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Deep-Sea Research II 96 (2013) 13–18

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Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2

The distribution and diversity of sea cucumbers in the coral reefs


of the South China Sea, Sulu Sea and Sulawesi Sea
Sau Pinn Woo n, Zulfigar Yasin, Siti Hasmah Ismail, Shau Hwai Tan
Marine Science Lab, School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia

art ic l e i nf o a b s t r a c t

Available online 25 April 2013 A study on the distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu
Keywords: Sea and Sulawesi Sea was carried out in July 2009. The survey was done using wandering transect
Diversity underwater with SCUBA. Twelve species of sea cucumber were found from four different families and
Holothuroidea nine genera. The most dominant family was Holothuriidae (five species), followed by Stichopodidae
Substrate (three species), Synaptidae (three species) and Cucumariidae with only one species. The most dominant
Depth species found around the island was Pearsonothuria graffei, which can be found abundantly on substrate
Coral reef of dead corals in a wide range of depth (6–15 m). The Sulawesi Sea showed a higher diversity of sea
cucumber with seven different species compared to the South China Sea with only six different species
and Sulu Sea with only two species. Ordination by multidimensional scaling of Bray–Curtis similarities
clustered the sampling locations to three main clusters with two outgroups. Previous studies done
indicated a higher diversity of sea cucumber as compared to this study. This can be indication that the
population and diversity of sea cucumbers in the reef is under threat.
& 2013 Elsevier Ltd. All rights reserved.

1. Introduction cucumber are particularly vulnerable to anthropogenic threat of


habitat degradation and overfishing due to effectiveness and increase
Sea cucumbers are an abundant and diverse group of worm- intensity of harvesting. Therefore there is a lot of fishing pressure on
like and usually soft-bodied echinoderm. They are categorized sea cucumbers and generally research on the biology and ecology of
in the Class Holothuroidea and are distributed throughout the commercially important sea cucumber species is crucial in strategizing
world's ocean with about 1500 species from 25 different families the management of sea cucumber stocks (Choo, 2004). In terms of the
(Toral-Granada, 2005). They can be found in almost all marine condition of coral reefs, sea cucumber is potential to be used as a
environments from the shallow intertidal area to the deepest floor biological indicator through the study of the diversity and distribution
of oceanic trenches. One of the earliest accounts of sea cucumbers of coral reef sea cucumber species as they are the benthic and reef
can be seen are isolated spicules from fossils of sea cucumber from dwelling animal.
the Silurian since 400 million years ago (Gilliand, 1992). Sea cucumber diversity in Malaysian waters has been dealt
In Malaysia, sea cucumbers are one of the important sea products with in several publications. Previous studies concentrated at coral
that fetches high price. They were considered as a delicacy especially reefs along the coastal area of the east coast of Peninsular Malaysia
among the Chinese communities. Sea cucumbers are also used in which is the southern part of the South China Sea by Baine
traditional medicinal ointment product called locally as ‘Minyak and Forbes (1998), Massin et al. (2002), Sim et al. (2008a,
Gamat’ (Choo, 2004). Sea cucumber from the Stichopdiidae family 2008b), Zulfigar et al. (2008). Among them were George and
are used to produce this ointment where it is reported for their George (1987), Kamarul et al. (2009). Most reports focuses on
medicinal properties in a variety of circumstances such as the the diversity at the Peninsular Malaysia and there is a lack of
treatment of wounds and their chemical composition has been found information at the Sulu and Sulawesi Seas which sits in the center
to be useful in reducing artharalgia and the saponins in sea cucumbers of maximum biodiversity (Hoeksema, 2007; Veron et al., 2009)
have anti-flammatory and anticancer properties (Awaluddin, 2001). and are part of the Coral Triangle Initiative for protection of coral
Uthicke and Benzie (2000) pointed that the population of sea reefs and marine resources. The increase of fishing pressure of
sea cucumber at the coastal waters of Sulu and Sulawesi Sea
n
Corresponding author. Tel.: +60 17 9020611.
inflict much change to species composition in the shallow reefs.
E-mail address: abe_woo@hotmail.com (S.P. Woo). Therefore this study attempts to review the knowledge on

0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.dsr2.2013.04.020
14 S.P. Woo et al. / Deep-Sea Research II 96 (2013) 13–18

the distribution and diversity of sea cucumbers at the reefs descriptions of species done by Clark and Rowe (1971), Massin
of the central-eastern of the South China Sea and the Sulu- et al. (2002) and Zulfigar et al. (2008).
Sulawesi Sea.

3. Results
2. Methodology
The result from this survey was shown in Table 2. Sea
This study was done during the Prime Scientific Voyage 2009 cucumbers from four families and nine genera were found in this
from the July 3rd to 29th, 2009. A survey of sea cucumber employing study. The most dominant family observed was Holothuriidae with
wandering transects were done by SCUBA diving in selected reefs as five species, followed by Synaptidae and Stichopodidae with three
shown in Fig. 1 up to the depth of 30 m. The numbers of individuals species each and Cucumariidae with the least number of species with
of all species found along transects and the estimated distances of only one species found. The most abundant species found in the
area surveyed (Table 1) were recorded underwater. The total number South China Sea was Pearsonothria graffei in Terumbu Mantanani and
of individual of the same species was then converted into relative Synaptula lamperti in Terumbu Siput both with three individuals per
abundance unit (individual per 100 m2) by dividing the total number 100 m2. Whereas in the Sulawesi seas, P. graffei and Bohadscia argus
of the same species to the estimated area coverage (Woo et al., 2010). were equally abundant with two individuals per 100 m2 found. There
Species that could not be identified were collected using labeled
sampling bags and brought back to the laboratory for further
Table 1
identifications. The ecological notes of depth and type of substrate
The number of sites and total area cover surveyed at each sampling location.
where the samples found were recorded. Type of substrate categories
were sand, dead coral, live coral, rock, seagrass, coral rubble and Sea Site no. Location Number Total area
sponges. Multivariate analyses were carried out using Bray–Curtis of site cover
index and ordination by non-metric multidimensional scaling using
South China 1 Pulau Layang-layang 3 300
Community Analysis Package Version 4.0 (Henderson and Seaby, Sea 2 Terumbu Ubi 1 100
2007). 3 Terumbu Peninjau 1 90
Species that could not be identified were collected using 4 Terumbu Siput 2 200
labeled sampling bags and brought back to the laboratory for 5 Terumbu 1 110
6 Mantanani
further identifications using spicule analysis. Specimens collected
were anesthetised using sea water added with menthol crystal to Sulu Sea 7 Pulau Banggi 2 180
8 Bilean 1 90
ensure all tube feet and papillae remain extent during preserva-
9 Pulau Lankayan 2 220
tion. Color photographs of living specimens were then taken
to assist identification process because the color and shape of Sulawesi Sea 11 Pulau Mabul 3 320
12 Pulau Kapalai 3 290
samples may change after preservation. Samples were then pre-
13 Pulau Sipadan 4 400
served in 95% alcohol. Identification was then done by using

Fig. 1. Map of survey locations during the Prime Scientific Voyage 2009 (Locations: 1¼ Pulau Layang-layang, 2¼ Terumbu Ubi, 3¼ Terumbu Peninjau, 4¼ Terumbu Siput,
5¼ Terumbu Mantanani, 6¼Pulau Banggi, 7¼ Bilean, 8¼ Pulau Lankayan, 9¼ Mumiang, 10¼ Pulau Mabul, 11¼ Pulau Kapalai, and 12¼Pulau Sipadan).
S.P. Woo et al. / Deep-Sea Research II 96 (2013) 13–18 15

Table 2
Diversity and abundance of sea cucumber (Locations: 1¼ Pulau Layang-layang, 2¼ Terumbu Ubi, 3¼ Terumbu Peninjau, 4 ¼Terumbu Siput, 5¼ Terumbu Mantanani, 6¼ Pulau
Banggi, 7¼ Bilean, 8 ¼Pulau Lankayan, 9¼ Mumiang, 10¼ Pulau Mabul, 11¼ Pulau Kapalai, 12 ¼Pulau Sipadan) and types of substrate in the South China Sea, Sulu Sea and
Sulawesi Sea.

Species Number of individuals per 100 m2 Number Substrate


of locations
South China Sea Sulu Sea Sulawesi Sea

1 2 3 4 5 6 7 8 9 10 11 12

Family Cucumariidae
Colochirus robustus – – – – – – – – – 1 – – 1 Live coral

Family Synaptidae
Euapta godeffroyi – – – – – – 1 – – – – – 1 Sand
Synaptula lamperti – – – 3 – – – – – 1 – – 2 Sponge
Synapta maculata 1 – – – – – – – – – – – 1 Sand

Family Holothuriidae
Bohadscia argus – – – – – – – – – 1 – 2 2 Sand and coral
Bohadscia marmorata 1 – – – – – – 1 – – – – 2 Sand
Holothuria leucospilota – 1 1 – – – – – – 1 – 1 4 Sand
Holothuria edulis – – – – – – – – – 1 – 1 2 Sand
Pearsonothuria graffei – – 2 – 3 – – – – 2 2 – 4 Dead coral

Family Stichopodidae
Stichopus vastus – – – – – – – 1 – – – – 1 Sand
Thelenota ananas 1 – – – – – – – – – – – 1 Dead coral
Thelenota anax – – – – – – – – – 1 1 – 2 Dead coral

Total species for each site 3 1 2 1 1 0 1 2 0 7 2 3

No. of individual/100 m2 1 1 2 3 1 0 1 1 0 1 2 1

Fig. 2. The diversity and abundance of sea cucumber in the different sampling locations of the South China Sea, Sulu Sea and Sulawesi Sea.

was no distinctive dominance of species in the Sulu Sea due to the 4. Discussion
very low abundance found with only three species in all the sampling
locations surveyed. Pulau Mabul has the highest diversity of sea The high diversity in the Sulawesi Sea was mostly contributed
cucumber with seven different species observed during the survey as by the seven different species found in Pulau Mabul. During this
shown in Fig. 2. study, Pulau Mabul was surveyed more intensively compared to
Fig. 3 showed that both the South China Sea and Sulawesi Sea the other reefs. Four main reefs were surveyed for sea cucumber in
shared the equal number of diversity of sea cucumbers with a total Pulau Mabul compared to other locations where only one to two
of seven species found as compared to the Sulu Sea with only three reefs were surveyed. Though there was higher diversity in Pulau
species found. In terms of total abundance, the Sulu and Sulawesi Mabul, Pulau Sipadan and Pulau Kapalai, the number of indivi-
recorded very low number of samples per 100 m2 as compared to duals per 100 m2 was low ranging from one to two individuals
South China Sea with a higher abundance of five individuals per only. This may be due to the excessive harvesting especially sea
100 m2 area surveyed. The substrate type for each species of sea cucumbers in the intertidal area by the sea gypsies (Travis, 2003)
cucumber was very specific. Most sea cucumbers were distributed at Pulau Mabul as one of their source of income and food.
in sand (44%) and dead coral (39%). This was followed by sponge Though the reefs in the South China Sea have lower diversity,
(13%) and live coral (4%) as shown in Fig. 4. the reefs generally have higher abundance of sea cucumber per
16 S.P. Woo et al. / Deep-Sea Research II 96 (2013) 13–18

A comparison was done with previous studies as shown in


Table 3 where all previous studies listed were done at the South
China Sea and there were yet any data discerning the diversity and
distribution of sea cucumber at the Sulu and Sulawesi Sea
particularly at the islands within Malaysian borders except one
by George and George (1987). The number of species found in
previous studies (Table 3) has relatively higher number of species
compared to this study because most of the records done were
from shallow reefs of islands in the southern part of the South

Table 3
Comparisons of species of sea cucumber reported by other authors in South China
Sea and Sulawesi Sea (1 ¼Baine and Forbes (1998), 2¼ Boss et al. (1999), 3 ¼Zulfigar
and Tan (1999), 4¼ Zulfigar et al. (2000), 5¼ Zainuddin and Forbes (2000),
6¼Massin et al. (2002), 7¼ Sim et al. (2008a), 8¼Sim et al. (2008b), 9¼ George
and George (1987)). No historical record for Sulu Sea.

Fig. 3. The diversity and abundance of sea cucumber grouped according to


South China Sea Sulawesi Sea
different seas.
Species This 9
This
1 2 3 4 5 6 7 8
study study

Actinopyga echinites – – –
Actinopyga lecanora – – – – – – –
Actinopyga miliaris – – – –
Actinopyga obesa –
Actinopyga mauritania – –
Bohadscia paradoxa –
Bohadscia marmorata – – – – – – – –
Bohadscia argus – – – – – – – –
Bohadscia bivittata –
Bohadscia vitienensis –
Colochirus robustus – –
Euapta godeffroyi – –
Holothuria arenicola –
Holothuria atra – – – – – – –
Holothuria coluber – – –
Holothuria edulis – – – – – – – – –
Holothuria

flavomaculata
Fig. 4. The percentages of the sea cucumber collected from the different substrates. Holothuria hilla – – – – –
Holothuria nobilis –
Holothuria pulla – –
100 m2 ranging from one to three individuals. This was because Holothuria pardalis – –
Holothuria parvicax –
there was lower fishing activities in the reefs of the South China
Holothuria impatiens – – –
Sea since strict regulations and security monitoring were imposed Holothuria scabra –
at the reefs due to overlapping of soverign claims by several Holothuria leucospilota – – – – – –
countries including Malaysia (Asri et al., 2009). The low diversity Labiodemas

and abundance of sea cucumber in the areas of the Sulu Sea can be semperianum
Neothyonidium
attributed to the severe destruction of the coral reefs. The reefs in –
magnum
the Sulu Sea experience a very heavy fishing pressure including Pearsonothuria graffei – – – – – – – – –
methods that were destructive to the reef. Although fish bombing Pseudocolochirus

was an illegal fishing method, locals still practise it due to the violaceus
Stichopus chloronotus – – – – – – – –
lack of enforcement causing serious damage of the reefs surveyed
Stichopus ocellatus –
especially in Pulau Banggi (Teh et al., 2005). The changes of the Stichopus hermanni – – – – – –
health as well as the coral cover at Pulau Banggi were immense Stichopus horrens – – – – – – –
within 5 years when Koh et al. (2002) characterized the south and Stichopus
– –
southeast of Pulau Banggi with high coral coverage (63.0% live rubermaculosus
Stichopus variegatus – – – –
coral) and light anthropogenic impacts but Teh and Cabanban
Stichopus vastus – – – –
(2007) reported poor coral cover (15.0% live coral) within the same Synapta maculata – – –
area of survey with overexploitation, destructive fishing bombing Synapta recta – –
activities and improper waste management caused extensive Synaptula lactea –
Synaptula media –
damage to coral cover within the five years gap of study. There
Synaptula reticulata –
were two blasts heard within the total duration of 90 min of Synaptula virgata –
survey in Pulau Banggi. Fragments of coral covered with algae Synaptula lamperti – – – – – –
due to fish bombing were observed underwater. The absence of Thelenota ananas – – – – – – – –
sea cucumbers in Pulau Banggi was also reported by Ismail et al. Thelenota anax – – – – –
Thelenota rubralineata –
(1999). Apart from fish bombing, habitat destruction was also
Opheodesoma clarki –
observed in the reef of Mumiang. Anchor dredges and bottom Polypectana kefersteini –
trawling trails were observed rendering the poor habitat condition
Total species 12 17 2 23 16 17 6 20 20 7 20
for the sea cucumbers around that reef.
S.P. Woo et al. / Deep-Sea Research II 96 (2013) 13–18 17

3
2
1 11

8
10

12

Stress: 0.0073677

Fig. 5. Two-dimensional multidimensional scaling of sea cucumber diversity and abundance of sampling locations (Locations: 1 ¼ Pulau Layang-layang, 2 ¼Terumbu Ubi,
3¼ Terumbu Peninjau, 4 ¼Terumbu Siput, 5¼ Terumbu Mantanani, 7¼ Bilean, 8¼ Pulau Lankayan, 10¼Pulau Mabul, 11¼ Pulau Kapalai, and 12¼ Pulau Sipadan) super-
imposed with the different water bodies.

China Sea which were part of Malaysian's marine protected area Oceanography, Ministry of Science, Technology and Innovation,
(MPA) which restricts harvesting and were protected from anthro- Malaysia (Program Pelayaran Saintifik Perdana Grant) and RU Grant
pogenic damages. The species C. robustus was only found in the (Determination of the Distribution and Diversity of Holothurians and
Sulawesi Sea and was never observed in any other survey done in Nudibranchs on the Sulu-Sulawesi Sea) for the funding support.
the South China Sea but was observed by George and George We would also like to thank Universiti Sains Malaysia (USM) and
(1987) in the Sulu Sea may implies that the Sulu Sea act as a Universiti Malaya (UM) for their assistance during our diving
species boundary for the colonization of C. rosbustus. Fig. 5 showed activities.
the two-dimensional scaling configuration of the diversity and
abundance of sea cucumber found all the sampling locations super-
imposed with the different water bodies (South China Sea, Sulu Sea
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