Marine Environmental Research 85 (2013) 45e53

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Marine Environmental Research

journal homepage: www.elsevier.com/locate/marenvrev

Species-diverse coral communities on an artificial substrate at a tuna

farm in Amami, Japan
Hiroki Hata a, *, Isao Hirabayashi a, Hideki Hamaoka a, b, Yoshio Mukai c, Koji Omori d, Hironobu Fukami e
a
Graduate School of Science and Engineering, Ehime University, 2-5 Bunkyo, Matsuyama, Ehime 790-8577, Japan
b
National Research Institute of Fisheries and Environment of Inland Sea, 2-17-5 Maruishi, Hatsukaichi, Hiroshima 739-0452, Japan
c
Fisheries Laboratory, Kinki University, 195 Keten, Setouchi, Oshima, Kagoshima 894-1853, Japan
d
Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo, Matsuyama, Ehime 790-8577, Japan
e
Faculty of Agriculture, University of Miyazaki, 1-1 Gakuen-Kibanadai-Nishi, Miyazaki 889-2192, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Tuna-farming is expanding worldwide, necessitating the monitoring/managing of its effects on the
Received 9 October 2012 natural environment. In Japan, tuna-farming is conducted on coral reefs that have been damaged by
Received in revised form mass-bleaching events and crown-of-thorns starfish (COTS) outbreaks. This study focused on the coral
14 December 2012
community on an artificial substrate of tuna-farm to reveal the possible effects of tuna-farming on the
Accepted 19 December 2012
natural environment. Corals flourished on ropes suspended in the farm in the Amami Islands, southern
Japan. These were moored 3 m below the sea-surface in 50-m-deep water. The coral community on the
Keywords:
rope was analyzed and compared with those on natural substrata on two adjacent COTS-damaged reefs
Tuna farm
Coral community
and with that in a protected reef. Corals were monitored throughout a year. Sixty coral species grew on
Artificial substratum the ropes, that corresponds to 27.3% of the 220 species known from Amami. The coral community was
Acanthaster planci unique, dominated by massive faviid corals. On the ropes, the water temperature rarely exceeded 30.0
C
Nature restoration and no corals on the rope were severely bleached or covered by sedimentation during the observations.
Biodiversity The tuna-farm infrastructure provided corals with a suitable habitat, and species-rich coral communities
Benthos were established. These coral communities are an important node connecting tuna-farms and the natural
Aquaculture environment.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction huge cages as well as frames, ropes, floats, and anchors supporting
the cages (Miyashita, 2008). Most cages are settled underwater for
Tuna farming in coastal waters is now increasing in the Medi- decades, and therefore they provide substrata for wild organisms.
terranean, Australia, and Japan, and monitoring and management of On a tuna farm in Amami Island, Japan, 6-cm-diameter ropes hold
wild stock of tunas and the effect of farming on natural environment the cages and frames and are suspended at a depth of 3 m irre-
are required. In Japan, Pacific Bluefin tuna, Thunnus orientalis, is spective of tides, and these ropes are covered with corals. Artificial
intensively farmed in the southern subtropical sea where water substrata can provide wild organisms with habitat and increase
temperature is moderately high, and therefore, tuna grow rapidly their densities (Bohnsack and Sutherland, 1985). This heteroge-
and spawn every year (Masuma et al., 2008; Masuma, 2011). As usual, neous habitat increases the total diversity of the region, that is, g
tuna farms are used to fatten wild caught tuna in cages for periods diversity, through enhancement of differentiation of communities
from a few months to up to 1e2 years (Miyake et al., 2003; Sumaila among habitats. The extent of the differentiation of communities
and Huang, 2012). In Japan, however, six organizations maintain among habitats is defined as b diversity (Whittaker, 1972). Artificial
bluefin-tuna broodstocks for longer periods and manage to produce substrata on coral reefs may help unique communities to occur
their eggs to supply juveniles for aquaculture as well as to aim for there, thus increasing the b diversity between natural and artificial
conservation of wild stock (Masuma et al., 2008; Normile, 2009). habitats (Perkol-Finkel and Benayahu, 2004; Perkol-Finkel et al.,
In the southern part of Japan, coral reefs are well established, and 2005, 2006a), and they also can be a tool for coral reef restoration
the tuna farms exist adjacent to the coral reefs. Tuna farms require (Spieler et al., 2001; Abelson, 2006).
At the same time, tuna farms discharge high levels of organic
* Corresponding author. Tel./fax: þ81 89 927 9638. particulate matter and nutrients as waste from feeds such as squids
E-mail address: [email protected] (H. Hata). and mackerels (Sawada et al., 2005) and as fish feces (Vita and

0141-1136/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marenvres.2012.12.009
46 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53

Marin, 2007). This high organic and nutrient loading damages

adjacent corals through outbreaks of competitive algae and
phytoplankton (Kru zi
c and Po zar-Domac, 2007), resulting in
detrimental effects (Loya and Kramarsky-Winter, 2003), including
adverse effects on coral reproduction (Loya et al., 2004). Nutrient
outflow itself can enhance coral growth (Bongiorni et al., 2003).
Coral reef ecosystems are degraded worldwide (Hughes, 1994;
Hoegh-Guldberg, 1999; Bellwood et al., 2004; De’ath et al., 2012).
Coral communities in Amami have also been severely damaged by
a global bleaching event in 1998 and by two outbreaks of crown-of-
thorns starfish (Acanthaster planci) during 1974e1983 (Hirata,
1980; Yamaguchi, 1986) and 2000e2007 (Council for Coral Reef
Conservation in Amami Island, 2012). In the Setouchi area of
Amami, 335,918 individuals of A. planci were eliminated during
1999e2008 at a total cost of 108,796,000 yen. However, this did not
serve to stop the outbreak of A. planci. Since 2003, only two sites
(Ankyaba and Derikyonma) have been selected as focal points for
the protection of corals and A. planci have been eliminated
intensively.
In this paper, we focused on coral communities on an artificial
substratum of a tuna farm, aiming to reveal the possible effects of
tuna-farming on the environment and to assess the possibility of
these corals on a tuna farm as a tool for coral reef restoration. We
Fig. 1. Study sites in the Setouchi area, Amami Islands, southern Japan. The tuna farm
hypothesized that the artificial substrata on a tuna farm would is in Keten Bay. East Keten and Kudadon were selected as disturbed sites, and Deri-
provide a refuge to corals during outbreak of A. planci and/or during kyonma as a protected site in this study.
periods of bleaching. To test this, we first described coral commu-
nities that had been established for 14 years on 60-mm-diameter
supporting ropes at a tuna farm in Setouchi, Amami, and we then
compared these with coral communities at a protected site and at natural reef. In this area, populations of A. planci are intensively
disturbed sites in adjacent waters. Corals and environmental controlled by reef managers. In these areas, 10-m lines were
stresses were monitored on the fish-farm ropes and at protected established at a depth of 3 m, and line intercept transects were
and disturbed sites for a year. conducted by scuba diving to survey coral species composition and
coverage in February 2010. The numbers of lines set were 7, 8, and 5
2. Materials and methods in Derikyonma, Kudadon, and the east coast of Keten, respectively.
At the same time, thirteen 10-m-long lines were established on 13
2.1. Coral communities on an artificial substratum at a tuna farm, randomly selected 45-m ropes of the fish farm, and line-intercept
on disturbed reefs, and on a protected reef transects were conducted. All coral colonies were recorded with
a scale using an underwater digital camera, and parts of colonies
This study was conducted on a fish farm and adjacent coral reefs were collected and bleached to make skeletal specimens. Using
in Setouchi Channel, Amami Island, Kagoshima, Japan (Fig. 1). A these photos and specimens, we classified corals into species
net-cage culture system for tuna farming was constructed on the following Veron and Pichon (1976, 1980, 1982), Veron et al. (1977),
west coast of Keten Bay by Kinki University. Currently, the third Veron and Wallace (1984), Nishihira and Veron (1995), Wallace
generation of an artificially bred strain is being reared in this cage (1999), and Veron (2000), and Benzoni et al. (2010). Using these
system (Normile, 2009; Sawada et al., 2005). Six floating cages, 30- photos, colony size of corals on the ropes, on natural reefs in
m in diameter  15-m in depth were established in 1997 for the Kudadon and East Keten sites were measured by the greatest (d1)
farming and breeding of Pacific Bluefin tuna, T. orientalis (Mukai, and the smallest (d2) diameter of the corals. Projected area of each
2011). These cages were arranged in two rows abutting each coral colony was calculated using the formula, (d1/2)  (d2/2)  p.
other. To moor the cages, seventeen 45-m lead-cored polyethylene Coral size was compared among sites using SteeleDwass multiple
ropes, 60 mm in diameter, were suspended from floats on the sea comparison tests or ManneWhitney U test.
surface to around 3-m in depth irrespective of tidal conditions Multivariate analyses of coral community structure were con-
(Fig. 2) (Miyashita, 2008). This study focused on zooxanthellate ducted with permutational multivariate analysis of variance using
coral populations that had developed on the ropes. Water distance matrices (PERMANOVA; Anderson, 2001) with 1000 null
temperatures on the surface and at a depth of 3.0 m were measured permutations and nonmetric multidimensional scaling (nMDS)
at around 14:00 every day during 2000e2010 on this fish farm. ordination using BrayeCurtis similarities among the species
Water clarity in the farm was measured using Secchi disc at the composition data. Number of colonies, number of species, coverage
same time during 2000e2010. on the line, and species diversity as ShannoneWiener index (H0 ),
The coral communities on the ropes were compared to coral and evenness (Pielou’s J) were compared using one-way analysis of
communities in adjacent, natural reefs. Two non-protected natural variance (ANOVA) with the site as a fixed factor. Levene’s test for
reefs and one protected natural reef were selected for this homogeneity of variance yielded significant results for all five
comparison. The two non-protected reefs were located at the east indices. Therefore all the data were log transformed. Each of the
coast of Keten and in the Kudadon Bay, which neighbors Keten but indices was compared among the sites using a post hoc multiple
is separated by a small cape (Fig. 1). In Kudadon, live corals have comparison test (least significant difference, LSD). Beta diversity
been decimated because of outbreaks of A. planci starfish. The among sites was measured using pairwise b1 (Harrison et al.,
protected area of Derikyonma, which is on the opposite side of 1992), which is calculated by (S/a  1)/(N  1)  100, where S is
Setouchi Channel (Fig. 1) was chosen as an example of a protected the number of species in the two focus sites combined, a is the
 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53 47

Fig. 2. A floating cage of a tuna farm in Amami Island. a Cage-supporting lead-cored polyethylene ropes 60 mm in diameter were the focus of this study and is colored in red;
b corals on the supporting rope. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

mean number of species of the two, and N is the number of sites. 2.3. Stable isotope analysis
b1 ¼ 0 means complete similarity between two sites, and
b1 ¼ 100 means complete dissimilarity between the two sites. The stable isotope ratio of nitrogen is useful in trophic level
Water temperature was compared between sea surface and 3 m analysis because the nitrogen pools of animals have regularly
below the surface using paired t-test. enriched d15N signatures relative to their food sources (Cabana and
Rasmussen, 1994). Three colonies of Porites lutea were collected
2.2. Monitoring of stresses on corals from tuna-farm ropes, and three P. lutea were collected from the
East Keten site. These colonies were preserved in 99.9% ethanol,
Coral bleaching, algal and sponge overgrowth on corals, infec- and tissues were removed using a Water Flosser WP-100, Water-
tion of Waminoa sp. and encysted parasitic trematodes on corals, pikÒ. Tissues were dried in an oven at 60
C for 24 h and powdered
sediment cover, and coral disease were monitored on 5e10 10-m with a mortar and pestle. Nitrogen stable isotope ratios (&) were
line transects separately settled along 45 m ropes of the tuna- measured using a gas chromatographyecombustioneisotope ratio
farm in May and August 2009 and February 2010. At the same mass spectrometer (GCeCeIRMS) (SerCon, Ltd., ANCA-SL). Results
time, on the east coast of Keten, corals were monitored using are presented as per thousand deviations from the standards,
10  2-m belt transect or 10-m line transect. Additionally, in August expressed as d15N by the following equation: d15N (&) ¼ (Rsample/
2009 and February 2010, corals in Kudadon and Derikyonma were Rstandard  1)  1000, where R is the corresponding ratio of 15N/14N.
monitored using 10  2-m belt transect or 10-m line transect. The Atmospheric nitrogen (N2) was used as the standard.
number of transects on which corals were monitored and the
number of coral colonies observed are shown in Table 1. Coral 3. Results
disease was diagnosed following Raymundo et al. (2008). Coral
bleaching were classified into three stages, (0) no bleaching; (1) 3.1. Coral communities
partially bleached (surface/tips) or pale but not white; (2) full
bleaching of entire colonies following Marshall and Schuttenberg Coral communities varied significantly among tuna-farm ropes,
(2006). The occurrence rate of these lesions was compared natural substrata on a protected site, and natural substrata on
among corals on the tuna-farm ropes and those on surrounding disturbed sites (Fig. 3; ADONIS, F ¼ 5.59, R2 ¼ 0.37, P < 0.01; see
reefs at each study times using one-way ANOVA with the site as Supplementary Table 1 for species list). Coral communities on the
a fixed factor, and using post-hoc LSD comparison tests. When ropes were dominated by massive faviid corals, whereas on the
Levene’s test yielded significant result, data were log-transformed protected site, branching pocilloporid and acroporid corals were
(See Supplementary Table 4 for results of Levene’s test). Compari- relatively abundant. On disturbed sites, massive poritid corals and
sons of data in May 2009 were conducted by t-test between corals siderastreid corals were relatively abundant compared with the
on the tuna-farm ropes and those on the east coast of Keten. All other sites.
statistical analyses were conducted using R (R Development Core nMDS ordination shows that coral communities are more
Team, 2011). similar to each other within sites than to coral communities from

Table 1
Number of line-transects (10 m) settled on the rope of tuna-farm, belt-transects (10  2-m) or line-transect (10 m) settled on natural reefs, and number of coral colonies per
transect monitored in this study. N indicates the number of transect. a, the number of belt-transects; b, the number of line-transects.

Data On the rope Derikyonma Kudadon East Keten

N Number of colonies N Number of colonies N Number of colonies N Number of colonies

(average  SD) (average  SD) (average  SD) (average  SD)
May 2009 5b 57.0  14.0 0 0 0 0 3a 28.0  23.1
Aug 2009 10b 52.5  14.6 3a 137.0  38.2 2a 17.5  6.4 5a 49.2  12.3
Feb 2010 10b 51.6  14.3 6b 21.3  3.6 9b 8.4  6.3 6b 7.0  3.8
48 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53

Fig. 3. Genera of zooxanthellate corals on the ropes of the tuna farm, a protected reef at Derikyonma, and two disturbed reef sites, Kudadon and East Keten in Amami Island on Feb.
2010. Data show the percent of the number of colonies on 10-m-long lines averaged among the number of samples. N ¼ number of samples.

other sites (Fig. 4). Only coral communities from Kudadon were species (Fig. 5). In total, 60 species occurred on the ropes, and 23 of
widely scattered. As nMDS ordination shows, pairwise beta diver- these were specific to ropes. In contrast, on the disturbed sites only
sity among study sites was relatively high, especially between ropes a limited number of species occurred (Fig. 5). The number of
and at East Keten, although these sites were located in the same bay colonies, number of species, coral coverage and species diversity
and were only 800 m away from each other (Table 2). On the other (H0 ) of coral communities on the rope either equaled or surpassed
hand, the b1 value between ropes and at the protected Deri- those on the protected site and were significantly higher than those
kyonma site was relatively low and shared more coral species. on the two disturbed sites (Fig. 5, see Supplementary Tables 2, 3 for
On the tuna farm, an average of nearly 40% of the 10-m lines statistical values).
settled along the ropes was covered by 30 coral colonies of 15 Coral colonies of various sizes inhabited the ropes of the tuna
farm (Fig. 6). The range of coral projected area was 2.6 (Favia favus)
to 6361.7 (Acropora hyacinthus) cm2 on the rope, 0.4 (Cyphastrea
chalcidicum) to 34.9 (Millepora sp.) cm2 in Kudadon, and 1.1 (Porites
lutea) to 170.6 (Montipora tuberculosa) cm2 in East Keten. After
log-normal conversion the size-frequency distributions of domi-
nant genera of corals approximate normality (for all genera,
KolmogoroveSmirnov test, P > 0.05), showing a size-frequency
distribution similar to natural coral populations (e.g. Bak and
Meesters, 1998; Glassom et al., 2004). On the disturbed reefs, East
Keten and Kudadon, colony sizes of the most corals were signifi-
cantly smaller than those on the ropes (SteeleDwass test or Manne
Whitney U-test, P < 0.05, see Supplementary Fig. 1 for coral sizes
and Supplementary Table 4 for statistical values).

3.2. Biological and physical stresses on corals

Corals on ropes on the tuna farm, on the protected site, and on

the disturbed sites exhibited different degree of vulnerability to the
different stresses investigated. On the ropes, bleaching and sedi-
mentation were much lower than on natural substrata in our three
sites, but Waminoa infection was higher (Fig. 7a, c, e, see
Supplementary Tables 5, 6 for statistical values). No single coral
colony among the 526 colonies on the ropes was killed by bleaching
during the one-year observation, and small numbers of Category 1
Fig. 4. Nonmetric multidimensional scaling (nMDS) ordination using BrayeCurtis
similarities among the coral species composition on tuna-farm ropes, a protected reef
[partially bleached (surface/tips) or pale but not white] corals were
(DQ, Derikyonma), and two disturbed reefs (KD, Kudadon; EK, East Keten). 2D stress found (Fig. 7a). Higher rates of partial bleaching and cover by
is 0.11. sediment were observed on the two disturbed sites, especially in
 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53 49

Table 2 January, February, or March at the sea surface and a depth of 3 m,

Pairwise beta diversity (b1) between four study sites. respectively. Water temperature at a depth of 3 m was significantly
On the rope Derikyonma Kudadon lower than sea surface temperature (t ¼ 38.26, d.f. ¼ 3855,
(tuna farm) (protected site) (disturbed site) P < 0.001). Vertical visibility of water was 16.3  3.6 m
Derikyonma (protected site) 47.9 (average  SD) during 2000e2010, and was highest in January,
Kudadon (disturbed site) 56.9 51.6 18.8  3.1 m, and lowest in June, 12.9  3.8 m.
East Keten (disturbed site) 72.1 55.1 63.6

3.3. Stable isotope analysis

East Keten, compared with those on ropes and on the protected site. The stable isotope value of d15N was higher in Porites lutea from
Algal overgrowth was relatively high at all study sites compared tuna-farm ropes than in those from natural reef in the same bay
with other biotic stresses (Fig. 7b, d, f). No infectious diseases were (Welch two sample t-test, t ¼ 4.16, d.f. ¼ 2.4, P < 0.05; Fig. 8). d15N
found either on the tuna farm or on natural substrata. No single A. values were positively correlated with trophic level, indicating that
planci occurred on the ropes in the tuna farm, and no scars of the trophic level of P. lutea on the rope was higher than that on
A. planci were found on corals on the ropes. natural substrata.
Water temperature in the tuna farm was 24.4  3.1
C
(average  SD) and 24.2  3.0
C at the sea surface and a depth of 4. Discussion
3 m, respectively, during 2000e2010. Annual maximum tempera-
ture was 30.1  0.6 and 29.7  0.6 in July, August, or September, and The ropes on the tuna farm are moored at a depth of 3 m in the
annual minimum temperature was 19.7  0.6 and 19.7  0.4 in water column at a site approximately 50 m in depth, and these

Fig. 5. Coral community structure on tuna-farm ropes, a protected reef (DQ, Derikyonma), and two disturbed reefs (KD, Kudadon; EK, East Keten). a total number of species;
b average number of species occurring on a 10-m line; c average number of colonies on a 10-m line; d average coral coverage on a 10-m line; e species diversity (ShannoneWiener
H0 ); and f evenness (Pielou’s J). Different letters indicate significant differences at the 5% level by LSD test (See Supplementary Tables 2, 3 for details of statistics). Error bars indicate
standard deviations.
50 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53

Fig. 6. Size-frequency distributions of (a) Porites, (b) Acropora, (c) Pocillopora, (d) Favia, (e) Favites, (f) Goniastrea, (g) Montastraea, (h) Platygyra corals on tuna-farm ropes in log-
arithmic scales of size. Normal distributions are fitted. N indicates the number of colonies.

ropes provide corals with habitat. This mooring situation above frequency distribution of corals on the tuna-farm ropes could be
a relatively deep bottom enables the substratum to remain free fitted to normal distribution after log-normal conversion. Note that
from sediment and its resuspension, from predation by crown-of- corals may grow faster under the tuna farm than on natural
thorns starfish, and from extreme high water temperatures, substrata due to additional nutrients released from the farm
making it quite suitable for coral settlement and growth (Shafir (Bongiorni et al., 2003), and if it is the case here coral age might be
et al., 2006). Water clarity in the fish farm was high, mean annual overestimated. Coral size distribution, however, shows that coral
value of vertical visibility measured by Secchi disk was 16.3  3.6 m, communities are not skewed to either large colonies or small
that exceeds a guideline value (>10 m) for healthy coral reef (De’ath colonies (Bak and Meesters, 1998, 1999), indicating that the coral
and Fabricius, 2010). Although the ropes measured only 765 m in community on the ropes has been established through continuous
length and 6 cm in diameter, they were inhabited by 60 coral recruitment since the rope was set 14 years ago.
species. This corresponds to 27.3% of the 220 species known from The coral community on the ropes was highly species diverse,
Amami Islands (Nishihira and Veron, 1995), and this artificial and was dominated by massive faviid corals. In these points, the
substratum increases g diversity based on species composition in coral community is unique comparing those on adjacent natural
the area through the enhancement of b diversity between habitats. reefs. The complex surface structure of the rope can provide diverse
The size-frequency distributions of corals show that corals species of corals with heterogeneous habitats, and various species
colonize the ropes continuously. The largest colony of Porites on the of larvae might settle on this new open space floated at 3-m depth.
ropes was a colony of Porites lobata with a projected area of Fourteen years is not long enough for coral succession (Perkol-
151.6 cm2, the greatest diameter being 15.6 cm. Growth rates of Finkel and Benayahu, 2005; Perkol-Finkel et al., 2006a), and this
Porites corals reported for the Ryukyu Islands range between 0.7 community is in an intermediate stage of succession, resulting in
and 1.1 cm in radius per year (Mitsuguchi et al., 2003; Morimoto high species diversity (Connell, 1978).
et al., 1998). Following these rates, the largest colony may have Regarding post-settlement survival, survival rates of coral
colonized the rope already shortly after its installation, and may species differ under various environmental conditions and types of
thus be around ten years old. Similarly, the largest colony of substrata (Perkol-Finkel and Benayahu, 2009). Especially on
Acropora was a colony of A. hyacinthus with a projected area of floating substrata, extreme water flow and the swinging of the
6361.7 cm2. This colony also may have colonized the rope for ropes affect coral survival (Perkol-Finkel et al., 2006b). Under these
more than ten years following the growth rate of A. hyacinthus stresses, massive faviid corals seem to have an advantage because
estimated for Okinawa Islands, (increased projected area/ of their tight anchoring to the substratum. On the ropes, the acoel
year) ¼ 1.228  (present projected area) þ 3.021 (Muko et al., worm Waminoa sp. colonized more coral colonies than on natural
2001). In regard to the other dominant genera, the largest colo- substrata surveyed in this study. This may be a specific stress on
nies are similarly estimated to have colonized the ropes more than corals on the ropes due to the physical shading of ambient light
ten years ago, following the growth rate of 21.3e43.7 mm in radius (Barneah et al., 2007), consumption of coral mucus (Naumann et al.,
per year for Pocillopora corals (Guzmán and Cortés, 1989), and 2.6e 2010), competition for planktonic food (Wijgerde et al., 2012).
4.6 mm in radius per year for faviid corals (Harriott, 1999). The size- Although the population dynamics of acoel worms are mostly
 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53 51

Fig. 7. Biotic and abiotic diseases on corals on tuna-farm ropes, a protected reef (DQ, Derikyonma), and two disturbed reefs (KD, Kudadon; EK, East Keten) in May and August 2009
and February 2010. a partial bleaching rate; b partially covered by algae; c infected by Waminoa sp.; d partially covered by sponge; e partially covered by sediment; f infected by
encysted parasitic trematodes. Different letters (among a, b, and C, among a0 , b0 and C0 , and among a00 , b00 , and C00 ) indicate significant differences at the 5% level by LSD test or t-test
(See Supplementary Tables 5, 6 for details of statistics). NS indicates no significant difference was found in any comparison. Error bars indicate standard deviations.

unknown on local and wide geographical ranges (Barneah et al., of-thorns starfish (Nakai and Oki, 2004). The coral communities
2007), eutrophication caused by fish pens may be a cause of their there mainly consisted of massive Porites and encrusting Psam-
increase, as shown here on a fish farm and on a reef in Eilat (Loya, mocora, which are non-preferred species for A. planci (Colgan, 1987;
2004). Faure, 1989; Pratchett et al., 2009), but all colonies were small
The nitrogen stable isotope ratio of Porites lutea was higher on (Supplementary Fig. 1). In Indo-Pacific coral reefs, outbreak of
the rope than on an adjacent natural substratum. This implies that A. planci can be a principal cause of coral reef degradation. For
the corals on the ropes of tuna farms may absorb waste from feeds example, on the Great Barrier Reef, coral cover decreased from
such as mackerel and squid and/or the feces of tuna that is higher in 28.0% to 13.8% during the last 27 years, and A. planci predation
trophic level. Manipulative experiment is needed to demonstrate accounts for 42% of the loss (De’ath et al., 2012). To control the
this hypothesis. It is known, however, that around 10% of feeds are A. planci population, improvement of water quality is first needed
uneaten, and around 6% of the nitrogen and 52% of the phospho- because nutrient-enriched water increases the survival of the
rous of those ingested are discharged as feces from the farm in this plankton-feeding A. planci juveniles (Brodie et al., 2005; Fabricius
tuna farming system (Aguado et al., 2004). et al., 2010). Therefore, control of nutrient loading from aquacul-
In contrast, on two disturbed reefs studied here, coral commu- ture is necessary. Further, development of effective method to
nities were severely deteriorated by recurring outbreaks of crown- directly exterminate A. planci, such as a novel biopesticide (Rivera-
52 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53

Environment Research and Technology (Charitable Trust) and JSPS

KAKENHI Grant Number 22770024.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://

dx.doi.org/10.1016/j.marenvres.2012.12.009.

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