The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea

The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea

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Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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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

Keywords: Diversity Holothuroidea Substrate Depth Coral reef

a b s t r a c t A study on the distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea was carried out in July 2009. The survey was done using wandering transect underwater with SCUBA. Twelve species of sea cucumber were found from four different families and nine genera. The most dominant family was Holothuriidae (five species), followed by Stichopodidae (three species), Synaptidae (three species) and Cucumariidae with only one species. The most dominant species found around the island was Pearsonothuria graffei, which can be found abundantly on substrate 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 Sea cucumbers are an abundant and diverse group of wormlike and usually soft-bodied echinoderm. They are categorized in the Class Holothuroidea and are distributed throughout the world's ocean with about 1500 species from 25 different families (Toral-Granada, 2005). They can be found in almost all marine environments from the shallow intertidal area to the deepest floor of oceanic trenches. One of the earliest accounts of sea cucumbers can be seen are isolated spicules from fossils of sea cucumber from the Silurian since 400 million years ago (Gilliand, 1992). In Malaysia, sea cucumbers are one of the important sea products that fetches high price. They were considered as a delicacy especially among the Chinese communities. Sea cucumbers are also used in traditional medicinal ointment product called locally as ‘Minyak Gamat’ (Choo, 2004). Sea cucumber from the Stichopdiidae family are used to produce this ointment where it is reported for their medicinal properties in a variety of circumstances such as the treatment of wounds and their chemical composition has been found to be useful in reducing artharalgia and the saponins in sea cucumbers have anti-flammatory and anticancer properties (Awaluddin, 2001).

n

Corresponding author. Tel.: +60 17 9020611. E-mail address: [email protected] (S.P. Woo).

Uthicke and Benzie (2000) pointed that the population of sea cucumber are particularly vulnerable to anthropogenic threat of habitat degradation and overfishing due to effectiveness and increase intensity of harvesting. Therefore there is a lot of fishing pressure on sea cucumbers and generally research on the biology and ecology of commercially important sea cucumber species is crucial in strategizing the management of sea cucumber stocks (Choo, 2004). In terms of the condition of coral reefs, sea cucumber is potential to be used as a biological indicator through the study of the diversity and distribution of coral reef sea cucumber species as they are the benthic and reef dwelling animal. Sea cucumber diversity in Malaysian waters has been dealt with in several publications. Previous studies concentrated at coral reefs along the coastal area of the east coast of Peninsular Malaysia which is the southern part of the South China Sea by Baine and Forbes (1998), Massin et al. (2002), Sim et al. (2008a, 2008b), Zulfigar et al. (2008). Among them were George and George (1987), Kamarul et al. (2009). Most reports focuses on the diversity at the Peninsular Malaysia and there is a lack of information at the Sulu and Sulawesi Seas which sits in the center of maximum biodiversity (Hoeksema, 2007; Veron et al., 2009) and are part of the Coral Triangle Initiative for protection of coral reefs and marine resources. The increase of fishing pressure of sea cucumber at the coastal waters of Sulu and Sulawesi Sea inflict much change to species composition in the shallow reefs.

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Please cite this article as: Woo, S.P., et al., The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.020

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Therefore this study attempts to review the knowledge on the distribution and diversity of sea cucumbers at the reefs of the central-eastern of the South China Sea and the SuluSulawesi Sea.

descriptions of species done by Clark and Rowe (1971), Massin et al. (2002) and Zulfigar et al. (2008).

3. Results 2. Methodology This study was done during the Prime Scientific Voyage 2009 from the July 3rd to 29th, 2009. A survey of sea cucumber employing wandering transects were done by SCUBA diving in selected reefs as shown in Fig. 1 up to the depth of 30 m. The numbers of individuals of all species found along transects and the estimated distances of area surveyed (Table 1) were recorded underwater. The total number of individual of the same species was then converted into relative abundance unit (individual per 100 m2) by dividing the total number of the same species to the estimated area coverage (Woo et al., 2010). Species that could not be identified were collected using labeled sampling bags and brought back to the laboratory for further identifications. The ecological notes of depth and type of substrate where the samples found were recorded. Type of substrate categories were sand, dead coral, live coral, rock, seagrass, coral rubble and sponges. Multivariate analyses were carried out using Bray–Curtis index and ordination by non-metric multidimensional scaling using Community Analysis Package Version 4.0 (Henderson and Seaby, 2007). Species that could not be identified were collected using labeled sampling bags and brought back to the laboratory for further identifications using spicule analysis. Specimens collected were anesthetised using sea water added with menthol crystal to ensure all tube feet and papillae remain extent during preservation. Color photographs of living specimens were then taken to assist identification process because the color and shape of samples may change after preservation. Samples were then preserved in 95% alcohol. Identification was then done by using

The result from this survey was shown in Table 2. Sea cucumbers from four families and nine genera were found in this study. The most dominant family observed was Holothuriidae with five species, followed by Synaptidae and Stichopodidae with three species each and Cucumariidae with the least number of species with only one species found. The most abundant species found in the South China Sea was Pearsonothria graffei in Terumbu Mantanani and Synaptula lamperti in Terumbu Siput both with three individuals per 100 m2. Whereas in the Sulawesi seas, P. graffei and Bohadscia argus were equally abundant with two individuals per 100 m2 found. There

Table 1 The number of sites and total area cover surveyed at each sampling location. Sea

Site no.

Location

Number of site

Total area cover

South China Sea

1 2 3 4 5 6

Pulau Layang-layang Terumbu Ubi Terumbu Peninjau Terumbu Siput Terumbu Mantanani

3 1 1 2 1

300 100 90 200 110

Sulu Sea

7 8 9

Pulau Banggi Bilean Pulau Lankayan

2 1 2

180 90 220

Pulau Mabul Pulau Kapalai Pulau Sipadan

3 3 4

320 290 400

Sulawesi Sea

11 12 13

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).

Please cite this article as: Woo, S.P., et al., The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.020

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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. Number of individuals per 100 m2

Species

South China Sea

Sulu Sea

Number of locations

Substrate

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 Synaptula lamperti Synapta maculata

– – 1

– – –

– – –

– 3 –

– – –

– – –

1 – –

– – –

– – –

– 1 –

– – –

– – –

1 2 1

Sand Sponge Sand

Family Holothuriidae Bohadscia argus Bohadscia marmorata Holothuria leucospilota Holothuria edulis Pearsonothuria graffei

– 1 – – –

– – 1 – –

– – 1 – 2

– – – – –

– – – – 3

– – – – –

– – – – –

– 1 – – –

– – – – –

1 – 1 1 2

– – – – 2

2 – 1 1 –

2 2 4 2 4

Sand and coral Sand Sand Sand Dead coral

Family Stichopodidae Stichopus vastus Thelenota ananas Thelenota anax

– 1 –

– – –

– – –

– – –

– – –

– – –

– – –

1 – –

– – –

– – 1

– – 1

– – –

1 1 2

Sand Dead coral 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 very low abundance found with only three species in all the sampling locations surveyed. Pulau Mabul has the highest diversity of sea cucumber with seven different species observed during the survey as shown in Fig. 2. Fig. 3 showed that both the South China Sea and Sulawesi Sea shared the equal number of diversity of sea cucumbers with a total of seven species found as compared to the Sulu Sea with only three species found. In terms of total abundance, the Sulu and Sulawesi recorded very low number of samples per 100 m2 as compared to South China Sea with a higher abundance of five individuals per 100 m2 area surveyed. The substrate type for each species of sea cucumber was very specific. Most sea cucumbers were distributed in sand (44%) and dead coral (39%). This was followed by sponge (13%) and live coral (4%) as shown in Fig. 4.

4. Discussion The high diversity in the Sulawesi Sea was mostly contributed by the seven different species found in Pulau Mabul. During this study, Pulau Mabul was surveyed more intensively compared to the other reefs. Four main reefs were surveyed for sea cucumber in Pulau Mabul compared to other locations where only one to two reefs were surveyed. Though there was higher diversity in Pulau Mabul, Pulau Sipadan and Pulau Kapalai, the number of individuals per 100 m2 was low ranging from one to two individuals only. This may be due to the excessive harvesting especially sea cucumbers in the intertidal area by the sea gypsies (Travis, 2003) at Pulau Mabul as one of their source of income and food. Though the reefs in the South China Sea have lower diversity, the reefs generally have higher abundance of sea cucumber per

Please cite this article as: Woo, S.P., et al., The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.020

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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 different seas.

South China Sea Species

Fig. 4. The percentages of the sea cucumber collected from the different substrates.

100 m2 ranging from one to three individuals. This was because there was lower fishing activities in the reefs of the South China Sea since strict regulations and security monitoring were imposed at the reefs due to overlapping of soverign claims by several countries including Malaysia (Asri et al., 2009). The low diversity and abundance of sea cucumber in the areas of the Sulu Sea can be attributed to the severe destruction of the coral reefs. The reefs in the Sulu Sea experience a very heavy fishing pressure including methods that were destructive to the reef. Although fish bombing was an illegal fishing method, locals still practise it due to the lack of enforcement causing serious damage of the reefs surveyed especially in Pulau Banggi (Teh et al., 2005). The changes of the health as well as the coral cover at Pulau Banggi were immense within 5 years when Koh et al. (2002) characterized the south and southeast of Pulau Banggi with high coral coverage (63.0% live coral) and light anthropogenic impacts but Teh and Cabanban (2007) reported poor coral cover (15.0% live coral) within the same area of survey with overexploitation, destructive fishing bombing activities and improper waste management caused extensive damage to coral cover within the five years gap of study. There were two blasts heard within the total duration of 90 min of survey in Pulau Banggi. Fragments of coral covered with algae due to fish bombing were observed underwater. The absence of sea cucumbers in Pulau Banggi was also reported by Ismail et al. (1999). Apart from fish bombing, habitat destruction was also observed in the reef of Mumiang. Anchor dredges and bottom trawling trails were observed rendering the poor habitat condition for the sea cucumbers around that reef.

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 Holothuria hilla Holothuria nobilis Holothuria pulla Holothuria pardalis Holothuria parvicax Holothuria impatiens Holothuria scabra Holothuria leucospilota Labiodemas semperianum Neothyonidium magnum Pearsonothuria graffei Pseudocolochirus violaceus Stichopus chloronotus Stichopus ocellatus Stichopus hermanni Stichopus horrens Stichopus rubermaculosus Stichopus variegatus Stichopus vastus Synapta maculata Synapta recta Synaptula lactea Synaptula media Synaptula reticulata Synaptula virgata Synaptula lamperti Thelenota ananas Thelenota anax Thelenota rubralineata Opheodesoma clarki Polypectana kefersteini Total species

This study

Sulawesi Sea

1

2 3

4

– – –

– – – –

– –

5

6 7

8

– –

– – –



This study

– –



– –

– –

– – –

– – – – –

– –

– – –

– –

– – – –

9





– –





– – –

– – –









– –



– –





– – –

– –

– –













– – –



– – –















– – – – – – –







– –









– –

– –

– –

– –

– –

– –

– –

– –





– –







– – –

– – –



– –



– –

– – –

– – – –



– – – –



– – 12

17 2 23 16 17 6 20 20 7

20

Please cite this article as: Woo, S.P., et al., The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.020

S.P. Woo et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

5

5 3

2

1

11

8 10 12 7

4

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) superimposed with the different water bodies.

China Sea which were part of Malaysian's marine protected area (MPA) which restricts harvesting and were protected from anthropogenic damages. The species C. robustus was only found in the Sulawesi Sea and was never observed in any other survey done in the South China Sea but was observed by George and George (1987) in the Sulu Sea may implies that the Sulu Sea act as a species boundary for the colonization of C. rosbustus. Fig. 5 showed the two-dimensional scaling configuration of the diversity and abundance of sea cucumber found all the sampling locations superimposed with the different water bodies (South China Sea, Sulu Sea and Sulawesi Sea). The clustering implies the similarity of species diversity and distribution found in each of the locations. Bilean and Terumbu Siput were found to be offset position from the three other major clusters due to the presence of only one species at the location and the species were considered rare as it was not found in other sampling locations such as E. godeffroyi at Bilean. The other major clusters showed similarities in their species composition but there was no pattern indicating that the different water bodies were correlated with the distribution and diversity of sea cucumbers. Microhabitat specialization has been suggested to be the main method of food partitioning among detritivores (Kohn, 1971) and determine the types of substrate sea cucumbers were found. Kerr et al. (1993) found that some sea cucumbers can be found at more than one type of substrate. In this study, the type of species always correlate to the same and specific types of substrate they were found. Woodby et al. (2000) found that sea cucumbers prefer harder substrate like sand, rocks and dead corals due to their locomotion that uses tube feet to adhere to the substrate. This was in congruence with this study that found most sea cucumbers at sand and dead corals. S. lamperti was specifically found associate to sponges due to their ability to gain nutrition and assimilating exudates from the sponge (Hammond and Wilkinson, 1985). A comprehensive survey is needed to assess the condition of the reef especially in the Sulu Sea to enable proper management strategy to be put in place to conserve the reefs as well as other marine resources from threat of habitat destruction.

Acknowledgments We would like to thank the Royal Malaysian Navy for kindly providing us ship services and accommodations during the Prime Scientific Voyage 2009. Special thanks to National Directorate of

Oceanography, Ministry of Science, Technology and Innovation, Malaysia (Program Pelayaran Saintifik Perdana Grant) and RU Grant (Determination of the Distribution and Diversity of Holothurians and Nudibranchs on the Sulu-Sulawesi Sea) for the funding support. We would also like to thank Universiti Sains Malaysia (USM) and Universiti Malaya (UM) for their assistance during our diving activities.

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Please cite this article as: Woo, S.P., et al., The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.020