Shallow-water Sea Cucumbers (Echinodermata: Holothuroidea) in Sarangani Bay, Mindanao ... · 2018. 8. 31. · One specimen for each species was collected for photo documentation

Key words: Actinopyga capillata, Holothuria immobilis, Holothuria isuga, holothurian, new species record, Sarangani

Shallow-water Sea Cucumbers (Echinodermata: Holothuroidea) in Sarangani Bay, Mindanao,

Philippines with Notes on Their Relative Abundance

1Animal Biology Division, Institute of Biological Sciences, University of the Philippines Los Baños, College, Laguna 4031 Philippines

2Department of Marine Biology, College of Fisheries, Mindanao State University, General Santos City 9500 Philippines

*Corresponding author: [email protected]

Kier Mitchel E. Pitogo1*, Jennelyn P. Sumin2, and Ariel T. Ortiz2

The Philippines is known for its high diversity of sea cucumbers; however, there is little done on sea cucumber diversity in the southern Philippines. To augment this paucity of information, a rapid survey of the shallow-water sea cucumbers was carried out in three sites in Sarangani Bay by using the transect method for four months in both the seagrass and coral reef habitats. We recorded 21 species of sea cucumbers – 17 of these species were found in the seagrass beds and 10 species in the coral reef areas. The three most abundant species observed were the Holothuria scabra (29.2%), Bohadschia marmorata (21.2%), and Actinopyga echinites (17.6%) (n=1,969). Aside from some economically important sea cucumbers observed, we also noted rare species such as the Holothuria immobilis and Actinopyga capillata, which only have a few records in the Philippines. We are also the first to document Holothuria isuga in the Philippines, which is previously known only from five localities. The results offer opportunities for sea cucumber studies in the southern Philippines, especially on the biology and ecology of the rare and newly recorded species.

Philippine Journal of Science147 (3): 453-461, September 2018ISSN 0031 - 7683Date Received: 21 Feb 2018

INTRODUCTIONThe Philippines harbors a high diversity of sea cucumber species, which is threatened by overfishing and habitat loss (Choo 2008). Of the over 170 species identified in the country (Olavides et al. 2010), 25 to 41 of these – mostly from the members of the families Holothuriidae and Stichopodidae – have commercial value (Gamboa et al. 2004; Olavides et al. 2010; Jontila et al. 2014). Being a major exporter of trepang or dried sea cucumbers worldwide (Akamine 2005), the Philippines has been identified as a sea cucumber

hotspot in Asia (Choo 2008). This demand may lead to overharvesting of sea cucumber resources, which may pose a great risk to their populations. The declining numbers of sea cucumbers in intertidal areas have serious consequences in the ecosystem such as habitat structure alteration, as they are the seas’ bioturbators and recyclers (Wolkenhauer et al. 2010). Moreover, sea cucumber species contain compounds that have medicinal properties that are of great importance to future research (Bordbar et al. 2011).

Most of the commercially-important sea cucumbers that inhabit the shallow waters have been fished with increasing intensity (Wolkenhauer et al. 2010). Shallow-water sea

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cucumbers, especially, are vulnerable to harvesting because of their high abundance and easy access to their habitats (Purcell et al. 2013). With this, it is imperative that baseline research (e.g., inventory studies) is needed to support science-based conservation and management measures as the demand for sea cucumbers increase. While there were several diversity studies of sea cucumbers conducted in the Philippines, none has been conducted in Sarangani Bay. Anecdotal evidence from local interviews shows that overharvesting caused a reduction of a high-valued Holothuria scabra in Macatimbol, Glan, Sarangani Province, as buyer boats from Davao once frequent the area to buy pails of H. scabra from the locals (Pitogo et al. 2016). If harvesting continues unregulated and if preferences shift to other species of similar or lower value, local sea cucumber populations may collapse leading to serious environmental repercussions. Thus, this study was carried out to provide a preliminary inventory of the sea cucumber species found in the shallow-water areas in the bay with information on their relative abundance. The results of this study may provide helpful insights in creating local policies regarding the management of the sea cucumber resources in the area.

MATERIALS AND METHODSSarangani Bay is in the southeastern Mindanao, Philippines between 5º33’25’’- 6º6’15’’N and 124º22’45’’-125º19’45’’E. There were three stations in Sarangani Bay selected in the study: Sitio Linao and Sitio S’nalang,

Figure 1. The map of Sarangani Bay showing the three study sites.

Maasim; and Sitio Macatimbol, Glan. The stations were chosen based on the reported high abundance of sea cucumbers. All stations have seagrass beds covered mainly by Cymodocea sp., Halodule sp., and Halophila sp. on a sandy and silty substrate. The Macatimbol station, however, had a patchier distribution of seagrass on a sandy and rubble substrate. Of the three sites, the Sitio Linao station had the most minimal wave action because of its placement in a cove. It also had the siltiest substrate dominated by the seagrass Enhalus acoroides. The reef formation in all three sites was dominated by massive and sub-massive corals creating pools of water during the lowest ebb. This leaves patches of sand and rubble usually exposed that were used as trails to minimize disturbance.

At each station, six transects measuring 4 m x 50 m were laid perpendicular to the shore with a 10-meter interval. Three transects were laid in the seagrass bed and the other three were laid in the coral reef area. We completed 24 night samplings during the lowest ebbing of the month from Oct 2014 to Jan 2015. Three investigators, with one local guide adept at collecting sea cucumbers, collected all sea cucumbers found within the 200 m2 transects by reef walking at around 22:00-23:00 to 02:00-03:00. For some species, we used our bare feet to locate individuals burrowed into the sand (a method used by some locals). One specimen for each species was collected for photo documentation. The species were identified by morphology using the book Commercially Important Sea Cucumbers of the World by Purcell and co-authors (2012). The photographs of identified and unidentified

Pitogo et al.: Sea Cucumbers in Sarangani Bay, Mindanao, Philippines

Philippine Journal of ScienceVol. 147 No. 3, September 2018

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species were sent to Dr. Gustav Paulay and Dr. Francóis Michonneau of the Invertebrate Zoology Division at the Florida Museum of Natural History for validation and identification.

RESULTS AND DISCUSSIONWe recorded 21 species of shallow-water sea cucumbers belonging to families Holothuriidae and Stichopodidae, 17 of these species were found in the seagrass beds and 10 species in the coral reef areas. This is relatively lower than the other species diversity studies in the Philippines (see dela Cruz et al. 2015). This low number recorded might be due to the shallowness of the area assessed or due to our limited number of sampling stations and the total area surveyed.

Of the 1,645 individuals counted in the seagrass beds, the species Holothuria scabra (34.9%), Bohadschia marmorata (25.3%), and Actinopyga echinites (20.8%) were the most commonly observed. Species belonging to these three genera tend to be the most common in the shallow seagrass beds, similar with the observations of

Jontila and co-authors (2017) and Olavides and co-authors (2010). Specifically, species belonging to Holothuria accounted for 52.1% of the sea cucumbers found in the seagrass beds, while Actinopyga and Bohadschia accounted for 21.2% and 26.1%, respectively.

Holothuria fuscocinerea, the most dominant in the coral reef areas, accounted for 68.2% of the 324 individuals found. Individuals of the species hid most of their body under rocks, leaving only a small portion outside the crevice. When disturbed, they start writhing and injecting numerous thick Cuvierian tubules, similar with a predatory escape behavior of H. fuscocinerea observed in the laboratory by Morton (1991). We suspect that H. fuscocinerea is sensitive to light as retraction was observed upon flashing light to individual organisms. This might be because of its strict nocturnal behavior (Kerr et al. 2006; Purcell et al. 2012; Jontila et al. 2017). Despite being a common species, ecological studies on H. fuscocinerea is very little to support our observations.

Fewer sea cucumber species was recorded in the coral reef areas. We had to move at a slower pace in the reef areas while we were sampling to avoid causing damage to

Table 1. The initial list of sea cucumber species found in the shallow waters of Sarangani Bay.

Species Common Name Local Name Habitata

1 Actinopyga capillata Hairy sea cucumber SG

2 Actinopyga echinites Deep-water redfish Bat-alaw/Hud-hud SG, C

3 Actinopya lecanora Stonefish Batseror SG

4 Actinopyga sp.b SG

5 Bohadschia argus Leopardfish Bangkungan C

6 Bohadschia koellikeri Mottled sea cucumber Tagukan SG,C

7 Bohadschia marmorata Brownspotted sandfish Tagukan SG

8 Bohadschia vitiensis Brown sandfish Tagukan SG,C

9 Holothuria albiventer Marten’s sea cucumber SG

10 Holothuria atra Lollyfish Bat-uwak SG,C

11 Holothuria fuscocinerea Variegated sea cucumber Gulay-gulay/Libud-buto SG,C

12 Holothuria hilla Tigertail sea cucumber Pula-pula/Iring-iring C

13 Holothuria immobilisb Libud-buto C

14 Holothuria isugab SG

15 Holothuria leucospilota White threadfish Patola SG,C

16 Holothuria notabilis SG

17 Holothuria rigida Rigid sea cucumber Bantunan SG

18 Holothuria scabra Sandfish Putian SG

19 Holothuria sp.b SG

20 Stichopus horrens Warty sea cucumber Hanginan C

21 Stichopus aff. horrensb Warty sea cucumber Hanginan SGa SG= seagrass; C= coral reefsbnot included in the list of the shallow-water sea cucumbers compiled by dela Cruz and co-authors (2015)



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the corals. There were instances that sea cucumbers have already retracted to crevices even before we approached them, probably because of the light emitted from our lamp. This factor, together with the fact that coral reef areas have a lot of nooks and crannies where sea cucumbers could hide, might have contributed to the low number of species recorded in this habitat. The rock crevices were favorite hiding spots of slender-bodied sea cucumbers such as the H. fuscocinerea (Purcell et al. 2012). Hiding in crevices is one of the most common self-protecting behaviors of sea cucumbers aside from burrowing (Purcell 2010). Unlike in coral reef areas, spotting sea cucumbers was easier in the seagrass beds as they were usually found exposed, except during extreme ebb conditions. Only a few of the recorded species in the seagrass beds bury their body underground such as the Holothuria rigida, Holothuria albiventer, and Holothuria notabilis, which made these species difficult to spot. This burrowing behavior of sea cucumbers, however, plays a critical role in mixing the sediment layers in the intertidal ecosystem. The commonly observed H. scabra that moves in and out of the sub-surface sediments are probably the most important bioturbators in this environment (Wolkenhauer et al. 2010). Sea cucumbers also increase the nutrient levels in the water column (Grall & Chauvaud 2002) and, as deposit feeders, clean the sediments by lowering its organic matter upon defecation (MacTavish et al. 2012). Collectively, holothurians play a significant role in the intertidal ecosystems by helping increase the productivity of these environments (Purcell

Figure 2. The pooled relative abundance of shallow-water sea cucumbers surveyed in the 1,200 m2 area of both coral reefs and seagrass beds in Sarangani Bay, Philippines from Oct 2014 to Jan 2015 (n=1,969).

et al. 2013). Uncontrolled harvesting of holothurians that perform this function would eventually lead the collapse of intertidal ecosystems (Wolkenhauer et al. 2010).

Of the 1,969 sea cucumber individuals recorded, H. scabra had the highest occurrence (29.2%), followed by B. marmorata (21.2%) and A. echinites (17.6%). H. scabra prefer seagrass beds, which they rely heavily on for settling cues and during their early life stages (Mercier et al. 2000). In all three sites, H. scabra had the highest occurrence in Sitio Linao where wave action was minimal and organic matter concentration was high (Pitogo et al. 2016). In 2013, however, sea cucumber pens were established in Sitio Linao to rear hatchery-produced H. scabra. The individuals were eventually released after the project, which might have influenced the increase in H. scabra abundance in succeeding years. Locals in Sarangani Province collect H. scabra, preferably during a new moon phase, where larger individuals occur (Pitogo et al. 2016). They are high-value species, which are harvested and exploited leading to the depletion of their natural population (Akamine 2005). Other commonly occurring species recorded in the seagrass beds were B. marmorata and A. echinites, low-value and medium-value species, respectively (Olavides et al. 2010).

Despite the limited number of our sampling stations and the total area surveyed, a few notable species were found. One of our interesting find was the species Holothuria isuga. It is a new record for the Philippines as the reported



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Figure 3. Photos of the four relatively rare sea cucumber species recorded: (A) Stichopus aff. horrens, (B) Actinopyga capillata, (C) Holothuria immobilis, and (D) Holothuria isuga.

ranges for this species are Japan, Australia, Tanzania, and Sri Lanka (IUCN 2013a). Very few studies have mentioned H. isuga: in Zanzibar, Tanzania (Eriksson et al. 2010); in Sri Lanka (Dissanayake & Stefansson 2010); and another in New Caledonia (Purcell et al. 2009). It was described by Purcell and co-authors (2009) as “rusty-brown, with large papillae and buries most of its soft body in sediments”. We only found one H. isuga partly buried in silt near the mangrove area at night. The time of our observation was not similar with Dissanayake and Stefansson (2010), who observed H. isuga at daytime. The

activity pattern of H. isuga is not yet fully known since it is rarely seen, at least in some areas. The H. isuga is characterized by its soft body covered with black papillae with a narrow orange streak along the dorsum and on the ventrum, with a high amount of similar color around its anal portion (see Figure 4). It also writhes and distorts its body when touched or handled. Divers do not often visit sandy and silty habitats where the H. isuga lives buried that is why this species is rarely cited in literature (Dr. Francóis Michonneau, pers. comm., 04 May 2016). Interestingly, Purcell and co-authors (2009) and Eriksson



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and co-authors (2010) collected them in lagoon reef areas while we saw our specimen in the silty substrate near a mangrove area. Our observation supports the habitat association of this species to silty environment, as the few previous studies only observed them in the reef areas. Despite their current rarity, their burrowing behavior still makes them an important bioturbator in the seagrass beds (Purcell et al. 2016). Unfortunately, they are being harvested in some parts of their distribution (Eriksson et al. 2010; Eriksson et al. 2012). Previous records of these species suggest that this species occurs throughout the western Pacific Ocean and in the northern Indian Ocean (IUCN 2013a). But with this new record, H. isuga is maybe more widespread than its current reported range.

The species Holothuria immobilis is also rarely cited in sea cucumber diversity studies and was only collected twice in the study of dela Cruz and co-authors (2015) in Samar and Leyte. It was noted by Cherbonnier (1967) that the species can be found in the Philippines as described by Semper in 1868, but generally has been lost in synonymy. Information regarding the population status, habitat, and ecology of this species is very little (IUCN 2013b). Although Clark reported the species in Torres Strait in 1921, it remained an invalid species and had been forgotten until it was rediscovered by Dr. Gustav Paulay and his team and confirmed its validity with genetic data (Dr. Francóis Michonneau, pers. comm., 28 Mar 2016).

Ten H. immobilis were found hiding in rock crevices in the coral reefs in Sitio Linao with two different coloration patterns: a dark brown and a light brown with dark blotches on its dorsum (see Figure 4). The dark morph of H. immobilis is quite similar with the H. fuscocinerea. However, it is easily distinguished by its blue-tipped papillae, as opposed to the dark white-ringed papillae of H. fuscocinerea (see Figure 4). The H. immobilis is known in two localities in Sarangani: Sitio Linao, Maasim (this study) and Sitio Pananggalon, Malapatan (Gino 2016). Gino (2016) also found H. immobilis along the reef flats hiding in rock crevices. Interestingly, all H. immobilis were observed during a new moon phase where it is relatively darker. This may suggest a strict nocturnal behavior of this organism like the A. capillata (Rowe & Massin 2006).

A strictly nocturnal species of sea cucumber, A. capillata, was recorded five times in the seagrass beds of Sitio S’nalang only during a new moon phase. It is characterized by its numerous hair-like papillae and mottled light to dark orange and white on its body (see Figures 3 & 4). It was only recently described by Rowe and Massin (2006) from a holotype specimen collected in La Réunion. We found all the individuals submerged in both sandy and rubble substrates in the seagrass area, which probably is a new habitat record for this species. The holotype and paratype specimens were collected in the inner reef and reef crests

Figure 4. (A) Holothuria isuga submerged in water highlighting its rusty brown papillae; (B) the blue-tipped papillae of Holothuria immobilis (above) and the dark white-ringed papillae of Holothuria fuscocinerea (below); (C) the appearance of the nocturnal Actinopyga capillata submerged in water in a seagrass bed in Sitio S’nalang, Maasim, Sarangani Province.



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similar with where Ducarme (2017), Lampe-Ramdoo and co-authors (2014), and Conand and co-authors (2010) observed them. Our observations, together with those of Kerr and co-authors (2006), extend the distribution of A. capillata from the seagrass beds and algal beds to the reef crest. Interestingly, the present distribution of A. capillata is disjunct with one in Mayotte to Mauritius and the other in the Philippines (Ducarme 2017). There used to be one record of A. capillata in the Philippines, but a few inventory studies mentioned the species though only in few numbers (Kerr et al. 2006; dela Cruz et al. 2015). It seems that based on records, the A. capillata’s current distribution in the Philippines is in the central (Kerr et al. 2006; dela Cruz et al. 2015; Ducarme 2017) and southern (Ducarme 2017, this study) part. In the study of Kerr and co-authors (2006), they recorded A. capillata in the central Philippines but they misidentified it (named it Holothuria sp.). While in a recent study of dela Cruz and co-authors (2015), 15 individuals were found in the shallow waters of Samar and Leyte, but they did not include field observations that could have been important information on its habitat associations. Most A. capillata data are only accounts with limited information on its biology and ecology. Our observations concur with the original description of Rowe and Massin (2006) that this species is nocturnal and occur in shallow-water habitats. We suspect that the Philippine population may also be cryptic and strictly nocturnal, like in some of its possible distributional range (Ducarme 2017), due to its rare appearance in the sea cucumber diversity studies in the country.

It is worth noting that a Stichopus aff. horrens was found in a silty substrate in a patch of seagrass near a mangrove area. The Stichopodids usually live exposed on sand and rubble in the reef areas and do not usually inhabit silty environments (Purcell et al. 2012). This reddish variant was not reported in previous literature, but something similar was once collected by Dr. Francis Michonneau in Papua New Guinea (Dr. Francóis Michonneau, pers. comm., 29 March 2016) (see Figure 3). However, further validation through ossicles and molecular data is needed to validate our identification.

Our results only provide a glimpse of the sea cucumber diversity in Sarangani Bay. Despite the limited sampling stations and the total area surveyed, we still managed to record 1,969 individuals belonging to 21 species of economic and ecological importance. We did not have enough information on the biology and ecology of the species since we only collected abundance data and took photographs. Our results, however, highlights the importance of Sarangani Bay in sea cucumber research, especially that anecdotal evidence shows that overharvesting and direct exploitation threatens the local sea cucumber populations in the area. Moreover,

our results warrant species-specific studies to provide significant information for the relatively rare species observed, which could provide helpful data for the formulation of conservation and management plans in the area.

ACKNOWLEDGMENTS

Gratitude is given to Dr. Gustav Paulay and Dr. Francóis Michonneau of the Invertebrate Zoology Division at the Florida Museum of Natural History for validating and identifying sea cucumber species, and for the useful information they shared that helped in finishing the manuscript. We thank the Sarangani Bay Protected Seascape (SBPS) Protected Management Board for allowing us to conduct research in Sarangani Bay (Certification No. SBPS-014-009). We would also like to extend our thanks to the two anonymous reviewers for their helpful comments and suggestions.

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Shallow-water Sea Cucumbers (Echinodermata: Holothuroidea) in Sarangani Bay, Mindanao ... · 2018. 8. 31. · One specimen for each species was collected for photo documentation