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Status of sea cucumber fishery and populations across sites with different levels of management in Palawan, Philippines
Ocean and Coastal Management 165 (2018) 225–234
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Ocean and Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman
Status of sea cucumber fishery and populations across sites with different levels of management in Palawan, Philippines
T
Jean Beth S. Jontilaa,b, Harold M. Monteclaroa,∗, Gerald F. Quinitioa, Sheila Mae Santander-de Leona, Jon P. Altamiranoc a
Institute of Marine Fisheries and Oceanology, College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, Iloilo, Philippines College of Fisheries and Aquatic Sciences, Western Philippines University, Puerto Princesa City, Philippines c Aquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan, Iloilo, Philippines b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biodiversity Species richness Fisheries management Sustainability
This study was conducted to investigate the sea cucumber fishery and compare populations between exploited and unexploited sites. Three islands were selected, the Arrecife Island as the unexploited site and the Johnson and Green Islands representing the exploited sites. In each site, sea cucumber species richness, diversity and densities were assessed by laying as much as 15 transects (50 m × 5 m) per habitat in each island. Differences in species richness, diversity and relative densities across sites and habitats were tested using a Two-way Analysis of Variance (ANOVA) and Tukey test for post hoc comparisons. An interview with gatherers, key informants and focus group discussions were also conducted to gather information on the sea cucumber fishery and its management. Results showed that the unexploited site had a higher species richness (14 vs. 7 and 7). Relative density of species was also higher in the unexploited site at 1245 ind ha−1 while it was only 78 and 39 ind ha−1 in exploited sites (p < 0.05). Interviews and a focus group discussion revealed that national regulations on permit system and size limits were not enforced at the local level and that gatherers had low levels of awareness regarding regulations on sea cucumber harvest. Current management measures appear to be ineffective and insufficient, leaving the sea cucumbers in areas open to exploitation at risk of depletion. Given that sea cucumbers provide substantial income to local communities, the depletion of this resource could compromise the livelihood of people in island communities that rely heavily on marine resources for living. Thus, this study highlights the need to review national policies on sea cucumber fishery and place the management at the local level.
1. Introduction Sea cucumbers are primarily harvested for the production of trepang locally called balat or balatan. Trepang refers to the dried body wall of a sea cucumber, which is a prime delicacy in some Asian cultures (Akamine, 2005; Choo, 2008). Sea cucumbers are also used in the production of various nutraceutical and pharmaceutical products and recent studies have shown that they have anti-fungal, anti-microbial and anti-cancer properties (Bordbar et al., 2011). Over 70 species of sea cucumbers are harvested in more than 70 countries all over the world but most are sourced from the wild fisheries of tropical countries (Purcell et al. 2012, 2018). The sea cucumber fishery forms a multi-million dollar industry (Gamboa et al., 2004) and the increasing demand in the world market fueled massive exploitation in many areas across the globe (Uthicke,
∗
2004; Conand, 2006; Purcell, 2010; Hasan and Abd El-Rady, 2012; Pakoa and Bertram, 2013; Conand et al., 2014). In fact, many sea cucumber stocks worldwide are overfished because of their high value and ease of capture. Among the overfished areas are Galapagos, Indonesia, Malaysia, Papua New Guinea, Solomon Islands, New Caledonia, Australia, Red Sea in Egypt, Madagascar, Fiji Islands and the Philippines (Uthicke and Conand, 2005). For most of the traded species, prices have increased tremendously with increasing size especially for the high valued ones like Holothuria fuscogilva, H. lessoni and H. scabra (Purcell et al., 2018). The Philippines is one of the major producers and exporters of trepang in the world (Choo, 2008; Anderson et al., 2010). About 20% of Philippine sea cucumber landings come from Palawan (Brown et al., 2010). In 2014, sea cucumbers ranked 9th among the major fishery exports of the country in terms of value (DA-BFAR, 2014). In 1992, the
Corresponding author. E-mail address: [email protected] (H.M. Monteclaro).
https://doi.org/10.1016/j.ocecoaman.2018.08.025 Received 13 March 2018; Received in revised form 21 August 2018; Accepted 24 August 2018 0964-5691/ © 2018 Elsevier Ltd. All rights reserved.
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Philippines contributed almost 16% of the world's production by volume but accounted only 8.2% of the global production value for the exports were mostly of low value (Akamine, 2005). Akamine (2002) also reported that the Philippines sea cucumber fishery had shifted from low-volume/high-value to high-volume/low value due to speculated shortage of supply from the wild. Despite being artisanal in scale, the sea cucumber fishery provides substantial income to many marginal fishers in the country (Labe, 2009). Its exploitation has not been regulated since the 1970s and in fact, the country has been identified as sea cucumber hotspot in Asia for the lack of regulations on its collection and trade and poor statistical records (Choo, 2008). The number of exploited species had also increased over the years from 24 in 2000 to at least 32 in 2012 (Schoppe, 2000; Jontila et al., 2014). The need for management of the Philippine sea cucumber fishery has long been emphasized (Gamboa et al., 2004) yet it was only in 2013 that the government released the Administrative Circular (AC) Order 248, which requires permits among collectors and traders and imposes a 5 cm size limit on dried products (DA-BFAR, 2013). However, the effectiveness or enforcement of this regulation is not known and preliminary information revealed that gathering of sea cucumbers remains open-access and unregulated. The proper management of the sea cucumber fishery is very important especially in island communities where marginal fishers have limited livelihood opportunities. This study was therefore conducted to investigate the sea cucumber fishery and its populations to generate information that can be used to improve its management. Specifically, it aims to assess the present status of sea cucumber population in terms of species richness, diversity and density between exploited and unexploited sites. It also aims to evaluate the enforcement of laws and regulations on sea cucumber fishery at the local level. Based from the data gathered, a management plan that can be adopted by the local government units in Palawan is suggested. Results of this study are useful for local and national officials who are tasked to manage valuable yet endangered aquatic resources such as sea cucumbers.
the afternoon while shallow coral reefs (∼1 m deep during lowest tide) were assessed through snorkeling at night as most of the reef species are nocturnal (Purcell et al., 2012). In situ photos were taken. Identification of species was based on the works of Conand (1998), Massin et al. (2002), Purcell et al. (2012) and Samyn (2013). To investigate the socio-demographic profile and harvesting practices of sea cucumber gatherers in exploited sites, a survey was conducted among 36 gatherers in Green Island and 43 in Johnson Island. This number represented about 13% of the total households in the two study sites. A structured questionnaire was used in the study which included questions on 1) harvesting method, 2) harvesting grounds, 3) time of harvesting, 4) number of persons involved in the harvesting, 5) gatherers’ perception on the abundance and diversity of sea cucumbers in their area, and 6) comparison of sea cucumber catch between the past (10 years before) and the present (study period). The gatherers were also asked to identify sea cucumber species that they were harvesting through the use of sea cucumber photos and pictures (Purcell et al., 2012). To gather information on the sea cucumber fishery and its management, key informant interviews (KIIs) were conducted involving three sea cucumber processors, three Barangay or village officials, one leader of a Fishers’ Association, two staff members of the Palawan Council for Sustainable Development (PCSD) and one from the Bureau of Fisheries and Aquatic Resources (BFAR)-Provincial Fishery Office (PFO). They were asked about existing national and local policies on sea cucumber collection (e.g., size limit) and the management measures implemented or adopted by their respective offices. A Focus Group Discussion participated by five personnel of the Roxas Municipal Fishery and Aquatic Resource Management Office (MFARMO) was also conducted to discuss implementation of national regulations on sea cucumber collection at the local level.
2. Materials and methods
Sea cucumber populations were assessed in terms of species richness, diversity and density. Species richness is simply the number of species found in each site while diversity relates to the number of sea cucumber species in the community to the relative abundance of each species. Diversity across habitats and sites was determined using the Shannon Diversity Index (SDI) with the formula:
2.3. Data analysis
2.1. Study sites Three islands were selected in this study - Arrecife Island, Johnson Island and Green Island. All islands are situated in the east coast of Palawan, Philippines (Fig. 1). Arrecife Island is a private island resort located in Honda Bay, Puerto Princesa City, Palawan. It represented the unexploited site for gleaning and fishing are not allowed in this area since its establishment in 1997. There were no fishing communities within the island and only the resort personnel and tourists were allowed to stay. Security personnel were stationed in strategic areas around the island for the safety of tourists and ensured that no fishers encroached inside and around the island. The exploited sites were represented by Johnson and Green Islands in Roxas, Palawan. Johnson Island had 154 households with a population of 617 while Green Island had 455 households with a population of 1813. As island communities, fishing was the main livelihood of residents.
S
H= − ∑i = 1 (Pi ∗ln Pi) where: H = the Shannon diversity index Pi = fraction of the entire population made up of species i S = numbers of species encountered ∑ = sum from species 1 to species S For density, only the commercial species were considered for these are the target of fishers. Relative density was calculated as number of individuals per hectare (Purcell et al., 2009). Relative density did not show normal distribution, thus these were log transformed and subjected to Two-way Analysis of Variance (ANOVA) to determine the differences in species richness, diversity and relative density among sites and across habitats. The Tukey test was used for post hoc analysis and all tests were performed using the Statistical Package for Social Sciences (SPSS) version 16. Results of the interviews and FGD were tabulated accordingly.
2.2. Data collection The study was conducted from 24 April to 5 June 2015. The various sea cucumber habitats such as sea grass beds, reef flats and coral reefs (Conand, 1998; Purcell et al., 2012) were assessed using a 50 m × 5 m (250 m2) transect line. Three stations were established in reef flats and five in seagrass beds and coral reefs. Each station had three transects rendering a total of 9750 m2 area covered per island. All commercially important species within the transect were identified and counted. Only one non-commercially important species was recorded in the study sites, i.e., Synapta maculata, which was noted for occurrence. The seagrass beds and reef flats were surveyed by walking during low tide in 226
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Fig. 1. A map of Palawan, Philippines showing the locations of the study sites. (Source: www.mapinfo.com and www.philgis.org).
3. Results and discussion
beyond 5 h because it would be difficult for them to dive when the tide was high. In addition, Stichopus species are sensitive such that the body liquefies once exposed to air thus, this species can only be kept in seawater for a short duration. By June, the gathering of sea cucumbers slowed down because the rough sea conditions brought by the southwest monsoon rendered it unsafe for fishers to travel far from the shore. Gleaners gathered sea cucumbers during low tide in the afternoon, but unlike divers, their activity was restricted in shallow seagrass areas around the island. Gleaning was generally performed between late March and early June because this was the time of the year when the lowest tide would be in the afternoon. This period also coincided with the end of the school year. With the extra available time, mothers and their children could spend about 4 h each day for gleaning. When school started again in mid June, gleaning activities started to decline. Also, gleaners said that the low tide in the afternoon during this time of the year would not be low enough and shorter in period which reduced gleaning efficiency. On the average, male fishers generated a monthly income of USD 153.35 (1 USD=PhP 51.9645). About 23% of their monthly income came from sea cucumber harvesting while the rest were mainly from fishing (56%), seaweed farming (18%) and other sources (2%). In contrast, gleaners only earned USD 55.73 each month but as much as 56% of this amount came from sea cucumber gathering with the rest mainly from seaweed farming (36%) and other sources (8%). This shows that gleaners were highly dependent on gathering of sea cucumbers. The income profile of all gatherers also showed that they belonged to the marginal sector, living below the poverty threshold. In 2015, a family of five needed at least USD 176 average monthly income to meet their basic food and non-food needs (PSA, 2016). Further, about 70% of the gatherers only attended primary school level, 28% were able to attend secondary education, while the 2% had no formal education.
3.1. Sea cucumber harvesting methods and trade in Palawan Local sea cucumber fishers employed two methods to harvest sea cucumbers. Male fishers performed skin diving while female fishers and children collected sea cucumbers through gleaning or handpicking during low tide. Fishers gathered sea cucumbers in coral reefs while gleaners only collected in seagrass beds and reef flats. Sea cucumbers were generally sold and traded in Puerto Princesa City, the capital of Palawan. All divers considered fishing as their main source of income and gathering of sea cucumbers was only by chance encounter during spear fishing at daytime, as the case of divers in Green Island. In Johnson Island, diving for sea cucumbers was more directed rather than by chance. In March until June at spring tide, fishers in Johnson Island go in fleets at night to gather mainly sea cucumbers in reefs near mainland Roxas. From interviews, fishers stated that at night during full moon and new moon, they observed that a lot of sea cucumbers in coral reefs would crawl out of crevices and stay on top of the reef. They termed this phenomenon “mass surfacing”, during which, over a hundred individuals of high-value, reef associated sea cucumbers like Stichopus species can be harvested in a single trip. In such trips, they could earn much more compared to what they normally earned when they go fishing. While it is not clear why Stichopus species exhibit mass surfacing, some protection must be done during this period as massive and unregulated harvesting could severely reduce their population. Normally, a group of 3–5 fishers would go out in a boat to gather sea cucumbers. They would leave at 7:00 or 8:00 p.m. and returned early in the morning at 3:00 or 4:00 a.m. Fishers spent 3–4 h of travel time so only about 4 h were actually devoted to gathering. They did not go
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Fig. 2. Sea cucumber species recorded in Arrecife, Green and Johnson Islands, Palawan, Philippines: a) Actinopyga echinites; b) Actinopyga lecanora; c) Bohadschia marmorata; d) Bohadschia vitiensis; e) Holothuria atra; f) Holothuria leucospilota; g) Holothuria edulis; h) Holothuria fuscocinerea; i) Holothuria gracilis; j) Holothuria leucospilota; k) Holothuria scabra (white variant); l) Holothuria scabra (black variant); m) Pearsonothuria graeffei; n) Stichopus horrens; o) Stichopus monotuberculatus; p) Stichopus rubermaculosus; q) Stichopus vastus; r) Synapta maculata. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
variants of Holothuria scabra), Stichopodidae and Synaptidae were recorded in this study (Fig. 2). All recorded species were commercially exploited and processed into trepang, except for Synapta maculata. Majority (14) of the recorded species were noted in Arrecife Island while only seven were encountered in Green Island and also seven in Johnson Island. Eight out of the 14 species encountered in Arrecife Island were exclusively noted in this island such as Actinopyga echinites,
This educational profile made it difficult for people in island communities to secure regular or high paying jobs thus, most of them generally relied on harvesting marine resources for living. 3.2. Species richness, diversity and relative density A total of 17 species belonging to families Holothuriidae (with two 228
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Fig. 2. (continued)
(p > 0.05, Tukey test). Arrecife Island had a mean diversity index of 0.58 which was significantly higher than that in Green Island (0.24) and Johnson Island (0.14) (p < 0.05, two-way ANOVA). This result indicates that the repeated encounter of a particular species in Arrecife Island was more frequent compared in Green and Johnson Islands. It could also mean that the abundance of sea cucumbers was distributed among all species in the community while it was fragmented in other habitats especially in Johnson Islands with diversity index of 0.14. This phenomenon is probably a consequence of the prevalent harvesting in Green and Johnson Islands. Mean diversity indexes across habitats were not significantly different (p > 0.05, two-way ANOVA). Table 2 shows sea cucumber mean density according to site, habitat and site-and-habitat interaction. Total mean density was highest in Arrecife Island at 1245 ind ha−1 while it was only 78 ind ha−1 in Green Island and 39 ind ha−1 in Johnson Island (p < 0.05, two-way ANOVA). Assuming that the three islands originally had similar levels of abundance, the remaining sea cucumbers in Green and Johnson Islands would be 6% and 3%, respectively of the original population. These values are way below the target reference level for sustainable
A. lecanora, Holothuria atra, H. edulis, H. leucospilota, Pearsonothuria graeffei, Stichopus rubermaculosus and S. vastus. A. echinites is a vulnerable species listed under the International Union for Conservation of Nature (IUCN) while S. rubermaculosus and S. vastus can be considered as rare species for they had not been reported in other parts of the country except in Palawan (Kerr et al., 2006; Olavides et al., 2010; Jontila et al., 2014; Romero and Cabansag, 2014; Dolorosa et al., 2017). There were also several rare species that were only noted in the exploited sites such as Holothuria gracilis, S. horrens and S. monotuberculatus although these species, except S. horrens, were previously reported in Arrecife Island (Jontila et al., 2017). Jontila et al. (2017) completed their study through SCUBA diving in deeper coral reefs while in this study, only snorkeling was done. In addition, the present study only assessed relatively shallow reef areas (∼1 m deep) and could be the reason why some reef-associated species were not recorded. Table 1 presents the species richness and diversity recorded in seagrass beds, reef flats and coral reefs of three islands. For species richness, analysis showed that it differed significantly across sites (p < 0.05) but not among habitats (p > 0.05, two-way ANOVA). In particular, species richness in Arrecife Island was significantly higher than those in Green and Johnson Islands (p < 0.05, Tukey test), but no significant differences were detected between the last two islands
Table 2 Sea cucumber relative density across habitats between unexploited and exploited sites.
Table 1 Sea cucumber species richness and diversity across habitats between unexploited and exploited sites. Habitat
Seagrass Reef Flats Coral Reefs Total Mean
Habitat
Relative Density (ind.ha−1)
Species Richness
Shannon Diversity Index (SDI)
Unexploited
Exploited
Unexploited
Unexploited
Arrecife
Green
Johnson
51 22 5 78b
21 4 13 39 b
Exploited
Exploited
Arrecife
Green
Johnson
Arrecife
Green
Johnson
9 4 7 14a
5 3 2 7b
3 1 4 7b
0.95 0.46 0.34
0.30 0.44 0.0
0.14 0.0 0.27
0.58a
0.24b
0.14b
Seagrass Reef Flats Coral Reefs Total
∗
1117 27 101 1245a
Mean
396 a 18 b 40 b
Letter notations indicate significant difference (p < 0.05, two way ANOVA). ∗ Indicates that sea cucumber mean density in Arrecife-seagrass beds is significantly different than other site-and-habitat interaction (p < 0.05, one way ANOVA).
Letter notations indicate significant difference (p < 0.05, two-way ANOVA). 229
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Table 3 Total mean densities (ind.ha−1) of each sea cucumber species across all habitats in unexploited and exploited sites. Species
Family Holothuriidae 1. Actinopyga echinites 2. Actinopyga lecanora 3. Bohadschia marmorata 4. Bohadschia vitiensis 5. Holothuria atra 6. Holothuria coluber 7. Holothuria edulis 8. Holothuria fuscocinerea 9. Holothuria gracilis 10. Holothuria leucospilota 11. Holothuria scabra 12. Pearsonothuria graeffei Family Stichopodidae 13. Stichopus horrens 14. Stichopus monotuberculatus 15. Stichopus rubermaculosus 16. Stichopus vastus Family Synaptidae 17. Synapta maculata∗ Total Density
Total mean density (ind.ha−1) Unexploited
Exploited Sites
Arrecife Is.
Green Is.
Johnson Is.
Characteristics
11 155 640 35 296 27 133 93 – 80 21 13
– – 64 21 – 13 – 59 – – 11 –
– – 27 – – 27 – – 13 – 5 –
Burying Nocturnal Burying Burying Non-burying Cryptic Non-burying Burying Cryptic, nocturnal Non-burying Burying Cryptic, nocturnal
27
Cryptic, Cryptic, Cryptic, Cryptic, Cryptic,
67 133
– –
13 27 – –
(17) 1704a
(29) 195b
(45) 112 b
nocturnal nocturnal nocturnal nocturnal nocturnal
* No commercial value, density is not included in the total. Letter notations indicate significant difference (p < 0.05, two-way ANOVA).
Other exploited sites in the country like Bolinao and Anda (both in Pangasinan province) also had lower densities of sea cucumbers at 0.3 to 9 ind ha−1 (Olavides et al., 2010). Similar studies also showed that areas open to exploitation have lower densities of sea cucumbers than protected sites (Conand and Muthiga, 2007). However despite the longterm pressure from unregulated gathering in Green and Johnson Islands, it is interesting that B. marmorata, B. vitiensis and H. scabra were able to maintain sizeable populations. Such circumstances might be attributed to the burying behavior of these species, which allow them to avoid predators including gatherers at certain times (Clouse, 1997, Mercier at al. 1999, Wolkenhauer et al., 2010). Notice that Bohadschia species along with H. atra were the most abundant in Arrecife Island but H. atra was not encountered in Green and Johnson Islands, probably because these species do not bury and were therefore prone to overharvesting. In fact, all the recorded species in Green and Johnson Islands were either burying, cryptic or nocturnal that come out of crevices only at night such as the Stichopus species (Purcell et al., 2012). Such behaviors limit their exposure to gleaners who would otherwise harvest them indiscriminately. Nonetheless, species with such behaviors remain vulnerable to depletion if unregulated harvesting continues. For instance in Red Sea, B. marmorata and B. vitiensis were exhausted after a decade of unregulated fishing (Hasan and Abd El-Rady, 2012).
harvesting which is about 40% of the original stock. These results suggest that sea cucumbers in Green and Johnson Islands are overfished. Across habitats, the highest mean sea cucumber density was recorded in seagrass beds (396 ind. ha−1) while mean densities between reef flats (18 ind. ha−1) and coral reefs (40 ind. ha−1) were not significantly different (p > 0.05, two-way ANOVA). In addition, relative densities as a result of interaction between sites and habitats displayed significant differences (p < 0.05, two-way ANOVA, Table 1). The highest density as a result of the site-and-habitat interaction was recorded in seagrass beds of Arrecife Island (p < 0.05, one-way ANOVA). The high relative density in Arrecife Island was attributed to the high density of some species in seagrass beds particularly the B. marmorata at 640 ind ha−1 and H. atra with 296 ind ha−1 (Table 3). In contrast, B. marmorata in Green and Johnson Islands was estimated at 64 and 27 ind ha−1, respectively. In addition, H. atra was not recorded in both exploited sites. These species were commonly found in shallow seagrass beds and coral reefs making them prone to overharvesting. All sea cucumber species in Green and Johnson Islands had low relative density estimates (< 100 ind ha−1) and most were in critical conditions (< 30 ind ha−1). This means that the number of individuals were not enough to successfully repopulate the area (Purcell et al., 2009). S. maculata, a species that is of no commercial value, was more abundant in Green and Johnson Islands than in Arrecife Island. This could possibly be due to the low level of competition for food and space among species in exploited sites. The low density of sea cucumbers in Green and Johnson Islands can likely be attributed to unregulated harvesting that started in the 1980's. Based on interviews with fishers in Green Island, they used to go in fleets around their island during low tide at night to gather fish and invertebrates including sea cucumbers. Fishers had identified at least 26 species that they used to collect around the island, but only six of those were encountered in this study (Table 4). Gatherers added that A. echinites, A. lecanora, B. marmorata, B. vitiensis, H. atra, H. edulis, H. leucospilota and H. scabra used to abound in seagrass beds, yet of these, only B. marmorata, B. vitiensis and H. scabra were recorded in this study. These species among other commercially important ones are usually the first to disappear in heavily exploited sites (Uthicke and Conand, 2005).
3.3. Perception on sea cucumber population and management All gatherers surveyed claimed that sea cucumbers were far more abundant and more diverse in the past 10 years than the present. They said that in the past, a one-hour gleaning trip could yield a bucket full with different sea cucumbers species. They added that they used to glean in seagrass beds and shallow reefs just around their area. However, they could no longer collect as many sea cucumbers in present times. During the study period, only nine women in Green island were engaged in gleaning of sea cucumbers. Many of them had shifted to seaweed farming because gleaning was no longer profitable due to scarcity of sea cucumbers around the island. As for the divers, they had to travel to farther reefs because sea cucumbers had become scarce in 230
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Table 4 Sea cucumber species that gatherers have been collecting in Green and Johnson Islands. Family Holothuriidae
Local name
Green Is.
Johnson Is.
Arrecife Is.
1. Actinopyga echinites 2. Actinopyga lecanora 3. Actinopyga sp. 4. Bohadschia argus 5. Bohadschia marmorata 6. Bohadschia vitiensis 7. Holothuria atra 8. Holothuria coluber 9. Holothuria edulis 10. Holothuria fuscocinerea 11. Holothuria fuscogilva 12. Holothuria fuscopunctata 13. Holothuria gracilis 14. Holothuria leucospilota 15. Holothuria scabra 16. Holothuria whitmaei 17. Pearsonothuria graeffei Family Stichopodidae 18. Stichopus chloronotus 19. Stichopus herrmanni 20. Stichopus horrens 21. Stichopus monotuberculatus 22. Stichopus rubermaculosus 23. Stichopus vastus 24. Thelenota anannas 25. Thelenota anax 26. Thelenota rubralineata No. of species noted in this study No. of species gatherers used to collect
Khaki, Brown beauty Munang, Buli-buli Hudhod Leopard, Matang-itik Lawayan, Hangad-langit, Tagukan Lawayan taba Black beauty Patola white, Tambor Hotdog, Lipstikan, Red beauty Labuyo Susuan Sapatos Patola Kurtido, Kiskisan, Putian Susuan Flower, Pinya-pinya
0 0 0 0 + + 0 + 0 + 0 0 0 0 + 0 0
0 0 0 0 + 0 0 + 0 0 0 0 + 0 + 0 0
+ + 0 0 + + + + + + 0 0 + + + 0 +
Tres/Cuatro cantos, Mani-mani, Dilawan Hanginan Hanginan Hanginan Emag, Hanginan Tinikan Legs Paag-daga, Hanginan
0 0 + 0 0 0 0 0 0 6 26
0 0 + + 0 0 0 0 0 6 26
0 0 + + + + 0 * 0 19
0 species that used to occur around the island. + species noted in this study. * Documented by Dive Instructor of Arrecife Island.
their traditional fishing areas. When asked to identify the causes of sea cucumber depletion in their locality, all respondents identified massive and unregulated harvesting as the main cause of the problem (Table 5). Several respondents (11%) attributed habitat destruction as a consequence of blast fishing that led to the decline of sea cucumber population. When asked to identify laws or regulations or any management measures pertaining to the regulation of sea cucumber collection, all could not identify any. Also, fishers were not aware that some sea cucumber species were threatened and therefore should not be collected (Table 6). Gatherers were also asked of their perceptions on the management of sea cucumbers in their area. Table 5 presents the questions asked to which all of them responded negatively. Gatherers did not know any regulations pertaining to the collection of sea cucumbers. They did not have permits and just freely collected and traded sea cucumbers in violation of AC 248 which requires gatherers and traders to secure a wildlife collector's permit and transport permit, respectively. It was learned that they never experienced having been prohibited from gathering sea cucumbers. The practice of selling small dried products (< 5 cm) to traders in Puerto Princesa City continued. While AC 248 prohibits the collection of threatened sea cucumbers, A. echinites, H.
scabra and S. herrmanni were freely collected and traded. This was a common scenario even in other sites in the province (Dolorosa et al., 2017). It seems there was a problem with the enforcement of policies related to sea cucumber. There was also a clear need to increase the awareness of key stakeholders on policies related to the sea cucumber fishery. Interestingly, gatherers mentioned that species like dugong (Dugong dugon), sea turtles, giant clams, top shell (Tectus niloticus) and Napoleon wrasse (Cheilinus undulatus) were protected species and must not be collected. They got the information from local radio and information campaign conducted by several non-government and government organizations. Respondents could not recall any similar campaign or propaganda for sea cucumbers. Interviews with key informants likewise showed that the fishery was not given attention in terms of management. All of them were not aware of size limits and AC 248 although the Bureau of Fisheries and Aquatic Resources (BFAR) monitors the outgoing volume of dried sea cucumbers and the Palawan Council for Sustainable Development (PCSD) included some threatened sea cucumbers (such as H. fuscogilva H. scabra, H. whitmaei and Thelenota ananas) in their printed information materials. The local government units (LGUs) neither adopted the
Table 5 Causes of sea cucumber population decline based on perception of gatherers. Issue/Concern
1. 2. 3. 4. 5.
Unregulated harvesting Habitat destruction Disease Predators Climate change (increase in seawater temperature) 6. Others (please specify)
Percentage of Respondents (N = 79) 100% 11% 0 0 0
Remarks
Blast fishing in the 90's Not observed Not observed The term is familiar only to few and though divers have observed bleaching of some corals, they did not associate it with the decline in population of sea cucumbers.
0
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Table 6 Gatherers’ perception on the management of sea cucumber populations. Question
1. Do you know of any regulation related to the collection of sea cucumbers? 2. Do you know of any regulation related to the management of sea cucumbers? 3. Are you aware which sea cucumber species is considered as threatened or endangered? 4. Do you have a permit to collect sea cucumbers? 5. Do you pay any fees for harvesting sea cucumbers? 6. Do you know at which size the sea cucumbers should be allowed to be collected? 7. Did any personnel from relevant national or local agency visit your area to conduct information campaign on sea cucumber collection?
Percentage of response (n = 80) Yes
No
0
100%
0
100%
0
100%
0 0 0
100% 100% 100%
0
100%
Remarks
Some gatherers mentioned that Dugong, sea turtles, giant clams, top shell (Tectus niloticus) and Napoleon wrasse (Cheilinus undulatus) are protected species
BFAR and LGU provided an assistance on seaweed farming only
It is suggested that the PCSD adopt the minimum size limit on dried sea cucumbers as implemented by other Pacific Islands like Papua New Guinea (PNG), Vanuatu and Solomon Island (Muthiga and Conand, 2014; NFA, 2016), only for the time being until local studies on reproductive biology of exploited species become available. For instance, the minimum size for dried sea cucumbers set by PNG for H. scabra, H. edulis and Bohadschia spp. is 10 cm and for H. atra, H. coluber and H. fuscogilva is 15 cm (NFA, 2016). By enforcing size regulations, gatherers and traders could gain more economic benefit as larger-sized trepang command higher prices. It is also suggested that the collection of endangered sea cucumber species, which are mostly high-value and sought after by gatherers, be strictly banned. Such policy can be adopted by the LGUs through a local ordinance and supported by local law enforcers. The LGU should also establish licensing and monitoring schemes for gatherers and traders. Setting of a closed season during peak of spawning can also be explored provided such is supported by studies (Muthiga and Conand, 2014). Rotational closure of identified gleaning sites around the island is also worth exploring to allow recovery of the wild stock while allowing gathering in other sites. Closures of fishery and ban in export have been implemented in some Pacific Island Countries to allow recovery of stocks (Pakoa and Bertram, 2013). However, since these measures seem drastic and will greatly affect a lot of marginal fishers in Palawan, this should be carefully studied. The LGU should also encourage the formation of cooperatives composed of sea cucumber gatherers. This can be helpful in ensuring quality and appropriate price for their product and leveraging funds for other livelihood programs. In addition, it shall be easier for local enablers to disseminate necessary information to the fishers and instill stewardship values among resource users. For some sea cucumber species with available technology for full cycle production, sea ranching is a promising way to achieve optimum economic benefit from farmed products while maintaining and enhancing the natural stock (Hair et al., 2016). There had been successful reports of similar efforts in other areas (e.g., Bolinao, Pangasinan, Philippines), wherein an organized group of locales co-manage the rearing of sandfish (Holothuria scabra). Since sea ranching requires hatchery-produced juveniles, the BFAR could probably facilitate its establishment in strategic locations in Palawan. This will provide supply of juveniles that can be used for grow-out culture, sea ranching and stock enhancement of depleted sites. Academic institutions can also be tapped to conduct studies on reproductive biology of commercially important sea cucumbers to determine the size at maturity, which is needed in establishing the size limit. Assessment and monitoring of wild population can also be done by HEIs as well as the conduct of information, education and communication (IEC) activities and production of IEC materials in
AC 248 nor implemented size limits or any management measure. The LGUs failed to monitor sea cucumber landings nor collected tax in the form of invoice issuance, as they did for fish and other marine products. The LGUs therefore need to consider monitoring and record keeping of sea cucumber harvest (through auxiliary invoice), which could also add to LGUs revenue. Other offices such as the Municipal Fishery and Aquatic Resource Management Office (MFARMO), which mainly focused on fishing, seaweed farming and live fish trading, also need to consider improving its monitoring and record keeping. It is recommended that LGUs, especially those with existing sea cucumber fisheries, should review local policies and adopt ordinances that provide management for these resources. In addition, a review of AC 248 seems to be necessary. For example, the administrative order sets the minimum size for all dried sea cucumbers at 5 cm. While this provision favors the conservation of sea cucumbers that mature at small size, it also promotes the exploitation of large species like T. ananas, T. anax and other Stichopus species that can grow to almost a meter in length. The size regulation should therefore be species specific.
3.4. Policy recommendations This study proposes a management framework (Fig. 3) that could be valuable in addressing the poor ecological state of the sea cucumber populations in Palawan, as well as improve its fishery. This plan is formulated based on the weaknesses/threats (i.e., weak implementation of laws, unregulated trade, weak monitoring system, poor knowledge on the resource, lack of political will of LGUs, loss of livelihood, etc.) and strengths/opportunities (i.e., sea cucumber hatchery and nursery technologies, sea ranching, local knowledge of the resource, presence of pro-active officials and research institutions, etc.) of the sea cucumber fishery in Palawan. It is recommended that the Palawan Council for Sustainable Development (PCSD) serve as the lead agency in the development of a management program for sea cucumbers in Palawan as PCSD is mandated to implement the Strategic Environmental Plan for the province (Republic Act 7611). The PCSD can be assisted by an ad hoc committee that shall be composed of other key players such as the PCSDS (which is the implementing arm of the PCSD), BFAR, Department of Environment and Natural Resources (DENR), higher education institutions (HEIs), Department of Education (DepEd), LGUs, the Philippine National Police, non-government and peoples' organizations, sea cucumber fishers’ cooperatives, traders, and other stakeholders. The ad hoc committee shall be tasked to formulate plans and programs, conduct regular monitoring, ensure law enforcement, and coordinate efforts of all stakeholders. Fig. 3 also shows the proposed management structure with recommended policy options and roles of stakeholders and agencies involved. 232
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Fig. 3. Proposed management scheme for the sea cucumber fishery in Palawan, Philippines.
to sustain the economic as well as the ecological benefits sea cucumbers provide. Policy development is the immediate need that must be addressed, followed by implementation and enforcement of pertinent laws and management programs at the local level. Conducting an information campaign is the most doable action that can be done immediately even in the absence of policy. Education might change the perspective of the gatherers, as such has been proven effective in gaining their support on conservation and proper utilization of some marine resources.
collaboration with PCSDS, BFAR, DENR, NGOs and LGUs. For grade school levels in coastal communities, the DepEd can facilitate the information campaign since children are also involved in gathering. 4. Conclusion This study shows that diversity and populations of commercially important sea cucumbers are negatively affected by unregulated harvesting. Some species in heavily-exploited sites might encounter the risk of depletion for their present estimates might not be enough to allow repopulation, especially that harvesting remained open. Sea cucumbers’ vulnerability to depletion was further heightened by the lack of regulations in the sense that pertinent laws were insufficient, not enforced, and therefore ineffective. It is feared that some species, such as A. echinites, A. lecanora and H. atra, which used to be collected in the area, might had been depleted already as they were not encountered during the survey, nor presently collected by the gatherers around their area. If unregulated harvesting will not be addressed, the sea cucumber population in areas open to exploitation could collapse, which could further affect the diversity and the overall productivity of the ecosystem they share (Mercier et al., 1999; Uthicke, 1999; Wolkenhauer et al., 2010). Sea cucumbers in nearby sites will likely soon be depleted for as mentioned, fishers were already venturing to farther areas. Like other small-scale fisheries, the sea cucumber fishery is also very important. It sustains the livelihood of people in coastal areas who have no other means to sustain their living other than relying on marine resources. Thus, it is important that its fishery should be managed at a local level
Acknowledgement This study was jointly funded by the Department of Science and Technology- Science Education Institute (DOST-SEI), the University of the Philippines Visayas and the Western Philippines University. The support and cooperation of the Municipality of Roxas, Palawan, the management of Arrecife Island especially Ms. Glesselle T. Batin, and the sea cucumber gatherers in Green and Johnson Islands are greatly appreciated.
Appendix A. Supplementary data Supplementary data related to this article can be found at https:// doi.org/10.1016/j.ocecoaman.2018.08.025.
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Status of sea cucumber fishery and populations across sites with different levels of management in Palawan, Philippines
T
Jean Beth S. Jontilaa,b, Harold M. Monteclaroa,∗, Gerald F. Quinitioa, Sheila Mae Santander-de Leona, Jon P. Altamiranoc a
Institute of Marine Fisheries and Oceanology, College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, Iloilo, Philippines College of Fisheries and Aquatic Sciences, Western Philippines University, Puerto Princesa City, Philippines c Aquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan, Iloilo, Philippines b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biodiversity Species richness Fisheries management Sustainability
This study was conducted to investigate the sea cucumber fishery and compare populations between exploited and unexploited sites. Three islands were selected, the Arrecife Island as the unexploited site and the Johnson and Green Islands representing the exploited sites. In each site, sea cucumber species richness, diversity and densities were assessed by laying as much as 15 transects (50 m × 5 m) per habitat in each island. Differences in species richness, diversity and relative densities across sites and habitats were tested using a Two-way Analysis of Variance (ANOVA) and Tukey test for post hoc comparisons. An interview with gatherers, key informants and focus group discussions were also conducted to gather information on the sea cucumber fishery and its management. Results showed that the unexploited site had a higher species richness (14 vs. 7 and 7). Relative density of species was also higher in the unexploited site at 1245 ind ha−1 while it was only 78 and 39 ind ha−1 in exploited sites (p < 0.05). Interviews and a focus group discussion revealed that national regulations on permit system and size limits were not enforced at the local level and that gatherers had low levels of awareness regarding regulations on sea cucumber harvest. Current management measures appear to be ineffective and insufficient, leaving the sea cucumbers in areas open to exploitation at risk of depletion. Given that sea cucumbers provide substantial income to local communities, the depletion of this resource could compromise the livelihood of people in island communities that rely heavily on marine resources for living. Thus, this study highlights the need to review national policies on sea cucumber fishery and place the management at the local level.
1. Introduction Sea cucumbers are primarily harvested for the production of trepang locally called balat or balatan. Trepang refers to the dried body wall of a sea cucumber, which is a prime delicacy in some Asian cultures (Akamine, 2005; Choo, 2008). Sea cucumbers are also used in the production of various nutraceutical and pharmaceutical products and recent studies have shown that they have anti-fungal, anti-microbial and anti-cancer properties (Bordbar et al., 2011). Over 70 species of sea cucumbers are harvested in more than 70 countries all over the world but most are sourced from the wild fisheries of tropical countries (Purcell et al. 2012, 2018). The sea cucumber fishery forms a multi-million dollar industry (Gamboa et al., 2004) and the increasing demand in the world market fueled massive exploitation in many areas across the globe (Uthicke,
∗
2004; Conand, 2006; Purcell, 2010; Hasan and Abd El-Rady, 2012; Pakoa and Bertram, 2013; Conand et al., 2014). In fact, many sea cucumber stocks worldwide are overfished because of their high value and ease of capture. Among the overfished areas are Galapagos, Indonesia, Malaysia, Papua New Guinea, Solomon Islands, New Caledonia, Australia, Red Sea in Egypt, Madagascar, Fiji Islands and the Philippines (Uthicke and Conand, 2005). For most of the traded species, prices have increased tremendously with increasing size especially for the high valued ones like Holothuria fuscogilva, H. lessoni and H. scabra (Purcell et al., 2018). The Philippines is one of the major producers and exporters of trepang in the world (Choo, 2008; Anderson et al., 2010). About 20% of Philippine sea cucumber landings come from Palawan (Brown et al., 2010). In 2014, sea cucumbers ranked 9th among the major fishery exports of the country in terms of value (DA-BFAR, 2014). In 1992, the
Corresponding author. E-mail address: [email protected] (H.M. Monteclaro).
https://doi.org/10.1016/j.ocecoaman.2018.08.025 Received 13 March 2018; Received in revised form 21 August 2018; Accepted 24 August 2018 0964-5691/ © 2018 Elsevier Ltd. All rights reserved.
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Philippines contributed almost 16% of the world's production by volume but accounted only 8.2% of the global production value for the exports were mostly of low value (Akamine, 2005). Akamine (2002) also reported that the Philippines sea cucumber fishery had shifted from low-volume/high-value to high-volume/low value due to speculated shortage of supply from the wild. Despite being artisanal in scale, the sea cucumber fishery provides substantial income to many marginal fishers in the country (Labe, 2009). Its exploitation has not been regulated since the 1970s and in fact, the country has been identified as sea cucumber hotspot in Asia for the lack of regulations on its collection and trade and poor statistical records (Choo, 2008). The number of exploited species had also increased over the years from 24 in 2000 to at least 32 in 2012 (Schoppe, 2000; Jontila et al., 2014). The need for management of the Philippine sea cucumber fishery has long been emphasized (Gamboa et al., 2004) yet it was only in 2013 that the government released the Administrative Circular (AC) Order 248, which requires permits among collectors and traders and imposes a 5 cm size limit on dried products (DA-BFAR, 2013). However, the effectiveness or enforcement of this regulation is not known and preliminary information revealed that gathering of sea cucumbers remains open-access and unregulated. The proper management of the sea cucumber fishery is very important especially in island communities where marginal fishers have limited livelihood opportunities. This study was therefore conducted to investigate the sea cucumber fishery and its populations to generate information that can be used to improve its management. Specifically, it aims to assess the present status of sea cucumber population in terms of species richness, diversity and density between exploited and unexploited sites. It also aims to evaluate the enforcement of laws and regulations on sea cucumber fishery at the local level. Based from the data gathered, a management plan that can be adopted by the local government units in Palawan is suggested. Results of this study are useful for local and national officials who are tasked to manage valuable yet endangered aquatic resources such as sea cucumbers.
the afternoon while shallow coral reefs (∼1 m deep during lowest tide) were assessed through snorkeling at night as most of the reef species are nocturnal (Purcell et al., 2012). In situ photos were taken. Identification of species was based on the works of Conand (1998), Massin et al. (2002), Purcell et al. (2012) and Samyn (2013). To investigate the socio-demographic profile and harvesting practices of sea cucumber gatherers in exploited sites, a survey was conducted among 36 gatherers in Green Island and 43 in Johnson Island. This number represented about 13% of the total households in the two study sites. A structured questionnaire was used in the study which included questions on 1) harvesting method, 2) harvesting grounds, 3) time of harvesting, 4) number of persons involved in the harvesting, 5) gatherers’ perception on the abundance and diversity of sea cucumbers in their area, and 6) comparison of sea cucumber catch between the past (10 years before) and the present (study period). The gatherers were also asked to identify sea cucumber species that they were harvesting through the use of sea cucumber photos and pictures (Purcell et al., 2012). To gather information on the sea cucumber fishery and its management, key informant interviews (KIIs) were conducted involving three sea cucumber processors, three Barangay or village officials, one leader of a Fishers’ Association, two staff members of the Palawan Council for Sustainable Development (PCSD) and one from the Bureau of Fisheries and Aquatic Resources (BFAR)-Provincial Fishery Office (PFO). They were asked about existing national and local policies on sea cucumber collection (e.g., size limit) and the management measures implemented or adopted by their respective offices. A Focus Group Discussion participated by five personnel of the Roxas Municipal Fishery and Aquatic Resource Management Office (MFARMO) was also conducted to discuss implementation of national regulations on sea cucumber collection at the local level.
2. Materials and methods
Sea cucumber populations were assessed in terms of species richness, diversity and density. Species richness is simply the number of species found in each site while diversity relates to the number of sea cucumber species in the community to the relative abundance of each species. Diversity across habitats and sites was determined using the Shannon Diversity Index (SDI) with the formula:
2.3. Data analysis
2.1. Study sites Three islands were selected in this study - Arrecife Island, Johnson Island and Green Island. All islands are situated in the east coast of Palawan, Philippines (Fig. 1). Arrecife Island is a private island resort located in Honda Bay, Puerto Princesa City, Palawan. It represented the unexploited site for gleaning and fishing are not allowed in this area since its establishment in 1997. There were no fishing communities within the island and only the resort personnel and tourists were allowed to stay. Security personnel were stationed in strategic areas around the island for the safety of tourists and ensured that no fishers encroached inside and around the island. The exploited sites were represented by Johnson and Green Islands in Roxas, Palawan. Johnson Island had 154 households with a population of 617 while Green Island had 455 households with a population of 1813. As island communities, fishing was the main livelihood of residents.
S
H= − ∑i = 1 (Pi ∗ln Pi) where: H = the Shannon diversity index Pi = fraction of the entire population made up of species i S = numbers of species encountered ∑ = sum from species 1 to species S For density, only the commercial species were considered for these are the target of fishers. Relative density was calculated as number of individuals per hectare (Purcell et al., 2009). Relative density did not show normal distribution, thus these were log transformed and subjected to Two-way Analysis of Variance (ANOVA) to determine the differences in species richness, diversity and relative density among sites and across habitats. The Tukey test was used for post hoc analysis and all tests were performed using the Statistical Package for Social Sciences (SPSS) version 16. Results of the interviews and FGD were tabulated accordingly.
2.2. Data collection The study was conducted from 24 April to 5 June 2015. The various sea cucumber habitats such as sea grass beds, reef flats and coral reefs (Conand, 1998; Purcell et al., 2012) were assessed using a 50 m × 5 m (250 m2) transect line. Three stations were established in reef flats and five in seagrass beds and coral reefs. Each station had three transects rendering a total of 9750 m2 area covered per island. All commercially important species within the transect were identified and counted. Only one non-commercially important species was recorded in the study sites, i.e., Synapta maculata, which was noted for occurrence. The seagrass beds and reef flats were surveyed by walking during low tide in 226
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Fig. 1. A map of Palawan, Philippines showing the locations of the study sites. (Source: www.mapinfo.com and www.philgis.org).
3. Results and discussion
beyond 5 h because it would be difficult for them to dive when the tide was high. In addition, Stichopus species are sensitive such that the body liquefies once exposed to air thus, this species can only be kept in seawater for a short duration. By June, the gathering of sea cucumbers slowed down because the rough sea conditions brought by the southwest monsoon rendered it unsafe for fishers to travel far from the shore. Gleaners gathered sea cucumbers during low tide in the afternoon, but unlike divers, their activity was restricted in shallow seagrass areas around the island. Gleaning was generally performed between late March and early June because this was the time of the year when the lowest tide would be in the afternoon. This period also coincided with the end of the school year. With the extra available time, mothers and their children could spend about 4 h each day for gleaning. When school started again in mid June, gleaning activities started to decline. Also, gleaners said that the low tide in the afternoon during this time of the year would not be low enough and shorter in period which reduced gleaning efficiency. On the average, male fishers generated a monthly income of USD 153.35 (1 USD=PhP 51.9645). About 23% of their monthly income came from sea cucumber harvesting while the rest were mainly from fishing (56%), seaweed farming (18%) and other sources (2%). In contrast, gleaners only earned USD 55.73 each month but as much as 56% of this amount came from sea cucumber gathering with the rest mainly from seaweed farming (36%) and other sources (8%). This shows that gleaners were highly dependent on gathering of sea cucumbers. The income profile of all gatherers also showed that they belonged to the marginal sector, living below the poverty threshold. In 2015, a family of five needed at least USD 176 average monthly income to meet their basic food and non-food needs (PSA, 2016). Further, about 70% of the gatherers only attended primary school level, 28% were able to attend secondary education, while the 2% had no formal education.
3.1. Sea cucumber harvesting methods and trade in Palawan Local sea cucumber fishers employed two methods to harvest sea cucumbers. Male fishers performed skin diving while female fishers and children collected sea cucumbers through gleaning or handpicking during low tide. Fishers gathered sea cucumbers in coral reefs while gleaners only collected in seagrass beds and reef flats. Sea cucumbers were generally sold and traded in Puerto Princesa City, the capital of Palawan. All divers considered fishing as their main source of income and gathering of sea cucumbers was only by chance encounter during spear fishing at daytime, as the case of divers in Green Island. In Johnson Island, diving for sea cucumbers was more directed rather than by chance. In March until June at spring tide, fishers in Johnson Island go in fleets at night to gather mainly sea cucumbers in reefs near mainland Roxas. From interviews, fishers stated that at night during full moon and new moon, they observed that a lot of sea cucumbers in coral reefs would crawl out of crevices and stay on top of the reef. They termed this phenomenon “mass surfacing”, during which, over a hundred individuals of high-value, reef associated sea cucumbers like Stichopus species can be harvested in a single trip. In such trips, they could earn much more compared to what they normally earned when they go fishing. While it is not clear why Stichopus species exhibit mass surfacing, some protection must be done during this period as massive and unregulated harvesting could severely reduce their population. Normally, a group of 3–5 fishers would go out in a boat to gather sea cucumbers. They would leave at 7:00 or 8:00 p.m. and returned early in the morning at 3:00 or 4:00 a.m. Fishers spent 3–4 h of travel time so only about 4 h were actually devoted to gathering. They did not go
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Fig. 2. Sea cucumber species recorded in Arrecife, Green and Johnson Islands, Palawan, Philippines: a) Actinopyga echinites; b) Actinopyga lecanora; c) Bohadschia marmorata; d) Bohadschia vitiensis; e) Holothuria atra; f) Holothuria leucospilota; g) Holothuria edulis; h) Holothuria fuscocinerea; i) Holothuria gracilis; j) Holothuria leucospilota; k) Holothuria scabra (white variant); l) Holothuria scabra (black variant); m) Pearsonothuria graeffei; n) Stichopus horrens; o) Stichopus monotuberculatus; p) Stichopus rubermaculosus; q) Stichopus vastus; r) Synapta maculata. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
variants of Holothuria scabra), Stichopodidae and Synaptidae were recorded in this study (Fig. 2). All recorded species were commercially exploited and processed into trepang, except for Synapta maculata. Majority (14) of the recorded species were noted in Arrecife Island while only seven were encountered in Green Island and also seven in Johnson Island. Eight out of the 14 species encountered in Arrecife Island were exclusively noted in this island such as Actinopyga echinites,
This educational profile made it difficult for people in island communities to secure regular or high paying jobs thus, most of them generally relied on harvesting marine resources for living. 3.2. Species richness, diversity and relative density A total of 17 species belonging to families Holothuriidae (with two 228
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Fig. 2. (continued)
(p > 0.05, Tukey test). Arrecife Island had a mean diversity index of 0.58 which was significantly higher than that in Green Island (0.24) and Johnson Island (0.14) (p < 0.05, two-way ANOVA). This result indicates that the repeated encounter of a particular species in Arrecife Island was more frequent compared in Green and Johnson Islands. It could also mean that the abundance of sea cucumbers was distributed among all species in the community while it was fragmented in other habitats especially in Johnson Islands with diversity index of 0.14. This phenomenon is probably a consequence of the prevalent harvesting in Green and Johnson Islands. Mean diversity indexes across habitats were not significantly different (p > 0.05, two-way ANOVA). Table 2 shows sea cucumber mean density according to site, habitat and site-and-habitat interaction. Total mean density was highest in Arrecife Island at 1245 ind ha−1 while it was only 78 ind ha−1 in Green Island and 39 ind ha−1 in Johnson Island (p < 0.05, two-way ANOVA). Assuming that the three islands originally had similar levels of abundance, the remaining sea cucumbers in Green and Johnson Islands would be 6% and 3%, respectively of the original population. These values are way below the target reference level for sustainable
A. lecanora, Holothuria atra, H. edulis, H. leucospilota, Pearsonothuria graeffei, Stichopus rubermaculosus and S. vastus. A. echinites is a vulnerable species listed under the International Union for Conservation of Nature (IUCN) while S. rubermaculosus and S. vastus can be considered as rare species for they had not been reported in other parts of the country except in Palawan (Kerr et al., 2006; Olavides et al., 2010; Jontila et al., 2014; Romero and Cabansag, 2014; Dolorosa et al., 2017). There were also several rare species that were only noted in the exploited sites such as Holothuria gracilis, S. horrens and S. monotuberculatus although these species, except S. horrens, were previously reported in Arrecife Island (Jontila et al., 2017). Jontila et al. (2017) completed their study through SCUBA diving in deeper coral reefs while in this study, only snorkeling was done. In addition, the present study only assessed relatively shallow reef areas (∼1 m deep) and could be the reason why some reef-associated species were not recorded. Table 1 presents the species richness and diversity recorded in seagrass beds, reef flats and coral reefs of three islands. For species richness, analysis showed that it differed significantly across sites (p < 0.05) but not among habitats (p > 0.05, two-way ANOVA). In particular, species richness in Arrecife Island was significantly higher than those in Green and Johnson Islands (p < 0.05, Tukey test), but no significant differences were detected between the last two islands
Table 2 Sea cucumber relative density across habitats between unexploited and exploited sites.
Table 1 Sea cucumber species richness and diversity across habitats between unexploited and exploited sites. Habitat
Seagrass Reef Flats Coral Reefs Total Mean
Habitat
Relative Density (ind.ha−1)
Species Richness
Shannon Diversity Index (SDI)
Unexploited
Exploited
Unexploited
Unexploited
Arrecife
Green
Johnson
51 22 5 78b
21 4 13 39 b
Exploited
Exploited
Arrecife
Green
Johnson
Arrecife
Green
Johnson
9 4 7 14a
5 3 2 7b
3 1 4 7b
0.95 0.46 0.34
0.30 0.44 0.0
0.14 0.0 0.27
0.58a
0.24b
0.14b
Seagrass Reef Flats Coral Reefs Total
∗
1117 27 101 1245a
Mean
396 a 18 b 40 b
Letter notations indicate significant difference (p < 0.05, two way ANOVA). ∗ Indicates that sea cucumber mean density in Arrecife-seagrass beds is significantly different than other site-and-habitat interaction (p < 0.05, one way ANOVA).
Letter notations indicate significant difference (p < 0.05, two-way ANOVA). 229
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Table 3 Total mean densities (ind.ha−1) of each sea cucumber species across all habitats in unexploited and exploited sites. Species
Family Holothuriidae 1. Actinopyga echinites 2. Actinopyga lecanora 3. Bohadschia marmorata 4. Bohadschia vitiensis 5. Holothuria atra 6. Holothuria coluber 7. Holothuria edulis 8. Holothuria fuscocinerea 9. Holothuria gracilis 10. Holothuria leucospilota 11. Holothuria scabra 12. Pearsonothuria graeffei Family Stichopodidae 13. Stichopus horrens 14. Stichopus monotuberculatus 15. Stichopus rubermaculosus 16. Stichopus vastus Family Synaptidae 17. Synapta maculata∗ Total Density
Total mean density (ind.ha−1) Unexploited
Exploited Sites
Arrecife Is.
Green Is.
Johnson Is.
Characteristics
11 155 640 35 296 27 133 93 – 80 21 13
– – 64 21 – 13 – 59 – – 11 –
– – 27 – – 27 – – 13 – 5 –
Burying Nocturnal Burying Burying Non-burying Cryptic Non-burying Burying Cryptic, nocturnal Non-burying Burying Cryptic, nocturnal
27
Cryptic, Cryptic, Cryptic, Cryptic, Cryptic,
67 133
– –
13 27 – –
(17) 1704a
(29) 195b
(45) 112 b
nocturnal nocturnal nocturnal nocturnal nocturnal
* No commercial value, density is not included in the total. Letter notations indicate significant difference (p < 0.05, two-way ANOVA).
Other exploited sites in the country like Bolinao and Anda (both in Pangasinan province) also had lower densities of sea cucumbers at 0.3 to 9 ind ha−1 (Olavides et al., 2010). Similar studies also showed that areas open to exploitation have lower densities of sea cucumbers than protected sites (Conand and Muthiga, 2007). However despite the longterm pressure from unregulated gathering in Green and Johnson Islands, it is interesting that B. marmorata, B. vitiensis and H. scabra were able to maintain sizeable populations. Such circumstances might be attributed to the burying behavior of these species, which allow them to avoid predators including gatherers at certain times (Clouse, 1997, Mercier at al. 1999, Wolkenhauer et al., 2010). Notice that Bohadschia species along with H. atra were the most abundant in Arrecife Island but H. atra was not encountered in Green and Johnson Islands, probably because these species do not bury and were therefore prone to overharvesting. In fact, all the recorded species in Green and Johnson Islands were either burying, cryptic or nocturnal that come out of crevices only at night such as the Stichopus species (Purcell et al., 2012). Such behaviors limit their exposure to gleaners who would otherwise harvest them indiscriminately. Nonetheless, species with such behaviors remain vulnerable to depletion if unregulated harvesting continues. For instance in Red Sea, B. marmorata and B. vitiensis were exhausted after a decade of unregulated fishing (Hasan and Abd El-Rady, 2012).
harvesting which is about 40% of the original stock. These results suggest that sea cucumbers in Green and Johnson Islands are overfished. Across habitats, the highest mean sea cucumber density was recorded in seagrass beds (396 ind. ha−1) while mean densities between reef flats (18 ind. ha−1) and coral reefs (40 ind. ha−1) were not significantly different (p > 0.05, two-way ANOVA). In addition, relative densities as a result of interaction between sites and habitats displayed significant differences (p < 0.05, two-way ANOVA, Table 1). The highest density as a result of the site-and-habitat interaction was recorded in seagrass beds of Arrecife Island (p < 0.05, one-way ANOVA). The high relative density in Arrecife Island was attributed to the high density of some species in seagrass beds particularly the B. marmorata at 640 ind ha−1 and H. atra with 296 ind ha−1 (Table 3). In contrast, B. marmorata in Green and Johnson Islands was estimated at 64 and 27 ind ha−1, respectively. In addition, H. atra was not recorded in both exploited sites. These species were commonly found in shallow seagrass beds and coral reefs making them prone to overharvesting. All sea cucumber species in Green and Johnson Islands had low relative density estimates (< 100 ind ha−1) and most were in critical conditions (< 30 ind ha−1). This means that the number of individuals were not enough to successfully repopulate the area (Purcell et al., 2009). S. maculata, a species that is of no commercial value, was more abundant in Green and Johnson Islands than in Arrecife Island. This could possibly be due to the low level of competition for food and space among species in exploited sites. The low density of sea cucumbers in Green and Johnson Islands can likely be attributed to unregulated harvesting that started in the 1980's. Based on interviews with fishers in Green Island, they used to go in fleets around their island during low tide at night to gather fish and invertebrates including sea cucumbers. Fishers had identified at least 26 species that they used to collect around the island, but only six of those were encountered in this study (Table 4). Gatherers added that A. echinites, A. lecanora, B. marmorata, B. vitiensis, H. atra, H. edulis, H. leucospilota and H. scabra used to abound in seagrass beds, yet of these, only B. marmorata, B. vitiensis and H. scabra were recorded in this study. These species among other commercially important ones are usually the first to disappear in heavily exploited sites (Uthicke and Conand, 2005).
3.3. Perception on sea cucumber population and management All gatherers surveyed claimed that sea cucumbers were far more abundant and more diverse in the past 10 years than the present. They said that in the past, a one-hour gleaning trip could yield a bucket full with different sea cucumbers species. They added that they used to glean in seagrass beds and shallow reefs just around their area. However, they could no longer collect as many sea cucumbers in present times. During the study period, only nine women in Green island were engaged in gleaning of sea cucumbers. Many of them had shifted to seaweed farming because gleaning was no longer profitable due to scarcity of sea cucumbers around the island. As for the divers, they had to travel to farther reefs because sea cucumbers had become scarce in 230
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Table 4 Sea cucumber species that gatherers have been collecting in Green and Johnson Islands. Family Holothuriidae
Local name
Green Is.
Johnson Is.
Arrecife Is.
1. Actinopyga echinites 2. Actinopyga lecanora 3. Actinopyga sp. 4. Bohadschia argus 5. Bohadschia marmorata 6. Bohadschia vitiensis 7. Holothuria atra 8. Holothuria coluber 9. Holothuria edulis 10. Holothuria fuscocinerea 11. Holothuria fuscogilva 12. Holothuria fuscopunctata 13. Holothuria gracilis 14. Holothuria leucospilota 15. Holothuria scabra 16. Holothuria whitmaei 17. Pearsonothuria graeffei Family Stichopodidae 18. Stichopus chloronotus 19. Stichopus herrmanni 20. Stichopus horrens 21. Stichopus monotuberculatus 22. Stichopus rubermaculosus 23. Stichopus vastus 24. Thelenota anannas 25. Thelenota anax 26. Thelenota rubralineata No. of species noted in this study No. of species gatherers used to collect
Khaki, Brown beauty Munang, Buli-buli Hudhod Leopard, Matang-itik Lawayan, Hangad-langit, Tagukan Lawayan taba Black beauty Patola white, Tambor Hotdog, Lipstikan, Red beauty Labuyo Susuan Sapatos Patola Kurtido, Kiskisan, Putian Susuan Flower, Pinya-pinya
0 0 0 0 + + 0 + 0 + 0 0 0 0 + 0 0
0 0 0 0 + 0 0 + 0 0 0 0 + 0 + 0 0
+ + 0 0 + + + + + + 0 0 + + + 0 +
Tres/Cuatro cantos, Mani-mani, Dilawan Hanginan Hanginan Hanginan Emag, Hanginan Tinikan Legs Paag-daga, Hanginan
0 0 + 0 0 0 0 0 0 6 26
0 0 + + 0 0 0 0 0 6 26
0 0 + + + + 0 * 0 19
0 species that used to occur around the island. + species noted in this study. * Documented by Dive Instructor of Arrecife Island.
their traditional fishing areas. When asked to identify the causes of sea cucumber depletion in their locality, all respondents identified massive and unregulated harvesting as the main cause of the problem (Table 5). Several respondents (11%) attributed habitat destruction as a consequence of blast fishing that led to the decline of sea cucumber population. When asked to identify laws or regulations or any management measures pertaining to the regulation of sea cucumber collection, all could not identify any. Also, fishers were not aware that some sea cucumber species were threatened and therefore should not be collected (Table 6). Gatherers were also asked of their perceptions on the management of sea cucumbers in their area. Table 5 presents the questions asked to which all of them responded negatively. Gatherers did not know any regulations pertaining to the collection of sea cucumbers. They did not have permits and just freely collected and traded sea cucumbers in violation of AC 248 which requires gatherers and traders to secure a wildlife collector's permit and transport permit, respectively. It was learned that they never experienced having been prohibited from gathering sea cucumbers. The practice of selling small dried products (< 5 cm) to traders in Puerto Princesa City continued. While AC 248 prohibits the collection of threatened sea cucumbers, A. echinites, H.
scabra and S. herrmanni were freely collected and traded. This was a common scenario even in other sites in the province (Dolorosa et al., 2017). It seems there was a problem with the enforcement of policies related to sea cucumber. There was also a clear need to increase the awareness of key stakeholders on policies related to the sea cucumber fishery. Interestingly, gatherers mentioned that species like dugong (Dugong dugon), sea turtles, giant clams, top shell (Tectus niloticus) and Napoleon wrasse (Cheilinus undulatus) were protected species and must not be collected. They got the information from local radio and information campaign conducted by several non-government and government organizations. Respondents could not recall any similar campaign or propaganda for sea cucumbers. Interviews with key informants likewise showed that the fishery was not given attention in terms of management. All of them were not aware of size limits and AC 248 although the Bureau of Fisheries and Aquatic Resources (BFAR) monitors the outgoing volume of dried sea cucumbers and the Palawan Council for Sustainable Development (PCSD) included some threatened sea cucumbers (such as H. fuscogilva H. scabra, H. whitmaei and Thelenota ananas) in their printed information materials. The local government units (LGUs) neither adopted the
Table 5 Causes of sea cucumber population decline based on perception of gatherers. Issue/Concern
1. 2. 3. 4. 5.
Unregulated harvesting Habitat destruction Disease Predators Climate change (increase in seawater temperature) 6. Others (please specify)
Percentage of Respondents (N = 79) 100% 11% 0 0 0
Remarks
Blast fishing in the 90's Not observed Not observed The term is familiar only to few and though divers have observed bleaching of some corals, they did not associate it with the decline in population of sea cucumbers.
0
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Table 6 Gatherers’ perception on the management of sea cucumber populations. Question
1. Do you know of any regulation related to the collection of sea cucumbers? 2. Do you know of any regulation related to the management of sea cucumbers? 3. Are you aware which sea cucumber species is considered as threatened or endangered? 4. Do you have a permit to collect sea cucumbers? 5. Do you pay any fees for harvesting sea cucumbers? 6. Do you know at which size the sea cucumbers should be allowed to be collected? 7. Did any personnel from relevant national or local agency visit your area to conduct information campaign on sea cucumber collection?
Percentage of response (n = 80) Yes
No
0
100%
0
100%
0
100%
0 0 0
100% 100% 100%
0
100%
Remarks
Some gatherers mentioned that Dugong, sea turtles, giant clams, top shell (Tectus niloticus) and Napoleon wrasse (Cheilinus undulatus) are protected species
BFAR and LGU provided an assistance on seaweed farming only
It is suggested that the PCSD adopt the minimum size limit on dried sea cucumbers as implemented by other Pacific Islands like Papua New Guinea (PNG), Vanuatu and Solomon Island (Muthiga and Conand, 2014; NFA, 2016), only for the time being until local studies on reproductive biology of exploited species become available. For instance, the minimum size for dried sea cucumbers set by PNG for H. scabra, H. edulis and Bohadschia spp. is 10 cm and for H. atra, H. coluber and H. fuscogilva is 15 cm (NFA, 2016). By enforcing size regulations, gatherers and traders could gain more economic benefit as larger-sized trepang command higher prices. It is also suggested that the collection of endangered sea cucumber species, which are mostly high-value and sought after by gatherers, be strictly banned. Such policy can be adopted by the LGUs through a local ordinance and supported by local law enforcers. The LGU should also establish licensing and monitoring schemes for gatherers and traders. Setting of a closed season during peak of spawning can also be explored provided such is supported by studies (Muthiga and Conand, 2014). Rotational closure of identified gleaning sites around the island is also worth exploring to allow recovery of the wild stock while allowing gathering in other sites. Closures of fishery and ban in export have been implemented in some Pacific Island Countries to allow recovery of stocks (Pakoa and Bertram, 2013). However, since these measures seem drastic and will greatly affect a lot of marginal fishers in Palawan, this should be carefully studied. The LGU should also encourage the formation of cooperatives composed of sea cucumber gatherers. This can be helpful in ensuring quality and appropriate price for their product and leveraging funds for other livelihood programs. In addition, it shall be easier for local enablers to disseminate necessary information to the fishers and instill stewardship values among resource users. For some sea cucumber species with available technology for full cycle production, sea ranching is a promising way to achieve optimum economic benefit from farmed products while maintaining and enhancing the natural stock (Hair et al., 2016). There had been successful reports of similar efforts in other areas (e.g., Bolinao, Pangasinan, Philippines), wherein an organized group of locales co-manage the rearing of sandfish (Holothuria scabra). Since sea ranching requires hatchery-produced juveniles, the BFAR could probably facilitate its establishment in strategic locations in Palawan. This will provide supply of juveniles that can be used for grow-out culture, sea ranching and stock enhancement of depleted sites. Academic institutions can also be tapped to conduct studies on reproductive biology of commercially important sea cucumbers to determine the size at maturity, which is needed in establishing the size limit. Assessment and monitoring of wild population can also be done by HEIs as well as the conduct of information, education and communication (IEC) activities and production of IEC materials in
AC 248 nor implemented size limits or any management measure. The LGUs failed to monitor sea cucumber landings nor collected tax in the form of invoice issuance, as they did for fish and other marine products. The LGUs therefore need to consider monitoring and record keeping of sea cucumber harvest (through auxiliary invoice), which could also add to LGUs revenue. Other offices such as the Municipal Fishery and Aquatic Resource Management Office (MFARMO), which mainly focused on fishing, seaweed farming and live fish trading, also need to consider improving its monitoring and record keeping. It is recommended that LGUs, especially those with existing sea cucumber fisheries, should review local policies and adopt ordinances that provide management for these resources. In addition, a review of AC 248 seems to be necessary. For example, the administrative order sets the minimum size for all dried sea cucumbers at 5 cm. While this provision favors the conservation of sea cucumbers that mature at small size, it also promotes the exploitation of large species like T. ananas, T. anax and other Stichopus species that can grow to almost a meter in length. The size regulation should therefore be species specific.
3.4. Policy recommendations This study proposes a management framework (Fig. 3) that could be valuable in addressing the poor ecological state of the sea cucumber populations in Palawan, as well as improve its fishery. This plan is formulated based on the weaknesses/threats (i.e., weak implementation of laws, unregulated trade, weak monitoring system, poor knowledge on the resource, lack of political will of LGUs, loss of livelihood, etc.) and strengths/opportunities (i.e., sea cucumber hatchery and nursery technologies, sea ranching, local knowledge of the resource, presence of pro-active officials and research institutions, etc.) of the sea cucumber fishery in Palawan. It is recommended that the Palawan Council for Sustainable Development (PCSD) serve as the lead agency in the development of a management program for sea cucumbers in Palawan as PCSD is mandated to implement the Strategic Environmental Plan for the province (Republic Act 7611). The PCSD can be assisted by an ad hoc committee that shall be composed of other key players such as the PCSDS (which is the implementing arm of the PCSD), BFAR, Department of Environment and Natural Resources (DENR), higher education institutions (HEIs), Department of Education (DepEd), LGUs, the Philippine National Police, non-government and peoples' organizations, sea cucumber fishers’ cooperatives, traders, and other stakeholders. The ad hoc committee shall be tasked to formulate plans and programs, conduct regular monitoring, ensure law enforcement, and coordinate efforts of all stakeholders. Fig. 3 also shows the proposed management structure with recommended policy options and roles of stakeholders and agencies involved. 232
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Fig. 3. Proposed management scheme for the sea cucumber fishery in Palawan, Philippines.
to sustain the economic as well as the ecological benefits sea cucumbers provide. Policy development is the immediate need that must be addressed, followed by implementation and enforcement of pertinent laws and management programs at the local level. Conducting an information campaign is the most doable action that can be done immediately even in the absence of policy. Education might change the perspective of the gatherers, as such has been proven effective in gaining their support on conservation and proper utilization of some marine resources.
collaboration with PCSDS, BFAR, DENR, NGOs and LGUs. For grade school levels in coastal communities, the DepEd can facilitate the information campaign since children are also involved in gathering. 4. Conclusion This study shows that diversity and populations of commercially important sea cucumbers are negatively affected by unregulated harvesting. Some species in heavily-exploited sites might encounter the risk of depletion for their present estimates might not be enough to allow repopulation, especially that harvesting remained open. Sea cucumbers’ vulnerability to depletion was further heightened by the lack of regulations in the sense that pertinent laws were insufficient, not enforced, and therefore ineffective. It is feared that some species, such as A. echinites, A. lecanora and H. atra, which used to be collected in the area, might had been depleted already as they were not encountered during the survey, nor presently collected by the gatherers around their area. If unregulated harvesting will not be addressed, the sea cucumber population in areas open to exploitation could collapse, which could further affect the diversity and the overall productivity of the ecosystem they share (Mercier et al., 1999; Uthicke, 1999; Wolkenhauer et al., 2010). Sea cucumbers in nearby sites will likely soon be depleted for as mentioned, fishers were already venturing to farther areas. Like other small-scale fisheries, the sea cucumber fishery is also very important. It sustains the livelihood of people in coastal areas who have no other means to sustain their living other than relying on marine resources. Thus, it is important that its fishery should be managed at a local level
Acknowledgement This study was jointly funded by the Department of Science and Technology- Science Education Institute (DOST-SEI), the University of the Philippines Visayas and the Western Philippines University. The support and cooperation of the Municipality of Roxas, Palawan, the management of Arrecife Island especially Ms. Glesselle T. Batin, and the sea cucumber gatherers in Green and Johnson Islands are greatly appreciated.
Appendix A. Supplementary data Supplementary data related to this article can be found at https:// doi.org/10.1016/j.ocecoaman.2018.08.025.
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