Conservation Status and Trends of Reef Invertebrates in Tubbataha Reefs with Emphasis on Molluscs and Sea Cucumbers - Roger G. Dolorosa
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Conservation Status and Trends of Reef
Invertebrates in Tubbataha Reefs with
Emphasis on Molluscs and Sea
Cucumbers
Roger G. Dolorosa
September 2010
2
ACKNOWLEDGMENTS
The completion of this report would have been very difficult without the
guidance, encouragement and support of my supervisors Prof. Alastair Grant and Dr.
Jennifer Gill. I am also very grateful to the support extended by my external
supervisor Dr. Benjamin J. Gonzales.
I would like also to thank the following members of the composite team of
Marine Park Rangers assigned at TRNP during the months of December 2009 -
January 2010, April -May 2010 and June - August 2010, whom without their
assistance, my fieldwork would have been very impossible to accomplish: Segundo
F. Conales, Jr. , Noel A. Bundal, Roy P. Magbanua , Julius A. Parcon, POIC Pedro
N. Gañalongo Jr., Federico V. Magbanua Jr., Patricio B. Mampay Jr., Amado T.
Cayabo, Romnick P. Molina, Roel Natividad, Jojie N. Solis, Sonny Tanay, POIC
Amelito A. Bungar, Zosimo I. Batacan, Jovanny Gonzales, Rod B. Patricio, Jayson
M. Villablanca, Rey Talavero, Luis Bundac, Renante Bonales, POIC Jonathan R.
Lopo, Napoleon Caballero, Javier E. Carceler, Quintin M. Fontanilla Jr., Ronnie
Calain, Glenn G. Redondo, Alexander T. Sanchez, and Laudemer Sansano.
I am also very grateful for the help and support of the following crew members
of the WWF’s M/V Navorca: Capt. Ronald de Roa, Darius Cayanan, Niño Rogalles,
Arnel Escubin, Jesus Gayoma, Jhun Magbanua and Abdon Dalanon.
Equally appreciated are the unconditional support of the Park Manager, Ms.
Angelique Songco and the following officers and staff of the TMO: Ma. Theresa R.
Aquino, Mary Grace D. Barber, Rowell C. Alarcon, Glenda G. Simon, Rochelle C.
Abdulla, Emmalyn N. Tura, Maria Retchie C. Pagliawan, Jose Majid A. Ibrahim ,
Edson S. Montenegro, Christine N. Longno, Jansen Jontilla and Jean Beth Jontilla.
Jennifer Selgrath provided the photos of T. anax and T. rubralineata. That of
Synaptula sp. was provided by Dr. Sabine Schoppe.
This research is supported in part by the Nagao Natural Environment
Foundation, the Ford Foundation International Fellowship Program, the University of
East Anglia, the Western Philippines University and the Tubbataha Management
Office.
Lastly, I would like to extend my warmest regards to everyone including those
whom I may have failed to mention but were instrumental in accomplishing this piece
of work.
RGD
3
SUMMARY
This report presents the current state of commonly encountered molluscs and
sea cucumbers at Tubbataha Reefs Natural Park (TRNP) in terms of abundance and
size structure. It also includes the growth and population trend of the Philippine
threatened reef gastropod Trochus niloticus. Modified Reef Check method was used
to assess the substrate and status of reef invertebrates in three types of habitat at
the seaward reef area (flat, boulder, complex). Distance sampling method was used
to determine sea cucumber abundance along the outer reef slope and drop off
areas. Depending on depth, sites were surveyed either by reef walking, snorkelling
or scuba diving. Fourteen of the 15 sampling sites were surveyed using modified
Reef Check and all 15 sites were covered with distance sampling. Samples of sea
cucumbers were collected and measured for length and live weight to establish
length-weight relationships.
Results showed that no definite pattern is noted on which type of habitat
trochus occur abundantly. Over all abundance of trochus at the North Islet and at the
park as a whole indicated that highest density was in boulder habitat (BH), but at the
South islet, highest abundance was recorded in complex habitat (CH). Larger
individuals were more common in CH. There were juveniles and few large individuals
in FH. Abundance trend was stable for sites close to the Ranger Station. In other
areas, density was a little lower than in the previous years. Abundance of other six
gastropods and six giant clam species occurred differently across three types of
habitat.
Sea cucumbers density obtained by distance sampling at the North Islet was
seven times higher than at the South Islet. In Jessie Beazley Reef, only two
individuals belonging to two species were recorded during the distance survey, but
two more species including the very rare Thelenota rubralineata was noted in the
deeper part of the wall. Abundance and species diversity was higher in gradually
sloping areas than in reef walls. Sea cucumbers were relatively big and in their
maximum sizes. High positive relationships between length and live weights were
noted among five sea cucumber species.
It appears that, among the invertebrates surveyed, only Trochus were
targeted by fishermen, causing its population to decline over the years. Although
Trochus recruitment was evident in exploited areas, populations of Trochus and
other macro benthic invertebrates at the park could be only enhanced through
stringent conservation measures. Survey of other potential reef invertebrate habitats
like the lagoon is suggested.
4
TABLE OF CONTENTS
ACKNOWLEDGMENTS ...................................................................................................................... 2
SUMMARY ............................................................................................................................................ 3
INTRODUCTION .................................................................................................................................. 6
RESEARCH METHODS ..................................................................................................................... 8
Study Site .......................................................................................................................................... 8
Data Gathering Procedure .............................................................................................................. 8
Species composition. ................................................................................................................... 8
Abundance and size structure .................................................................................................... 8
Growth of Trochus niloticus ........................................................................................................ 9
Length-weight relationships in sea cucumbers........................................................................ 9
RESULTS ............................................................................................................................................ 10
Habitat Characteristics .................................................................................................................. 10
Species Composition ..................................................................................................................... 10
Abundance ...................................................................................................................................... 10
Size Structure ................................................................................................................................. 11
Growth of Trochus niloticus .......................................................................................................... 12
Length-Weight Analyses ............................................................................................................... 12
DISCUSSION...................................................................................................................................... 14
LITERATURE CITED......................................................................................................................... 17
FIGURES ............................................................................................................................................. 20
Figure 1. The sampling sites. ....................................................................................................... 20
Figure 2. Substrate composition of the three types of habitat. ................................................ 21
Figure 3. Abundance of T. niloticus and T. pyramis in three types of reef habitat.............. 21
Figure 4. Abundance (ind.100m-2) of giant clams and sea cucumbers. ................................ 22
Figure 5. Average density of different invertebrates at TRNP. ............................................... 23
Figure 6. Size structure of T. niloticus per type of habitat........................................................ 23
Figure 7. Size structure of T. pyramis per type of habitat. ....................................................... 24
Figure 8. Size structure of T. crocea per type of habitat. ......................................................... 24
5 Figure 9. Size structure of T. maxima per type of habitat. ....................................................... 24 Figure 10. Size structure of Hippopus spp. per type of habitat. .............................................. 25 Figure 11. Average sizes (±sd) of Holothuria spp. at TRNP. .................................................. 25 Figure 12. Average sizes (±sd) of B. Argus, P. graeffei and S. chloronotus at TRNP. ....... 26 Figure 13. Average sizes (±sd) of three species of Thelenota at TRNP. .............................. 26 Figure 14. Growth trends of T. niloticus in and out of the lagoon at TRNP. ......................... 27 Figure 15. Abundance trend of T. niloticus at TRNP (2006-2010). ........................................ 27 TABLES ............................................................................................................................................... 28 Table 1. Number of 20 m transect per habitat per site. ............................................................ 28 Table 2. The coordinates and length of transects covered in distance sampling. ............... 28 Table 3. Density (ind.ha-1) of sea cucumbers in the North Islet. ............................................. 29 Table 4. Density (ind.ha-1) of sea cucumbers in the South Islet. ............................................ 29 Table 5. Density (ind.ha-1) of sea cucumbers per islet and in TRNP as a whole. ................ 30 Table 6. Summary statistics for the total lengths of sea cucumber species encountered during the distance survey. ........................................................................................................... 30 Table 7. Summary of sea cucumbers’ length and weight data subjected to regression analyses........................................................................................................................................... 31 Table 8. Summary table for the regression analysis between length and weight of sea cucumbers at TRNP. ..................................................................................................................... 31 PLATES ............................................................................................................................................... 32 Plate 1. Some common gastropods at TRNP. ........................................................................... 32 Plate 2. Giant clam species at TRNP. ......................................................................................... 34 Plate 3. Sea cucumber species under the genus Holothuria. ................................................. 35 Plate 4. Sea cucumber species under the genera Bohadschia and Stichopus.................... 37 Plate 5. Sea cucumber species under the genus Thelenota................................................... 38 Plate 6. Sea cucumbers under the genera Pearsonothuria, Euapta and Synaptula. .......... 39 Plate 7. Abundance survey in flat (a) and boulder habitats (b & c). ....................................... 40 Plate 8. Abundance survey in complex habitat (Photos of J. Selgrath). ................................ 41 Plate 9. Trochus tagging (a & b) and releasing (c). .................................................................. 42 Plate 10. Sampling of trochus with tag (a) and sea cucumbers (b)........................................ 43
6
INTRODUCTION
The Tubbataha Reefs Natural Park (TRNP) is an offshore park that lies in the
middle of the Sulu Sea, the heart of the Coral Triangle – world’s centre of marine
biodiversity and a conservation hot spot (Renema and Hoeksema 2007, Allen 2008).
Harbouring a total area of 96,828 ha, the park has extensive coral reefs of about
10,000 ha, home to an astounding diversity of marine life; many of these are
endangered or threatened species. Studies shows that there are more than 600 fish
species, 359 coral species representing 80% of the known Philippine species, 66
species of algae, 7 species of seagrass, 12 species of sharks, 13 species of whales
and dolphins, 7 species of seabirds (TRNP Primer), two species of marine turtles, 7
species of giant clams (Calumpong and Cadiz 1993, Estacion et al. 1993) and a
number of other reef invertebrates such as molluscs (Dolorosa and Schoppe 2005,
Yamaguchi 1996) and sea cucumbers at the park.
However, in spite of the number of researches that had been conducted at
TRNP along with the recent yearly monitoring, very little is known about the other
macrobenthic molluscs and sea cucumbers at the park. Trochus niloticus or Trochus
is continuously exploited, requiring information on its population trend, recruitment
and other relevant data which could be used as basis in developing conservation
measures specific for this species. As to the status of other invertebrates like giant
clams and sea cucumbers, very limited information is available. For sea cucumbers,
it was only in the 1990 research expedition in Tubbataha Reefs, that the genus
Stichopus was noted (Estacion et al. 1993) probably due to previous massive
resource exploitation until around 1999 (Arquiza and White 1999). Also, the yearly
monitoring at the park jointly conducted by the Tubbataha Management Office
(TMO), Conservation International (CI) and World Wide Fund for Nature (WWF) only
focused on corals, fishes and sea birds (Sabater 2004, Ledesma et al. 2008). It was
only in 2006 that research on Trochus was initiated (Dolorosa et al. 2010).
Mollusc species such as giant clams (Tridacna spp., Hippopus spp.), Cassis
cornuta, Charonia tritonis and many other species are listed under CITES Appendix
II (CITES 2010) which means that the species may be threatened with extinction,
unless trade is strictly regulated. The Fisheries Administrative Order 208 series of
2001 issued by the Bureau of Fisheries and Aquatic Resources also prohibits the
collection of all giant clam species and other CITES listed species (DA and BFAR
2001). In spite of these protection measures, exploitation continued to be a problem
for management.
There is also a growing awareness on the conservation of sea cucumbers. In
the Philippines, 100 species are known to date and around 30 species are utilised as
food. Sea cucumbers, as inhabitants of shallow marine ecosystems are threatened
because of habitat degradation, while several edible species are now suffering from
heavy exploitation and population depletion (Schoppe 2000, Bruckner 2006). As a
consequence, the Bureau of Fisheries and Aquatic Resources (BFAR) drafted an
Administrative Order to implement conservation efforts to limit and regulate harvest
of wild sea cucumber based on size limits (Pagdilao 2009), in response to the
identified two most urgent conservation needs (1. development of national fishery
management plans and 2. harmonized trade reporting) for sea cucumbers during the
7
Convention on International Trade of Critically Endangered Species (CITES)
international workshop on the conservation of commercially exploited sea cucumbers
in Malaysia in 2004 (Bruckner 2006).
However, because of the limited information on the ecology and biology
(Pagdilao 2009) and the state of stocks (Bruckner 2006) of sea cucumbers in the
Philippines, management of populations in the wild became a problem. In response,
a nationwide effort to monitor the status of sea cucumbers in the wild, studies on
production, sea ranching and restocking are currently undertaken (Bruckner 2006,
Pagdilao 2009).
This study therefore aimed to continuously provide data on the state of
trochus and complement the nationwide sea cucumber monitoring program of the
government, at the same time to expand knowledge on the state of other macro
benthic molluscs at TRNP. Specifically, this study looks into species diversity,
abundance and size structure of macro benthic molluscs and sea cucumbers.
Growth study on T. niloticus was also conducted to help the management monitor
the status of its population in the park.
8
RESEARCH METHODS
Study Site
The study was conducted at TRNP, Philippines. The park lies within 8°43’-
8°57’ N latitude and 119°48’-120°3’ E longitude, about 150 km southeast of Puerto
Princesa City, Palawan and 130 km south of the municipality of Cagayancillo (Fig.
1).
The surveyed area at the reef flat and shallow slopes were categorised into
three habitats: (1) Flat habitat (FH) - the reef crest or the highest part of the reef,
firstly exposed at low tide, composed of rubbles and few rocks. This area seems to
be a repository of coral fragments and it divides the inner and outer reef flats. (2)
Boulder habitat (BH) – generally at the middle part of the outer reef flat composed of
dead massive/sub massive coral rocks. Except the one at Site 3, all other BHs are
sub tidal in nature, generally around 2-3 m deep at highest high tide. And (3)
complex habitat (CH) - about 3 – 5 m deep at highest high tide characterised by a
mixture of dead and live corals of various life forms. All surveyed sites were at the
seaward part of the reef. In some sites, not all three types of habitats were found or
surveyed. A total of 14 sites were surveyed out of 15 proposed sites. No survey was
conducted at Site 12 due to bad weather and limited time (Fig. 1).
Because very few sea cucumbers were noted on the three habitats, distance
sampling using scuba gears was conducted in deeper reef slopes and walls where
large individuals were found. A total of 15 sites were surveyed (Fig. 1), six of which
were reef walls: one at North Atoll and Jessie Beazley Reef and four at South Islet.
The reef walls are characterised by sudden drop off with series of deep narrow
grooves with sand and rubbles substrate which extends towards the shallow area.
The reef slopes have wide sandy area with patches of soft and hard corals colonies.
Data Gathering Procedure
Species composition. Photos of molluscs and sea cucumbers encountered
on sandy flats, shallow reef flats and deeper reef slopes and walls were taken using
an underwater digital Canon D10. The species were identified using the works of
Schoppe (2000), and Carpenter and Niem (1998).
Abundance and size structure. The three types of habitats (Plates 7 & 8)
were surveyed using modified reef check method (Hodgson et al. 2004). Depending
on area and habitat availability, four to eight 2 x 20 m belt transects were laid per
habitat type (Table 1). Sizes of molluscs (Trochidae and Tridacnidae) and sea
cucumbers found one meter on both sides of the transects were measured either
with a ruler glued on a slate board or with a tape measure. Data collection was
conducted for three months (December 2009, January and April 2010).
Distance sampling method (Thomas et al. 2010) was conducted by two scuba
divers, swimming about 5 m apart parallel the edge of the reef, estimating the
perpendicular distance and approximate size of any sea cucumber species. Because
of small size and big numbers per colony, Synaptula sp. was disregarded during the
survey. Although the divers were trained to estimate fish size underwater, we found
9
a 5-10 cm difference between the estimated and actual lengths of sea cucumbers.
The distance covered per dive was estimated using Garmin e Trex GPS. About 400 -
1100 m long imaginary transect lines was covered per 40-60 min dive. Distance
covered was dependent on water current and species abundance (Table 2). Data
were analyzed using the software Distance 6 release 2 (Thomas et al. 2010).
Growth of Trochus niloticus. Mark-recapture method was used to estimate
the growth of T. niloticus in a reef flat in and out of the lagoon near the Ranger
Station. A total of 403 adult T. niloticus of different sizes were collected in October
2009 in a seaward shallow subtidal reef in front of the Ranger Station. Pre-numbered
dymo tags were glued on the shell and allowed to dry for an hour before measuring
the shell’s maximum basal diameter (MBD) with callipers to the nearest 0.1 mm. The
tagged trochus were then returned back into the area of capture. In December 2009,
another batch of 107 trochus collected from the seaward reef flat were tagged and
released at a subtidal reef flat (leeward) inside the lagoon (Plates 9 &10). Recapture
of tagged trochus were conducted in April and June 2010. Rate of recapture at the
seaward area after six (April) and eight (June) months were 38 and 30%
respectively. Recapture rates inside the lagoon after four (April) and six (June)
months were 57 and 43% respectively.
The von Bertalanffy growth model (Lt = L∞ [1-e (-k(t-to)) ] ) on a FiSAT software
was fitted to the data on sizes of recaptured marked individuals where Lt – is the size
at time t; L∞ - is the maximum attainable basal diameter of the shell in mm; K – is the
Brody growth coefficient, and t0 is the theoretical age at size zero (Gayanilo et al.
2005). The L∞ and K values for T. niloticus were obtained between the date of
release and the month of April, and then from April to June.
Length-weight relationships in sea cucumbers. Between December 2009
and June 2010, samples of sea cucumbers from Sites 1 and 2 were collected and
brought at the Ranger Station. At the station, the animals were allowed to relax for a
few minutes in a shallow tidal pool before taking the length with a ruler/ tape
measure to the nearest cm (Plate 10). Each cucumber was then carefully lifted out of
the water to release some water in its cavity before weighing with a digital scale to
the nearest gram. In cases where sites were too far from the Ranger Station,
sampling was done while on the boat. In such cases, the animals were allowed to
relax in plastic crates submerged in water. The weights were measured with a spring
balance to the nearest 25 g before releasing back in their natural habitat.
10
RESULTS
Habitat Characteristics
Substrate at FH was mainly composed of rubbles (RB) with very few hard
corals (HC), rocks (RC) and some sand (SD) deposits especially in Sites 1 and 2.
Boulder and complex habitats were generally characterised by rocky substrate with
no more than 20% hard coral cover. There were very few soft corals (SC) in the
area. Excellent HC cover was only encountered at Site 7 (Fig. 2) yet Crown-of-thorn
starfish noted during the survey is expected to cause massive coral mortalities.
Species Composition
Aside from T. niloticus, there were quite a number of gastropod species at the
park. Species that needed attention however include T. pyramis that was
accidentally gathered with T. niloticus (Dolorosa et al. 2010), and the endangered
Charonia tritonis tritonis and Cassis cornuta. Six giants clams species (Bivalves)
were also noted (Tridacna crocea, Tridacna maxima, Hippopus porcellanus, H.
hippopus, Tridacna derasa and Tridacna squamosa) (Plates 1 & 2).
A total of 14 sea cucumber species belonging to six genera and three families
were recorded at TRNP (Plates 3-6). Nine of these were noted during the distance
survey. Two unidentified species probably under the genus Holothuria were
encountered at Sites 2 and 7 (Plate 4). Bohadschia marmorata and Euapta sp. were
only encountered at the sand/reef flat around the Ranger Station.
Abundance
Abundance of trochus varied across sites and types of habitat. In Site 8,
highest density occured at FH, while in Sites 3,4,5,9 and 10, BH held the highest
numbers. In Site 3, density in a small strip of BH was very high, reaching more than
80 ind.100m-2. On the other hand, the highest number of trochus were recorded at
CH in Sites 1, 6,7, and 11-14. Irrespective of these variations, there was a general
declining density trend from Sites 1-15, with only areas close to the Ranger Station
(Sites 1-5) having the highest trochus abundance (Fig. 3). Density of the associated
trochid Tectus pyramis indicated high abundance in CH. Among the three species of
giant clams encountered, T. crocea was the most commonly occuring in all sites
especially in BH where densities could reach as high as 65 ind.100m-2 (Fig. 4).
Species such as T. maxima and Hippopus spp. were scarcely encountered. Sea
cucumbers were also very few, occuring in 4 out of 14 surveyed sites. Density was
only up to 1ind.100m-2 (Fig. 4).
Looking into the average abundance per islet (Fig. 5), it appeared that T.
niloticus density at the North Islet was three times higher than at the South Islet. No
living T. niloticus were encountered at JB Reef. Tectus pyramis, though in low11
densities, were encountered in most complex habitats around the park. Among the
three giant clams species, T. crocea was the most abundant, occuring mostly in BH
at about 9 ind.100m-2. All three sea cucumber species (H. atra, S. chloronotus and
B. argus) were only encountered at the North Islet and at very low densities.
The abundance of all sea cucumbers obtained through distance sampling at
the North Islet ranged from 4.12 -182.5 ind.ha-1 (Table 3). The lowest density and
number of species occurred in Site 3, a drop off. Densities in reef slopes ranged
between 18.2-182.5 ind.ha-1. Stichopus chloronotus and H. atra appeared to be the
most abundant species. Bohadschia argus was consistently encountered in all sites
but in very small numbers. Holothuria whitmaei and T. rubralineata were not
encountered at the North Islet.
Densities were much lower at the South Islet, ranging between zero - 29.26
-1
ind.ha (Table 4). Drop off areas (Sites 10, 11, 12 and 14) showed very low
abundances of sea cucumbers with 1-3 species per site. On the other hand sloping
reefs such as Sites 9 and 13 held the highest densities at 27.48-29.26 ind.ha-1.
Thelenota ananas occurred in four of six sites and had the highest density ranging
from 2-22 ind.ha-1. Pearsonothuria graeffei was recorded in all sampling sites yet it
occurred in very small numbers. The very rare T. rubralineata was only recorded at
Site 13. Stichopus chloronotus and T. anax were not encountered at the South Islet.
In general, sea cucumber density at the North Islet was approximately 70
-1
ind.ha (Table 5). Stichopus chloronotus was the most abundant, followed by H. atra
and B. Argus. At the South Islet, total density was much lower (10.21 ind.ha-1) with T.
ananas as the most abundant, followed by H. atra. In Jessie Beazley Reef, only two
individuals belonging to two species were encountered during the distance survey.
However, two more species (T. rubralineata and B. argus) were noted by the other
research team at 25 m deep along the reef wall. Snorkelling at the shallow reef flat
surrounding the small sand bar did not reveal the presence of any sea cucumbers.
When all the data was treated as a whole, sea cucumbers density at TRNP
was about 42 ind.ha-1 (Table 5). Stichopus chloronotus was the most abundant,
followed by H. atra, B. argus, and T. ananas. Rarely encountered species and those
with limited area of occurrence were T. rubralineata, T. anax and H. Whitmaei.
Size Structure
Size distribution of T. niloticus encountered per habitat suggested an
increasing trend in basal diameter towards the deeper parts of the reef. At FH,
although the size ranged between 22-112 mm, smaller individuals with size ranging
from 22-47 mm were more abundant comprising 74 % of all individuals encountered
in FH. Larger individuals with size ranging from 82-102 mm (76 %) were dominant in
BH, while in CH, 87-112 mm (83 %) in size were most common (Fig. 6). For T.
pyramis and T. maxima, larger individuals and high number of samples were also
noted at CH (Figs. 7 & 9). But for T. crocea, all sizes could be encountered in all
habitats yet abundance was higher at BH comprising about 55 % of all encountered
individuals in all three types of habitats. Larger individuals of T. crocea appeared12
more common in CH (Fig. 8). Hippopus spp., on the other hand, appeared abundant
in FH yet no individuals were encountered at CH (Fig. 10).
Results of the distance sampling indicated that among the three species
under the genus Holothuria (Fig. 11), H. atra appeared to have the wider distribution,
occurring in nine of 15 surveyed sites. Higher numbers of H. atra were noted in Sites
5 and 7. While the average size of H. atra was 46 cm, larger individuals of 100 cm in
length were encountered. None of the three species occurred on the reef wall or
drop off (Sites 3, 10, 11, 12, 14, and 15). A large number of Holothuria nobilis were
only encountered in Sites 7 and 13. Holothuria whitmaei seemed very rare and was
only noted in Site 9 but, in our recent dive, we spotted few individuals at Site 7.
Bohadschia argus were encountered in all sites at North Islet but only in one
of the six sites at the South Islet. The average size was 33 cm and ranged between
20-45 cm. Pearsonothuria graeffei although very few in numbers, it appeared to be
well distributed, occurring both in reef slopes and drop off areas. Average size was
34 cm, though larger individuals (45 cm) were recorded. Stichopus chloronotus
seemed to be only well distributed in the North Islet. It occurred in large colonies in
wide sand flats resulting to a total of 241 encountered individuals, comprising 43% of
all recorded species. Average size was 28 cm (10-40 cm) (Fig.12).
Three species under the genus Thelenota were also encountered during the
distance survey (Fig. 13). Of these, T. ananas seemed the most abundant, occurring
in most sites except in Sites 1, 10 and 14. This species was often found lying on
wide sand flats at the reef slope (10-25 m deep). In some cases, they were found
clinging on dead corals or hiding in rock crevices at the edge of the drop off.
Thelonota anax and T. rubralineata seemed very rare and were only encountered in
one or two sites. Average size per site for all three species generally ranged
between 50-60 cm. A summary table for the sizes and frequencies of sea
cucumbers encountered during the distance survey is reflected in Table 6.
Growth of Trochus niloticus
Trochus niloticus released inside the lagoon (L∞ = 122.735, K=0.2825)
appeared to have faster growth rate than those at the seaward reef area (L∞ =
126.99, K=0.202) (Fig.14). The data obtained suggested that one year old trochus
at the seaward and leeward reefs of TRNP could reach a size of 26.22-30.21 mm,
then 45.19-52.98 mm and 60.70-70.14 mm at ages two and three years
respectively. Growths were very fast in the first four years, and then it gradually
slowed down, reaching 113.11-115.46 mm at the age of 10 years (almost 89.07-
94.07 % of the L∞). Growth could be very slow from 10 years onward.
Length-Weight Analyses
Of the seven sea cucumber species collected for length-weight relationship
estimation, high positive correlation was only obtained among five species (Tables 713 & 8). However, regression values for some species could not be used for biomass estimation due to limited number of samples.
14
DISCUSSION
While higher trochus density is known to occur in elevated and exposed reef
as in the case of the Great Barrier Reefs (Nash 1993), it was only in BH of Sites 3, 4
and 5 where highest trochus density was encountered. Site 1 had been the release
area of confiscated trochus and such might have affected this pattern of abundance.
The very low abundance of trochus in another site close to the Ranger Station could
be due to heavy sand deposits. Sand restrains trochus’ movement and growth of its
natural food (Heslinga et al. 1984) thus habitat change such as increase in sand
brought about by natural calamities can cause population decline (Zoutendyk 1997).
Shifting sand was also noted to cover and caused mortality among Hippopus spp. in
the inner reef near Site 1.
At the South Islet, trochus density per site was very low. Numbers of
individuals at CH were higher than at BH, a usual condition for heavily exploited area
like in Cartier Reef, Australia (Smith et al. 2002). Sizes of trochus increase towards
deeper waters (Nash 1993, Smith 1987) as also noted in the overall size structure
(Fig. 6). Largest individuals noted during the survey corresponded with the estimated
maximum length (L∞) that trochus could attain, although a 160 mm trochus was
reported to occur in the area (Ledesma et al. 2008). Projected growth rates of T.
niloticus at TRNP are comparable to some growth studies from New Caledonia but
either slower or faster compared to other studies (see Nash 1993). Factors affecting
growth include food availability (Purcell 2002, Clarke et al. 2003), density and
season (Nash 1985, 1993). No live trochus was encountered at Jessie Beazley Reef,
only shells occupied by hermit crabs were found, suggesting they were once in the
area.
Trochus population trend (2006, 2008, 2009 and 2010) suggests that only
Sites 1 & 3 were not affected by illegal collection probably because of their proximity
to the Ranger Station. All other sites still show a declining trend as this year’s
densities at BH and CH (last two bars per site) were lower than the density records
in 2009 (Fig. 15). This declining trend is still the possible effect of the on-going illegal
activities at the park although the number of apprehended trochus collectors
declined from nearly 100 fishers in 2007 to less than 20 persons in 2009 (Jontilla et
al. 2010). It is not known as to what factors influenced the decline in number of
apprehended fishers but it is presumed here that only a few illegal fishers were left or
others may have shifted to different activities due to the declining trochus catch in
the area.
Even with a very low trochus population at the South Islet, the presence of
smaller individuals in un-surveyed FH suggests an on-going recruitment and the
potential to restore trochus population in few years time when illegal fishing is totally
controlled. The occurrence of high number of juveniles at FH in Site 8 at the North
Islet further reflects on-going recruitment in exploited areas. Smaller juveniles with
sizes lesser than 15 mm occur in areas with very shallow water during low tide, while
the larger ones inhabit deeper intertidal pools (Castell 1997) so that the low
abundance in other FH does not mean absence of recruitment. The park has
extensive reef flat suitable for juveniles only that these areas are difficult to assess.15
There were few trochus of varied sizes at the inner reefs, suggesting settlement and
presence of an unknown breeding population inside the lagoon.
The low abundance of other species along the transects could be habitat-
related. For example, the boring giant clam Tridacna crocea was very abundant
especially in boulder habitats at inner reefs which were not covered in this survey.
Flattened heads of large massive corals exposed at low tide were often colonised by
T. crocea, sometimes occurring > 20 individuals in one small coral head with 1 m
diameter. There was also a large population of Hippopus spp. at the shallow inner
reef flat in Site 8 where the average density could reach 25 ind.100m-2 while not a
single individual was noted in FH, BH and CH of the same site.
The recorded number of sea cucumber species at TRNP only comprised 14%
of the known Philippine species, but the high abundance of large individuals of
species with economic value probably makes TRNP the last stronghold of these
species and a hot spot for illegal fishers.
The size structures of sea cucumbers presented in this study are only of those
adults found freely exposed in deeper habitats. Smaller individuals are often cryptic
and difficult to find. During my one month stay at TRNP in April 2010, only one small
T. ananas (about 15 cm long) was noted in our numerous dives. The smaller
individuals of varied species are probably found at the intertidal or shallow subtidal
areas just like for H. atra which were abundant at sand/coral flat around the Ranger
Station. Similarly, there were B. marmorata (~30 cm) partly buried on the sand flat at
the eastern and southern sides of the Ranger Station. Only one very small B.
marmorata (~5 cm) was accidentally found under a coral rock. Clearly, an
understanding of which intertidal habitat juveniles of different sea cucumber species
occur in abundance is essential in stock recruitment monitoring.
By visual examination of data, sea cucumber diversity and abundance are
higher at the reef slopes than at the reef walls, which probably explains why
abundance is higher at the North Islet. While there is a limited habitat
range/preference for sea cucumbers at the outer reefs in South Islet, areas inside
the lagoon may support a good population of these species. Other reasons to
explain variation in density between species may include growth, maturity and
fecundity. For example, species like H. nobilis is slow growing and occurs in very low
numbers even in well managed reef areas (Bruckner 2006). Other environmental
factors may also influence species distribution and abundance.
The sizes of sea cucumbers at TRNP are comparable to the report of
Carpenter and Niem (1998). Maximum sizes of H. atra and S. chloronotus at TRNP
were even larger than the reported maximum lengths, suggesting that these
individuals are in their reproductive stage and thus perform a significant role in
naturally replenishing other depleted areas within the Sulu Sea thru larval dispersal.
To determine the biomass of the sea cucumbers, the regression values obtained for
H. atra and S. chloronotus may be used. As for the other species, additional
numbers of samples of different sizes are needed for length-weight analyses. The
abundance of large sized sea cucumbers at the park further suggests the possible
absence of any form of exploitation which could be attributed to the nature and depth
of the habitat. Sampling sites far from the Ranger Station that were already depleted16
with trochus still hold an abundance of sea cucumbers. In most cases, illegal fishers
caught at the park engaged in collecting fishery resources other than sea
cucumbers. However, stock depletion of target species (like trochus) at TRNP
(Dolorosa et al. 2010, Jontilla et al. 2010, Ledesma et al. 2008) and the increasing
sea cucumber price and demand in the world market (Bruckner 2006) may drive
fishermen to engage in harvesting these species at the park. When such illegal
activity becomes uncontrolled, some species like H. nobilis and T. ananas would be
easily overfished because of their slow growth, low fecundity and late maturity
(Bruckner 2006). Adequate patrol support facilities are therefore needed to prevent
all forms of illegal activities around the park.
Yearly monitoring of sea cucumbers especially in reef slope areas and initial
survey at the lagoon is suggested. It may be essential to establish separate survey
areas for periodic monitoring of Hippopus spp. and T. crocea. Transfer of Hippopus
spp. and other non boring giant clams away from areas susceptible to sand shifting
may be conducted. Population survey for other large molluscs such as Tridacna
gigas, Cassis cornuta and Charonia tritonis tritonis may be conducted. Exact
locations of T. gigas may be recorded with GPS to facilitate yearly monitoring. Prior
to any monitoring activity, the TMO is advised to conduct training among Marine
Park Rangers/Researchers matters related to data gathering techniques which may
include species size estimation, distance estimation and taxonomy of sea cucumbers
and other reef invertebrates.17
LITERATURE CITED
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Palawan, Philippines. Science Diliman. 17:2, 1-8.
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Population structure and abundance of Trochus niloticus in Tubbataha Reefs
Natural Park, Palawan, Philippines with notes on poaching effects. SPC
Trochus Information Bulletin. No. 15:17-23.
Estacion, J.E., Palaganas, V.P., Perez, R.E. and M.N. R. Alava. 1993. Benthic
characteristics of Islands and Reefs in the Sulu Sea, Philippines. Silliman
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Hodgson, G., Kiene, W., Mihaly, J., Liebeler, J., Shuman, C., and Maun, L. 2004.
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Calderon. 2008. Tubbataha Reefs Natural Park Research and Monitoring Report
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Philippines. 65 pp.18
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send caution for seeding. SPC Trochus Information BulletinNo.9: 6-8.
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and time. Unpublished Report, Tubbataha Conservation Project, World Wide
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Princesa City, Palawan, Philippines, 14 pp.
Schoppe S. 2000. A guide to the common shallow water sea stars, brittle stars, sea
urchins, sea cucumbers and feather stars (Echinoderms) of the Philippines.
Time Media Private Limited, Singapore. 144 pp.
Smith, B.D. 1987. Growth rate, distribution and abundance of the introduce topshell
Trochus niloticus Linnaeus on Guam, Mariana Islands. Bulletin of Marine
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beche-de-mer at Cartier Reef: 2001 surveys. Australian Institute of Marine
Science. 26pp
Thomas, L., Buckland, S. T., Rexstad, E. A., Laake, J. L., Strindberg, S., Hedley, S.
L., Bishop, J. R., Marques, T. A. and Burnham, K. P. 2010. Distance software:
design and analysis of distance sampling surveys for estimating population
size. Journal of Applied Ecology, 47: 5–14. doi: 10.1111/j.1365-
2664.2009.01737.x
Yamaguchi, M. 1996. Shallow water molluscan assemblages of the Tubbataha Reef,
Republic of the Philippines. p: 61-71. In: Department of Environment and
Natural Resources (DENR) and Marine Parks Centre of Japan (MPCJ). 1996.
The Report of the Project for Resources Survey and Conservation of
Tubbataha Reefs National Marine Park. 200pp.
Zoutendyk, D. 1997. Report on Aitutaki trochus (T. niloticus) research trips of 29
January- 6 February and 12-15 March 1990. p. 115-118. In: Workshop on
Trochus Resource Assessment and Development. Integrated Coastal19 Fisheries Management Project, Technical Document No. 13, South Pacific Commission, Noumea, New Caledonia. 140pp.
20
FIGURES
Figure 1. The sampling sites.21 Figure 2. Substrate composition of the three types of habitat. Figure 3. Abundance of T. niloticus and T. pyramis in three types of reef habitat.
22 Figure 4. Abundance (ind.100m-2) of giant clams and sea cucumbers.
23 Figure 5. Average density of different invertebrates at TRNP. Figure 6. Size structure of T. niloticus per type of habitat.
24 Figure 7. Size structure of T. pyramis per type of habitat. Figure 8. Size structure of T. crocea per type of habitat. Figure 9. Size structure of T. maxima per type of habitat.
25 Figure 10. Size structure of Hippopus spp. per type of habitat. Figure 11. Average sizes (±sd) of Holothuria spp. at TRNP.
26 Figure 12. Average sizes (±sd) of B. Argus, P. graeffei and S. chloronotus at TRNP. Figure 13. Average sizes (±sd) of three species of Thelenota at TRNP.
27 Figure 14. Growth trends of T. niloticus in and out of the lagoon at TRNP. Figure 15. Abundance trend of T. niloticus at TRNP (2006-2010).
28
TABLES
Table 1. Number of 20 m transect per habitat per site.
Habitat Number of 20 m Transect per Site
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Flat 8 4 8 8 8 4 4
Boulder 4 4 8 8 8 8 4 8 8 8 8 4 4 4
Complex 8 4 8 8 8 8 4 8 8 4 4 4
Table 2. The coordinates and length of transects covered in distance sampling.
Length of
Site Name of Transect Coordinates Transect (m)
1 South Park to Ranger 8o50.820’N 119o 55.778’E
Station 8o50.770’N 119o 55.226’E 1013.89
2 Ranger Station to 8o50.778’N 119o55.152’E
Amos Rock 8o50.695’N 119o54.589’E 1062.17
3* Amos Rock to Wall 8o51.004’N 119o53.236’E
Street 8o51.402’N 119o52.930’E 933.42
4 8o53.225’N 119o53.567’E
Malayan Wreck 8o53.130’N 119o53.380’E 370.15
5 8o54.522’N 119o56.058’E
Channel 8o54.835’N 119o56.375’E 820.77
6 8o55.747’N 119o57.024’E
Terraces 8o56.099’N 119o57.290’E 820.77
7 8o55.539’N 120o00.600’E
Sharks Airport 8o55.870’N 120o00.970’E 901.23
8 8o55.491’N 120o00.009’E
Bird Islet 8o55.075’N 119o59.588’E 1094.35
9 8o44.356’N 119o48.814’E
Staghorn Point 8o44.503’N 119o49.156’E 692.02
10* 8o45.146’N 119o48.804’E
South West Wall 8o45.492’N 119o48.758’E 643.74
11* 8o48.312’N 119o48.367’E
Kook 8o47.985’N 119o48.364’E 611.55
12* 8o48.420’N 119o49.259’E
T Wreck to Black Rock 8o48.172’N 119o49.790’E 1078.26
13 8o47.772’N 119o50.205’E
Black Rock 8o48.083’N 119o50.548’E 852.95
14* 8o45.319’N 119o49.707’E
Delsan Wreck 8o45.813’N 119o49.954’E 1013.89
15* 9o02.667’N 119o49.040’E
Jessie Beazly Reef 9o02.963’N 119o48.622’E 1050.00
*Reef wall or vertical edge of the reef.29
Table 3. Density (ind.ha-1) of sea cucumbers in the North Islet.
Density per Site (ind.ha-1)
Species
1 2 3* 4 5 6 7 8
Bohadschia argus 8.63 5.93 0.8 6.9 5.77 6.03 5.55 8.38
Holothuria atra 6.58 3.58 10.9 70.27 24.03 32.15 12.57
H. nobilis 8.11
H. whitmaei
Pearsonothuria graeffei 3.3 8.04 1.44 3.05 1.04
Stichopus chloronotus 65.65 44.7 144.10 144.10 40.06
Thelenota ananas 1.34 0.23 14.1 4.27 5.63 13.27 0.86
T. anax 0.62 0.34
T. rubralineata
Total 18.2 82.15 4.12 75.1 182.5 182.4 92.47 20.91
*drop off
Table 4. Density (ind.ha-1) of sea cucumbers in the South Islet.
Species Transects
9 10* 11* 12* 13 14*
Bohadschia argus 2.71 2.38
Holothuria atra 3.61 2.25 0.99
H. nobilis 2.44
H. whitmaei 0.00
Pearsonothuria graeffei 6.02 0.00 0.00 1.74 0.46 0.00
Stichopus chloronotus
Thelenota ananas 11.43 4.09 2.32 21.82
T. anax
T. rubralineata 2.93
Total 27.48 0 12.3 2.32 29.26 1.48
* drop off30
Table 5. Density (ind.ha-1) of sea cucumbers per islet and in TRNP as a whole.
JB
North Islet South Islet Reef TRNP
Species
Density LL-UL Density LL-UL Density Density LL-UL
-1
(ind.ha ) (ind.ha-1) (ind.ha-1) (ind.ha-1)
Bohadschia
argus 7.24 5.02-10.44 0.46 0.12-1.81 4.20 2.64-6.67
Holothuria atra 16.73 9.59-29.14 4.38 1.52-12.45 9.65 5.42-17.18
H. nobilis 1.04 0.24-4.46 0.39 0.07-2.06 0.71 0.21-2.33
H. whitmaei 0.00 0.00
Pearsonothuria
graeffei 1.56 0.78-3.12 2.36 1.0-5.55 0.48 2.04 1.17-3.56
Stichopus 24.82- 12.63-
chloronotus 42.30 72.05 22.91 41.55
Thelenota
ananas 3.89 1.85-8.17 5.16 1.74-15.31 0.12 4.20 2.23-7.89
T. anax 0.05 0.01-0.22 0.03 0.01-0.12
T. rubralineata 0.46 0.1-2.15 0.19 0.04-0.81
46.37- 27.15-
Total 70.27 106.48 10.21 4.11-25.37 0.24 41.93 64.74
LL – lower limit at 95% confidence level; UL- upper limit at 95 % confidence level.
Table 6. Summary statistics for the total lengths of sea cucumber species
encountered during the distance survey.
Mean Min. Max. Confidence
Species Frequency Length Length Length Level Relative
(cm) (cm) (cm) (95.0%) Frequency
B. argus 36 33.33 20.00 45.00 2.59 6.43
H. atra 156 46.66 10.00 100.00 1.31 27.86
H. nobilis 14 33.57 30.00 40.00 2.87 2.50
H. whitmaei 1 20.00 20.00 20.00 0.18
P. graeffei 19 33.53 30.00 45.00 2.62 3.39
S. chloronotus 241 27.63 10.00 40.00 0.89 43.04
T. ananas 90 53.20 40.00 70.00 1.54 16.07
T. anax 2 60.00 60.00 60.00 0.00 0.36
T. rubralineata 1 50.00 50.00 50.00 0.18
Total 560 10031
Table 7. Summary of sea cucumbers’ length and weight data subjected to
regression analyses.
No. of Confidence
Species Measurements Mean Min. Max. ind. Level
(95 %)
Length 34.29 29 43 1.91
Bohadschia argus 17
Weight 1947.06 1000 3750 374.14
B. marmorata Length 25.68 17 37 18 2.99
Weight 1076.72 380 2000 246.55
length 26.00 22 30 50.82
B. whitmaei 2
Weight 2000.00 2000 2000 0.00
Holothuria atra Length 25.29 7 52 101 2.23
Weight 666.56 50 2800 149.95
H. nobilis Length 35.57 33 40 7 2.13
Weight 2800.00 2000 3000 337.71
Stichopus Length 26.44 9 40 1.02
chloronotus 104
Weight 389.38 75 1100 35.35
Thelenota ananas Length 52.27 36 65 11 6.47
Weight 3754.55 1700 5500 830.64
Table 8. Summary table for the regression analysis between length and weight
of sea cucumbers at TRNP.
Species Regression Equation R2
Bohadschia argus (n=17) 156.4x - 3419 0.640
B. marmorata (n=18) y = 66.69x - 635.8 0.654
Holothuria atra (n=101) y = 46.23e0.083x 0.838
Stichopus chloronotus (n=104) y = 1.043x1.785 0.617
Thelenota ananas (n=11) y = 2.691x1.822 0.86332
PLATES
Plate 1. Some common gastropods at TRNP.33 Plate 1. Continued . .
34 Plate 2. Giant clam species at TRNP.
35 Plate 3. Sea cucumber species under the genus Holothuria.
36 Plate 3. continued
37 Plate 4. Sea cucumber species under the genera Bohadschia and Stichopus.
38 Plate 5. Sea cucumber species under the genus Thelenota.
39 Plate 6. Sea cucumbers under the genera Pearsonothuria, Euapta and Synaptula.
40 Plate 7. Abundance survey in flat (a) and boulder habitats (b & c).
41 Plate 8. Abundance survey in complex habitat (Photos of J. Selgrath).
42 Plate 9. Trochus tagging (a & b) and releasing (c).
43 Plate 10. Sampling of trochus with tag (a) and sea cucumbers (b).
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