Marine Environmental Research 85 (2013) 45e53

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Marine Environmental Research

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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
Tuna farming in coastal waters is now increasing in the Medi-
terranean, Australia, and Japan, and monitoring and management of
wild stock of tunas and the effect of farming on natural environment
are required. In Japan, Pacific Bluefin tuna, Thunnus orientalis, is
intensively farmed in the southern subtropical sea where water
temperature is moderately high, and therefore, tuna grow rapidly
and spawn every year (Masuma et al., 2008; Masuma, 2011). As usual,
tuna farms are used to fatten wild caught tuna in cages for periods
from a few months to up to 1e2 years (Miyake et al., 2003; Sumaila
and Huang, 2012). In Japan, however, six organizations maintain
bluefin-tuna broodstocks for longer periods and manage to produce
their eggs to supply juveniles for aquaculture as well as to aim for
conservation of wild stock (Masuma et al., 2008; Normile, 2009).
In the southern part of Japan, coral reefs are well established, and
the tuna farms exist adjacent to the coral reefs. Tuna farms require
* Corresponding author. Tel./fax: þ81 89 927 9638.
E-mail address: hata@sci.ehime-u.ac.jp (H. Hata).
huge cages as well as frames, ropes, floats, and anchors supporting
the cages (Miyashita, 2008). Most cages are settled underwater for
decades, and therefore they provide substrata for wild organisms.
On a tuna farm in Amami Island, Japan, 6-cm-diameter ropes hold
the cages and frames and are suspended at a depth of 3 m irre-
spective of tides, and these ropes are covered with corals. Artificial
substrata can provide wild organisms with habitat and increase
their densities (Bohnsack and Sutherland, 1985). This heteroge-
neous habitat increases the total diversity of the region, that is, g
diversity, through enhancement of differentiation of communities
among habitats. The extent of the differentiation of communities
among habitats is defined as b diversity (Whittaker, 1972). Artificial
substrata on coral reefs may help unique communities to occur
there, thus increasing the b diversity between natural and artificial
habitats (Perkol-Finkel and Benayahu, 2004; Perkol-Finkel et al.,
2005, 2006a), and they also can be a tool for coral reef restoration
(Spieler et al., 2001; Abelson, 2006).
At the same time, tuna farms discharge high levels of organic
particulate matter and nutrients as waste from feeds such as squids
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
hypothesized that the artificial substrata on a tuna farm would
provide a refuge to corals during outbreak of A. planci and/or during
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
disturbed sites in adjacent waters. Corals and environmental
stresses were monitored on the fish-farm ropes and at protected
and disturbed sites for a year.
2. Materials and methods
2.1. Coral communities on an artificial substratum at a tuna farm,
on disturbed reefs, and on a protected reef
This study was conducted on a fish farm and adjacent coral reefs
in Setouchi Channel, Amami Island, Kagoshima, Japan (Fig. 1). A
net-cage culture system for tuna farming was constructed on the
west coast of Keten Bay by Kinki University. Currently, the third
generation of an artificially bred strain is being reared in this cage
system (Normile, 2009; Sawada et al., 2005). Six floating cages, 30-
m in diameter  15-m in depth were established in 1997 for the
farming and breeding of Pacific Bluefin tuna, T. orientalis (Mukai,
2011). These cages were arranged in two rows abutting each
other. To moor the cages, seventeen 45-m lead-cored polyethylene
ropes, 60 mm in diameter, were suspended from floats on the sea
surface to around 3-m in depth irrespective of tidal conditions
(Fig. 2) (Miyashita, 2008). This study focused on zooxanthellate
coral populations that had developed on the ropes. Water
temperatures on the surface and at a depth of 3.0 m were measured
at around 14:00 every day during 2000e2010 on this fish farm.
Water clarity in the farm was measured using Secchi disc at the
same time during 2000e2010.
The coral communities on the ropes were compared to coral
communities in adjacent, natural reefs. Two non-protected natural
reefs and one protected natural reef were selected for this
comparison. The two non-protected reefs were located at the east
coast of Keten and in the Kudadon Bay, which neighbors Keten but
is separated by a small cape (Fig. 1). In Kudadon, live corals have
been decimated because of outbreaks of A. planci starfish. The
protected area of Derikyonma, which is on the opposite side of
Setouchi Channel (Fig. 1) was chosen as an example of a protected
Fig. 1. Study sites in the Setouchi area, Amami Islands, southern Japan. The tuna farm
is in Keten Bay. East Keten and Kudadon were selected as disturbed sites, and Deri-
kyonma as a protected site in this study.
natural reef. In this area, populations of A. planci are intensively
controlled by reef managers. In these areas, 10-m lines were
established at a depth of 3 m, and line intercept transects were
conducted by scuba diving to survey coral species composition and
coverage in February 2010. The numbers of lines set were 7, 8, and 5
in Derikyonma, Kudadon, and the east coast of Keten, respectively.
At the same time, thirteen 10-m-long lines were established on 13
randomly selected 45-m ropes of the fish farm, and line-intercept
transects were conducted. All coral colonies were recorded with
a scale using an underwater digital camera, and parts of colonies
were collected and bleached to make skeletal specimens. Using
these photos and specimens, we classified corals into species
following Veron and Pichon (1976, 1980, 1982), Veron et al. (1977),
Veron and Wallace (1984), Nishihira and Veron (1995), Wallace
(1999), and Veron (2000), and Benzoni et al. (2010). Using these
photos, colony size of corals on the ropes, on natural reefs in
Kudadon and East Keten sites were measured by the greatest (d1)
and the smallest (d2) diameter of the corals. Projected area of each
coral colony was calculated using the formula, (d1/2)  (d2/2)  p.
Coral size was compared among sites using SteeleDwass multiple
comparison tests or ManneWhitney U test.
Multivariate analyses of coral community structure were con-
ducted with permutational multivariate analysis of variance using
distance matrices (PERMANOVA; Anderson, 2001) with 1000 null
permutations and nonmetric multidimensional scaling (nMDS)
ordination using BrayeCurtis similarities among the species
composition data. Number of colonies, number of species, coverage
on the line, and species diversity as ShannoneWiener index (H0 ),
and evenness (Pielou’s J) were compared using one-way analysis of
variance (ANOVA) with the site as a fixed factor. Levene’s test for
homogeneity of variance yielded significant results for all five
indices. Therefore all the data were log transformed. Each of the
indices was compared among the sites using a post hoc multiple
comparison test (least significant difference, LSD). Beta diversity
among sites was measured using pairwise b1 (Harrison et al.,
1992), which is calculated by (S/a  1)/(N  1)  100, where S is
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.
b1 ¼ 0 means complete similarity between two sites, and
b1 ¼ 100 means complete dissimilarity between the two sites.
Water temperature was compared between sea surface and 3 m
below the surface using paired t-test.
2.2. Monitoring of stresses on corals
Coral bleaching, algal and sponge overgrowth on corals, infec-
tion of Waminoa sp. and encysted parasitic trematodes on corals,
sediment cover, and coral disease were monitored on 5e10 10-m
line transects separately settled along 45 m ropes of the tuna-
farm in May and August 2009 and February 2010. At the same
time, on the east coast of Keten, corals were monitored using
10  2-m belt transect or 10-m line transect. Additionally, in August
2009 and February 2010, corals in Kudadon and Derikyonma were
monitored using 10  2-m belt transect or 10-m line transect. The
number of transects on which corals were monitored and the
number of coral colonies observed are shown in Table 1. Coral
disease was diagnosed following Raymundo et al. (2008). Coral
bleaching were classified into three stages, (0) no bleaching; (1)
partially bleached (surface/tips) or pale but not white; (2) full
bleaching of entire colonies following Marshall and Schuttenberg
(2006). The occurrence rate of these lesions was compared
among corals on the tuna-farm ropes and those on surrounding
reefs at each study times using one-way ANOVA with the site as
a fixed factor, and using post-hoc LSD comparison tests. When
Levene’s test yielded significant result, data were log-transformed
(See Supplementary Table 4 for results of Levene’s test). Compari-
sons of data in May 2009 were conducted by t-test between corals
on the tuna-farm ropes and those on the east coast of Keten. All
statistical analyses were conducted using R (R Development Core
Team, 2011).
2.3. Stable isotope analysis
The stable isotope ratio of nitrogen is useful in trophic level
analysis because the nitrogen pools of animals have regularly
enriched d15N signatures relative to their food sources (Cabana and
Rasmussen, 1994). Three colonies of Porites lutea were collected
from tuna-farm ropes, and three P. lutea were collected from the
East Keten site. These colonies were preserved in 99.9% ethanol,
and tissues were removed using a Water Flosser WP-100, Water-
pikÒ. Tissues were dried in an oven at 60
C for 24 h and powdered
with a mortar and pestle. Nitrogen stable isotope ratios (&) were
measured using a gas chromatographyecombustioneisotope ratio
mass spectrometer (GCeCeIRMS) (SerCon, Ltd., ANCA-SL). Results
are presented as per thousand deviations from the standards,
expressed as d15N by the following equation: d15N (&) ¼ (Rsample/
Rstandard  1)  1000, where R is the corresponding ratio of 15N/14N.
Atmospheric nitrogen (N2) was used as the standard.
3. Results
3.1. Coral communities
Coral communities varied significantly among tuna-farm ropes,
natural substrata on a protected site, and natural substrata on
disturbed sites (Fig. 3; ADONIS, F ¼ 5.59, R2 ¼ 0.37, P < 0.01; see
Supplementary Table 1 for species list). Coral communities on the
ropes were dominated by massive faviid corals, whereas on the
protected site, branching pocilloporid and acroporid corals were
relatively abundant. On disturbed sites, massive poritid corals and
siderastreid corals were relatively abundant compared with the
other sites.
nMDS ordination shows that coral communities are more
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
widely scattered. As nMDS ordination shows, pairwise beta diver-
sity among study sites was relatively high, especially between ropes
and at East Keten, although these sites were located in the same bay
and were only 800 m away from each other (Table 2). On the other
hand, the b1 value between ropes and at the protected Deri-
kyonma site was relatively low and shared more coral species.
On the tuna farm, an average of nearly 40% of the 10-m lines
settled along the ropes was covered by 30 coral colonies of 15
Fig. 4. Nonmetric multidimensional scaling (nMDS) ordination using BrayeCurtis
similarities among the coral species composition on tuna-farm ropes, a protected reef
(DQ, Derikyonma), and two disturbed reefs (KD, Kudadon; EK, East Keten). 2D stress
is 0.11.
species (Fig. 5). In total, 60 species occurred on the ropes, and 23 of
these were specific to ropes. In contrast, on the disturbed sites only
a limited number of species occurred (Fig. 5). The number of
colonies, number of species, coral coverage and species diversity
(H0 ) of coral communities on the rope either equaled or surpassed
those on the protected site and were significantly higher than those
on the two disturbed sites (Fig. 5, see Supplementary Tables 2, 3 for
statistical values).
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
[partially bleached (surface/tips) or pale but not white] corals were
found (Fig. 7a). Higher rates of partial bleaching and cover by
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.
Algal overgrowth was relatively high at all study sites compared
with other biotic stresses (Fig. 7b, d, f). No infectious diseases were
found either on the tuna farm or on natural substrata. No single A.
planci occurred on the ropes in the tuna farm, and no scars of
A. planci were found on corals on the ropes.
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
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
annual minimum temperature was 19.7  0.6 and 19.7  0.4 in
The stable isotope value of d15N was higher in Porites lutea from
tuna-farm ropes than in those from natural reef in the same bay
(Welch two sample t-test, t ¼ 4.16, d.f. ¼ 2.4, P < 0.05; Fig. 8). d15N
values were positively correlated with trophic level, indicating that
the trophic level of P. lutea on the rope was higher than that on
natural substrata.
4. Discussion
The ropes on the tuna farm are moored at a depth of 3 m in the
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
a relatively deep bottom enables the substratum to remain free
from sediment and its resuspension, from predation by crown-of-
thorns starfish, and from extreme high water temperatures,
making it quite suitable for coral settlement and growth (Shafir
et al., 2006). Water clarity in the fish farm was high, mean annual
value of vertical visibility measured by Secchi disk was 16.3  3.6 m,
that exceeds a guideline value (>10 m) for healthy coral reef (De’ath
and Fabricius, 2010). Although the ropes measured only 765 m in
length and 6 cm in diameter, they were inhabited by 60 coral
species. This corresponds to 27.3% of the 220 species known from
Amami Islands (Nishihira and Veron, 1995), and this artificial
substratum increases g diversity based on species composition in
the area through the enhancement of b diversity between habitats.
The size-frequency distributions of corals show that corals
colonize the ropes continuously. The largest colony of Porites on the
ropes was a colony of Porites lobata with a projected area of
151.6 cm2, the greatest diameter being 15.6 cm. Growth rates of
Porites corals reported for the Ryukyu Islands range between 0.7
and 1.1 cm in radius per year (Mitsuguchi et al., 2003; Morimoto
et al., 1998). Following these rates, the largest colony may have
colonized the rope already shortly after its installation, and may
thus be around ten years old. Similarly, the largest colony of
Acropora was a colony of A. hyacinthus with a projected area of
6361.7 cm2. This colony also may have colonized the rope for
more than ten years following the growth rate of A. hyacinthus
estimated for Okinawa Islands, (increased projected area/
year) ¼ 1.228  (present projected area) þ 3.021 (Muko et al.,
2001). In regard to the other dominant genera, the largest colo-
nies are similarly estimated to have colonized the ropes more than
ten years ago, following the growth rate of 21.3e43.7 mm in radius
per year for Pocillopora corals (Guzmán and Cortés, 1989), and 2.6e
4.6 mm in radius per year for faviid corals (Harriott, 1999). The size-
frequency distribution of corals on the tuna-farm ropes could be
fitted to normal distribution after log-normal conversion. Note that
corals may grow faster under the tuna farm than on natural
substrata due to additional nutrients released from the farm
(Bongiorni et al., 2003), and if it is the case here coral age might be
overestimated. Coral size distribution, however, shows that coral
communities are not skewed to either large colonies or small
colonies (Bak and Meesters, 1998, 1999), indicating that the coral
community on the ropes has been established through continuous
recruitment since the rope was set 14 years ago.
The coral community on the ropes was highly species diverse,
and was dominated by massive faviid corals. In these points, the
coral community is unique comparing those on adjacent natural
reefs. The complex surface structure of the rope can provide diverse
species of corals with heterogeneous habitats, and various species
of larvae might settle on this new open space floated at 3-m depth.
Fourteen years is not long enough for coral succession (Perkol-
Finkel and Benayahu, 2005; Perkol-Finkel et al., 2006a), and this
community is in an intermediate stage of succession, resulting in
high species diversity (Connell, 1978).
Regarding post-settlement survival, survival rates of coral
species differ under various environmental conditions and types of
substrata (Perkol-Finkel and Benayahu, 2009). Especially on
floating substrata, extreme water flow and the swinging of the
ropes affect coral survival (Perkol-Finkel et al., 2006b). Under these
stresses, massive faviid corals seem to have an advantage because
of their tight anchoring to the substratum. On the ropes, the acoel
worm Waminoa sp. colonized more coral colonies than on natural
substrata surveyed in this study. This may be a specific stress on
corals on the ropes due to the physical shading of ambient light
(Barneah et al., 2007), consumption of coral mucus (Naumann et al.,
2010), competition for planktonic food (Wijgerde et al., 2012).
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.,
2007), eutrophication caused by fish pens may be a cause of their
increase, as shown here on a fish farm and on a reef in Eilat (Loya,
2004).
The nitrogen stable isotope ratio of Porites lutea was higher on
the rope than on an adjacent natural substratum. This implies that
the corals on the ropes of tuna farms may absorb waste from feeds
such as mackerel and squid and/or the feces of tuna that is higher in
trophic level. Manipulative experiment is needed to demonstrate
this hypothesis. It is known, however, that around 10% of feeds are
uneaten, and around 6% of the nitrogen and 52% of the phospho-
rous of those ingested are discharged as feces from the farm in this
tuna farming system (Aguado et al., 2004).
In contrast, on two disturbed reefs studied here, coral commu-
nities were severely deteriorated by recurring outbreaks of crown-
of-thorns starfish (Nakai and Oki, 2004). The coral communities
there mainly consisted of massive Porites and encrusting Psam-
mocora, which are non-preferred species for A. planci (Colgan, 1987;
Faure, 1989; Pratchett et al., 2009), but all colonies were small
(Supplementary Fig. 1). In Indo-Pacific coral reefs, outbreak of
A. planci can be a principal cause of coral reef degradation. For
example, on the Great Barrier Reef, coral cover decreased from
28.0% to 13.8% during the last 27 years, and A. planci predation
accounts for 42% of the loss (De’ath et al., 2012). To control the
A. planci population, improvement of water quality is first needed
because nutrient-enriched water increases the survival of the
plankton-feeding A. planci juveniles (Brodie et al., 2005; Fabricius
et al., 2010). Therefore, control of nutrient loading from aquacul-
ture is necessary. Further, development of effective method to
directly exterminate A. planci, such as a novel biopesticide (Rivera-
52 H. Hata et al. / Marine Environmental Research 85 (2013) 45e53
Fig. 8. Nitrogen stable isotope ratio, d15N (&), of Porites lutea on tuna-farm ropes and
on natural substrata in the same bay. Error bars indicate standard deviations.
Posada et al., 2011), is awaited to regenerate the coral communities
in this area.
In this study, a highly diverse coral community, which had
escaped from an outbreak of crown-of-thorns starfish on
surrounding natural substrata, was found on floating ropes on
a tuna farm. This overlooked coral community may fulfill several
ecosystemic functions and could be a new node to indirectly link
fish farms with surrounding natural environments. Given the fact
that cage cultures release nutrients and organic matter, thus
enhancing potential outbreaks of A. planci and overgrowth by algae,
it is recommended to exclude cage culture practices from areas in
the vicinity of natural coral reefs. Nevertheless, when positioned
further away, cage cultures may be beneficial to natural coral reefs:
they may provide a refuge for corals during outbreak of A. planci
and/or during periods of bleaching and they can be efficiently used
as nurseries for coral production for reef restoration purposes
(Horoszowski-Fridman et al., 2011). Conversely, the fish farm could
be a source of pathogens for corals and wild animals in the
surrounding environment (Garren et al., 2008, 2009), and therefore
continuous monitoring is necessary to prevent the coral commu-
nities on the ropes from becoming a source of pathogens. Addi-
tionally, the coral communities on the rope differed structurally
from those in natural habitat and cannot be compensate for the loss
of natural habitat (Burt et al., 2009).
This study could form one step toward coral “gardening”
(Rinkevich, 1995, 2006), which incorporates the farming of corals
on artificial substrata for transplantation to disturbed natural
substrata. This action for coral reef restoration is now ongoing
worldwide in areas such as the Gulf of Eilat in the Red Sea (Shafir
et al., 2006; Horoszowski-Fridman et al., 2011), Tanzania (Mbije
et al., 2010), the Philippines (Shaish et al., 2008), Singapore
(Bongiorni et al., 2011), and Florida in the Caribbean Sea (Herlan
and Lirman, 2008). In Japan, coral reefs have severely declined
over the last 40 years, but the restoration process is just beginning
(Omori, 2011). This temporal species-diverse coral community on
a tuna farm should receive attention and be well utilized toward
the recovery of coral reefs from outbreaks of crown-of-thorns
starfish.
Acknowledgments
We are grateful to Dr. Shigeru Miyashita at Fisheries Laboratory,
Kinki University for support field research, Ms. Yuko Kitano at Kyoto
University and Mr. Kodai Hibino for field research and identification
of corals. This study is supported by ESPEC Foundation for Global
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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