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Scuba diving damage and intensity of tourist activities increases coral
disease prevalence
Joleah B. Lamb
a,b,c,
, James D. True
d
, Srisakul Piromvaragorn
c,d
, Bette L. Willis
a,b,c
a
School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia
b
Australian Institute of Marine Science & James Cook University (AIMS@JCU), Townsville, Queensland 4811, Australia
c
Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies, Townsville, Queensland 4811, Australia
d
Center for Biodiversity in Peninsular Thailand, Faculty of Science, Prince of Songkla University, Hat Yai, Songkla 90112, Thailand
article info
Article history:
Received 25 March 2014
Received in revised form 27 June 2014
Accepted 29 June 2014
Keywords:
Ciliates
Coral disease
Damage
Diving
Koh Tao
Scuba
Skeletal eroding band
Sedimentation
Snorkelling
Thailand
Tourism
White syndrome
Wounds
abstract
Recreational diving and snorkeling on coral reefs is one of the fastest growing tourism sectors globally.
Damage associated with intensive recreational tourist use has been documented extensively on coral
reefs, however other impacts on coral health are unknown. Here, we compare the prevalence of 4 coral
diseases and 8 other indicators of compromised coral health at high and low use dive sites around the
island of Koh Tao, Thailand. Surveys of 10,499 corals reveal that the mean prevalence of healthy corals
at low use sites (79%) was twice that at high use sites (45%). We also found a 3-fold increase in coral
disease prevalence at high use sites, as well as significant increases in sponge overgrowth, physical injury,
tissue necrosis from sediment, and non-normally pigmented coral tissues. Injured corals were more
susceptible to skeletal eroding band disease only at high use sites, suggesting that additional stressors
associated with use intensity facilitate disease development. Sediment necrosis of coral tissues was
strongly associated with the prevalence of white syndromes, a devastating group of diseases, across all
sites. We did not find significant differences in mean levels of coral growth anomalies or black band dis-
ease between high and low use sites. Our results suggest that several indicators of coral health increase
understanding of impacts associated with rapid tourism development. Identifying practical management
strategies, such as spatial management of multiple reef-based activities, is necessary to balance growth of
tourism and maintenance of coral reefs.
Ó2014 Elsevier Ltd. All rights reserved.
1. Introduction
Global decline in coral reef health is a critical conservation con-
cern, especially for the estimated 275 million people that live
within 30 km of coral reefs and draw extensively on them for live-
lihood and food security (Bellwood et al., 2004; Burke et al., 2011).
There is pressing demand to find income-generating alternatives to
destructive and extractive uses of marine resources (Birkeland,
1997). Tourism is generally considered a favorable alternative,
typically providing an incentive to preserve natural areas, thereby
contributing to environmental protection, sustainable use prac-
tices, and the restoration of biological diversity (Buckley, 2012).
Coral reef-based tourism is one of the fastest growing tourism
sectors worldwide (Ong and Musa, 2011). However, because the
majority of coral reefs are located in developing and often
undermanaged island and coastal regions (Donner and Portere,
2007), the unrestricted growth and rapid development of
reef-based tourism often undermines the conservation priorities
necessary to sustain it.
Coral disease outbreaks are now recognized as a significant fac-
tor in the accelerating degradation of coral reefs, and it is com-
monly assumed that a variety of human-related activities have
altered environmental conditions, potentially impairing coral
resistance to microbial infections or increasing pathogen virulence
(Altizer et al., 2013). Anthropogenic activities implicated in disease
outbreaks and rising prevalence levels (i.e., the number of cases of
a disease in a given population at a specific time) include proximity
to human population centers (Aeby et al., 2011a), coastal land
alteration and dredging (Guilherme Becker et al., 2013; Pollock
et al., 2014), terrestrial runoff of sediment or agricultural herbi-
cides (Owen et al., 2002; Haapkylä et al., 2011), sewage outfalls
containing human enteric microorganisms (Patterson et al.,
2002), increases in nutrient concentrations (Bruno et al., 2003),
aquaculture and fish farms (Harvell et al., 1999; Garren et al.,
2009), a reduction in the diversity of reef fish assemblages
(Raymundo et al., 2009), and sunscreens (Danovaro et al., 2008).
http://dx.doi.org/10.1016/j.biocon.2014.06.027
0006-3207/Ó2014 Elsevier Ltd. All rights reserved.
Corresponding author. Present Address: Cornell University, Department of
Ecology and Evolutionary Biology, Ithaca, NY 14850, USA. Tel.: +1 607 216 5021.
E-mail address: joleah.lamb@jcu.edu.au (J.B. Lamb).
Biological Conservation 178 (2014) 88–96
Contents lists available at ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Until recently, recreational reef-based activities, such as diving
and snorkeling, were thought to have little direct impact on coral
assemblages. However, over the past two decades, numerous stud-
ies have been conducted on the physical impacts and management
of diving on coral reefs worldwide. Most concluded that diving
could adversely affect coral assemblages through physical injury
(e.g., Hawkins and Roberts, 1992, 1993; Davis and Tisdell, 1995;
Hawkins et al., 1999, 2005) or sediment deposition (Zakai and
Chadwick-Furman, 2002). In a few studies, coral disease has been
associated with the presence of concentrated tourist activities
(Hawkins et al., 1999; Winkler et al., 2004; Lamb and Willis,
2011), however no studies have attempted to directly link coral
susceptibility or disease prevalence with measures of dive site
use intensity, such as levels of physical injury or sediment deposi-
tion. Minor damage and resuspension of sediment by most divers
may seem trivial, but by compounding other reef stresses associ-
ated with tourism, they could undermine the resilience of local reef
ecosystems (Nyström et al., 2000) and reduce recovery rates fol-
lowing natural disturbances (Connell, 1997). In addition, a variety
of other factors could increase coral disease prevalence and reduce
health at intensively dived tourist sites in rapidly developing
regions, including possible increases in nutrients from vessel sew-
age and wastewater and elevated levels of resuspended sediment
associated with shoreline erosion from boat wakes and crowding.
The island of Koh Tao, located in the western Gulf of Thailand,
has rapidly grown as a tourist and recreational destination, leading
to the replacement of small-scale hook-and-line or traditional
hand net fisheries by reef-related tourist activities (Yeemin et al.,
2006). From 1992 to 2003, the number of tourists increased by
375% and now considered the hub of scuba diving certification in
Southeast Asia, estimated to generate US$62 million per year to
the local economy (Larpnun et al., 2011). At present, the island
has approximately 50 dive operators that accommodate greater
than 300,000 visitors per year to a total reef area of 2 km
2
(Weterings, 2011; Larpnun et al., 2011), reaching intensities of
use beyond levels seen even in regions heavily impacted by dam-
age, such as the Red Sea (<250,000 divers/year to 4 km
2
of reef
area: Zakai and Chadwick-Furman, 2002).
Here, we use the prevalence of four coral diseases and eight addi-
tional indicators of compromised coral health to assess the effects of
recreational diving intensity on coral reefs surrounding Koh Tao. To
date, the concurrent use of multiple field-based signs of disease and
other indicators of compromised health to classify stress associated
with human activities on reef corals has not been undertaken. Using
a multitude of indicators to assess coral health may, for the first time,
improve our capacity to identify more specific sources of impacts
from tourism on reef corals. In light of predicted increases in tourism
and recreational activities globally, the results of this study will aid
in the development of practical management strategies to mitigate
the impacts of frequent visitation that increase the likelihood of
coral disease outbreaks and ensure long-term persistence of corals
reefs and livelihoods in developing coastal regions.
2. Methods
2.1. Data collection
We conducted surveys around the island of Koh Tao in Septem-
ber 2011, approximately 1 year following a bleaching event and
subsequent wet season in the Gulf of Thailand (Fig. 1 and Supple-
mentary Material). We selected a total of 10, 90 m
2
sites distrib-
uted around the island and located approximately 100 m from
shore. Based on questionnaires from 23 of the largest dive opera-
tors on the island, Weterings (2011) found that most of the dive
sites around Koh Tao were unevenly visited and a select number
were often frequented by up to 10 dive operators in a single day.
Due to ease of access, dive sites with the highest levels of use are
often located nearest to the large number of operators located in
the west and southwest regions of the island (Fig. 1). We surveyed
the top 5 dive sites that are heavily and constantly used by visitors
throughout the year (i.e., more than 5 boat operators with a mini-
mum of 50 in-water visitors/site/day) (high use sites), and 5 sites
that had similar coral assemblages but had few to no in-water vis-
itors each year (low use sites).
At each site, three 15 m 2 m belt transects were laid randomly
along reef contours at 3–6 m in depth and approximately 5 m apart,
consistent with standardized protocols developed by the Global
Environment Facility (GEF) and World Bank Coral Disease Working
Group (Beeden et al., 2008), which allow the data from this study to
be directly compared to other coral disease datasets collected glob-
ally. Specifically, within each 30 m
2
belt transect (90 m
2
per dive
site), every scleractinian coral over 5 cm in diameter was identified
to genus and further classified as either diseased (i.e., affected by
one or more of the following disease classes recorded in the Indo-
Pacific region (see Fig. 1): white syndromes, skeletal eroding band,
black band disease, brown band disease, and/or growth anomalies);
showing other signs of compromised health (i.e., affected by one or
more of the following: tissue necrosis due to sediment, bleaching,
non-normal pigmentation of tissue, overgrowth by sponges, red
or green algae, and cuts and scars from predation by crown-
of-thorns starfish and corallivorous marine snails); physically
damaged (recently exposed skeleton from breakage or severe
abrasions); or healthy (i.e., no visible signs of disease lesions, other
compromised health indicators or physical damage) (Willis et al.,
2004; Lamb and Willis, 2011). Standard line-intercept surveys were
used to determine coral cover and community composition by esti-
mating the linear extent of each coral to the nearest centimeter
along the central line of each 15 m transect.
2.2. Data analyses
The prevalence of coral disease and other signs of compromised
health was calculated within each 30 m
2
belt transect by dividing
the number of colonies with one of the four diseases or eight other
compromised health categories recorded in this study by the total
number of colonies present, i.e., 15 prevalence values per disease
or category, both for the group of high use and low use sites.
Differences in overall disease assemblages were investigated
using multivariate community analyses. A nested permutational
multivariate analysis of variance (Anderson et al., 2008) was used
to test for differences between high and low use levels, with site
(random factor) nested within use-level (fixed factor). The analysis
was based on a zero-adjusted Bray–Curtis similarity matrix (Clarke
and Gorley, 2006), type III partial sums of squares, and 999 random
permutations of the residuals under the reduced model. To identify
indicators of disease and other signs of compromised coral health
between the two use-levels (those contributing most to the pat-
terns in multivariate space), we used a principal coordinates anal-
ysis (PCO) performed on a Bray–Curtis similarity matrix using
square root transformed data due to strong linear pairs of variables
(Clarke and Gorley, 2006; Anderson et al., 2008). We calculated
Pearson correlations of the ordination axes with the original dis-
ease and other compromised health data, where indicators with
strong correlations (defined in this study as P0.6) were then over-
laid as vectors on a bi-plot.
Similarities between coral communities at the family-level
were illustrated using a non-metric multidimensional scaling plot
(nMDS), with hierarchical clusters overlaid from dendrograms
based on a Bray–Curtis similarity matrix from square-root
transformed data at the transect level (Clarke and Gorley, 2006).
We used a nested analysis of similarity (ANOSIM) to test differ-
ences in coral assemblages between use-levels, where we nested
J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96 89
site (random factor) into use-level (fixed factor). Multivariate
analyses were performed in PRIMER v6 and PERMANOVA+ add-in
(PRIMER-E Ltd., Plymouth, UK).
To analyze patterns of coral disease among broad taxonomic
groups (e.g., Veron, 2000), coral families were assigned to 1 of 3 dis-
ease susceptibility categories on the basis of previous studies of
coral disease prevalence in the Indo-Pacific region (Willis et al.,
2004; Kaczmarsky, 2006; Aeby et al., 2011a,b; Lamb and Willis,
2011; Ruiz-Moreno et al., 2012): the highly disease susceptible
and abundant family, Acroporidae; the disease susceptible families
Pocilloporidae and Poritidae; and the disease resistant families
Agariciidae, Faviidae, Fungiidae, Merulinidae, and Mussidae. Differ-
ences in mean prevalence of disease, other signs of compromised
health and physical damage among high and low use sites were
compared using a 2-way nested analysis of variance (ANOVA),
where site (random factor) was nested within use-level (fixed fac-
tor). We tested associations between continuous variables with
Pearson product moment correlations (PPMC) with the confidence
interval set at 0.95. Coral disease susceptibility as a result of visu-
ally assessed compromised health was evaluated using a Pearson’s
chi-square test. Prior to all univariate analyses, assumptions of nor-
mality (Shapiro–Wilks) and homogeneity of variance (Levene’s test
of homogeneity) were tested and data were transformed to meet
assumptions of normality where necessary. Univariate statistics
were performed in R v3.0.2 (R Core Team, 2013).
3. Results
3.1. Effects of intensive use on coral health and disease
Assemblages of disease and other compromised health signs
differed significantly between use-level (pseudo-F
1,8
= 3.63,
P= 0.008), with the prevalence of visually healthy corals
contributing most strongly to driving this separation (39.5% of var-
iation on the PCO1 axis: Fig. 2 and Table S1). The mean prevalence
of healthy corals recorded at high use sites was 45.2% ± 6.2 SE
(range = 31–63%, n= 5983 corals surveyed), approximately half
the mean percentage of healthy corals recorded at low use sites
(78.8% ± 2.5 SE, range = 71–84%, n= 4516 corals surveyed).
3.1.1. Disease prevalence
Mean overall coral disease prevalence was approximately 3-fold
greater at sites with high visitation (mean ± SE = 14.5% ± 4.0; 727
cases of disease) compared to low use sites (5.2% ± 1.3; 197 cases
of disease; Table 1). At low use sites, disease prevalence ranged
between 1.2% and 8.5% (median = 5.6%), whereas it ranged
between 6.9% and 29.9% (median = 11.4%) at high use sites. Both
the maximum prevalence and maximum number of cases of each
of the four diseases were recorded at high use sites (Table 1). No
cases of brown band disease, a common ciliate disease in the
Indo-Pacific (Willis et al., 2004), were recorded during these sur-
veys. The two most prevalent diseases, skeletal eroding band
(SEB) and white syndromes (WS), were 2-fold and 4-fold greater,
respectively, at high use sites than at low use sites (Table 1 and
Fig. 3a). Mean black band disease (BBD) prevalence was low at
all sites, however it was 9-times greater at high use sites than
low use sites, although it did not differ significantly between use
levels (Table 1 and Fig. 3a). There was no difference in the mean
prevalence of growth anomalies between the two use levels
(Table 1 and Fig. 3a).
3.1.2. Prevalence of other signs of compromised health and physical
damage
When combined, overall mean prevalence of the 8 other
compromised health categories was approximately 2 times greater
at high use sites (mean ± SE = 32.3% ± 9.4; 1897 corals with other
Fig. 1. Locations of survey sites with high (solid squares, numbered 1–5) and low visitor use (open circles, numbered 6–10) around the island of Koh Tao, Thailand. Individual
pie charts represent the mean proportion of coral colonies at each site classified within 4 health status categories
a
: disease (including (A) white syndromes, (B) black band
disease, (C) growth anomalies, and (D) skeletal eroding band disease); (E) physical damage (recently exposed skeleton); other compromised health indicators (including (F)
sponge overgrowth, (G) non-normally pigmented tissue responses, (H) algae overgrowth, (I) sediment damage, and (J) bleaching; or healthy. Category means were calculated
from 3 transects per site. Percentages indicated within each pie graph represent healthy colonies.
a
Standardised signs of disease and compromised coral health as per Beeden
et al. (2008), an output of the Global Environment Facility and World Bank Coral Disease Working Group.
90 J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96
signs of compromised health) compared to low use sites
(15.0% ± 4.1; 752 cases; Table 1). Four of these compromised health
categories were significantly more prevalent at high use sites
(Table 1 and Fig. 3b). Specifically, there was a 12-fold increase in
corals with tissue necrosis from sediment and a 9-fold increase
in corals with exposed skeleton (physical damage) at sites with
high use (Table 1). In addition, approximately 3 times as many
corals at high use sites had non-normally pigmented tissue (pig-
mentation responses) or were actively overgrown by sponges
(Table 1 and Fig. 3b). There was no significant difference in the
prevalence of bleaching, algal overgrowth or cuts and scars associ-
ated with predation between the two use levels (Table 1 and
Fig. 3b).
3.1.3. Patterns and susceptibility of diseases and other signs of
compromised coral health
Sites with a high prevalence of corals showing other signs of
compromised health also had high levels of disease (r
28
= 0.54;
P< 0.005; Fig. 4a). Patterns in the assemblages of diseases and
other compromised health indicators differed among sites within
use-level (pseudo-F
8,20
= 4.073, P< 0.01), although differences
(19.7% of variation on the PCO2 axis: Fig. 2 and Table S1) were lar-
gely driven by the prevalence of skeletal eroding band and physical
damage, which were strongly correlated across all sites (r
28
= 0.78,
P< 0.001; Fig. 4b), and the prevalence of white syndrome and sed-
iment necrosis, which were also strongly correlated across all sites
(r
28
= 0.67, P< 0.001; Fig. 4c). Coral colonies with recently exposed
skeleton were more likely to also have skeletal eroding band dis-
ease (22%) than colonies without recent physical damage (6%) at
high use sites (
v
2
1
= 136.1, P< 0.001), but at low use sites, recent
physical damage did not affect the susceptibility of corals to SEB
(7% compared to 5%:
v
2
1
= 0.45, P= 0.51). Colonies with tissue necro-
sis associated with sediment were also more likely to have white
syndrome lesions than colonies without sediment damage at both
high (26% compared to 3%:
v
2
1
= 256.0, P< 0.001) and low use sites
(31% compared to 4%:
v
2
1
= 28.2, P< 0.001).
3.2. Host density, cover and composition as potential drivers of disease
Mean coral density (number of colonies per m
2
) did not vary
significantly between low (mean ± SE = 10.0/m
2
± 1.1) and high
use sites (13.3/m
2
± 1.9; F
1,8
= 0.8, P= 0.40). Moreover, the number
of disease cases (Table 1) was not associated with coral density at
sites with low (r
13
= 0.30, P= 0.28) or high recreational use
(r
13
= 0.13, P= 0.63).
The composition of coral assemblages was at least 60% similar
among all transects surveyed in this study (Bray–Curtis similarity),
and did not differ significantly between high and low use sites
(Global R = 0.11, P= 0.18; Fig. 5a). On average, corals in the disease
resistant families (Agariciidae, Faviidae, Fungiidae, Merulinidae,
and Mussidae) accounted for the largest percentage of coral cover
at both low and high use sites (F
1,8
= 0.5, P= 0.51; Fig. 5b), and ben-
thic cover of disease resistant coral families was not associated
with coral disease prevalence at low (r
13
= 0.32, P= 0.24) or high
use sites (r
13
= 0.04, P= 0.89; Fig. 5f). Percent cover of Acroporidae
and the disease susceptible families, Pocilloporidae and Poritidae,
was marginally greater at high use sites (F
1,8
= 0.7, P= 0.41 and
F
1,8
= 1.7, P= 0.22, respectively; Fig. 5b), but disease prevalence
was not correlated with cover of these groups (low: r
13
= 0.12,
P= 0.68 and r
13
= 0.11, P= 0.69; high: r
13
= 0.09, P= 0.76 and
r
13
= 0.14, P= 0.62; Fig. 5d and e). Total percent cover of all coral
families combined did not influence disease prevalence at high
use sites (r
13
= 0.45, P= 0.10), however there was a significant posi-
tive correlation between total disease prevalence and total coral
cover at low use sites (r
13
= 0.54, P= 0.04; Fig. 5c).
4. Discussion
This study reveals that intensive site use associated with
reef-based tourist activities significantly reduces the overall health
of corals, undermining the value of the resource necessary for sus-
taining the growing nature-based tourism industry. Consistency in
the pattern of substantially elevated levels of disease at high use
sites highlights the urgent need to identify and mitigate potential
0
-20 -10 10 20
PCO1 (38.5% of total variation)
-20
-10
0
10
20
WS
SED
SEB
PD
PCO2 (19.7% of total variation)
Low use
High use
BBD
GA
SPG
RA
PR
ALG
CS
Fig. 2. Principal coordinates analysis (PCO) of coral health and disease variables.
Spatial variation in 4 coral disease and 8 other compromised coral health indicators
at the transect level, for high use (solid squares) and low use sites (open circles) for
the first two principal components. Analysis performed on a Bray–Curtis similarity
matrix using square root-transformed data, with vectors depicting original
variables and Pearson correlation values (gray vectors P0.2, black vectors P0.6)
representing relative contributions of disease or other compromised coral health
signs on the observed variation in use-level. Coral diseases: SEB = skeletal eroding
band, WS = white syndromes, BBD = black band disease, GA = growth anomalies;
other compromised coral health indicators: PD = physical damage, SED = sediment
necrosis, SPG = sponge overgrowth, ALG = algal overgrowth, PR = pigmentation
response, RA = red algal overgrowth, CS = cuts and scars from predation, and
BL = bleaching.
Table 1
Number of cases of coral disease and other signs of compromised health at sites with
low levels of recreational use (n= 15 transects, 4516 colonies surveyed) and high
levels of recreational use (n= 15 transects, 5983 colonies surveyed), and results of the
main effects nested analysis of variance of mean prevalence (%) between use-level
groups. Mean prevalence for each variable (±SE) shown in Fig. 3. Analyses performed
on data transformed to the square root.
Variable Number of cases Main effect
Low use High use FP
Total disease 197 727 23.4 <0.001
*
Skeletal eroding band 153 464 10.9 <0.004
*
White syndromes 32 185 9.0 <0.007
*
Black band 4 51 0.8 <0.37
Growth anomalies 8 27 <0.2 <0.73
Total other compromised health 752 1927 35.3 <0.001
*
Algal overgrowth 324 416 1.3 <0.27
Pigmentation response 107 337 5.5 <0.03
*
Physical damage 31 339 22.3 <0.001
*
Sediment necrosis 13 192 16.6 <0.001
*
Red algal overgrowth 133 265 0.7 <0.41
Sponge overgrowth 46 216 19.9 <0.001
*
Predation scars 84 136 3.6 <0.09
Bleaching 14 26 <0.1 <0.84
*
Indicate significant differences set at
a
= 0.05.
J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96 91
causes of increased disease prevalence at these sites, particularly
as additional impacts are anticipated with accelerated develop-
ment of infrastructure along coastal regions to support tourism
growth.
Differences in coral cover, density or family composition are
unlikely to have caused the striking differences in disease preva-
lence among sites, given that percent cover of all corals and of dis-
ease-susceptible families did not differ among high and low use
sites. Similarities in coral cover, density and composition among
sites that clearly differed in a range of coral health indicators con-
tribute to the emerging consensus that percent cover of live coral is
of limited value as an indicator of ecosystem health, as it typically
failed to separate areas affected by human activities from those
less affected (Muthiga and McClanahan, 1997; Hawkins et al.,
1999; Dinsdale and Harriott, 2004). We conclude that percent
cover is not appropriate as the sole indicator of impacts when
assessing reef-based activities, but is useful when used in conjunc-
tion with other indicators. We note, however, that in the group of
low use sites, disease prevalence was positively correlated with
total cover, potentially reflecting transmission of pathogens via
direct colony-to-colony contact (Riegl, 2002). At high use sites, it
is more likely that increased susceptibility to infection associated
with localized environmental stressors led to higher prevalence
of coral disease.
4.1. New approaches to identifying and managing stressors affecting
coral health
Linking indicators of stress with potential causes, so that action
can be initiated before irreversible declines in health occur, has
been challenging for corals. Bleaching is one of the few readily
identifiable signs of coral stress, but bleaching has been associated
with a wide range of stressors, like changes in water temperature
and light (Brown, 1997), ocean acidification (Hoegh-Guldberg
et al., 2007), bacterial infections (Kushmaro et al., 1997), herbicides
(Jones et al., 2003), and sunscreen (Danovaro et al., 2008). Our
study of coral health impacts associated with the intensity of div-
ing-related activities provides valuable insights for linking a range
of compromised health indicators with potential stressors, and
highlights the need for multiple metrics of coral health and disease
to deduce sources of stress on coral reefs and aid in developing
practical management strategies for mitigating them. Moreover,
while multiple metrics of coral health increase capacity to differen-
tiate between human impacts and other drivers of disease in this
study, monitoring the prevalence of healthy corals can be readily
implemented into existing coral survey programs with little to
no additional training, thereby providing more comprehensive
and meaningful reef health assessments. Inclusion of this basic
metric in monitoring programs would also contribute to much-
needed baseline data (e.g., Willis et al., 2004) to enable future
detection of changes in the health of reef corals and the success
of management intervention.
4.1.1. Sediment stress
The 12-fold greater prevalence of sediment-associated tissue
necrosis at high use sites represented one of the greatest differ-
ences in coral health indicators between sites exposed to high ver-
sus low intensity recreational diving. Recreational divers
significantly increased turbidity and resuspended sediment at pop-
ular dive sites in the Red Sea, each causing approximately nine sed-
iment clouds to settle back onto corals per dive (Zakai and
Chadwick-Furman, 2002). In addition, wakes generated by boat
traffic can redistribute and increase turbidity from sediment resus-
pension and shoreline erosion, with turbidity taking between 4 and
24 h to return to background levels following disturbance (Yousef
et al., 1980; Jones, 2011). Although corals possess mechanisms to
actively remove sediment particles, such mechanisms are energet-
ically costly (Hubbard and Pocock, 1972; Rogers, 1990; Philipp and
Fabricius, 2003), thus corals at intensively used sites suffer
depleted energy budgets from even low levels of chronic sediment
deposition (Rogers, 1990; Philipp and Fabricius, 2003), leading to
localized bleaching and tissue necrosis.
The high correlation found between the prevalence of sedi-
ment-associated tissue necrosis and the prevalence of white syn-
dromes, regardless of site use intensity, signifies that localized
direct contact with sediment may be a primary factor contributing
to this disease. Sediment could act as both a disease reservoir and
potentially a vector when resuspended as a result of tourist-related
activities, and could also increase the likelihood of infection by
stressing coral hosts (Lafferty and Holt, 2003; Pollock et al.,
2014). On hurricane-damaged reefs, Brandt et al. (2013) reported
that another tissue loss disease, white plague, occurred primarily
on fragments in direct contact with sediment, and hypothesized
a link with bacterial overgrowth. Evidence that sediment damage
to corals is reduced following treatment with antibiotics
(Hodgson, 1990), and that growth rates of coral-associated
microbes increased 10-fold and led to rapid tissue loss following
exposure to elevated levels of carbon (Kline et al., 2006), further
support this link. Whether sediment accumulation causes coral
disease by introducing pathogens or is a general sign of coral stress
to other environmental stressors warrants further study. Practical
and readily-introduced solutions for reducing sedimentation
include limiting boat traffic and site crowding, and the establish-
ment of no-wake zones and speed limits when traveling within
close proximity to reefs.
Fig. 3. Effect of use-level on coral disease and other compromised health indicators. Prevalence (mean ± SE) of (A) coral disease (SEB = skeletal eroding band, WS = white
syndromes, BBD = black band disease, GA = growth anomalies) and (B) other compromised coral health signs (ALG = algal overgrowth, PR = pigmentation response,
PD = physical damage, SED = sediment necrosis, RA = red algal overgrowth, CS = cuts and scars from predation, SPG = sponge overgrowth, and BL = bleaching) at low use sites
(open bars, 4516 colonies surveyed) and high use visitor sites (solid bars; 5983 colonies surveyed). Analyses performed on data transformed to the square root and asterisks
indicate significant differences set at
a
= 0.05 for each individual indicator.
92 J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96
Although overall levels of black band disease (BBD) were low
and not significantly different between high and low use sites,
the 9-fold increase of BBD at high use sites further corroborative
evidence that sediment accumulation plays a key role in diving-
related disturbances. The biogeochemical microenvironment
beneath BBD microbial mats, which represent complex and diverse
polymicrobial consortia (Sutherland et al., 2004; Kaczmarsky,
2006; Sato et al., 2009), is characterized by anoxia, high sulfide
concentrations and low pH, conditions that are lethal to underlying
coral tissues (Glas et al., 2012). These toxic conditions are most
pronounced under low light conditions (Glas et al., 2012), therefore
sediment accumulation on coral surfaces could provide an anaero-
bic microenvironment conducive to microbial mat formation,
while increased turbidity (and associated decreased light levels)
could facilitate the rapid establishment of conditions characteristic
of the disease.
4.1.2. Nutrient enrichment
The marked increase in sponge overgrowth at high use sites fur-
ther suggests that nutrient enrichment is a significant issue associ-
ated with intensive tourist use. Increased primary production
associated with nutrient enrichment and sediment favors benthic
filter-feeding organisms, particularly sponges, which then typically
outcompete corals (Pastorok and Bilyard, 1985). On Grand Cayman,
a 5-fold increase in the biomass of Cliona delitrix,a sponge over-
growing the coral Montastrea cavernosa, and a 6-fold increase in
bacterial biomass was recorded on fringing reefs exposed to dis-
charges of untreated fecal sewage compared to a control site
1 km away (Rose and Risk, 1985). In other studies, widespread
overgrowth of corals by the cyanobacteriosponge Terpios hoshinota
on Japanese reefs was particularly noteworthy in pollution-
stressed zones (Rützler and Muzik, 1993), and bacteria similar to
those detected in black band disease were detected on sponge-cov-
ered but not on sponge-free corals (Tang et al., 2011), suggesting
that T.hoshinota might benefit from the presence of bacteria asso-
ciated with unhealthy corals.
Inputs of nutrients, pathogens, and other wastewater-derived
pollution have also been linked to several other coral diseases
(Bruno et al., 2003). For example, sewage outfalls containing the
human gut microbe Serratia marscens have been associated with
a type of white syndrome infecting and decimating acroporid cor-
als off the coast of Florida (Patterson et al., 2002). Nutrient enrich-
ment from sewage and wastewater pollution is one of the few
stressors that, with proper research, policy, and management,
can be effectively mitigated. Fecal indicator bacteria, such as
Enterococcus,can be monitored (Gronewold et al., 2008) or alterna-
tively, stable isotope analysis can detect the presence of sewage-
derived nitrogen within an ecosystem. In Mexico, d
15
N values of
the common sea fan were more variable near a developed tourist
site than at an undeveloped site, with 84% of the observed varia-
tion explained by tourist visitations in the preceding year (Baker
et al., 2013). Due to the unregulated and rapid expansion of dive
tourism in many developing countries, most tourist vessels are
not equipped with proper storage systems for wastewater and
sewage. Tertiary treatment systems on fitted to vessels can remove
up to 90% of nutrients (Judd, 2010). Because pollutants cannot be
isolated in open marine systems and may have implications
beyond local coral assemblages (McCallum et al., 2004), the possi-
bility of disease dispersing from sites with higher levels of environ-
mental stress is concerning. It is also possible that land-based
pollutants are elevated on the western side of the island near ter-
restrial tourism infrastructure and the main shipping pier, however
our paired high and low use site in this location further indicates
that reef-based tourism intensity can still cause significant dispar-
ities in disease levels adjacent to developed coastal areas.
4.1.3. A general indicator of stress
Non-normal pigmentation of coral tissue, or pigmentation
response, has been characterized as a general immune response
to a physical or pathogenic challenge (Willis et al., 2004;
Bongiorni and Rinkevich, 2005; Palmer et al., 2008). Pigmented tis-
sues possess high levels of melanin, an important component of
invertebrate innate immunity that can act as a defensive barrier
against foreign bodies (Palmer et al., 2008), therefore the elevated
prevalence of pigmented tissue recorded at high use sites may
0
10
20
30
40
Total disease prevalence (%)
Total compromised health (%)
A
P < 0.005
r = 0.54
0
10
20
30
40
SEB prevalence (%)
Physical damage (%)
B
P < 0.001
r = 0.78
0
2
4
6
8
0 204060 80
0102030
0 5 10 15
WS prevalence (%)
C
r = 0.67
Sediment necrosis (%)
P < 0.001
Fig. 4. Associations between the prevalence of (A) total coral disease and other
signs of compromised coral health, (B) recent physical damage and skeletal eroding
band (SEB) disease, and (C) tissue necrosis due to sediment and white syndromes
(WS). Open circles indicate low use sites and black squares indicate high use sites in
each panel. Pearson product–moment correlations conducted on transects pooled
from low and high use sites.
J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96 93
represent signs of a general immune response to a multitude of
factors, including invading foreign pathogens, physical injury or
sediment accumulation.
4.2. Coral physical injury increases disease susceptibility
The 9-fold increase in the prevalence of recent coral damage at
high use sites suggests that physical injury and lacerations from
direct diver contact play an important role in increased disease
prevalence at these sites. Moreover, corals with physical injury
were four times more susceptible to skeletal eroding band disease
compared to colonies without injury at high use sites. Ongoing
chronic injuries could reduce immune function associated with
the regeneration of coral tissue, resulting in increased susceptibil-
ity to disease (Mydlarz et al., 2006). In experimental studies, artifi-
cially-inflicted wounds enhanced the ability of ciliates associated
with skeletal eroding band disease to form dense band-like aggre-
gations that caused tissue loss of up to 0.3 cm day
1
on the Great
Barrier Reef (Page and Willis, 2008). Increased presence of this cil-
iate disease has been documented near other tourist locations
(Winkler et al., 2004; Lamb and Willis, 2011), however our study
is the first to demonstrate a strong link between the prevalence
of physical injury and the presence of skeletal eroding band dis-
ease. Repair of broken tips takes up to 2 months (Kobayashi,
1984), therefore physical injury may provide a primary site for
the invasion of pathogens and ciliates or reduce immune system
function, extending the impact timeframe well beyond the imme-
diate time of injury.
Additional microbial or environmental factors at high use sites
may be necessary for the development of the band-like ciliate
aggregations that cause tissue loss characteristic of skeletal erod-
ing band disease. In contrast to high use sites, injury did not appear
to affect the likelihood of skeletal eroding band infections at low
use sites. While mean levels of damage found in this study were
two times higher than on frequently dived reefs of Saba and
Bonaire in the Caribbean (Hawkins et al., 1999, 2005), they were
markedly lower than on the more heavily dived reefs of Egypt
and Israel, where approximately 10% of colonies were broken
(Riegl and Velimirov, 1991; Hawkins and Roberts, 1992). Signifi-
cant increases in loose fragments of coral at heavily dived sites
(Hawkins and Roberts, 1993) raises the possibility of colony-
to-colony pathogen transmission if fragments are already infected
(Brandt et al., 2013). While marine-based tourist activities do not
represent disease agents themselves, they nevertheless appear to
cause lesions that compromise the health of corals.
4.3. Spatial and remedial management strategies to manage coral reef
health
Results from this study suggest that spatial management strat-
egies to reduce or restrict activities that impact coral health will
benefit reef corals, such as in developing coastal regions of Thai-
land, where fisheries and tourism are valuable for both nutritional
and employment purposes (Tapsuwan and Asafu-Adjaye, 2008).
Like Koh Tao, many coral reefs are located in poor, developing
countries (Donner and Portere, 2007), where use restrictions can
undermine local livelihoods and are difficult to justify and enforce
(McClanahan et al., 2005). Total prohibition on use, while perhaps
ideal from an ecosystem management perspective, may pose an
unrealistically difficult burden on local communities and conse-
quently result in little support or compliance (Cinner et al.,
2009). Users are generally more likely to support restrictions on
specific types of use rather than outright closures (McClanahan
et al., 2005). In addition to suggestions discussed above, rotational
dive site use or mooring exclusivity to a single operator may be
preferred to complete site restrictions. On the Great Barrier Reef,
mean disease prevalence was generally less than 1% at several pop-
ular dive sites that were visited irregularly or frequently rotated by
permitted operators (Lamb and Willis, 2011). Since divers visiting
Koh Tao are often diving for the first time, it may be possible to
construct alternative training sites by installing appropriate struc-
tures, or artificial reefs, in ecologically unobjectionable locations.
Using multiple metrics of coral health may be a more suitable
indicator for selecting appropriate management strategies and
assessing their success and failure on reefs facing increasing levels
of human and disturbance. When site access is unrestricted, indi-
vidual users have little or no incentive to conserve it, therefore
alternative and practical management options that have greater
potential for compliance in developing tropical countries are
urgently required. The economic value of coral reef tourism for
developing coastal communities highlights the importance of
improved management practices for conserving the coral reef
2D Stress: 0.08
Low use
High use
60
70
80
Similarity
A
0
10
20
30
40
0
10
20
30
40
0 20 40 60 80 0 20 40 60 80 100
Total disease prevalence (%)
Coral cover (%)
CTotal cover Acroporidae
Susceptible families Resistant families
D
E F
Low: P < 0.05
High: P = 0.10
Low: P = 0.68
High: P = 0.76
Low: P = 0.69
High: P = 0.62
Low: P = 0.24
High: P = 0.89
0
10
20
30
40
50
Low use High use
Mean coral cover (%)
Acroporidae
Susceptible families
Resistant families
r = 0.54
100
B
Fig. 5. (A) Spatial variation in the taxonomic composition of percent coral cover by family at the transect level assessed using a non-metric multidimensional scaling (nMDS)
plot and hierarchical clusters overlaid from dendrograms based on a Bray–Curtis similarity matrix on square root-transformed data. Distances between transects signifies
similarity of coral community composition and the similarity scale on clusters indicates the percentage of similarity between transects (range = 0–100). Taxonomic patterns
of (B) mean coral cover (±SE) between sites with low visitor use and associations between prevalence of overall coral disease and percent (C) total coral cover, (D)
Acroporidae, (E) susceptible coral families, and (F) resistant coral families at sites. Low use = open circles, High use = black squares. Disease resistant families: Agariciidae,
Faviidae, Fungiidae, Merulinidae, and Mussidae; disease susceptible families: Pocilloporidae and Poritidae; and the highly disease susceptible family Acroporidae.
94 J.B. Lamb et al. / Biological Conservation 178 (2014) 88–96
resource underpinning the industry. Educating and involving local
communities in sustainable practices that provide long-term reve-
nues can decrease over-exploitation for short-term profits.
Acknowledgements
Funding for this study was provided by an Australian Institute
of Marine Science and James Cook University (AIMS@JCU) Interna-
tional Research Award to JBL, an Australian Research Council Dis-
covery Grant to BLW, and Prince of Songkla University Research
Grant No. SCI530221S to JDT and SP. We thank Chad Scott and Dev-
rim Zahir of the New Heaven Dive School in Koh Tao and Aorn Sil-
lapasathitwong and Theeranai Phetsom from the Prince of Songkla
University for logistical and field support.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.biocon.2014.06.
027.
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... Several studies had noted the impact of tourism and diving activities on coral ecosystem [74][75][76][77][78]. Inexperienced divers with low buoyancy control skill have higher physical contact rate with coral reefs compare to experienced divers causing coral breakage [79]. This scenario not only will reduce the coral biomass but also cause the injured coral to suffer from slower growth rates and become more susceptible to disease and predation [80], altering the reefs state into a less structural complex state as well as impacting the benthic assemblage [81,82], thus, the lower species diversity index in S1. ...
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... Several sources of non-extractive disturbances associated with human presence are considered potential drivers of impacts upon benthic cover and reef fish communities (Gil et al., 2015;Hawkins et al., 1999;Lamb et al., 2014). For benthic organisms, non-extractive disturbances occur through boat anchorage (Creed and Amado Filho, 1999;Giglio et al., 2017), diver's physical contact (Giglio et al., 2016), trampling (Casu et al., 2006), and chemical contamination with products such as sunscreen (Danovaro and Corinaldesi, 2003;Downs et al., 2016). ...
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... climate change causing heat stress and acidifying waters making it harder to build their skeletons (Mollica et al., 2018); rising sea levels, more frequent and severe storms (Hughes et al., 2017); increasing pollution with sediments, fertilizers, oil and toxic chemicals (Jones et al., 2016;Silbiger et al., 2018;van Dam et al., 2011;Zaneveld et al., 2016); overfishing, including destructive methods (Fox, 2004;MacNeil et al., 2020;Madeira and Calado, 2019;Zaneveld et al., 2016); damage from tourism (Al-Jufaili et al., 1999;Lamb et al., 2014;Saphier and Hoffmann, 2005) and habitat loss (Jackson, 2008). Tropical corals will likely disappear within a few decades unless drastic action is taken (Hoegh-Guldberg et al., 2007;Jackson, 2008). ...
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Koh Tao is a small, 21 km-2 island north of Koh Samui in the Gulf of Thailand. It attracts 300,000 to 400,000 tourists every year to enjoy the climate, clean beaches and coral reefs. It is the hub of scuba diving instruction and certification for Southeast Asia, and diving forms the base of the local economy. Tourism generates US $62 million each year from clean, healthy coral reefs. All this is threatened by rapid development and over- exploitation of the fisheries and coral reef resources. There are few waste water treatment ...