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Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
47
THE OCCURENCE OF TWO BLACK SEA CUCUMBER SPECIES
AT POMBO ISLAND, CENTRAL MALUKU, INDONESIA
Ana Setyastuti1*
1Research Center for Oceanography-LIPI
*Correspondence author: ana.setyastuti@gmail.com
Received: January 2015 Accepted: December 2015
ABSTRACT
The so-called “black sea cucumber”in Indonesia consists of several species, including Holothuria atra, H.
leucospilota, H. coluber, H. excellens and H. turriscelsa. The local community near Pombo Island
(Wainuru village) stated that most sea cucumbers inhabiting the island are the black sea cucumbers they
call “teripang hitam”which are sometimes eaten but not exploited excessively. The goals of the present
study are to identify the species of black sea cucumbers inhabiting Pombo Island and to map their local
distribution in order to get a further understanding of their specific habitat. Surveys were conducted twice,
in March and April 2014, which successfully obtained data on >550 individual black sea cucumbers from
two species: Holothuria (Halodeima) atra Jaeger, 1833 and Holothuria (Mertensiothuria) leucospilota
(Brandt, 1835). Mapping the local distribution of those two species showed that both are found only on
the south-east and south-west coast of the Island. This may relate to the availability of boulders and
stones as shelter areas and marine vegetation. Mapping shows H. atra has a wider distribution over
Pombo Island than H. leucospilota. However, H. Leucospilota is known by its semi-cryptic habit (hiding
its posterior body under rocks or crevices) making its distribution restricted to areas well-provided with
shelters.
Key words:Holothuria atra,Holothuria leucospilota, distribution, Pombo Island.
INTRODUCTION
Black sea cucumbers in Indonesia
consist of several species, including Holothuria
atra Jaeger, 1833; H. leucospilota (Brandt,
1835); H. coluber Semper, 1868; H. excellens
Ludwig, 1875; and H. turriscelsa Cherbonnier,
1980 (Purwati, 2005; Purwati & Wirawati, 2009;
Setyastuti, 2009; Setyastuti et al, 2014;
Setyastuti & Purwati, 2015). The first three
species were the most common in Indonesian
intertidal water while the lat two were recorded
only twice, in Spermonde and Situbondo
(Massin, 1999; Setyastuti et al., 2014). A study
of the distribution of Indonesian commercial sea
cucumbers by Purcell et al. (2012) and
Setyastuti et al., (2014) showed that the
geographic distribution of those black sea
cucumbers was mostly widespread in the Indo-
West Pacific (Fig. 1). Only H. excellens and H.
turriscelsa had a limited distribution. However,
they are probably much more widely distributed
than shown in the map, but that high
morphological resemblance between those
species and other holothuroidea species might
have caused misidentification while field
observation was being conducted.
Pombo Island is positioned on the
Haruku Straits, between the islands of Ambon
and Haruku. Administratively it is located in the
Central Maluku Regency (Fig. 2). In 1973,
Pombo was established as a marine park
sanctuary by an Agriculture Ministerial
regulation. Its conservation area covers 1000
hectares (including the Island, reef flats and
lagoon) and is uninhabited. The island runs
lengthwise from north east (NE) to south west
(SW). The Seram Sea lies to the north and the
Banda Sea to the south (Fig. 3). The intertidal
zone on the north coast is the only open area of
white sandy substrate without any vegetation;
on the east coast is a dead coral flat with a white
sandy substrate, boulders and rocks. The only
vegetation is seaweed of Sargassum sp., in
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
48
patches. The intertidal area on south coast has a
similar geomorphology to the east coast but it is
more extensive, and the vegetation includes not
only Sargassum sp., but also Padina sp., (Fig. 4).
Massin (1996) states that Ambon Isl. is
in a zone where the marine fauna is the richest
in the Indo-Pacific region. This means that the
possibility of finding more species is to be
expected since the islands of Pombo, Haruku
and Saparua, together with Ambon, geologically
form a group of islands.
The local community near Pombo
Island (Wainuru village) stated that most sea
cucumbers inhabiting Pombo Isl. are the black
sea cucumbers called “teripang hitam”. This
black sea cucumber is sometimes eaten but not
exploited excessively.
We present evidence confirming that
two species of black sea cucumbers inhabit
Pombo Isl. and created a map of their local
distribution in order to provide further
understanding about their specific microhabitat.
This information is important as biodiversity
data and for the sustainable management of
these species.
MATERIALS AND METHODS
The black sea cucumbers studied were
those inhabiting the intertidal zone of Pombo
Island (Fig. 2). Surveys were conducted twice,
on 20-21 March and 15-16 April 2014,
respectively.
Species confirmation
Samples of sea cucumber were identified by
observing the characteristics of their external
bodies and examined the ossicles from the body
wall, tentacle, dorsal papillae and ventral tube
feet. Ossicles needed to be isolated prior to
examination. Small pieces (1-5 mm2) of each
part of the body were rinsed, put on a slide and
dipped in several drops of NaClO for 5-10
minutes. Afterward, they were rinsed (4-7 times)
with several drops of distilled water, and then
with 70% ethanol, ready to be observed under a
compound microscope.
Mapping of sea cucumber distribution
The method used to develop a
distribution map was modified from Visual
Encounter Surveys (Heyer et al., 1994). It
involved walking along the beach around the
island covering the area exposed at low tide.
This method was followed by mapping the
positions of individual black sea cucumbers
using a Global Positioning System (GPS) series
Garmin GPS map 60CS (Purwati, 2006; Purwati
& Syahailatua, 2008; Purwati et al., 2008). This
method avoided the problem of double-counting
the same individuals because specific location
of each of them has been documented. Using
this method might also help in understanding
the local distribution of each species inhabiting
the studied location. While tracking the sea
cucumber individuals, other information was
also collected: the body length of each individ.,
coordinates (way-points), species identity,
substrate type, water temperature and salinity.
The coordinates for each sea
cucumber’s position were analyzed and
mapped using ArcGis 10.1.
RESULTS
The black sea cucumbers at Pombo
Island consist of two species: Holothuria atra
and Holothuria leucospilota . These two species
can be distinguised from each other by several
characteristics as shown in Table 1, Fig. 5 and 6.
The color of H. atra is black, usually
covers itself with a coating of coral sand which
held in place by its podia. The integument is
thick and firm. It lacks a cuvierian organ and
thus can be handled without the annoyance of
adhesive threads, as described by Bonham &
Held (1963) but frequently it extrudes its
internal organs when stressed. H. leucospilota is
almost black in color, does not cover itself in
sand. The integument is softer with fine
protuberances giving a prickly appearance. It is
quickly expels the cuvierian organ during hand
contact. The ossicles in the integument (dorsal
and ventral) of the two species are different: in
H. atra the tables are tall and have no buttons,
while in H. leucospilota the tables are short and
squat and there are a lot of buttons (Rowe, 1969;
Clark & Rowe, 1971; Cannon & Silver, 1986;
Cherbonnier, 1988; Massin, 1996; Massin, 1999;
Samyn et al., 2006; Setyastuti, 2009; Setyastuti,
2013).
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Figure 1. Geographic distribution of the called “black sea cucumber”. Source A-D: Setyastuti et al.
(2014); Source E: Setyastuti (2009), Purcell et al. (2012).
Holothuria atra and H. leucospilota are
common species inhabiting the shallow water of
Pombo Island. They occupy the intertidal area
where beach rocks (or dead coral) are present and
also pools of water that are a few centimeters to
about one meter deep at low tide. The two species
were found only along the intertidal zone from the
east to the south of Pombo Isl. No H. atra or H.
leucospilota were found on the north to west coast
of the island during the observation.
Pombo Island is surrounded by an atoll
as shown in satellite images (Fig. 3). Inside the
atoll, at the north-western side of the island, there
is a deep pool like a narrow trench with an
approximate depth of more than 8 meters. The
pool is more like a sand valley, since as far as
could be seen there was only white sandy
substrate with no stones or boulders or even any
vegetation. Those were generally the conditions
on the north-western side of the island (Fig. 4A).
The habitat at the east to the south side of the
Island was quite different, where the presence of a
dead coral flat and white sandy substrate was
prominent. Several species of marine vegetation,
such as Sargassum spp. and Padina spp. were
found in patches (Fig. 4B-D). The number of each
species found in the areas studies, the length
distribution and local distribution are presented in
Table 2, Figure 7-9.
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Figure 2. Study site: Pombo Island on Haruku Straits, between Ambon Isl. and Haruku Isl., Central
Maluku. Dashed line shows the area observed.
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Figure 3. Satellite image of the atoll surrounding the Pombo Island (Source:
http://wikimapia.org/#lang=en&lat=-3.529184&lon=128.377476&z=16&m=bh)
Figure 4. Types of the intertidal zone of Pombo Isl. A: North part of west coast, B: East coast, C:
South coast, D: South part of east coast.
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Table 1. Morphology and behavior differences between Holothuria atra Jaeger, 1833 and Holothuria
leucospilota (Brandt, 1835). BW: body wall.
External morphology
Holothuria atra
Holothuria leucospilota
1.
Fresh BW color
Uniformly black
Uniformly ash-grey to black
2.
Preserved BW color
Uniformly black
Uniformly brown
3.
Cross section (live only)
Cylindrical
Cylindrical
4.
Lateral appearance
Straight
Straight
5.
Body wall texture
Soft, smooth
Soft, smooth
6.
Average thickness of BW
<5 mm
<10 mm
7.
Tentacle size
Short
Long
8.
Tentacle shape
Peltate, indentions shallow
Peltate with branches
9.
Number of tentacles
15-20
20
10.
Position of mouth
Ventral
Ventral
11.
Position of anus
Terminal
Terminal
12.
Collar around mouth
Absent
Absent, but prickly oral papillae
made them looks like a collar
around mouth
13.
Tube feet
Present
Present
14.
Arrangement of ventral
tube feet
Overall spreading (distributed
over the ventral side, not in
rows)
Mostly in radial areas, but some
also spread in interadial areas
15.
Arrangement of dorsal
papillae
Distributed over the dorsal side
Distributed over the dorsal side
Ossicles
Dorsal BW
Ventral BW
Dorsal BW
Ventral BW
1.
Tables
nd
2.
Rosettes
Absent
Absent
Absent
3.
Buttons
Absent
Absent
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4.
Rods
Absent
Absent
Absent
5.
Perforated plates
Absent
6.
Pseudo plates
Absent
Absent
Absent
7.
Large perforated plates
Absent
Absent
Absent
Note on behaviour
1
Body covering with sand
Usually with distinctive bare
spots
Sometimes
2
When capture
Usually in open area
Usually with anterior part
exposed and the posterior part
under a rock or dead
coral/crevices.
3
Solitary/aggregation
Usually found individually
Solitary and sometimes in an
aggregation
4
When stressed
Expel internal organ
Expel cuvierian tubulus
5
Reproduction
Sexual and asexual through
fission
Sexual and asexual through
fission
Table 2. Number of black sea cucumbers at each survey in Pombo Island.
Observation period
Trip 1 (20-21 March 2014)
Trip 2 (22-23 April 2014)
Holothuria (Halodeima) atra
Jaeger, 1833
158 individ.
319 individ.
Holothuria (Mertensiothuria)
leucospilota (Brandt, 1835)
65 individ.
24 individ.
Total
223 individ.
343 individ.
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Figure 5. Holothuria (Halodeima) atra Jaeger, 1833.
Figure 6. Holothuria (Mertensiothuria) leucospilota (Brandt, 1835).
Table 3. Physical parameters at Pombo Island during survey.
Observation time
Trip 1 (20-21 March 2014)
Trip 2 (22-23 April 2014)
Temperature
30C
29-30C
Salinity
34-35‰
33-35‰
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Figure 7. Length distribution of both species Holothuria atra Jaeger, 1833 and Holothuria leucospilota
(Brandt, 1835). Size categorization based on Setyastuti (2014): Small class (0-9.9 cm);
Medium class (10-30.99 cm) and Large class (≥31 cm).
Figure 8. Geographical position of Holothuria atra Jaeger, 1833 (158 individ.) and Holothuria
leucospilota (Brandt, 1835) (65 individ.) on Pombo waters in March-2014.
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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Figure 9. Geographical position of Holothuria atra Jaeger, 1833 (319 individ.) and Holothuria
leucospilota (Brandt, 1835) (24 individ.) on Pombo waters on April-2014.
DISCUSSION
Species confirmation
Holothuria atra Jaeger, 1833 and
Holothuria leucospilota (Brandt, 1835) have
morphological resemblances such as body color,
body shape and size. Furthermore, they were
frequently found together in the same habitat,
especially intertidal areas. In addition, they are
described as benthic, deposit feeder, detritus
feeder, inshore and tropical (Rowe & Gates,
1995). However, the detailed observations
showed that they could be distinguished based
on their morphologies and behaviors (Table 1).
Local distribution
Concerning the absence of individuals of
either species H. atra and/or H. leucospilota on
the NE coast of Pombo Isl., the possible reasons
may relate to: (1) the lack of shelter and food or
organic materials and the strong current in the
areas Those reasons were also suggested in the
studies by Bonham & Held (1963), Massin &
Doumen (1986), Conand & Mangion (2002),
Slater & Jeffs, (2010), Dissanayake &
Stefansson (2011). Shelter areas such as shelves
of rock along the beach will give an insulating
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
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effect, cooling the temperature of water runoff
during hot days and also providing protection
from high waves. Based on visual observation,
the NE coast has no shelter such shelves, rock
or dead coral, only a white sandy substrate. In
addition, this side is directly exposed to
northerly winds coming from the Seram Sea
that create high wave energy on the sandy beach.
However, there is no quantitative measurement
of the current, though visually it can perceived
that the current at this side is stronger than on
the opposite side (SE coast). Since this side has
no shelter areas that could reduce wave energy
from the ocean to the beach, this could be an
argument for the absence of any marine
vegetation or, in particular, any seagrass species.
This might impact on the level of deposits of
organic materials at this intertidal area. No
specific measurement was undertaken to
quantify the level of organic material during the
survey. Yet, literature which focuses on the
habitat preferences of sea cucumbers, concludes
that the presence of organic material is one of
the most important factors influencing the sea
cucumber’s choice of habitat (Dissanayake &
Steffansson, 2011; Purcell et al., 2009; Purcell,
2004; Conand & Mangion, 2002; Conand,
1990). Higher levels of organic material are
influenced by the presence of seagrasses,
because they can trap nutrients at their base
making the accumulation of particulate matter
and detritus higher (Komatsu et al., 2004;
Dissanayake & Steffansson, 2011).
All the individuals of black sea
cucumber found were on the south east (SE) to
south west (SW) coast only. The argument for
this distribution pattern must be the reverse of
the reason for the absence of black sea
cucumbers on the NE coast.
Geomorphologically, the SE to SW coast
offered better or more stable protection from the
high wave energy/currents, because most of the
area on this side is dead coral reef flat. The flat
is extensive with many spots of marine
vegetation. Therefore, despite this side being
directly exposed to the Banda Sea, which is
known to have high wave energy, conditions
there may offer a suitable substrate to reduce the
current flow. This condition similar with the
result of Zhou & Shirley (1996) that observed
high density of sea cucumber on the rock walls
of Barlow Cove-Southeast Alaska.Most of the
individuals of H. atra covered their bodies with
the white sandy substrate or rubble. It has been
suggested that the sand coating could reflect
light, thus enabling H. atra to have a slightly
lowered body temperature (Aziz, 1995). The
mapping of H. atra showed that they were only
found on the SE to SW coast of Pombo Island
(Fig. 7-8), usually in the open areas with sand or
beach rocks, or pools of water at low tide. The
highest frequency of H. atra was in the sandy-
rocky habitat with algae of Sargassum spp. and
Padina spp. These habitat preferences and the
aggregation of H. atra could be their self
defense against waves and currents, since they
were mostly found in the intertidal area
(Bonham & Held, 1963; Massin & Doumen,
1986; Conand & Mangion, 2002). H. atra
protects itself from the waves and currents by
maintaining its position in depressions and
holding onto the relatively smooth reef flat or
beach rock using its tube feet (Bonham & Held,
1963).
Another way was displayed by all
individuals of H. leucospilota in this study,
which were found underneath rocks or in a
holes in the reef floor. This result confirms the
finding of Massin & Doumen (1986) who never
found this species on dry surface, nor on living
corals or sites where there was high water
turbulence. They also noted this species
anchoring its posterior under shelter and
described it as a semi-cryptic habit.
The number of H atra in April 2014 was
more than twice than that of March 2014. This
can be explained by several possible reasons: (1)
More small to medium size individuals were
captured in April than in March (Fig. 7), and
careful observation showed that those small-
medium size individuals were showing signs of
having undergone asexual reproduction through
fission. Those individuals observed only had its
anterior part (A) and/or only had its posterior
part (P), and were only separated from each
other by a short distance (less than 0.5 m). The
other small size individuals were captured as Ap
specimens (showed signs of regenerating their
posterior part) and/or Pa specimen (showed
signs of regenerating their anterior part), several
specimens’Ap and Pa were separated by a
longer distance (about 1-1.5 m). Similar
observation was obatained by previous author
(Conand et al. (1997); Jaquemet et al. (1999);
Purwati (2001); Conand & Mangion (2002); and
Dwiono et al. (2008). (2) The abundance of sea
weed may take effect on sea cucumber
population only after a couple of months.
In contrast to H. atra, it found that the
number of H. leucospilota in April 2014 was
fewer than in March 2014. The reasons are
unknown, but the most likely reason is directly
Mar. Res. Indonesia Vol.40, No.2, 2015: 47−60
58
related to the hiding behavior of this species
under the boulders/stones/rocks and crevices as
shelter areas. The individuals might be moved
to other shelter areas that probably lack of
thoroughness during the sampling. This findings
of H. leucospilota’s behavior and type
distribution were similar to Purwati’s (2006)
observation in West Lombok, Indonesia.
Mapping (Fig. 8, 9) shows that the H.
atra was distributed more extensively than H.
leucospilota. The possible reason may be that
suitable living areas for H. atra were more
extensive than for H. leucospilota.H. atra do
not hide like H. leucospilota so they do not need
a specific place to live. In opposition, H.
leucospilota always anchors its posterior under
a stable rock or hole in the reef floor, making its
distribution more limited to specific places. This
finding was similar to the work of Bonham &
Held (1963) which conducted at Rongelap Atoll
and Massin & Doumen (1986) who observed in
the reef flat of Laing Island, Papua New Guinea
that the distribution of H. atra was broader and
the individual numbers were higher than those
of H. leucospilota. Other works, by
Dissanayake & Stefansson (2011) and Conand
& Mangion (2002), suggest that H. atra are
more able to live over a broader area in the
intertidal zone than any other Holothurian
species.
CONCLUSION
Pombo Island has two dominant
species of black sea cucumber: Holothuria atra
Jaeger, 1833 and Holothuria leucospilota
(Brandt, 1835). Those two species have a
morphological resemblance, but detailed
observation shows they are quite different. The
presence of H. atra was higher with wider
distribution than those of H. leucospilota.H.
atra were found in a broader area on the reef
flats with or without the presence of
boulders/rocks, while H. leucospilota was
captured only in areas where there were many
rocks or holes in the reef floor. Both H. atra and
H. leucospilota were found on the SE to SW
coast. This is an evidence that the availability of
shelter influence the distribution of sea
cucumbers in Pombo Island.
ACKNOWLEDGEMENT
This project is part of Coral Reef
Rehabilitation at Pombo Island, Maluku,
Indonesia which was funded by DIPA-LIPI
Ambon 2014. The author thanks Mr. Daniel
Pelasula as project coordinator, and the student
and technician who were involved in the project
for their assistance in the field. The author also
thanks to A.S. Adji (LIPI Ambon) and K.
Anggraeni (LIPI RC Oceanography) for their
assistance and discussion in data processing
using ArcGis, as well to Pradina Purwati, M.Sc,
A.J. Wahyudi, Prof. Dr. Suharsono, Dr. H.Y.
Sugeha, D.L. Rahayu for the discussion and
comments, also to the referees for their
invaluable corrections to the manuscript.
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