Blackwell Science, LtdOxford, UKFISFisheries Science0919-92682005 Blackwell Science Asia Pty LtdApril 2005712263270Original ArticleCulture of coral by sexual reproductionM

Okamoto
et al.

FISHERIES SCIENCE 2005; 71: 263–270

A basic experiment of coral culture using sexual

reproduction in the open sea
Mineo OKAMOTO,1* Satoshi NOJIMA,2 Yasuo FURUSHIMA3 and William C. PHOEL4

1
Tokyo University of Marine Science and Technology, Tokyo 108-8477, 2AMBL, Kyushu University,
Kumamoto 863-2507, 3JAMSTEC, Yokosuka 237-0061, Japan and 4Underwater Research Foundation
International Inc., New Jersey 08753, USA

ABSTRACT: Coral larvae, produced from a mass spawning event, were successfully settled on
special stone settlement sticks and raised in situ for eventual transport to other reefs. The test area,
Sekisei lagoon, Okinawa Prefecture, Japan, is located close to the warm Kuroshio current and is sur-
mised to be the source from which major Japanese corals are derived. A total of 131 settlement sticks,
with small holes in their sides to increase protection from grazing (4 mm in diameter and approxi-
mately 5 mm deep), were deployed in the lagoon the day before the coral’s mass spawning. After
3 months, 61 sticks were recovered containing 71 corals, mostly in the holes. After 1 year, three corals
were confirmed to be growing well and extending outside the holes of the three sticks out of 70 sticks
left in the water at the lagoon site. They survived two potentially lethal conditions, that is, high water
temperatures with associated extensive coral bleaching and continuous grazing pressure from pred-
ators. This procedure is applicable for large-scale coral transplantation, not only in Japan but also in
other tropical countries.

KEY WORDS: coral, mass spawning, settlement, sexual reproduction, transplantation.

INTRODUCTION the corals of Okinawa Island where those corals are

facing extinction due to the effect of repetitive
Coral reefs in the world have suffered drastic bleaching. Sekisei lagoon is surmised to be the
declines in the past several decades due to many main source of coral larvae for the Japanese Islands
stresses but especially climate change, pollution along Kuroshio and there is concern that the dis-
and overfishing.1–4 Mass coral bleaching involving appearance of the corals in Sekisei lagoon may lead
many of the world’s coral reefs in 1997–1998 high- to the extinction of the major Japanese coral reefs.
lighted a serious potential impact on coral reef The recovery of corals by the transplantation of
ecosystems.5 coral fragments has been examined,2,12 however,
The major coral reefs of Japan are distributed this method has become difficult to apply for
along the warm Kuroshio current. The largest coral Japanese coral reefs. Coral community as fragment
reef in Japan is Sekisei lagoon, which is located donors is decreasing drastically in Japan except
near the origin of the Kuroshio.6,7 This highly Sekisei lagoon. Thus, the recruitment of corals by
diverse area has recorded 363 species of her- mass spawning is thought to be very important for
matypic corals.8,9 Japanese coral reefs suffered the prevention of local extinction.13–18
severe bleaching in the summer of 1998 and again Our experiment was to obtain coral larvae
in the summer of 2001. In 1998, 90% of the corals through natural mass spawning and raise them in
around Okinawa Island (450 km north-west of situ for future transplantation to coral reefs that
Sekisei lagoon) died due to the effect of the bleach- have been decimated by bleaching.
ing event,10,11 and the remaining corals were dam-
aged again in 2001. The damage to the corals in
Sekisei lagoon was not as severe as the damage to LOCATION, MATERIALS AND METHODS

Sekisei Lagoon is located between Ishigaki-jima

*Corresponding author: Tel: 81-3-5463-0485. and Iriomote-jima of the Yaeyama Islands in
Fax: 81-3-5463-0518. Email: okamotom@s.kaiyodai.ac.jp Okinawa Prefecture, Japan (Fig. 1). The dimensions
Received 19 May 2004. Accepted 29 September 2004. of the lagoon are approximately 25 km east and
264 FISHERIES SCIENCE
west, and 20 km north and south. The lagoon is
bounded by coral reef in the north and south and
by the islands in the east and west. In the lagoon,
the water depth reaches about 15 m and there are
many patch reefs and small-scale reefs distributed
on the flat, shallow and sandy bottom. Outside of
the reef there is a rocky stretch, which continues to
a depth of 20–25 m, then a sandy bottom which
spreads to depths of over 1000 m.6,7
Water temperatures were measured around the
site at 3, 6 and 9 m depths between October 1998
and 2002 at 10 min intervals using temperature
loggers (24∞15.8¢N, 124∞05.8¢E).
The idea of coral culture was produced from our
coral recruitment study produced from the mass
spawning in Sekisei lagoon between 1999 and 2001
(S. Nojima & M. Okamoto, unpubl. data, 2001).
The settlement plates (pottery stone, 100 mm ¥
100 mm ¥ 13 mm) were fixed on an anchoring
block with a 10 mm horizontal clearance between
them. A similar space also existed between the bot-
tom plate and the anchoring block as shown in
Fig. 2. The plates were set on the block within a
week before mass spawning of corals. The plates
were recovered after about 3 months in water to
enumerate and roughly identify the settled corals.
Several plates were left in the sea to examine the
survival rate of settled corals after 1 year and more.
At 3 months after the mass spawning, corals were
observed on the underside of the plates within 15–
20 mm from the edge, but not on the upper surface
or on the sides of the plates. As the corals age they
grow towards the sides of the plates, probably to
reach the sunlight, and can reach a size of approx-
imately 10 mm in about 15 months as shown in
M Okamoto et al.
Fig. 1 Map of Sekisei Lagoon.
Fig. 2. We were convinced that the corals obtained
by this manner would be suitable for transplanta-
tion use, since they survived more than 1 year of
grazing pressure and other natural phenomena.
Two new types of settlement devices were con-
structed with small holes along the sides of the
sticks to increase coral settlement and survival.
The horizontal holes were 4 mm in diameter and
5 mm in depth, the size of which was derived from
our previous experience with settlement plates (S.
Nojima & M. Okamoto, unpubl. data, 2001). Two
kinds of stone were used for the larvae settlement
experiment; pottery stone produced in Amakusa
and limestone produced in Okinawa. The pottery
stone was manufactured into cylindrical sticks
(30 mm ¥ 125 mm) with a total of 16 holes hol-
lowed out around the upper 75 mm. Plates of
limestone were cut into square sticks (30 mm ¥
30 mm ¥ 100 mm) and 24 horizontal holes were
hollowed out in the upper 50 mm of each stick with
six holes to a side in three levels. The lower 50 mm
of all the sticks were covered by vinyl tape. The pot-
tery stone is dense and easy to manufacture into
settlement sticks. The limestone, however, is
coarse with many small cracks and holes so it is
difficult to process into small sticks (Fig. 3).
A total of 72 cylindrical settlement sticks were set
into a stainless steel frame (42 cm ¥ 45 cm ¥ 40 cm)
and 59 square settlement sticks were set into
another frame of the same dimensions. For our
control, 288 settlement plates (100 mm ¥
100 mm ¥ 13 mm) with a 6.5 mm in diameter hole
in the center of it were set in another six similar
frames with 48 plates per frame. The plates were
fixed onto each frame using bolts (6 mm in diameter
Culture of coral by sexual reproduction FISHERIES SCIENCE 265

Fig. 2 Standard settlement

plates used for coral recruitment
study and 15-month-old corals.
Upper plate, Millepora sp.; lower
plate, Acropora sp.

Fig. 3 Settlement sticks with

small holes. Cylindrical stick,
30 mm ¥ 125 mm with 16 holes
made with pottery stone. Square
stick, 30 ¥ 30 ¥ 100 mm with 24
holes made with limestone.

¥150 mm in length) and nuts (10 mm in
diameter ¥ 10 mm in height) and arranged into
eight sets of six plates per set, with a 10 mm space
between each plate (Fig. 4).
The eight frames containing the stick-type set-
tlement devices and the settlement plates were
deployed on the bottom at a depth of 4 m in Sekisei
lagoon (24∞17.0¢N, 124∞02.1¢E) on 6 May 2001, the
day before a full moon. The experimental site is
located in the center of the lagoon and surrounded
by reef. The site is normally calm, in water 3–5 m
deep, and the bottom is flat for a diameter of about
50 m.
All the settlement plates (288) were recovered on
17 and 18 August 2001 and 32 cylindrical sticks and
29 square sticks were recovered on 18 August, after
266 FISHERIES SCIENCE M Okamoto et al.

Fig. 4 Frames containing settle-

ment sticks and settlement
plates. Left, Settlement Plate;
center, Square sticks; right, Sylin-
drical sticks.

approximately 3 months in place. During the time Table 1 Number of corals observed on the sticks and
the plates and sticks were on the bottom, we plates 3 months after mass spawning
observed an increase in water temperature, even- Total no. ACR POC OT
tually exceeding 30∞C, with associated heavy coral
bleaching. Also, since a strong typhoon was Cylindrical sticks (n = 32)
In holes (512 holes) 16 11 4 1
approaching the area, we decided to recover most
Out of holes 2 2 0 0
of the settlement devices to prevent them from Subtotal 18 13 4 1
being tumbled and moved. The recovered plates
Square sticks (n = 29)
and sticks were dried and transported to the labo-
In holes (696 holes) 43 42 1 0
ratory where the settled corals were examined Out of holes 10 9 1 0
for rough identification (generally to genus) and Subtotal 53 51 2 0
enumerated.
Plate (n = 288)
Visual observations of the two types of stone Undersides 267 210 31 26
sticks left at the site were conducted three times Topsides 12 10 2 0
during the next year (15 April, 26 June and 31 Sides 0 0 0 0
August 2002). Subtotal 279 220 33 26

No corals observed on the topside of sticks nor on the sides of

RESULTS
The mass spawning of corals at the experimental
site was observed to have occurred under a full
moon, mainly between 22.00 hours and 23.00
hours local time on 7 May 2001, the day after
deployment of the settlement devices. Acropora
hyacinthus, A. cytherea, and A. formosa were dom-
inant among the coral species that were observed
to have spawned.
Tables 1 and 2 show the number of corals that
settled on the 288 plates and 61 sticks. The 71 cor-
als observed on the sticks were only on the sides
and none were observed on the top surfaces.
Almost all of the corals that settled on the plates
were on the undersides, with few corals observed
on the upper surfaces and none on the sides.
plates.
Exposed surface area of settlement devices: cylindrical stick
(sides, 51.2 ¥ 102 mm2; holes, 2.0 ¥ 102 mm2); square stick (sides,
57.0 ¥ 102 mm2; holes, 3.0 ¥ 102 mm2); plate (topside, 99.2 ¥
102 mm2; sides, 5.2 ¥ 102 mm2; underside, 99.2 ¥ 102 mm2).
ACR, Acroporidae; OT, Other group; POC, Pocilloporidae.
There was a difference between the number of
corals that settled on the cylindrical stick and that
settled on the square stick (Table 1). The average
number of corals on the cylindrical stick (32 sticks
with 16 holes each) was 0.56 (standard deviation
[SD], 0.70), and was 1.83 (SD, 1.39) on the square
sticks (29 sticks with 24 holes each). The average
number of corals per hole was 0.031 (SD, 0.17) on
the cylindrical sticks (n = 512) and 0.062 (SD, 0.24)
Culture of coral by sexual reproduction FISHERIES SCIENCE 267

per hole on the square sticks (n = 696). The average
number of corals settled on the plates (n = 288) was
0.97 (SD, 1.25), and the number settled on the
underside was 0.93 (SD, 1.23). The settled corals
were roughly classified as Acroporidae, Pocil-
loporidae, and others. The most abundant coral
settled was Acroporidae at 72% of the cylindrical
stick’s coral (n = 18), 96% of the square stick’s coral
(n = 53), and 75% of the coral on the plates
(n = 279).
Visual observations of the two types of stone
sticks left at the site were conducted three times
during the next year (15 April, 26 June and 31
August 2002). Three corals were observed growing
on three sticks (Fig. 5). They were Acropora (cf.)
carduus on one square stick (out of 40 square
sticks) and Acropora sp. and Millepora sp. on two
cylindrical sticks (out of 30 cylindrical sticks). We
observed that even though small fishes such as
Labridae often grazed the sticks, these three corals
apparently survived such grazing. These three
corals also survived the high water temperatures
during the summer of 2001 when the water
temperatures in Sekisei lagoon appeared too high
for young corals to survive, as evidenced by the
heavy coral bleaching which occurred.
During 1999, 2000 and 2002, temperatures at 3 m
depth rarely exceeded 30∞C. However, in 2001 the
average daily temperatures exceeded 30.0∞C for
36 days. As a result of the increased temperatures,
heavy coral bleaching was observed in August and
September of 2001, all around Sekisei lagoon. The
highest temperature measured there was 31.0∞C
(Fig. 6).

Fig. 5 Three corals 15 months

old growing on the sides of settle-
ment sticks. Left, Acropora sp.
growing from a hole on a cylindri-
cal stick; center, Millepora sp.
growing outside a hole on a cylin-
drical stick; right, Acropora (cf.)
carduus growing from a hole on a
square stick.

Table 2 Number of corals observed on the plate per layer

Topsides of 288 plates (48 plates per layer) Undersides of 288 plates (48 plates per layer)
†
Layer Total no. ACR POC OT Total no. ACR POC OT
6 0 0 0 0 74 64 8 2
5 4 4 0 0 41 33 5 3
4 1 1 0 0 45 33 4 8
3 2 2 0 0 39 30 5 4
2 4 3 1 0 41 28 8 5
1 1 0 1 0 27 22 1 4
Total 12 10 2 0 267 210 31 26
†
Layer 6 is the top layer, layer 1 is the bottom layer.
ACR, Acroporidae; OT, Other group; POC, Pocilloporidae.
268 FISHERIES SCIENCE
DISCUSSION
Horizontal holes for settlement sticks
Two types of coral settlement devices were
designed and examined in situ. The new devices
were designed to satisfy three criteria: (i) they had
to be of a shape conducive for settlement of the
coral larvae; (ii) they had to afford the settled larvae
and juvenile corals protection from predation; and
(iii) they had to be easy to handle underwater,
especially during transplantation. The most
important consideration for designing a new set-
tlement device is to determine how the coral larvae
could settle and be protected on all sides of the
device.
On the natural reef, coral larvae settle and grow
in small crevices within the reef structure. To sim-
ulate this we used stone sticks with small holes
along the sides of the sticks to increase the survival
rate of the settled coral. The horizontal holes were
4 mm in diameter and 5 mm in depth, the size of
which was derived from our experience with the
standard plates as the smallest size for coral larvae
(S. Nojima & M. Okamoto, unpubl. data, 2001).
Larvae settlement
This experiment, comparing the two different set-
tlement sticks with the plates, produced some new
and interesting findings. The number of corals that
settled on the square stick was four times greater
than those settled on the cylindrical stick. The
square sticks also had more than twice as many
corals settled in the holes than the cylindrical
sticks. All corals settled on the sides of either stick
type, mostly in the holes, but 19% of the coral
which settled on the square sticks (n = 53) and 11%
M Okamoto et al.
Fig. 6 Water temperature at 3 m
depth. Missing data: 4 January 2002
to 15 April 2002.
of the coral that settled on the cylindrical sticks
(n = 18) were settled on the sides outside of the
holes.
Though it is difficult to explain why settlement
on the sides of the sticks, outside the holes, unex-
pectedly survived predation, we hypothesize that
the narrow space between each of the sticks, when
they are fixed on the stainless steel frame (Fig. 4),
would probably keep many grazers from reaching
the sides of the sticks. Why there was a difference in
survival between the two types of settlement sticks
is also unknown, however, the difference in the
material of the sticks, that is, the limestone square
sticks, is that they have many small grooves and
cracks on its surface that are more suitable for
larvae settlement and survival than the smoother
pottery stone, which may be a factor.
Another unexpected finding was that although
most of the corals that survived to 3 months had
settled on the underside of the plates, 12 corals
(4.3% of 279) had settled on the upper surface of
the plates. This is contradictory to our previous
experiences in Sekisei lagoon where no coral had
survived on the plate’s sides and upper surfaces.
The only difference between this settlement plate
experiment and the previous experiences was in
the number and arrangement of the plates (S.
Nojima & M. Okamoto, unpubl. data, 2001). In pre-
vious settlement experiments we normally had two
layers of plates (Fig. 2) but in this experiment there
were six layers of plates arranged on the frame as
shown in Fig. 4. Table 2 shows that the coral settled
only on the upper surface of the plates in layers one
through five (of each stack of six plates), but not on
the surface of the top plates of each stack (layer 6).
Immediately after mass spawning, the number of
corals settled were estimated to be much more
abundant than the number existing after 3 months
due to predation and other natural causes. While
Culture of coral by sexual reproduction FISHERIES SCIENCE
the same number of larvae originally settled on the
upper surfaces of the plates, the corals that settled
on the upper surfaces of the top plates in each
stack were exposed to predators.
Coral recruitment study have been reported in
many papers as reviewed.19,20 In the case of settle-
ment plates, corals are reported to settle not only
on the underside of plates but also on the upper
surface and side of plates. and no numerical infor-
mation about the distance of settlement corals
from the edge is described. As we have no idea why
corals in Sekisei lagoon settled mainly on the
underside of plates, one of the possible reason may
be the effect of predators.
Sexual reproduction for transplantation use
Corals are known to propagate by both asexual and
sexual reproduction. However, sexual reproduc-
tion has been thought to be difficult to use for coral
transplantation because it is a lengthy procedure
to grow coral from the larval stage. The metho-
dology of choice, therefore, was to transplant
branches and colonies of the coral.12,21 Major fac-
tors influencing the use of sexual reproduction are
that the number of coral larvae produced during
mass spawning is innumerable, the natural settle-
ment of larvae is thought to be near random, and
growth after settlement depends on environmental
conditions and protection from predation.22
In this study, we have examined the use of in situ
sexual reproduction to produce young corals for
transplantation to other areas. Because our settle-
ment devices provided increased substrate suit-
able for settlement and survival, the coral larvae
that did set on the devices would most likely have
died without this additional protective substrate.
We have determined the major variables associ-
ated with the sexual reproduction of Sekisei lagoon
corals. These are: (i) time of mass spawning; (ii) the
drifting pattern of the fertilized eggs and larvae;23
(iii) the areas in which the larvae settle; (iv) the rates
of survival after settlement; and (v) lethal water
temperatures. We are confident that by applying
these variables we will be successful in using sexual
reproduction to produce juvenile coral in Sekisei
lagoon for transplantation to other areas. In proof
of this hypothesis we succeeded in having the coral
larvae settle on an artificial substrate (holes in the
settlement sticks) and after 1 year, three of the set-
tled corals were living and growing.
At 3 months after the mass spawning, 71 corals
were observed on the 61 recovered sticks (18 corals
among the 32 cylindrical sticks, 53 corals among the
29 square sticks). We assumed that the 70 sticks left
in the sea after the 3 months were thought to keep
269
nearly the same number of corals as the 61 sticks
recovered, however, only three corals were
observed on the sticks after 1 year. The reason why
this decrease occurred is thought to be lethal high
water temperatures in summer 2001 (as shown in
Fig. 6) and the size of the horizontal holes. The size
of the holes, 4 mm in diameter and 5 mm deep, was
determined by estimating the smallest size in which
coral larvae could settle. In earlier experiments with
settlement plates before this experiment, corals set-
tled on the undersides of it within 15–20 mm from
the edge (S. Nojima & M. Okamoto, unpubl. data,
2001). Therefore, a 5 mm deep hole is thought prob-
ably too shallow for growing corals to survive from
predation and other natural causes. Thus, deeper
holes in the stick’s sides may be required. Screening
placed over the frames to keep away predators is a
possibility for increasing survival. This is a standard
aquaculture practice but might require more study
in the case of coral. Another possible procedure
method for increasing the survival rate of juvenile
coral is to move the frame with the sticks to a grow-
out facility where temperature can be controlled
and predators excluded.
An additional advantage of using sexual repro-
duction from the mass spawning event is that the
coral larvae settle in proportion to the species
composition of the original coral community. As
indicated in this experiment, after 3 months, 72–
96% of the corals settled on the sticks and plates
were Acroporidae; the numerically dominant coral
and major mass spawning species in the natural
community around the experimental site. This
means that the majority of coral species involved
in the mass spawning could be settled successfully,
and those larvae would most likely be settled on
the settlement sticks and plates.
Corals are thought to have some potential to
acclimatize to elevated temperatures24 and, if so,
moving the juvenile coral to an applicable depth
and location25 in the Sekisei lagoon would give the
coral time to adapt to rising sea temperatures.3
Although we have not yet perfected the tech-
nique for using the natural phenomenon of mass
spawning to provide coral for transplantation, we
are working towards that end.
ACKNOWLEDGMENT
The authors wish to thanks Mr. I. Oguro, retired
diving superintendent of JAMSTEC, and Mr. M.
Yarabu, master diver of diving service Marine
Point, for their technical assistance, and Professor
W. Sakamoto, Kinki University, and Professor T.
Sugimoto, Tokai University, for helpful suggestions
on this experiment.
270 FISHERIES SCIENCE
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