing for Management Program (for more
about climate and anthropogenic chang-
community (Harvell et al., 2004).
information, go to http://www.gefcoral.
es that threaten coral reef sustainability.
Pollutants and other anthropogenic
org). As the Coral Disease Working
By building the capacity to manage these
stressors could potentially impact any
Group within this project, the goals of
ecosystems, we hope to enhance reef re-
component of the holobiont, caus-
our program are to fill critical informa-
silience and recovery, worldwide.
ing a disruption in the symbiosis and
tion gaps about coral reef disease, build
a concomitant loss of health. This
capacity to study and monitor disease
1. global preValeNce
loss of health could translate into a
internationally, and help develop solu-
The CRTR program's four Centers of
breakdown in host resistance and a
tions for managing and conserving reef
Excellence are located in Meso-America,
potential elevation of disease sever-
ecosystems. We describe here the coop-
Australia, East Africa, and Philippines/
ity or rate of infection. Sedimentation
erative research effort being guided by
Southeast Asia (Figure 1). Working from
could alter the microbial community
our international team of microbiolo-
these centers as well as other localities in
within the surface mucous layer of the
gists, ecologists, and physiologists toward
each region, we are assessing the global
coral holobiont. Nutrient loading could
these ends. Working out of four Centers
range, prevalence, and impact of coral
enhance both algal and pathogen growth
of Excellence, our research priorities in-
diseases. We standardized protocols for
(Bruno et al., 2003; Smith et al., 2006;
clude assessing the global prevalence of
conducting coral and disease surveys in
Kuntz et al., 2005).
coral disease, investigating the environ-
coordinated teams that allow compari-
This paper details the priorities of a
mental drivers of disease, identifying the
son of disease levels in highly diverse
World Bank/Global Environment Facil-
pathogens that cause disease, and under-
reefs such as those in the Indo-Pacific
ity initiative, the Coral Reef Targeted
standing the coral's ability to resist dis-
with those in the Caribbean. Although
Oceanography march 2007
175

---

the Indo-Pacific has far and above the
A. Croquer, University of Puerto Rico,
meso-america: caribbean basin
highest coral diversity (Figure 2), the
pers. comm., December 2006) to a high
The Caribbean has historically been
most reports of disease come from the
of up to 20 percent on the Yucatán and
dubbed a disease "hotspot" because of
Caribbean. Overall, prevalence of all
at other Caribbean localities (Jordán-
the fast emergence, high prevalence, wide
coral diseases combined within a region
Dalgren et al., 2005; Weil et al., 2006;
geographic distribution, and virulence of
ranges from lows of less than 5 percent
Ward et al., 2006). What prevalence does
coral reef diseases there. Although only
in Australia, Palau, and E. Africa, and
not reveal is the dynamics of disease out-
8 percent of all coral reefs (by area) are
8 percent in the Philippines (Weil et al.,
breaks that have been recorded sporadi-
found in the Caribbean (Spalding and
2002; Willis et al., 2004; Raymundo et
cally in all regions, but most regularly
Greenfell, 1997), over 70 percent of all
al., 2005; Page et al., 2006; E. Weil and
in the Caribbean.
disease/syndrome reports come from
300
figure 2. species richness
of reef corals within fami-
Elsewhere
lies (x-axis) and suborders
Atlantic Ocean
(colored bar below x-axis)
250
Indian Ocean
and their distributions
Pacific Ocean
Indo-Pacific
across reef regions (col-
ored portions within each
histogram). Insets illus-
200
trate species within the
most abundant and typi-
cally dominant coral fam-
150
ilies (from left to right:
e
r

o
f

s
p
e
c
i
e
s
pocilloporidae, acropo-
ridae, faviidae, and pori-
Numb
tidae). unlabeled subor-
100
ders are: caryophylliina
(yellow), poritiina (light
orange), dendrophyllina
(dark orange). Photos by
50
J. Veron and B. Wil is
0
u
s
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Archaeocoeniina
Fungiina
Faviina
Meandriina
176
Oceanography Vol. 20, No. 1

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this region. While past bleaching events
urchins have resulted in signifi cant losses
cent) of zooxanthellate coral species, ten
in the Caribbean did not produce high
in coral cover, biodiversity, and habitat
octocorals (soft coral), nine sponges,
mortality rates like those reported for the
of many Caribbean coral reefs (Lessios
one zoanthid, and two crustose coralline
Indo-Pacifi c (McClanahan, 2004), this
et al., 1984; Hughes, 1994; Aronson and
algae in the region (Table 1). Potential
rate may be changing. The 2005 bleach-
Precht, 2001; Weil 2004).
pathogens have only been identifi ed for
ing event was the worst recorded and
The fi rst Caribbean coral-related dis-
seven of the commonly found coral dis-
produced signifi cant mortalities in some
eases were reported in the early 1970s
eases and Koch's postulates have only
scleractinian (hard-coral) populations in
(Antonius, 1973; Garret and Ducklow,
been fulfi lled for fi ve of these (Figure 3;
several reef localities. Today, diseases of
1975). There are now about 20 reported
see following section titled "Pathogens").
corals and other keystone species such as
diseases affecting 45 (that is, 75 per-
Several other common and highly viru-
table 1. some of the most commonly found coral diseases.
presented here are
# of Species Infected some of the most com-
Disease
Acronym
Pathogen
COR
OCT
monly found coral dis-
eases with their names,
carIbbeaN
acronym, pathogen (if
black band
bbd
P. coral yticum, Desulfovibrio, Beggiatoa sp
19
6
known), and Number
of taxa aff ected for
White band I
Wbd-I
gram (-) bacterium
2
"hard" or scleractin-
ian coral (cor) and
White band II2
Wbd-II
Vibrio carchariae
2
"soft" or octocoral
White plague I
Wp-I
gram (-) bacterium
12
(oct). each disease
is generally named for
White plague II2
Wp-II
Aurantimonas coralicida
41
its symptoms. Th is
informal classifi cation
aspergillosis2
asp
Aspergil us sydowi
10
system has caused
White pox2
WpX
Serratia marcescens
1
some confusion in the
literature, as the no-
growth anomalies1
tum
A. endozoica (algae) and other causes
7
5
menclature is not yet
red band
rbd
Oscillatoria sp. and other cyanobacteria
13
1
standardized (adapted
from Weil et al., 2006).
yellow blotch
ybs
Vibrio sp ?
11
dark spots I
dss-I
Vibrio sp ?
10
dark bands
dbs-II
?
8
INdo-pacIfIc-medIterraNeaN
Porites trematodiasis
ptr
Podocotyloides stenometra
4
skeletal eroding band
seb
Halofolliculina corallasia
2
brown band
brb
New species of ciliate--not described
2
Porites ulcerative white spots
puWs
Vibrio sp
3
bacterial bleaching2
bbl
Vibrio shiloi
1
bacterial bleaching2
bbl
Vibrio coral i lyticus
1
White-plague
Wp
Th alassomonas loyona
5
1growth anomalies include hyperplasias and algal tumors.
2koch's postulates fulfi lled.
Oceanography march 2007
177

---

bacterIal
WhIte plague II
WhIte baNd II
WhIte poX
aspergIllosIs
bleachINg
Diploria labyrinthiformis
Acropora palmata
Acropora palmata
Gorgonia ventalina
Oculina patagonica
Aurantimonas coralicida
Vibrio carchariae
Serratia marcescens1
Aspergil us sydowi 2
Vibrio coral i lyticus
(bacterium)
(bacterium)
(bacterium)
(fungus)
(shown) and
V. shiloi
1
(bacterium)
source: http://commtechlab.msu.edu/sites/dlc-me/zoo/microbes/serratia.html
2 source: http://www.cdc.gov/ncidod/dbmd/mdb/images/aspergillos.Jpg
figure 3. 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. briefly, 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.
lent syndromes, such as yellow blotch
crustose algae (Figure 4J­O).
potentially affecting Caribbean coral
(Figure 4A), dark band (Figure 4D),
Surveys conducted from 1999 through
reef resilience. (3) Most outbreaks oc-
white blotch, and tissue necrosis (Fig-
2004 on more than 40 reef sites in over
cur during the warmest season of the
ure 4E­F) have become more prevalent
ten geographic locations in the wider
year and produce significant loss of coral
and widespread in recent years, posing
Caribbean (Weil et al., 2002; Weil, 2004;
cover. (4) Different diseases affect their
an increasing threat to coral and octo-
Smith and Weil, 2004) revealed several
hosts differently over their geographic
coral populations (Gil-Agudelo et al.,
patterns. (1) Disease prevalence increases
distribution. (5) Prevalence of colonies
2004; Cervino et al., 2004; Smith and
from north to south in the Caribbean
with multiple diseases/syndromes is in-
Weil, 2004). Furthermore, extensive
region and is highly variable both spa-
creasing. (6) The newly described ciliate
surveys in many coral reefs around the
tially and temporarily. (2) Most virulent
disease in the Caribbean (Croquer et al.,
wider Caribbean revealed a suite of new
infectious diseases (white plague, yellow
2006) is expanding geographically, in-
syndromes and problems that produce
blotch, and white band) have a wide-
fecting not only diseased colonies, but
tissue necrosis and/or colony mortalities
spread distribution and are significantly
healthy colonies as well (Miller et al.,
in other important components of coral
impacting the ten most important reef-
2006; Weil et al., 2006; Aldo Croquer and
reef communities such as hydrocorals,
building species around their geographic
Ernesto Weil, University of Puerto Rico,
sponges, zoanthids, and calcareous-
distribution in the wider Caribbean,
pers. comm., December 2006).
178
Oceanography Vol. 20, No. 1

---

figure 4. common diseases affecting corals and other coral reef organisms in the caribbean. (a) yellow blotch; (b and c) dark spots;
(d) dark band; (e and f) necrotic tissue; (g) purple band; (h) dark line of ciliates (Halofoliculina sp) in Montastraea; (I) colony
with multiple diseases; (J) coralline white band in crustose alga; (k and l) necrotic tissue in crustose octocorals; (m) a zoanthid; and
(N and o) sponges. Photos by E. Weil
Oceanography march 2007
179

---

meso-america: yucatán coast
While the hurricanes may have had
reveal that the most abundant coral taxa
The Meso-American Reef consists of
an impact on overall community struc-
(Montastraea) had the highest disease
barrier-like reefs that border the Yucatán
ture, diseases seem to be the main factor
prevalence (Figures 6 and 7). In addition,
coastline from the Mexican Caribbean
in the declining cover of scleractinian
some coral species are facing challenges
to the coast of Honduras. Using SCUBA,
corals in the surveyed areas. Data on
from multiple pathogens. For example,
baseline surveys were conducted in 1985
diseases from ten sites clustered in the
white band disease severely reduced the
using a standard sampling protocol. This
central Yucatán, adjacent to Akumal,
extent of Acropora palmata coral cover,
same protocol was used to resurvey the
sites in 2005. Comparison of total coral
cover from these two surveys revealed a
drastic decrease in coral coverage over
the 20-year period, particularly in the
reefs in the Biosphere Preserve (the
60
Mahahual site--see Figure 5).
While the decline in coral cover may
1985
50
2005
have different causes, the most likely are
)
hurricanes and disease outbreaks. In the
40
early 1980s, there were massive die-offs
o
v
e
r

(
%
30
of acroporid (staghorn) corals due to
white band disease and the sea urchin
C
o
r
a
l

C
20
Diadema antillarum (Lessios et al.,
1984). Then, in 1988, the northern Mexi-
10
can Caribbean reefs (near Puerto More-
0
los) were severely impacted by Hurricane
P. Morelos
Akumal
Uvero
Mahahual
Xcalac
Gilbert (Class V), which destroyed most
figure 5. coral cover surveys conducted in 1985 and 2005 on the mexican
yucatán show a significant decrease in overall coral cover over the 20-year period.
of the remaining Acropora stands. The
central-section reefs of El Uvero and
Akumal were damaged to a variable de-
70
gree by Hurricane Roxanne (Class III)
Mann 1985
60
in 1995, but by then, most acroporids
Mann 2005
had died due to another outbreak of
Apal 1985
) 50
Apal 2005
white band disease. The southern reefs of
Mahahual and Xcalac were again affected
o
v
e
r

(
%
40
by the sea swell generated by Hurricane
o
r
a
l

C
Mitch (Class IV) in 1998. Recovery from
30
the damage was patchy, but notice-
20
able (Jordán-Dahlgren and Rodríguez-
R
e
l
a
t
i
v
e

C
Martínez, 1998). By 2000, a variety of
10
diseases were affecting many species, but
only yellow blotch became an important
0
P. Morelos
Akumal
Uvero
Mahahual
Xcalac
disease on Montastraea hosts.
figure 6. coral cover surveys conducted in 1985 and 2005 on the mexican yucatán show
a decrease in key reef building species. mann = Montastraea annularis species complex.
apal = Acropora palmata.
180
Oceanography Vol. 20, No. 1

---

but current declines of A. cervicornis may
Although Figures 5 and 6 show moder-
australia: great barrier reef
also be the result of this disease. Simi-
ate disease levels from 2005, surveys in
Until recently, it was assumed that dis-
larly, yellow blotch on Montastraea spp.
2006--after the hurricane and bleach-
ease has had little impact on the popu-
has caused large mortalities (Jordán-
ing events of 2005--revealed an order of
lation dynamics and structure of coral
Dahlgren et al., 2005), and this effect is
magnitude increase (Eric Jordan, Uni-
assemblages on the Great Barrier Reef
now further enhanced by a white plague
versidad Nacional Autónoma de México,
(GBR). The GBR is the largest coral reef
outbreak on the remaining colonies.
pers. comm., September 2006).
system in the world, stretching 2300 km
along Australia's northeast coast and
comprised of more than 2800 reefs.
Considered among the healthiest and
most pristine, the majority of GBR reefs
are located between 20 and 150 km off-
Abundance
0
5
10
15
20
25
30
shore and adjacent to either unpopu-
Montastrea
lated coastlines or generally low-density
urban development. The entire GBR was
Porites
accorded Marine Park status in 1975,
Siderastrea
and the area of highly protected zones
Agaricia
elevated from 4.5 to 33 percent of the
Diploria
Marine Park in 2004. Prior to 2000, only
Dichocoenia
two studies had focused on coral disease
Stephanocoenia
in the region, one on black band dis-
ease (Dinsdale, 2002) and the other on
Acropora
skeletal eroding band (Antonius, 1999;
Oculina
Antonius and Lipscomb, 2001). Howev-
Meandrina
er, dramatic increases in the abundance
Mycetophyllia
of white syndrome (described below) on
Isophyllastrea
a number of reefs in 2002­2003 (Willis
Colpophyllia
et al., 2004) heralded an increasing
Madracis
awareness of coral disease on the GBR.
Quantitative surveys between 2002
Dendrogyra
and 2006 revealed generally low
Eusmilia
(< 5 percent) disease prevalence on reefs
Helioseris
surveyed in the northern, central, and
Scolymia
southern regions of the GBR (Willis et
Isophyllia
al., 2004; Bette Willis and Cathie Page,
Solenastrea
James Cook University, pers. comm.,
December 2006). The surveys sam-
0
5
10
15
20
25
30
Disease Prevalence (%)
pled a range of habitats and reef types
figure 7. The abundance of major coral genera (bar) and preva-
along north-south gradients more than
lence of disease (circle) in the yucatán (2004). Note that some
2000 km in length and cross-shelf (east-
of the most important reef-building coral also have the highest
west) gradients ranging up to 100 km
prevalence of disease. Replotted from Ward et al. (2006)
from the coast. Overall, seven disease
types have been recorded: black band
Oceanography march 2007
181

---

disease, skeletal eroding band, white
common disease recorded in surveys.
loss on Indo-Pacific corals; it is used to
syndrome, brown band disease, growth
The ciliate erodes both coral tissue and
describe progressive exposure of skeleton
anomalies, atramentous necrosis, and
skeleton as it produces a black test (An-
in white bands behind receding tissue
cyanobacterial syndromes (other than
tonius, 1999); it affects at least 31 species
fronts (Willis et al., 2004). The role of
black band disease). Detection of some
in six coral families on the GBR (Willis
secondary pathogens, such as ciliates (see
of the more common and infectious Ca-
et al., 2004). Although initially thought
brown band disease description below)
ribbean diseases (black band disease and
to be restricted to the Indo-Pacific, re-
in escalating rates of tissue loss requires
potentially some of the white diseases),
cords of a new species of Halofolliculina,
further investigation. White syndrome
in combination with discovery of dis-
causing similar signs on corals from six
has been recorded to affect 17 coral spe-
eases unique to the region such as brown
families in the Caribbean (Croquer et al.,
cies in four families on the GBR, with
band disease (Willis et al., 2004), suggest
2006), now suggest that halofolliculinid
species of Acropora being important
that coral diseases are common on Indo-
infections are global in distribution.
hosts (Willis et al., 2004).
Pacific reefs and may have a greater role
Cases of white syndrome (Figure 8C)
Brown band disease (Figure 8D) is a
in structuring coral communities in the
reached peak abundance in 2002­2003,
new syndrome and has been recorded
region than previously thought.
concurrent with the most severe bleach-
on corals in all three sectors of the GBR
All seven of the coral diseases detected
ing event so far recorded on the GBR,
(Willis et al., 2004). The distinctive mac-
are widespread throughout the GBR.
but have since declined to low levels in
roscopic field sign is a brown zone of
Black band disease (Figure 8A) occurs
all regions (Bette Willis and Cathie Page,
variable width flanked by healthy tissue
on more than 70 percent of reefs sur-
James Cook University, pers. comm., De-
on one side and exposed white skeleton
veyed (19 in all) and in all three sectors,
cember 2006). The twentyfold increase
on the other as the band advances over
although its prevalence is typically low
in white syndrome on some outer-shelf
the surface of the colony. Dense popula-
tions of an unidentified ciliate, packed
with zooxanthellae from engulfed coral
tissue, cause the brown coloration of
the band. At high densities, the ciliates
...innovative microbiological approaches to
can cause rapid tissue loss. Brown band
coral defense coupled with improved molecular
disease has been reported on 16 species
diagnostics of pathogenic microorganisms
from three families on the GBR, with
acroporid corals being important hosts
and attempts to approach coral resistance
(Willis et al., 2004).
with genomics tools, are emerging
Growth anomalies (Figure 8E)
have been found primarily on species
areas in the study of coral disease.
of Acropora in disease surveys on the
GBR, although they also affect species
of Montipora and Porites (Willis et al.,
(~ 0.1 percent of scleractinian corals)
reefs in the northern and southern sec-
2004). Reports of coral tumors grow-
(Page et al., 2006). It has infected at least
tors between 1998 and 2003 suggests that
ing on 18­24 percent of Platygyra pini
32 coral species in 10 families on the
the prevalence of white syndrome may
and P. sinensis' populations on Mag-
GBR, with branching pocilloporid and
be correlated with elevated temperatures,
netic Island in the central GBR (Loya
acroporid corals being important hosts
but possibly only when host densities are
et al., 1984) indicate that they have af-
(Willis et al., 2004). Skeletal eroding
high (Selig et al., 2006). White syndrome
fected corals on the GBR for more than
band (Figure 8B), caused by the protozo-
is a collective term for conditions pro-
two decades and may be moderately
an Halofolliculina corallasia, is the most
ducing white signs associated with tissue
prevalent on local scales. Atramentous
182
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---

necrosis (Figure 8F) has primarily been
recorded on a Montipora species at Mag-
netic Island (Jones et al., 2004), although
it has also recently been recorded in dis-
ease surveys in the northern and south-
ern regions of the GBR (Bette Willis and
Cathie Page, James Cook University, pers.
comm., December 2006). Cyanobacterial
syndromes (other than black band dis-
ease) (Figure 8G) affect a range of corals
in at least five families, but acroporids
and pocilloporids are primary hosts
(Bette Willis and Cathie Page, James
Cook University, pers. comm., December
2006). A number of other macroscopic
field signs are classified as indicators of
compromised coral health, including
pigmentation response (pink or purple
tissue pigmentation adjacent to sites of
competitive interactions and lesions),
algal overgrowth (algal filaments grow-
ing directly on live coral tissue), and
unusual bleaching patterns (e.g., distinct
and unusual patches, spots, and stripes
of bleached tissue that differ from typi-
cal patterns of whole colony bleaching or
paling seen during thermal anomalies)
(Willis et al., 2004).
figure 8. common diseases affecting corals on
the great barrier reef. (a) black band disease
Very little is known about pathogens
on Montipora; (b) skeletal eroding band on
or abiotic triggers associated with coral
branching Acropora; (c) white syndrome on
disease on the GBR. Of the seven disease
plating Acropora; (d) brown band on branching
Acropora; (e) growth anomalies on branching
types described, two are associated with
Acropora; (f) atramentous necrosis on Montipora;
cyanobacterial infections (black band
(g) other cyanobacterial syndrome on Pocillopora.
disease, other cyanobacterial syndromes)
Photos by B. Wil is
and two with protozoan infections (skel-
etal eroding band, brown band disease).
White syndrome and atramentous ne-
crosis have been associated with Vibrio
infections (Meir Sussman, James Cook
University, and David Bourne, Australian
Institute of Marine Science, pers. comm.,
September 2006). Carbon-14 studies
near boundaries of lesions on tabular
Oceanography march 2007
183

---

Acropora colonies suggest that photo-
reefs. Coral disease has recently been
(Kaczmarksy, 2006). In 2006, coralline
assimilates are preferentially translocated
added to the list of stressors these reefs
lethal orange disease, affecting crustose
away from lesions in an apparent shut-
face. With the current effort to deter-
coralline algae, was also recorded for the
down reaction, potentially as a result of
mine the nature of linkages between
first time in Philippine reefs, in low prev-
abiotic factors or pathogens triggering
anthropogenic drivers and disease pro-
alence (Laurie Raymundo, University of
an apoptotic pathway in the host (Roff et
gression and infection rates, and the
Guam, pers. comm., December 2006).
al., 2006). Clearly, further studies of coral
compelling evidence in support of such
A putative causal agent has been de-
pathogens would significantly enhance
a link, it is likely that coral diseases will
termined for black band disease from
current understanding of coral diseases
become a major source of mortality on
Palau corals: an unidentified cyanobac-
on the GBR and increase the potential
many Philippine reefs already stressed.
terium identical to that associated with
for mitigating their impacts.
Antonius (1985) was the first to re-
black band disease in Caribbean corals
cord diseases affecting Philippine reefs.
(Sussman et al., 2006). While it has not
philippines/southeast asia
Black band disease, while found in eight
been determined if the Philippine black
Philippine coral reefs comprise the
different species of primarily faviids, was
band disease infections contain the same
second largest reef area in Southeast
relatively uncommon. Almost 20 years
cyanobacterial consortium, infected cor-
Asia, covering an estimated 26,000 km2.
later, combined surveys and monitor-
als from Palau and the Philippines show
They are among the most diverse reefs
ing efforts have revealed a number of
strong similarities at both gross and
known, with over 500 species of scler-
diseases affecting a broad range of host
microscopic levels. A causal agent for
actinian corals recorded (Veron, 2000).
species. Mean total disease prevalence,
skeletal eroding band affecting GBR cor-
However, these reefs are also among
established from surveys of eight reefs
als has also been determined (Table 1),
the most stressed in the world, facing
in two regions in 2003, was 8 percent
though, again, it is not known if the
multiple threats that include bleaching,
(Raymundo et al., 2005). The two con-
ciliate causing skeletal eroding band in
overfishing, destructive fishing, siltation,
sistently most prevalent diseases affect-
the Philippines is the same species. A
and outright destruction for coastal
ing Philippine reefs are Porites ulcer-
putative causal agent for PUWS appears
development. Due to a human popula-
ative white spot disease (PUWS) and a
to be an undescribed species of Vibrio,
tion growth rate of 2.3 percent per year,
growth anomaly affecting massive Porites
which is currently under investigation.
98 percent of Philippine reefs are con-
(Raymundo et al., 2003; Raymundo et
Many of these diseases appear to target
sidered to be under medium-to-high
al., 2005; Kaczmarsky, 2006) (Figure 9).
the dominant reef-building genus Porites
risk from these anthropogenic impacts
PUWS affects at least 14 different spe-
(Raymundo et al., 2005; Kaczmarsky,
(Burke et al., 2002). In an attempt to ad-
cies, with some localized areas having
2006). Preliminary data suggest a link
dress the rapid loss of these highly pro-
a prevalence of 72 percent of host spe-
between disease prevalence and proxim-
ductive systems, the Philippine govern-
cies (Raymundo et al., 2005). Growth
ity to human population centers (Kac-
ment has enacted a number of laws over
anomalies, likewise, show localized
zmarsky, 2006). These results suggest
the past decade to manage remaining
areas of prevalence as high as 39 per-
the potential for long-term impacts on
reefs, largely through the establishment
cent of massive Porites (Kaczmarsky,
reef communities.
of Marine Protected Areas (MPAs).
2006). Black band disease was recorded
The end result of this legislation has
in very low prevalence in 2002­2003
east africa
been the designation of approximately
(Kaczmarsky, 2006) and in 2006 (Laurie
The corals reefs of East Africa range
500 MPAs throughout the country, one
Raymundo, University of Guam, pers.
from the coast of South Africa to
of the largest MPA networks currently in
comm., December 2006). In addition,
Somalia. Encompassing approximately
place (Aliño et al., 2000). Therefore, the
skeletal eroding band and white syn-
7000 km2, these highly diverse reefs are
diverse Philippine reef system contains
drome (as described above on the GBR)
home to over 300 coral species. There
both highly impacted and well-managed
have been found on a variety of genera
are four major reef systems: isolated
184
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Kenya in 2005 (Figure 10; Ernesto Weil,
University of Puerto Rico, pers. comm.,
December 2006).
One of the most destructive forces on
coral reefs in the western Indian Ocean
has been coral bleaching. High water
temperatures associated with the 1998
El Niño Southern Oscillation caused a
widespread bleaching event that resulted
in 50 percent mortality in some areas
(McClanahan, 2004). Other serious but
more regional bleaching events occurred
in 2003 and 2005. Recent studies show
that recovery has occurred in some reefs,
while others suffered serious bio-erosion
due to the destruction of the underlying
figure 9. common diseases of philippine
reef framework (Obura, 2005).
corals. (a) black band disease; (b) growth
While these reefs have historically
anomaly affecting a massive Porites; (c) skel-
been considered relatively isolated
etal eroding band on Pocillopora verrucosa;
(d) Porites ulcerative white spot disease on
and pristine, rapid human population
a Porites cylindrical; (e) white syndrome on
growth has been driving a decrease in
massive Porites. Photos by L. Raymundo
water quality (due to nutrients and sedi-
mentation), and an increase in destruc-
tive fishing methods (Obura, 2005).
Working with local and international
nongovernmental organizations, many
countries have set up MPAs to try to
alleviate and prevent reef destruction.
The national coral reef task forces have
implemented monitoring programs that
reefs along the coast of South Africa to
(McClanahan, 2004). More recently, a
observe general reef status and diversity
Mozambique, a barrier and island reef
limited outbreak of a newly described
(Obura, 2005). It is critical that these
system near Tanzania, fringe reefs off
white syndrome occurred off the Kenya
programs begin to look for coral dis-
southern Kenya, and patchy reefs to the
coast. This outbreak, associated with
ease and identify outbreaks in what has
north (Obura et al., 2004).
an infection of fungal hyphae, almost
been a highly understudied area. To this
There have been few studies on coral
eliminated Montipora from affected
end, we held a coral disease workshop
disease in this area; thus, infectious dis-
Kenyan reefs (McClanahan et al., 2004).
in April 2006 at the Center of Excellence
ease outbreaks have not been commonly
Observations in Zanzibar and Kenya
in Zanzibar for regional scientists and
reported. Bacteria-induced bleach-
revealed low levels of PUWS, brown
government personnel to train in mi-
ing was found in Zanzibar (Ben-Haim
band, white syndromes, growth anoma-
crobiology and help foster local moni-
and Rosenberg, 2002). Black band,
lies, and tissue necrosis affecting corals,
toring and reporting of any outbreaks
white band, and yellow band diseases
octocorals, and sponges in several reef
in the region.
were reported in isolated outbreaks
localities off the coast of Zanzibar and
Oceanography march 2007
185

---

figure 10. most common diseases and syndromes in east africa. White syndrome affecting Montipora (a) and Echinopora (d) colo-
nies in Zanzibar. growth anomaly (puffy syndrome) on massive Porites in kenya (b) and on Acropora in Zanzibar (e). Acropora with
brown band disease (ciliates) (c). Porites ulcerative white spots (puWs) on massive Porites (f) and black band on Montipora (g) in
Zanzibar. compromised tissue responses in Porites (necrotic tissue) (h) and pigmentation response in Porites (I). other important
reef organisms affected included crustose coralline algae with white band-type syndrome (J), tube sponges with necrotic areas (k),
and crustose octocorals with necrotic areas (l). Photos by E. Weil
186
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2. eNVIroNmeNtal drIVers
On the GBR, seasonal patterns in
of temperature values derived from the
temperature
coral disease show dramatic increases
US National Oceanic and Atmospheric
One of our research goals is to inves-
in prevalence between winter and sum-
Administration Advanced Very High
tigate the relationship between disease
mer surveys in all major families of
Resolution Radiometer (AVHRR) Path-
outbreaks and ocean-warming anoma-
coral (Willis et al., 2004). For example,
finder (a radiation-detection imager that
lies. Our hypothesis is that coral disease
disease increased fifteenfold in acropo-
can determine surface temperature), we
is enhanced by ocean warming. There
rids, twelvefold in faviids, and doubled
detected a highly significant relationship
is evidence for this relationship in the
in pocilloporids in summer surveys.
between the frequency of warm tem-
mass mortality of the gorgonian coral
Prevalence of three coral diseases in-
perature anomalies and the incidence of
Briareum asbestinum following the 1998
creased significantly in summer surveys,
white syndrome, indicating a relationship
El Niño event (Harvell et al., 2001). An
with skeletal eroding band increasing
between temperature and disease. Inter-
increase in disease following warming
more than twofold, black band and other
estingly, this relationship also depends
events may occur because corals are less
cyanobacterial infections more than
on a high degree of coral cover, as would
able to fight disease while under tem-
threefold, and white syndrome more
be expected for transmission of an infec-
perature stress, or because pathogens
than fiftyfold.
tious agent (Bruno et al., in press).
are more virulent at higher tempera-
To investigate whether coral disease
tures. In at least three cases (Aspergil-
was correlated with warm-temperature
Water Quality
lus sydowii, Vibrio shiloi, and Vibrio
anomalies, we used disease-prevalence
Scientists generally agree that environ-
coralliilyticus), pathogen growth and/or
surveys spanning 500 km of a latitudi-
mental stress can impact coral health. As
virulence factors increase to an optimal
nal gradient along the GBR (Selig et al.,
human populations continue to increase,
temperature (Israely et al., 2001; Banin
2006). In 1998, the Australian Institute of
nutrients, terrigenous silt, pollutants,
et al., 2000; Alker et al., 2001; Ben-Haim
Marine Science's Long-Term Monitoring
and even pathogens themselves can be
et al, 2003a, b).
Program began to systematically monitor
released into nearshore benthic com-
Seasonal patterns in disease preva-
white syndrome, which affects more than
munities (Harvell et al., 2004). The det-
lence in the northeastern Caribbean
provide further support for a link be-
tween warming ocean waters and disease
outbreaks. Recurrent outbreaks of the
two most virulent and damaging dis-
If habitat deterioration and climate
eases, white plague and yellow blotch,
warming continue at the same rates, we
developed during the summer and fall
seasons (highest water temperatures) of
are faced with unprecedented challenges
the past four years on Puerto Rican reefs
in managing coral reef communities.
(Ernesto Weil and Edwin Hernandez-
Delgado, University of Puerto Rico, pers.
comm., December 2006) and in the US
Virgin Islands (Miller et al., 2006; Rogers
and Miller, 2006). Immediately following
15 coral species, including the domi-
rimental effects of such inputs may vary
the peak of the 2005 bleaching event, the
nant plating acroporids. Using SCUBA,
between species and at different life-
most devastating recorded in the north-
divers conducted annual coral disease
history stages within species, and may
eastern Caribbean, outbreaks of white
surveys on 47 reefs from 1998 to 2004
be affected by the nature and timing of
plague and yellow blotch were even more
to quantify the number of cases of white
delivery. Effects of environmental stress
extensive in these areas.
syndrome. Using a weekly 4-km data set
on development, growth, reproduction,
Oceanography march 2007
187

---

and survival have been demonstrated in
often observed to possess large patches
3. pathogeNs
a variety of benthic nearshore taxa. And
of dead, exposed skeleton bordered by
Unfortunately, the identities of most
while the link between anthropogenic
apparently receding margins of healthy
coral pathogens are not known. The
stress and disease susceptibility is cur-
tissue. While coral tissue mortality was
classic way to prove a particular
rently poorly understood, our hypoth-
previously assumed to be the result of
microorganism causes disease is to prove
esis is that coral disease is facilitated by
direct smothering, microbial agents
Koch's postulates (see Figure 3). The five
a decrease in water quality, particularly
may also be implicated. Early work by
diseases for which the microbial cause
due to eutrophication and sedimentation
Hodgson (1990) identified silt-associated
has been established via Koch's Postulates
(Bruno et al., 2003).
bacteria as a possible cause for necrosis
include white band II (Ritchie and Smith,
Eutrophication poses a number of
in sediment-damaged corals, as antibi-
1998), white plague type II (Richardson
threats, including enhanced disease pro-
otic-treated water reduced the amount
et al., 1998), aspergillosis (Smith et al.,
gression. Although corals are known to
of tissue damage in experimentally silted
1998; Nagelkerken et al., 1997; Geiser
grow in high-nutrient water (Atkinson
corals. More recently, opportunistic
et al., 1998), white pox (Patterson et al.,
et al., 1995), recent evidence suggests a
terrestrial pathogens (the soil fungus
2002), and bacterial bleaching of Oculina
synergistic relationship between elevated
Aspergillus sydowii and the human en-
patagonica by Vibrio shiloii (Kushamaro
nutrients and disease. High-nutrient
terobacterium Serratia marcescens) have
et al., 1997) and of P. damicornis by
levels (nitrogen and phosphorus) were
been demonstrated as causal agents for
Vibrio coralliilyticus (Ben Haim et al.,
associated with accelerated tissue loss
two diseases currently impacting domi-
2003b). Some diseases seem to be caused
in both yellow band- and Aspergillosis-
nant corals in the Caribbean (Geiser et
by a single organism while others ap-
infected corals in field manipulations
al., 1998; Patterson et al., 2002). Eolian
pear to be caused by complex consortia
(Bruno et al., 2003), and in black band-
transport of dust from an expanding
of microbes. For example, black band
affected corals (Voss and Richardson,
Sahara desert has been hypothesized as
disease, found throughout the Carib-
2006), although high-nutrient levels
a source of Aspergillus spores (Garrison
bean and the Indo-Pacific, appears to
alone were not associated with increased
et al., 2003), suggesting a mechanism
contain at least 50 different bacterial
tissue loss in healthy corals. This obser-
that at least partially explains develop-
types (Sekar et al., 2006).
vation is consistent with the findings of
ment of the Caribbean basin as a global
This complex relationship of mi-
Kuntz et al. (2005) that there is rapid tis-
disease "hotspot." Thus, terrigenous
crobes that constitutes many coral dis-
sue sloughing in healthy corals exposed
inputs may not only be a cause of physi-
eases makes a definitive comparison of
to elevated carbon sources, but little
cal stress for shallow, benthic organ-
disease with similar symptoms difficult.
effect from elevated nitrogen and phos-
isms such as corals, but may also act as a
Without knowing what to look for, it
phorus. Thus, corals may seem to thrive
pathogen reservoir.
is extremely difficult to follow these
under high-nutrient conditions, but the
This evidence suggests that anthro-
pathogens through the environment to
combination of an active infection and
pogenic stressors are linked with disease
determine their reservoirs and modes of
elevated nutrients increases disease-
severity in complex ways. It is important
transmission. In addition, because dis-
progression rates. It is unclear whether
to establish and quantify such linkages,
eases are often identified by their symp-
this effect is due to an impact on host
as understanding these factors may make
toms alone, there has been confusion
resistance or a positive effect on patho-
it possible to mitigate stressors via im-
over whether certain reported diseases
gen growth or virulence.
proved reef management and land-use
were the same or different. Nevertheless,
Siltation offers yet another challenge
practices. The challenge lies in demon-
our knowledge of their pathology (isola-
to host disease resistance. The impacts of
strating these linkages in the complex
tion and identification of the pathogen),
terrigenous sedimentation on nearshore
system of diverse stressors acting upon
etiology (symptoms and relationships
communities are visible and well docu-
the coral holobiont.
between the host and pathogen), and
mented; corals inhabiting silted reefs are
epizootiology (e.g., geographic distri-
188
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c a s e s t u d y : b a c t e r I a l b l e a c h I N g o f c o r a l s
on a global scale, coral bleaching is the most devastating coral disease. coral bleaching is the disruption
of the symbiosis between the coral animal and intracellular dinofl agellate algae, commonly known as
zooxanthellae. as a result of the degeneration and/or expulsion of zooxanthellae from the coral host, the
white skeleton becomes visible through the transparent coral tissue, giving the organism a "bleached"
white appearance. bleaching is fatal to the coral unless the symbiotic relationship is reestablished.
studies over the last 20 years have indicated a correlation between "higher than normal" seawater
temperature and coral bleaching (reviewed by Jokiel, 2004). Th e most widely accepted hypothesis to
explain this correlation is that photo-inhibition and damage to the photosynthetic apparatus of the
zooxanthellae cannot be repaired at elevated temperatures (reviewed by stambler and dubinsky,
2005). studies showing that some bacterial pathogens become more virulent at higher temperatures
(rosenberg and falkovitz 2004) raise questions about the potential contribution of bacterial diseases to
mass bleaching events.
two cases of bacterial bleaching of corals have been well documented: bleaching of Oculina pata-
gonica in the mediterranean sea by Vibrio shiloi (kushmaro et al., 1996, 1997) and bleaching of Pocillo-
pora damicornis in the Indian ocean and red sea by Vibrio coral i lyticus (ben haim et al., 2003 a, b). Th e
V. shiloi/O. patagonica system has been studied in considerable detail. Th e bacterium shows chemotaxis
to its coral host (banin et al., 2001a) and then binds to a -galactoside receptor in the coral mucus (toren
et al., 1998). It then penetrates into the epidermal layer of the coral (banin et al. 2000), where it multiplies
intracellularly to cell densities of over 108 cells per cm3. Vibrio shiloi produces a proline-rich peptide called
toxin p, which causes a rapid decrease in the photosynthetic quantum yield of zooxanthellae (banin et
al., 2001b). several of the virulence factors essential for a successful infection of O. patagonica by V. shiloi
are synthesized at elevated summer seawater temperatures. Th ese factors include (1) a protein on the
bacterial cell surface that recognizes a receptor in the coral mucus (toren et al., 1998; banin et al., 2001a);
(2) superoxide dismutase, which allows the bacteria to survive in the oxygen-rich coral tissue (banin et
al., 2003); (3) toxin p, which binds to zooxanthellae membranes and inhibits photosynthesis (banin et al.,
2001b); and (4) enzymes that lyse zooxanthellae (ben-haim et al., 1999).
knowledge of reservoirs and modes of transmission has proven useful in the past for developing tech-
nologies for controlling the spread of disease. using fl uorescence in situ hybridization with a V. shiloi-
specifi c deoxyoligonucleotide probe, it was found that the marine fi reworm Hermodice carunculata is a
winter reservoir for V. shiloi (sussman et al., 2003). Worms taken directly from the sea during the winter
contained approximately 108 V. shiloi per worm. Worms carrying the pathogen could serve as vectors for
transmission of the disease, as they feed on coral tissue during the summer.
how general is bacterial bleaching of corals? several investigators have reported the patchy spatial
distribution and spreading nature of coral bleaching (e.g., Jokiel and coles, 1990; edmunds, 1994). patchy
distribution and spreading are highly symptomatic of infectious disease. clearly, more microbiological
research is necessary during a mass-bleaching event to test the bacterial hypothesis of coral bleaching.
Oceanography march 2007
189

---

butions, environmental factors, host
It is not known if the normal differences
development of a specialized symbiotic
ranges, prevalence, vectors, reservoirs,
in the chemical composition of the SML
microbial community (Figure 11), not
and spatial and temporal variability)
are due to variations in the zooxanthel-
unlike those found in microbial mats
is limited. Disease reservoirs have only
lae or variations in the metabolism of
(Ritchie and Smith, 2004). It appears
been identified for black band disease
the coral host.
that certain bacteria may be characteris-
(biofilms in reef sediments were found
In contrast to the relatively nutrient-
tic of specific coral species (Rowher and
to contain non-pathogenic aggregates
poor environment of the open water, the
Kelly, 2004). Although microbial com-
of the black band community) (Carlton
coral SML has a high concentration of
munities may vary from coral species to
and Richardson, 1995), and possibly for
organic compounds. As such, it hosts a
coral species, their metabolic activities
aspergillosis (atmospheric African dust
dense, complex community of micro-
are likely to be similar.
has been suggested to contains spores of
organisms that differ significantly from
Just as the normal microbial flora of
the fungus Aspergillus sydowii) (Shinn et
the microorganisms present in the open
humans protects us from infection, it is
al., 2000). The only coral-disease vectors
water. A number of spatial models have
likely that the normal microbiota associ-
identified are the fireworm Hermodice
been proposed for the SML and the mi-
ated with the surface layer of corals pro-
carunculata, whose gut has been found
crobial communities living there (see
tects the coral from invading microbes.
to harbor Vibrio shiloi (the pathogen in-
Brown and Bythell, 2005). One model
Ritchie (2006) found that mucus from
ducing bacterial bleaching in a Mediter-
suggests that the spatial stratification of
a healthy coral was able to inhibit the
ranean coral) (Sussman et al., 2003), and
various organic and inorganic nutrients
growth of other bacteria by tenfold. In
damselfish, which harbor one life-history
within the mucous layer results in the
addition, the competition of the normal
stage of a digenean (trematode) that in-
fects Porites (Aeby and Santavy, 2006).
4. dIsease resIstaNce
microbial surface mucous layers:
a barrier to disease
surface mucopolysaccharide layer
While all corals secrete a layer of mu-
cus over their surface (SML), we do not
organic
Water
understand much about its production,
exudates
mass
microbial
composition, or function within the ho-
community
lobiont. Most of the carbon that makes
up the SML originates from the symbi-
secondary
otic zooxanthellae (Patton et al., 1977),
coral tissue
surface
products
but is secreted by coral epidermal mucus
co
co
cells as an insoluble, hydrated, glyco-
2
2
protein that forms a gel-like layer over
Zooxanthellae
o2
the coral surface (Ducklow and Mitchell
o
1979; Meikle et al., 1988). The thickness
2
of the SML can vary from less than one
organic
Nitrogen
fixation
millimeter in some scleractinians, to a
Nitrogen
N2
few centimeters in some gorgonians. The
chemical composition of the SML from
figure 11. This model of coral surface mucopolysaccharide layer shows the movement of nutrients
through the layer of slime that coats the surface of coral. organic carbon from the zooxanthellae help
different coral species varies qualitatively
feed the complex community of microorganisms within the slime layer. These microbes most likely
and quantitatively (Meikle et al., 1988).
provide a critical layer of protection for corals against infection.
190
Oceanography Vol. 20, No. 1

---

flora for nutrients could prevent other
coral Immunity and the effects
In addition, corals make more slowly
potential pathogens from becoming
of environmental stress
developed anti-microbial chemicals
established. Changes in the carbon and
While lab studies of model organisms
(Mullen et al., 2004; Geffen and Rosen-
nitrogen pools (due to changes in the
such as Drosophila provide a basis for
berg, 2005), which have been detected
normal coral holobiont physiology, i.e.,
understanding invertebrate innate (non-
in a number of gorgonian cell extracts
disease or stress) could result in changes
specific) immunity, we have little un-
(Kim et al., 2000a). Antimicrobials are
in the SML microbial communities.
derstanding about nonmodel organisms
also produced by SML-associated mi-
We are investigating the hypothesis
that environmental factors can alter
the SML microbial community. Studies
show that shifts in heterotrophic micro-
We are still far away from any miracle
bial populations within the SML occur
when corals are stressed, either due to

"vaccine" or remediation protocol against
disease or during bleaching (Ritchie and
any of the current coral reef diseases.
Smith, 1995a, b; Frias-Lopez et al., 2002;
Koren and Rosenberg, 2006; Gil-Agudelo
et al., 2006). Because qualitative changes
have been reported in coral mucus dur-
like corals and about the interactions
croorganisms, as some specific anti-
ing bleaching, the change in community
between host immunity and pathogen-
microbial agents have been identified
may be a response to changes in avail-
esis in nature. Our work (Harvell) is
as products of resident bacteria in the
able carbon sources. It appears that as
focused on understanding the primary
mucus (Ritchie, 2006). Thus, we con-
corals recover from bleaching, their spe-
elements of immunity in a gorgonian
tinue to embrace a holistic approach to
cific microbial populations also recover.
coral-fungal pathosystem. A primary line
resistance of the holobiont, while at the
McGrath and Smith (1999) showed that
of gorgonian defense against pathogens
same time working through the various
Vibrio sp. populations tend to increase
is the circulating amoebocytes, which
mechanistic elements to come to an even
during bleaching but return to previous
encapsulate invaders (Mullen et al., 2004;
rudimentary understanding of how cor-
levels during recovery, while popula-
Mydlarz et al., 2006) and are induced in
als resist pathogenic infections.
tions of Pseudomonas sp. decrease during
large numbers during infections (Laura
There is evidence that heat-stressed
bleaching, but also return to previous
Mydlarz, University of Texas, pers. comm.,
corals are more susceptible to disease,
levels during recovery.
December 2006). In addition, propheno-
although it is not clear whether warmer
As the microbial communities change,
loxidase is activated to catalyze melanin
temperatures inhibit coral defenses by
so do their physiological functions, in-
deposition, as well as other downstream
altering the immune response or because
cluding the production of anti-microbial
reactions (Mydlarz et al., 2006). In in-
of bleaching, or whether temperature
compounds and the establishment of co-
fected gorgonians, melanin builds up as a
enhances the virulence of pathogens.
metabolic relationships, both among the
barrier to advancing fungal hyphae, thus
Efforts to unveil this link between tem-
microbes and between zooxanthellae and
preventing its spread (Petes et al., 2003).
perature stress and coral disease require
coral animals. Ritchie (2006) recently
This melanin buildup results in visible
careful experimentation with host im-
showed loss of antibiotic activity from
dark purple halos that are often associ-
mune responses and with pathogen viru-
coral mucus of Acropora palmata dur-
ated with fungal infections like Aspergil-
lence and infectivity. Pathogen response
ing a prolonged bleaching event. Thus,
lus. Other fast-acting enzymes such as
to increased temperatures may be a key
changes in the normal microbial com-
peroxidase (Mydlarz and Harvell, 2006)
element in the dynamics of coral dis-
munities may ultimately result in the
and chitinases (Douglas et al., 2006) play
eases. For example, Aspergillus sydowii,
development of disease.
a role in defense.
the fungal pathogen of the sea fan dis-
Oceanography march 2007
191

---

ease aspergillosis, grows at a faster rate at
micro-niche characteristics (Koren and
microorganisms and attempts to
higher temperatures (Alker et al., 2001),
Rosenberg, 2006; Rohwer et al., 2001;
approach coral resistance with genom-
and the bacterial pathogen of hard cor-
Richardson et al., 2001; Kellog, 2004).
ics tools, are emerging areas in the study
als, Vibrio coralliilyticus (Ben-Haim et
Recent research also shows that some
of coral disease.
al., 2003a), produces more lytic proteins
of these invertebrates can actively re-
If habitat deterioration and climate
when grown at elevated temperatures,
spond to the infections. Recent research
warming continue at the same rates, we
which increases its virulence. Adhesion
ability, a critical virulence factor in the
causative agent in coral bleaching (Vibrio
the complex symbiotic nature of the
shiloi) is also temperature-sensitive
(Toren et al., 1998). In addition to adhe-

coral holobiont offers one of the greatest
sion, production of anti-algal toxins and
challenges in invertebrate immunity,
superoxide dismutase (which detoxifies
oxygen radicals) are also temperature-

requiring an unraveling of the roles of
dependent virulence factors that seem to
sml, zooxanthellae, and coral tissue in
be induced in V. shiloi by elevated seawa-
orchestrating defenses against microbes.
ter temperatures (Banin et al., 2003).
dIscussIoN aNd
coNclusIoN
summarized in coral immunity shows
are faced with unprecedented challenges
After 20 years of research, we are still
the dynamic of an active immune re-
in managing coral reef communities. We
unable to explain the source or sud-
sponse to microbial infections. More fo-
are still far away from any miracle "vac-
den emergence of the majority of dis-
cus on understanding active mechanisms
cine" or remediation protocol against
ease syndromes in coral reefs. Warm-
of holobiont resistance, both in the SML
any of the current coral reef diseases.
temperature anomalies may facilitate
and in tissue of the coral, may suggest
Terrestrial disease managers use tools
the emergence and spread of pathogens
approaches to buffering immunity. The
that include quarantine, culling, and
or spread of other stressful agents that
complex, symbiotic nature of the coral
vaccination, which are not practical in
could affect the natural resistance (i.e.,
holobiont offers one of the greatest chal-
ocean systems. The fact that other key-
the "physiological equilibrium" between
lenges in invertebrate immunity, requir-
stone members of the reef community
coral hosts and their natural flora), or
ing an unraveling of the roles of SML,
are also being affected by new syndromes
could stimulate other bacteria living in
zooxanthellae, and coral tissue in orches-
complicates the picture even more. Ma-
reef sediments into becoming virulent.
trating defenses against microbes. New
rine pathogens can move faster and for
Very little is known about the composi-
advances in enhancing coral immunity
longer distances than ever before due
tion and dynamics of the natural micro-
are also emerging through the design-
to human activities such as commercial
bial communities living in association
ing of microbial defense systems, such as
and military shipping and the transport
with most corals, but recent findings re-
phage therapy. Phage therapy of corals
of marine species for aquaculture and
veal an impressive diversity of microbial
was shown by isolating from nature
the aquarium trade (McCallum et al.,
communities. They range from single
phage viruses that consume pathogenic
2003). One major question is whether
fungal or bacterial species to loosely or
bacteria and resulted in non-diseased
our current management tool, the estab-
tightly structured bacterial consortia that
corals (Efrony et al., 2006). These
lishment of MPAs, increases resilience of
include a wide variety of phototrophic
innovative microbiological approaches
coral reef ecosystems to regional-scale,
and heterotrophic bacterial species with
to coral defense, coupled with improved
water-borne pathogens such as the ones
a wide range of metabolic modes and
molecular diagnostics of pathogenic
that have caused mass mortalities in the
192
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