Marine algal species and marine protected area management: A case study in Phu Quoc, Kien Giang, Vietnam

Ocean and Coastal Management 178 (2019) 104816

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Marine algal species and marine protected area management: A case study in Phu Quoc, Kien Giang, Vietnam

T

Huynh Van Tiena, Tan Phong Nguyenb,∗ a b

Faculty of Natural Resources & Environment, Kien Giang University, Viet Nam Faculty of Environment and Labour Safety, Ton Duc Thang University, Ho Chi Minh City, Viet Nam

A R T I C LE I N FO

A B S T R A C T

Keywords: Co-management Marine algal species Marine protected area Phu Quoc Zoning

As with many other marine protected areas in Vietnam, little is known of the marine algal species and their status within the Phu Quoc Marine Protected Area (Phu Quoc MPA), Kien Giang, Vietnam, although these species are known to have economic and conservation value. The knowledge limitations may partly be due to the fact that marine algal species have not been a major focus of surveys and monitoring programmes. This study applied a mixed methods approach for developing an adequate understanding of the status of marine algal species occurring in the An Thoi coral reef strictly protected zone of Phu Quoc MPA. 41 marine algal species were fully described, along with details about habitats, biodiversity, economic and conservation values, and challenges to the conservation of these species. Three of 41 species recorded are listed in the Vietnam Red Data Book, a list of rare and endangered floral and faunal species native to Vietnam. This listing adds a new dimension to the literature with regard to distribution and habitats. The remaining species are known to be of economic value. Two islands, which are not strictly protected zones, are home to two vulnerable algal species. Marine algal species have been poorly managed and monitored as a consequence of insufficient legal frameworks, resulting in little documentation of the effects of socio-economic and tourism development on the marine algal species. The current zoning plan should be revised to expand core zones for the effective management of the algal species. Technical guidelines on zoning and zoning permit should be developed to promote the co-management of algal species for the protection of the species and livelihoods, and to ease illegal exploitation of marine algal species in Phu Quoc MPA.

1. Introduction Marine protected areas (MPAs) include both coastal and offshore marine protected areas (IUCN, 2000). MPAs are established as a nature based tool for protecting coastal and marine ecosystems, fisheries, and biodiversity (Gaines et al., 2010). MPAs are, ideally, managed within ecological zones to effectively protect critical marine or coastal habitats, species, and ecological functions, all of which contribute to restoring and replenishing marine resources for social, economic and cultural enrichment (Day et al., 2012; Len et al., 2013; WWF, 2015). Although the establishment of a network of sixteen Vietnamese MPAs by the end of 2015 was planned (Vietnamese Prime Minister, 2010), by 2016, only eight MPAs had been established (IUCN, 2015). The Phu Quoc Marine Protected Area (Phu Quoc MPA), one of the eight MPAs, was established in 2007, primarily to protect seagrasses and coral reefs in the region (Kien Giang Provincial People's Committee (Kien Giang PPC) 2007). Coral reefs and seagrasses have been regularly

∗

surveyed and monitored in Phu Quoc MPA (Vo, 2010; Nguyen, 2015). However, the literature suggested that Phu Quoc MPA and its surrounding areas contained a high diversity of algal species, with approximately 145 species (brown, green, and red algal species) recorded by 2018 (Vo, 2010; Nguyen et al., 2013; Phang et al., 2016; Hien et al., 2018; Soc et al., 2018). By 2011, marine algal species had been over-exploited in and around Phu Quoc MPA (Le, 2011), and many marine algal species were reported to have been vulnerable or even threatened by tourism related activities (Le, 2011). Many marine algal species found in the Phu Quoc area were recommended to be listed in the 2007 Vietnam Red Data Book - a list of rare and endangered floral and faunal species native to Vietnam due to increased threats to these species (Le, 2011). Marine algal species play an important ecological role in marine ecosystem. They function as primary and secondary producers, and form the base of the ocean's food web. These species, upon decomposition, provide nutrients for small marine organisms. Marine algal

Corresponding author. E-mail address: [email protected] (T.P. Nguyen).

https://doi.org/10.1016/j.ocecoaman.2019.104816 Received 9 November 2018; Received in revised form 4 May 2019; Accepted 15 May 2019 Available online 22 May 2019 0964-5691/ © 2019 Elsevier Ltd. All rights reserved.

Ocean and Coastal Management 178 (2019) 104816

H.V. Tien and T.P. Nguyen

species support the proliferation of other marine species such as fish populations by providing refuge and seasonal habitats for juveniles (Chapman, 2013; Fulton et al., 2019). Some species are also used as indicators in water quality monitoring programmes (Sophie and Nicholas, 2015). Many red algae species (Rhodophyta) comprise an alternative resource of sustainable biomass to produce biofuels, biochemicals, and food (Wells et al., 2017; Khan et al., 2017; Suhahkar et al., 2018) and for the pharmaceutical sectors (Shalaby, 2011; Thomas and Kim, 2011). Many marine algal species, particularly red and brown marine algal species have been listed in the Vietnam Red Data Book because of their distribution, and population status (Science and Technics Publishing House, 2007). The list of marine algal species recorded in the Phu Quoc region contained no information with regard to locations, threats, morphological descriptions, and conservation status. Lists, therefore, served only as a technical reference and did not contribute to the protection of marine algal species, and especially endangered species occurring in protected areas. The literature shows that protection of a species requires precise information in connection with population and population viability, geographical range size, distribution, and threats (Meynell, 2005; Davidson-Hunt et al., 2017). Furthermore, the information related to species of conservation value needs to be frequently updated to effectively protect the species (IUCN, 2017). Due to the above issues, it is crucial to thoroughly understand the status of marine algal species that occur in Phu Quoc MPA. This understanding is important to ensure the effective protection of marine algal species in particular and Phu Quoc MPA in general, especially in the context of increased tourism and other socio-economic development in the region. Therefore, this study aims to develop an adequate understanding of the status of marine algal species occurring in Phu Quoc MPA through the description of their habitats, measurement of species diversity, and documentation of the challenges to the conservation of these species. The adequate understanding of these species will form the first step toward effectively managing marine algal species and provide recommendations for developing a regular monitoring program for marine algal species and Phu Quoc MPA. The study was undertaken with Phu Quoc MPA Management Authority and local communities being involved as co-investigators.

Pham, 1969; Nguyen, 1997), and semi-structured interviews (Ayres, 2008), using BioDiversity Pro software 2.0 and debriefing (Kindon et al., 2008). In March 2017, reports and maps relevant to marine algal species were analyzed using secondary data analysis to extract secondary data in relation to marine algal species, occurrence, and locations. Semistructured interviews were undertaken in April 2017 with staff working for the Phu Quoc MPA, and with local fishermen to collect further secondary data with respect to locations of, and local use of, marine algal species. With permission from the Phu Quoc MPA Management Authority, 14 field visits were organized in May 2017 using local fishing boats and GPS hand-held units to 14 islands around and within the strictly protected zone of Phu Quoc MPA to collect data on the diversity of, and distribution of, marine algal species. Five random (0.5 m × 0.5 m) quadrats were established at each island. Samples were collected at a varying depth dependent on the physical conditions (see Table 2 for more information with respect to the depth during the sampling). Physical oceanographical data in relation to geographic coordinates, water temperature, pH, and salinity were recorded at each island. Numbers of species in each quadrat were recorded along with photographs of the habitats within each quadrat. Samples were then collected and stored in 50 ml Falcon conical tubes containing sea water concurrently collected at each site. The Falcon conical tubes were stored in ice boxes and transported to the lab of Can Tho University, Vietnam for additional analysis. At the Can Tho University lab, samples were photographed and curated. Species diversity and evenness was calculated from this data using BioDiversity Pro Software 2.0 in June 2017. Two debriefings were organized in June 2018 and August 2018 with representatives of the Phu Quoc MPA Management Authority, the Phu Quoc District Economic Development Board, Phu Quoc fishing communities, the Kien Giang Department of Science & Technology, Kien Giang, Department of Agriculture & Rural Development, Kien Giang University, and Can Tho University. These briefings included discussions of the findings and the development of recommendations for effectively managing the marine algal species in particular and Phu Quoc MPA in general, in the context of climate change and increased tourism and other socio-economic development. The methods are summarized as Fig. 2.

2. Materials and methods 3. Results 2.1. Site description 3.1. Marine algal species, their habitats, and values Phu Quoc MPA, located in Phu Quoc District, Kien Giang province, Vietnam, was established in 2007 with a total water surface area of approximately 27,000 ha (Kien Giang Provincial People's Committee (Kien Giang PPC) 2007). Phu Quoc MPA was zoned into three ecological zones including strictly protected zones, buffer zones, and development zones. Two strictly protected zones, demarcated with GPS coordinates (locally called boundary points), are the Ham Ninh seagrass strictly protected zone (6825 ha) and the An Thoi coral reef strictly protected zone (9720 ha). An Thai coral reef strictly protected area includes five core zones which are May Rut Trong island, Vong island, Xuong island, Gam Ghi island, and Mong Tay island. Thom island is the biggest island with a population of approximately 4000 inhabitants. The remaining islands are sparsely populated. Buffer zones and development zones were not demarcated (Fig. 1 & Table 1).

Oceanographical conditions including coordinates, water temperature, pH, and salinity of 14 islands were recorded during the field visits (Table 2). A total of 70 samples were collected and photographed for further analysis. Of 70 samples collected, 41 marine algal species were identified, along with detailed site information in relation to their locations. These 41 species were then evaluated with respect to their economic value and conservation status using the relevant literature and the 2007 Vietnam Red Data Book (Table 3). Of these 41 species recorded, three species are of conservation concern. Kappaphycus cottonii is listed as an endangered species while Hypnea japonica and Turbinaria decurrens are listed as vulnerable species. The remaining species are all economically valuable. 3.2. Current management of marine algal species in Phu Quoc MPA

2.2. Methods The semi-structured interviews with staff working for Phu Quoc MPA revealed that 5 core zones of the An Thai coral reef strictly protected areas were established mainly to protect coral reefs. There were no action plans for monitoring other marine species, including marine algal species in the Phu Quoc MPA management plan. The Phu Quoc MPA Management Board did not directly monitor nor manage the marine resources, nor possess the requisite expertise in managing

This study was undertaken in the An Thoi coral reef strictly protected zone of Phu Quoc MPA between March 2017 and August 2018. The study applied mixed methods (Morse, 2003) for undertaking the study activities. Mixed methods included secondary data analysis (a desk-top review) (Schutt, 2009), field visits (Kindon et al., 2008), the Quadrat method (Misra, 1968), classification methods (Dawson, 1954; 2

Ocean and Coastal Management 178 (2019) 104816

H.V. Tien and T.P. Nguyen

Fig. 1. Phu Quoc MPA; (A) the location of Phu Quoc island in Vietnam (Google image); B; Phu Quoc island and Phu Quoc MPA; C) The islands within the Coral Reef Protection Zone and sites of sampling.

these islands to attract tourists. However, there has been no study of negative effects on marine natural resources. The semi-structured interviews with the staff revealed that Phu Quoc MPA was not fully equipped to measure tourism induced effects on marine wildlife. The field surveys showed that the number of the species recorded ranged from 2 to 12. The H′ index ranged between 0.217 and 1.023. The J’ index ranged from 0.722 to 0.948. Of the 5 core zones within the reef strictly protected area, Vong island had the highest level of biodiversity, followed by Xuong island, May Rut Trong island, and Gam Ghi island respectively. Mong Tay island had the lowest. Meanwhile, other islands in non-core areas such as Thom island, Dua island, Kim qui island, Vang island, and Kho island had the similar level of biodiversity as other core zones like Xuong island, May Rut Trong island, and Gam Ghi island (Fig. 3). During the field work, marine algal species were observed to die within approximately 1 m of the water surface in areas of Dua Island, Roi Island, Dam Trong Island and Dam Ngoai Island. These islands are close to populated areas in the An Thoi Town. Marine algal species were buried mainly by construction sediment which likely originated from local construction sites (Fig. 4). Furthermore, these species were negatively affected by overfishing around Dua and Roi islands. The status of marine algal species, the current management, and factors influencing these species are summarized in Fig. 5.

Table 1 The geographic coordinates of Phu Quoc MPA (Kien Giang PPC, 2007). Boundary point

Longitude

The Ham Ninh seagrass strictly protected zone 1 104000’58″ 2 104002’36″ 3 104005’46″ 4 104007’14″ 5 104006’24″ 6 104004’46″ The An Thai coral reef strictly protected zone a 104000’01″ b 104003’00″ c 104003’01″ d 103057’51″ e 103057’51″ f 103059’41″

Latitude

10025’56″ 10025’43″ 10023’47″ 10018’21″ 10014’36″ 10014’36″ 09059’21″ 09059’21″ 09053’17″ 09053’17″ 09056’24″ 09057’28″

marine resources. Surveys of marine biodiversity including marine algal species were undertaken by external agencies recruited by the Management Board. Survey's results were supplied as a list of marine species to the Phu Quoc MPA Management Board for consideration. Residents of Thom island and May Rut Trong island (within the strictly protected zone) and Roi island, Dam Ngoai island, Dam Trong island (outside the strictly protected zone) derive a major proportion of their income from their involvement in marine tourism activities within Phu Quoc MPA. Activities such as recreational fishing, scuba diving, and snorkeling are permitted in Phu Quoc MPA. Tourism service facilities including hotels, resorts, restaurants using floating aquaculture farming cages, and water sports facilities have been constructed on

3.3. Current use of marine algal species Semi-structured interviews with local fisherman indicated that marine algal species were collected mainly for domestic food consumption in Dua island, Dam Trong island, Dam Ngoai island, and 3

Coordinates

9°59′36.2″N 104°00′51.6″E

9°59′04.2″N 104°01′06.4″E

9°57′19.4″N 104°00′46.7″E

9°55′11.1″N 103°58′52.1″E

9°54′47.2″N 103°59′40.3″E

9°55′03.4″N 103°59′59.6″E

9°54′56.2″N 104°01′26.1″E

9°55′38.8″N 104°01′06.7″E

9°59′28.8″N 104°02′31.3″E

10°00′20.8″N 104°01′46.2″E

9°55′45.3″N 103°59′32.5″E

9°54′13.2″N 103°59′29.8″E

9°54′38.2″N 104°00′46.0″E

9°54′35.2″N 104°01′20.7″E

Location No.

1

2

3

4

5

6

7

8

4

9

10

11

12

13

14

29.07

28.84

28.92

29.63

24.79

28.86

28.73

27.82

27.94

22.69

27.53

23.81

24.61

23.59

Water temperature (°C)

7.82

7.95

8.22

8.08

7.67

7.85

8.12

8.01

7.91

7.78

7.61

8.25

7.92

8.15

pH

9.18

8.95

9.02

9.03

8.22

8.81

8.79

8.68

8.57

8.76

8.63

7.94

7.82

7.61

Salinity (%)

Negatively affected by overfishing; close to populated areas, construction sites and tourism sites; polluted with construction sediment; with relatively gentle slope; with low coverage with brown and red algae species. Samples collected at more or less 1 m of the water surface. Negatively affected by overfishing; close to populated areas, construction sites and tourism sites; polluted with construction sediment; with relatively gentle slope; with low coverage with brown and red algae species. Samples collected at more or less 1 m of the water surface. Being the largest area; relatively gentle slope; high coverage with a variety of red and brown algae species. Samples collected at more or less 1.5 m of the water surface. Being the smallest area; relatively steep slope; with low coverage with red and brown algae species. Samples collected at more or less 1 m of the water surface. Good environment for fishes; mainly covered with coral reefs and many inert growth media; with low coverage with red and brown algae species. Samples collected at more or less 0.8 m of the water surface. Well protected by surrounding islands; relatively gentle slope with many inert growth media good for marine algal species to grow; with rich diversity and high coverage with three marine algal species. Samples collected at more or less 1 m of the water surface. With relatively gentle slope with many inert growth media; with high coverage with red algae species. Samples collected at more or less 0.9 m's depth of the water surface. With relatively gentle slope with many inert growth media; high coverage with red algae species. Samples collected at more or less 0.9 m's depth of the water surface; Close to construction site in the An Thoi; heavily polluted with construction sediment; being relatively large areas covered with brown algae species and a few red algae species. Samples collected at more or less 0.8 m of the water surface. Marine algal species died at deeper levels because they were buried with suspended sediment. Close to construction site in the An Thoi; heavily polluted with construction sediment; being large areas covered with brown algae species and a few red algae species. Samples collected at more or less 0.8 m of the water surface. Marine algal species died at deeper levels because they were buried with suspended sediment. Being relatively small area; relatively gentle slope with many inert growth media providing good conditions for marine algal species to grow; relatively high coverage with red and green algae species. Samples collected at more or less 1 m of the water surface. Relatively steep slope with less inert grow media; with low coverage with red algae species only. Samples collected at more or less 0.6 m of the water surface. Relatively steep slope with less inert grow media; with low coverage with red algae species only. Samples collected at more or less 0.6 m of the water surface. Relatively steep slope with less inert grow media; with low coverage with red algae species only. Samples collected at more or less 0.6 m of the water surface.

Site description and methods of sampling

Table 2 Oceanographical conditions of the islands surveyed. Please refer to Fig. 1 for understanding the location numbers.

H.V. Tien and T.P. Nguyen

Ocean and Coastal Management 178 (2019) 104816

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Fig. 2. Summary of the methods used in the study.

Publishing House, 2007). Of the 3 species of conservation value, only one species occurred in the core zone of the strictly protected area being Gam Ghi island. The two remaining species are located around the islands of Dua and Roi, which are outside of core zones. By 2011, marine algal species in the An Thoi coral reef strictly protected zones have been increasingly threatened by tourism activities (Le, 2011). Phu Quoc MPA and its surrounding areas have been designated as a regional, marine based, high quality tourism destination in Vietnam and the South East Asia (Vietnamese Prime Minister, 2004, 2009, 2013a,b; 2015; Kien Giang PPC, 2015). The designation has attracted significant numbers of developers, tourists and migrants to the region. Approximately 1600 tourism companies have been operating in Phu Quoc since 2015 (Environment News, 2015), while approximately one million tourists visited Phu Quoc in 2016 (Tuoi Tre Online, 2016). At present, Dua island, Roi Island, and Thom island, where species of conservation value were recorded, are popular tourism destinations. Therefore, human-induced pressures on marine resources of these islands in particular or Phu Quoc MPA in general are expected to increase in the future, with accompanying threats to species of conservation value. Vulnerable or endangered marine algal species require specific conservation strategies (Brodie et al., 2009). Therefore, the current zoning plan should be revised to incorporate the findings of this study to ensure the survival of the algal species of conservation concern. In particular, Dua island, Dam Ngoai island, and Dam Trong island should be designated as strictly protected zones because of their natural values. Zoning plans and permitting should be developed in order to regulate development activities in all core zones. In addition, the Phu Quoc MPA should be fully resourced and staffed to allow the effective monitoring of human impacts on marine biodiversity in Phu Quoc MPA (Fig. 5).

Thom island. Recent algal harvest in the region have unexpectedly increased due to the preference for organic or natural products, especially marine algal species on a daily basis among the Vietnamese community for general good health or long life or as herbal medicines to treat cancers. Phu Quoc MPA is an important location of choice for purchasing marine algal species for consumption, particularly for tourists coming from the Mekong Delta of Vietnam. The exploitation is seasonally undertaken, typically occurring between January and May when the weather permits. However, the exploitation of algal species for food consumption and its effects on marine resources have not been adequately reported. 4. Discussion 4.1. This inventory of marine algal species and its importance The results of the study show the distribution of the 41 marine algal species, thus complementing the studies of Vo (2010) and Nguyen (2015). Together with the findings of Soc et al. (2018) and Hien et al. (2018) in relation to the confirmation of the brown and green algae species in Phu Quoc MPA, this survey significantly improves our understanding of the status of the marine algal species occurring in Phu Quoc MPA. This list also serves a baseline for future monitoring programmes in the area. Marine algal species in the area had not been previously described in detail, as they were not targeted for protection in MPAs as confirmed by WWF (2015) and few efforts had been made to establish complete lists of marine algal species for protection. The comprehensive list of marine algal species developed in this study establishes an example for other MPAs in Vietnam in this regard, and shows that MPAs have many species of economic and conservation value other than coral reefs and seagrasses.

4.3. Marine algal species and co-management options Dua island, Dam Ngoai island, Dam Trong island, which are not within core zones, are home to many algal species of economic value. However, these species have been increasingly threatened either by over-exploitation or siltation from construction as shown in this study. We also recommend that Dua island, Dam Ngoai island, Dam Trong island, and Thom island should be co-managed, with local fishermen

4.2. Current management of marine algal species The presence of three species of conservation concern within Phu Quoc MPA is a significant finding as these species had previously only been reported from the central Vietnam (Science and Technics 5

6

Turbinaria murayana Turbinaria ornata Turbinaria turbinata Ulva intestinalis Ulva lactuca Linnaeus Valonia utricularis

36 37 38 39 40 41

– – –

–

– – –

–

– – – – – –

– – – – – – – – – – –

– – – – – –

– – – – – –

– – – – –

– –

– – – – – – – – – – – – – – –

– – – – – – – – – – – – – – –

–

2

1

Location

– – –

–

– – – – –

– – – – –

–

–

–

–

– – – – – – – – –

– – – – –

3

– – – – –

– – – – – – –

– – – – –

– –

–

– – –

– – – – – – – – – – – – – –

4

– – – – –

– – – –

–

–

– – – –

– – –

–

– – –

– – – – – – – – – – – – – – –

5

– –

–

–

– – –

–

– –

–

– –

– – –

–

– – –

– – –

– – –

– – –

6

– – – – – –

– – – – – – – – –

– – –

–

–

– – –

–

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–

7

– – – – – –

– – – –

– – – – – – – –

– –

–

– – –

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–

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– –

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–

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– – – – – –

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9

8

– – – – –

– – – – – – – – – – – – –

– – –

–

– –

– – – – – – – – – –

– – – –

10

– – – – –

–

– – – – – – – – –

–

– – –

–

– –

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11

– – – – – –

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– – –

–

– – –

– –

– – – – – – – – – – –

12

– – – – –

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– – –

– –

–

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13

– – – – – –

– – – – – – – – – – – – –

– – –

–

– – –

– – – – – – – – –

– – – –

14

value value value value

(Abdel-Raouf et al., 2015) (Irie and Suzuki, 1965; Mohammed et al., 2004) (Fukuzawa et al., 1986; Ji et al., 2016) (Norte et al., 1994; Cen-Pacheco et al., 2011)

value (Vairappan, 2003) value (Vairappan, 2003; Al-Enazi et al., 2018) value (Suzuki and Vairappan, 2005; McDermid et al.,

Pharmaceutical value (Tytlyanov et al., 2012) Pharmaceutical value (Minghou et al., 1984; Fong et al., 2018) Pharmaceutical value (Tytlyanov et al., 2012; Hammed et al., 2017) Pharmaceutical value (Peasura et al., 2016) Medical value (Sangeetha and Saravanan, 2014) Medical value (Wang et al., 1994; Büchner et al., 1987)

Medical value (Delma et al., 2015; Alwarsamy et al., 2016) Pharmaceutical value (Pádua et al., 2015; Meenakshi et al., 2016)

Environmental indicator (Caragnano et al., 2014) Pharmaceutical value (Karthikeyan et al., 2010; Rajamani et al., 2018) Pharmaceutical value (Kladi et al., 2004; Valentão et al., 2010) Pharmaceutical value (Errea and Matulewicz, 2003) Nutrient food production and animal feed (Borazjani et al., 2018)

Pharmaceutical Pharmaceutical Pharmaceutical 2005) Pharmaceutical Pharmaceutical Pharmaceutical Pharmaceutical

Pharmaceutical value (Rajamani et al., 2018; Khambhatya et al., 2012)

Biological value/environmental indicator (Stimson et al., 1996) Pharmaceutical value (Pereira et al., 2005) Pharmaceutical value (Mittal et al., 2017; Mittal and Raghavarao, 2018) Fisheries feed (Al-Asgah et al., 2016; Younis et al., 2018) Nutrient food production and agar production (Fukunaga et al., 2014; Minghou et al., 1988) Agriculture production value; agar production value (Carton et al., 2011) Pharmaceutical value (Selim et al., 2015) Nutrient food and carrageenan production (Wong et al., 2004)

Pharmaceutical value (Kannan et al., 2013; Lee et al., 2017)

Pharmaceutical value (Kerr and Kerr, 1999; Simmons et al., 2005) Pharmaceutical value (Kumar et al., 2015)

Pharmaceutical value (Ballesteros et al., 1992) Pharmaceutical value (Ballesteros et al., 1992)

Pharmaceutical value (Salem et al., 2011; Sayed et al., 2017)

Economic value

Listed as Vulnerable (VU - A1a,c,d+2c.) - Vietnam Red Data Book (2007)

Listed as Vulnerable (VU - A1a,c,d) - Vietnam Red Data Book (2007) Listed as Endangered (EN - A1a,c,d, B1+2b, e) - Vietnam Red Data Book (2007)

Conservation value

Note present; (−): absent. The economic value of the above marine algal species was predicted using the current relevant publications. The conservation value was evaluated using the Vietnam Red Data Book published in 2007.

Laurencia microcladia Laurencia obtusa Laurencia pinnata Laurencia viridis Liagora viscida Lithophyllum kotschyanum Padina boergesenii Plocamium cartilagineum Pterocladiella capillacea Sargassum angustifolium Solieria robusta Turbinaria conoides Turbinaria decurrens

Kappaphycus cottonii

19

23 24 25 26 27 28 29 30 31 32 33 34 35

Hydropuntia edulis Hypnea esperi Hypnea japonica

16 17 18

Laurencia cartilaginea Laurencia majuscula Laurencia mcdermidiae

Actinotrichia fragilis Akalaphycus setchelliae Amphiroa beauvoisii Amphiroa cryptarthrodia Amphiroa fragilissima Callithamnion granulatum Champia parvula Codium arabicum Codium geppiorum Codium tenue Dictyosphaeria cavernosa Gelidium crinale Gelidium pusillum Gracilaria arcuata Gracilaria salicornia

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

20 21 22

Species

No.

Table 3 Presence of the marine algal species in the coral protection zone of Phu Quoc MPA and their economic and conservation value. Please refer to Fig. 1 C for understanding the location numbers.

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Fig. 3. Summary of species numbers, and the indices f species diversity and evenness from each island.

(Fig. 5). Co-management of MPAs has been shown to be one of the most effective MPA management tools by assisting in balancing the competing demands for socio-economic development and marine resource protection (WWF, 2015). Co-management has been promoted regionally and globally in order to share the benefits of marine resources with those communities dependent on MPAs (IUCN, 1999). Co-management of marine biodiversity in protected areas in Vietnam has been legally promugated since 2004; for example the 2004 Vietnam Law on Forest Protection and Development (Vietnamese National Assembly, 2004), the 2008 Vietnam Law on Biodiversity (Vietnamese National Assembly, 2008), and the 2014 Vietnam Strategy for Managing SpecialUse Forests and MPAs and inland Wetland Protected Areas (Vietnamese Prime Minister, 2014). Currently, a pilot co-management scheme of Phu Quoc MPA has been established to protect marine resources in the Ham Ninh seagrass strictly protected zone of Phu Quoc MPA (Kien Giang PPC, 2017). Therefore, co-management of marine resources occurring in and around these islands of the An Thoi coral reef strictly protected zone is highly likely to be approved for pilot implementation. Popular alternative income in the co-management of MPAs include permitted marine tourism activities such as boating, recreational

Fig. 4. Marine algal species in Dua Island were buried by construction dirt originally from the An Thoi construction sites.

involved in managing and culturing algal species for alternative livelihood improvement. In doing so, socio-economic development will be more sustainable and marine algal species will be better protected 7

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Fig. 5. Spatial presentation of the status of algal species, management plan, influencing factors, and proposed zoning.

fishing and snorkeling and restaurants using floating net cages. Currently, these activities have been implemented in and around the An Thoi coral reef strictly protected zone. However, marine tourism often involves a large influx of tourists into a relatively small area, and the constructions of buildings and other tourism infrastructure, thus

creating environmental pressures (Kurniawan et al., 2016). Apart from the substantial investment, efforts, and time required, fish aquaculture often caused water pollution (AFCD, 2016) and may produce toxic gases due to bacterial metabolism (Wu, 1995). The Food and Agricultural Organization of the United Nations

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(FAO) (2003) stated that red and brown algae species could be cultivated for commercial purposes. The 2007 Vietnam Red Data Book also recommends that marine algal species of economic and/or conservation value be cultivated for commercial purpose. In practice, marine aquaculture, particularly of marine algal species have become widespread (Buschmann et al., 1995; Halling et al., 2005; Ganesan et al., 2011; Ugarte et al., 2006; Mantri et al., 2017). Thus, the cultivation of marine algal species is entirely in keeping with the policy of the Government of Vietnam in relation to sustainable exploitation of marine resources and marine environment protection in 2020, with a vision up to 2030 (Vietnamese Prime Minister, 2013a,b). Therefore, the cultivation of marine algal species is very likely to form one of the feasible options for creating alternative livelihoods within the co-managed An Thai coral reef strictly protected zone. However, before this option becomes economically feasible, additional studies in relation to marine cultivation of algal species are needed in order to gain a thorough knowledge of cultivation of these species. Cultivation models could be then developed to improve local livelihoods and to reduce the illegal exploitation of marine algal species in Phu Quoc MPA.

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5. Conclusions and recommendations The study recorded the distribution of, and status of, marine algal species within Phu Quoc MPA, resulting in an inventory of 41 marine algal species, supplemented with detailed information regarding habitats, levels of biodiversity, economic and conservation values, and the challenges to the conservation of these species. Three of the 41 species are of conservation importance, thus adding a new dimension to our knowledge of their distribution and habitats. The remaining species were shown to be economically valuable. The current zoning plan does not fully protect algal species, and particularly those of conservation concern. This is due to poor management and monitoring of the effects of socio-economic and tourism development on marine algal species as a consequence of deficient legal foundations. The current zoning plan should be revised to expand core zones for effective management of the algal species. Technical guidelines on zoning and permitting should be developed to promote co-management of marine resources including algal species for their protection and livelihoods, and to ease the illegal exploitation of marine algal species in Phu Quoc MPA. Acknowledgements The authors would like to thank the Vietnam Ministry of Education & Training for grant No. B2016k-KGU-01; Mr. Thao and Mr. Binh for their involvement in field trips and sampling, the Kien Giang Department of Agriculture & Rural Development, the Kien Giang Department of Natural Resources & Environment, the Management Board of Phu Quoc Economic Development Zone and Phu Quoc MPA Management Authority for administrative assistance facilitating our research work in Phu Quoc, Kien Giang province, Vietnam; Associate Professor Truong Trong Ngon for technical advice. During manuscript preparation, NGUYEN Tan Phong was supported by an Australia Awards – Endeavour Research Fellowship. The authors would also like to thank Dr. James Moloney for proofreading and editorial service, and three anonymous reviewers for their helpful comments. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ocecoaman.2019.104816. References Abdel-Raouf, N., Al-Enazi, N.M., Al-Homaidan, A.A., Ibraheem, I.B.M., Al-Othman, M.R., Hatamleh, A.A., 2015. Antibacterial β-amyrin isolated from Laurencia microcladia. Arab. J. Chem. (8–1), 32–37.

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