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Philipp. Scient. 45: 1–61 © 2008, University of San Carlos

REVIEW ARTICLE

Review of the Biodiversity of Southern Philippine

A.C. Alcala1, J.A. Ingles2 and A.A. Bucol1 1Silliman University-Angelo King Center for Research and Environmental Management, Silliman University, Dumaguete City 6200, 2World Wide Fund for Nature (WWF), JBD Plaza, No. 65 Avenue, Bagong Pag-asa, Quezon City 1105, Philippines

ABSTRACT

The marine biodiversity of the four seas in southern Philippines, namely, the , the Gulf, the Sarangani Bay, and the Sulawesi , was reviewed. The biodiversity in the shallow marine waters is similar to those in other parts of the country. The biodiversity is also in a similar conservation status, that is, in various degrees of depletion. But it is possible that there are marine species that are unique to these seas. This is especially true of the Sulawesi Sea, which is characterized by great variation in terms of habitat and depth. The importance of the resources in the four seas lies in the contributions of some species, such as tuna fishes, to the livelihoods of coastal populations in the area.

INTRODUCTION

Some research and development projects on marine biodiversity and fisheries have been conducted in the marine waters of southern Philippines. The Department of Environment and Natural Resources (DENR) 2006 list of projects includes 11 coastal and marine resource management projects dealing partly with marine biodiversity in the shallow seas of southern Mindanao. Among the institutions and agencies involved in marine biodiversity studies in the area are the Southern Philippines Agribusiness, Marine and Aquatic School of Technology 2 The Philippine Scientist, Volume 45 (2008)

(SPAMAST) in Malita, , the State College (DNSC) in City, Davao del Norte, the University of the Philippines in the Visayas (Miagao, Iloilo), and the Mindanao State University (Naawan campus). The development projects of the Department of Environment and Natural Resources and the Bureau of Fisheries and Aquatic Resources, usually in partnership with international funding institutions, typically included research on fisheries and biodiversity. The research findings of these aforementioned institutions have been brought together in the present paper in an attempt to construct a biodiversity profile of the whole area that can serve various purposes such as establishment of marine protected areas. In the course of this review, some gaps and deficiencies in our current knowledge on the biodiversity of the area have been identified and discussed. The socioeconomic importance of the southern Philippine seas lies in the fact that more than 10 million people now live in the four regions (Western Mindanao, Southern Mindanao, Central Mindanao, and ARMM) in the vicinity of the four seas, namely, the Davao Gulf, the Moro Gulf (including Illana Bay), the Sarangani Bay (including Sarangani Islands), and the Sulawesi Sea. This population figure comes from the National Statistics Office in 2002, and a substantial proportion is probably directly and economically dependent on marine and coastal resources of these seas. The four seas are known for their economic importance (see Fisheries Statistics 2003–2005). Davao Gulf is a well- known international shipping center. Samal Island in Davao Gulf is known for pearl culture and tourism. Moro Gulf is well known for its fisheries. Sarangani Bay, the home of the skipjack tuna, has become a center for aquaculture for milkfish and top predatory fish species. The Sulawesi Sea serves as a highway for movements of the tuna species and other fish species, marine turtles, and cetaceans, among others.

Brief Description of the Study Seas

This review is focused on four seas: the Moro Gulf and the Illana Bay as part of the Gulf (enclosed by the Zamboanga Peninsula, the Lanao provinces, province and Sultan Kudarat province), the Davao Gulf (enclosed by the Davao provinces and Compostela Valley province), and Sarangani Bay (enclosed by Sarangani and South provinces). The Sarangani Strait separates the Sarangani and Balut Islands at the southern tip of Sarangani and Davao del Sur

Alcala et al.: Biodiversity of Southern Philippine Seas 3

provinces from the Mindanao mainland. These three southern Philippine seas are continuous with the Sulawesi Sea, the fourth sea covered in this review. They have a diverse marine environment because of the variable depths and the presence of shallow marine habitats that include coral reefs, seagrass beds and mangroves. Different shallow marine ecosystems dominate in some parts of the area according to information provided by the DENR. Zamboanga provinces, Basilan, and are still relatively rich in mangroves. Davao del Sur and lead in seagrass beds. Sarangani, Davao del Sur and Zamboanga del Sur lead in coral reef ecosystems. However, the present status of these ecosystems needs verification. The four seas are interconnected (Fig. 1) and have a greater proportion of waters 1,000 m and deeper, compared to other areas in the country such as the Palawan area.

Figure 1. Map of the Sulawesi Sea. Isobath in meters. (Modified from: NASA Blue Marble, : US Defense Agency)

Moro Gulf

The Moro Gulf is a deep body of water with an area of about 22,000 km2. About 40% of it is deeper than 2,000 m. Its deepest part near

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its eastern portion is about 5,000 m. The western part of the Gulf is shallow, less than 200 m deep, with extensive mangroves and coral reefs (Zamboanga del Sur and Zamboanga Sibugay provinces) (Fig. 2). Within the Gulf is the Illana Bay.

Illana Bay

Figure 2. Map of Moro Gulf. Isobath in meters. (Modified from: NASA Blue Marble, Bathymetry: US Defense Agency)

Davao Gulf

Davao Gulf is about 7,300 km2 in area (Fig. 3). It is a fairly deep body of water. The southern half is about 1,800 m deep. The deepest part is near the mouth at 2,800 m. Only a thin strip near the shoreline is shallow, with a depth of less than 100 m, where mangroves, seagrasses, and coral reefs may still exist. Inside the bay is Samal Island, a conservation and tourism island and site of giant clam (Tridacna gigas) introduction by the University of the Philippines Marine Science Institute and the Davao del Norte State College. A small, privately-owned island with coral reef and mangrove in the northern part of the gulf belonging to the province of Compostela Valley is also a conservation island. The DENR has established a marine protected area mostly of seagrass beds along the shore of Davao Gulf in this province.

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Figure 3. Map of Davao Gulf and Sarangani Bay. Isobath in meters. (Modified from: NASA Blue Marble, Bathymetry: US Defense Agency)

Sarangani Bay and Sarangani Islands

Sarangani Bay is the smallest body of seawater in the study area (ca 480 km2) and generally shallower compared to the other two seas (Fig. 4). Inside the bay, the water depth ranges from 200 m to 1,000 m. At the mouth of the bay the depth reaches 2,000 m. The bottom substratum is dominated by mud. The northern part of the bay contains coral reef. Off the southern tip of Sarangani and Davao del Sur provinces are the Sarangani Islands composed of two small islands, Balut and Sarangani, separated from the Mindanao mainland by the Sarangani Strait. In the shallow waters around these islands are coral reefs. Currents in the vicinity of Balut Island are almost constant and swift; one measurement registered at 7 knots (A. Ong, pers comm). Currents are probably due to the Mindanao Current flowing southward along the eastern coast of Mindanao. In August 2006, a fish-kill involving coral reef fishes occurred, which, according to the Bureau of Fisheries and

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Aquatic Resources (BFAR), was caused by the high sulfur content of the water (A. Ong, pers comm). Beyond the 183 m isobath are deeper waters ranging from 200 m to 1,946 m in depth. Sarangani Islands are well known for rare shells. Although over-fished in terms of the major tuna species, the Sarangani Bay and Sarangani Strait are still relatively rich in pelagic fish species and are favorite areas for sport and recreational fishing (A. Ong, pers comm).

The Sulawesi Sea: Topography and Oceanography

The Sulawesi Sea is a large marine ecosystem (LME) with variable depths and varied bottom topography that partly explain its complex oceanography (Tomascik et al. 1997). The Sulawesi Sea alone is about 450,000 km2 in area. The total area of the Sulawesi Sea and the plus the Visayan inland seas (= Sulu-Sulawesi Sea Ecoregion of WWF [Ingles & Trono 2004]), is about 900,000 km2. The Sulawesi Sea lies at the center of the world’s highest marine biodiversity area (DeVantier et al. 2004). The Sulawesi Sea, with which the southern Philippine seas are continuous, varies in depth, reaching 4,000 to 5,780 m in the Sarangani Strait southwest of the Sarangani Islands and 1,000 to 4,200 m towards the southeast (Fig. 4). This highlights the importance of the mesopelagic and bathypelagic realms suspected of favoring speciation of certain marine species in this tropical sea (Madin 2008). The influences the direction of surface currents in the three Philippine seas and the Sulawesi Sea (Wyrtki 1961, Villanoy 1988, Villanoy & Udarbe 1995) (Fig. 5). This current moves westward. Upon reaching the sea area between northern Samar and Catanduanes (Zheng et al. 2006), it splits into the Kuroshio or Japan Current heading north and the Mindanao Current flowing south. During the southwest monsoon months (June to November), the Mindanao Current spits into two in the Sulawesi Sea, one stream proceeding south and another stream flowing counterclockwise as the Equatorial Countercurrent. During the northeast monsoon months (November to May), the Mindanao Current flows south and southeastward and proceeds counterclockwise as the Equatorial Countercurrent; and a small component flows counterclockwise in the eastern portion of the Sulawesi Sea and Moro Gulf. The Mindanao Current joins with the current from the South China to form the (Zheng et al. 2006) moving

Alcala et al.: Biodiversity of Southern Philippine Seas 7

Figure 4. The Islands in the Sulawesi Sea. Isobath in meters. (Modified from: NASA Blue Marble, Bathymetry: US Defense Agency)

south via the Makassar Strait east of Kalimantan and allowing marine propagules and migratory marine species from the Pacific Ocean, the and the Sulu Sea to reach the (see discussion on whales and dolphins). The nature of the deep-water circulation in the four seas is not clearly understood. But it is clear that the deep-sea currents are complex partly because of the varied topography of the sea bottom. The seawater quality of the Davao Gulf and the Sarangani Bay as well as nearby areas has been assessed to be Marginal (barely acceptable) for Sarangani Bay and General Santos, Satisfactory for the western part of Davao Gulf but Unsatisfactory for and

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Figure 5. (A) Surface current patterns in the Philippines and adjacent waters during northeast and southwest monsoon (source: Villanoy & Udarbe 1995); (B) Surface currents in December in the Pacific and Indian Oceans. (Source: Wyrtki 1961)

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environs without giving the basis for such a classification (Philippines Environment Monitor 2003). This situation should be addressed by agencies responsible for maintaining good water quality.

Earthquakes and Tsunamis

Fig. 6 shows a subduction zone, the Cotabato-West Sangihe Trench), in the Sulawesi Sea and the Moro Gulf (Hamilton 1979). A tsunami hit Cotabato and Lanao Sur in 1976 killing some 7,000 people. An eyewitness living on Bongo Island off Cotabato City once described to the first author the impact of that tsunami on this island. The Sulawesi Sea, the Moro Gulf, and the Davao Gulf have been the epicenters of many shallow earthquakes of magnitudes 7.0 or more from 1918–1973 (Fig. 7) (MRDP-CMBC 2003).

OBJECTIVES

The main objective of this review is to assemble secondary data and information inclusive of those from gray literature that will contribute to the building of a biodiversity profile of the seas of southern Philippines. The other objectives are the identification of the major threats to the biodiversity and the determination of gaps in our current knowledge of the biodiversity.

METHODS AND MATERIALS

This paper is a table review of the findings of research and development projects on the biodiversity of southern Mindanao, whether published or unpublished. The documents examined consisted of (1) papers in refereed and non-refereed journals, (2) books, (3) unpublished project reports, (4) newsletters, (5) maps and charts, (6) selected papers posted on the Internet, and (7) posters produced by government agencies. Telephone and e-mail facilities have also been used to access information. The information gathered from the aforementioned sources was supplemented with interviews from knowledgeable persons involved in marine resource-related business in General Santos City and Davao City. The data and information on the biodiversity of southern Philippine seas are discussed in relation to those in other areas of the Philippines, where possible, to give the reader an idea of how the biodiversity of

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Figure 6. Island arc-elements in the central and southern Philippines. (Source: Hamilton 1979)

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Figure 7. Earthquake Map of Mindanao. (Source: MRDP-CMBC 2003 Baseline Survey Report)

southern Mindanao compares with those in other parts of the country, and to highlight gaps in our knowledge of the four southern Philippine seas. No statistics except the mean have been used in this report. There are no SE estimates because the authors of the papers and reports reviewed (except those dealing with fish density and biomass estimates from MPAs and non-MPAs in the Visayas, Spratlys, Maguindanao and Sultan Kudarat) did not include them.

RESULTS AND DISCUSSION

Under this section, we present our findings on the biodiversity of southern Philippines and compare it (where possible) with those of other parts of the country.

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Seagrasses, Mangroves, and Corals

The three shallow-water marine ecosystems common in the Philippines are seagrass beds, mangroves and coral reefs. Their health status indicates the conservation status of the marine environment as well. Fig. 8 shows the species richness of seagrass and mangrove areas in five localities, two protected areas (Sultan Kudarat and Maguindanao) and three unprotected areas (Sarangani Bay, Davao Gulf, and Bay). There were 6 to10 species of seagrass (Table 1) and 6 to17 species of mangrove trees (Table 2). Also shown is the percentage of live hard coral in six localities (two protected areas, Sultan Kudarat and Maguindanao, and four others unprotected) ranging from 25% in Maguindanao (protected in 2005) to 68% in Sarangani (unprotected in 1987).

Table 1. Seagrass species identified in southern Philippines. *Excluding Malalag Bay

SEAGRASS SPECIES Paril- Bongo Sarangani Davao Malalag Sangay Is. Bay Gulf* Bay Potamogetonaceae Halodule uninervis X X X Halodule pinifolia X X X X X Cymodocea serrulata X X X Cymodocea rotundata X X X X X Syringodium isoetifolium X X X X X Thalassodendron ciliatun X

Hydrocharitaceae Enhalus acoroides X X X X X Thalassia hemprichii X X X X X Halophila spinulosa X X Halophila ovalis X X X X X Total 10 6 7 10 9 7

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Table 2. Mangrove species identified in southern Mindanao. *Excluding Malalag Bay

Paril- Bongo Sarangani Davao Malalag FAMILY SPECIES Sangay Is. Bay Gulf* Bay

Rhizophoraceae Rhizophora X X X mucronata Rhizophora X X X X apiculata Ceriops X X decandra Ceriops tagal X X Bruguiera X parviflora Bruguiera X cylindrica Bruguiera X sexangula Avicenniaceae Avicennia X X X marina Avicennia X X X X alba Avicennia X X lanata Avicennia X officinalis Sonneratiaceae Sonneratia X X X X alba Sonneratia X X X caseolaris Combretaceae Terminalia X X catappa Lumnitzera X littorea Lumnitzera X racemosa Myrsinaceae Aegiceras X floridum Aegiceras X corniculatum Euphorbiaceae Excoecaria X X X agallocha Fabaceae Pongamia X X pinnata Prosopis X vidaliana Lythraceae Pemphis X X acidula

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Table 2. continued.

Paril- Bongo Sarangani Davao Malalag FAMILY SPECIES Sangay Is. Bay Gulf* Bay

Palmae Nypa fruticans X X X X Acanthaceae Acanthus X ilicifolius Bignoniaceae Dolichandrone X X spathacea Melaiceae Xylocarpus X X granatum Xylocarpus X moluccensis Xylocarpus sp. X

TOTAL 12 28 17 6 10 7 16

In the country in general, areas with good seagrass meadows harbor more than 10 species. The localities sampled did not exhibit a high species richness for seagrass. For excellent mangrove forests, 20 or more species are expected. An example is southern Palawan, which has 27 species of mangrove trees out of more than 30 species reported from the Philippines (Matillano 2005). The remaining mangrove forest patches in southern Philippines appear to show various degrees of disturbance. The live coral cover at the lower end of the range (25–40%) in southern Mindanao appears to be similar to those on unprotected reefs in other parts of the country. But protected coral reefs in the Central Visayas have generally higher live coral cover, about 50–60% (see Alcala et al. 2006).

Biodiversity in Marine Protected Areas (MPAs) and Unprotected Areas

In the area, 31 MPAs have been established or are being established (SUAKCREM unpubl data): one in Zamboanga del Sur, eight in Sarangani, seven in Davao del Sur, 11 in Davao del Norte and one each in Sultan Kudarat, Maguindanao, Compostela Valley, and Davao Oriental. However, in only few of them is the biodiversity known. The only available data are from two MPAs, and these are summarized in this report. This is because monitoring through time has not been done for most of the MPAs. As most MPAs are located along shallow coastal areas, the biodiversity reported from them concerns the shallow water species

Alcala et al.: Biodiversity of Southern Philippine Seas 15

Figure 8. (A) Seagrass species richness, (B) Mangrove species richness, and (C) Live coral cover (%) in southern Mindanao. Sultan Kudarat and Maguindanao sites are MPAs. (Sources: MRDP-CMBC Annual Impact Assessment 2005; Mindanao State University-Naawan 1995; Calumpong et al. 1997a; Calumpong et al. 1997b) Figure in parenthesis after site indicates number of stations surveyed. Year indicates time of survey.

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commonly distributed at water depths not exceeding 50 m. Essentially, similar groups of shallow-water marine species have been reported throughout the country, and deep-water, globally important biodiversity such as whale sharks, dolphins, and dugongs have been observed only in certain areas. The occurrence of these species in or near MPAs depends on the presence of food sources. This is true for example of dugongs, which are dependent on the presence of a couple of species of seagrass used as food. Seagrass and mangrove species. The 6,000-ha MPA in Maguindanao was established on Bongo Island in 2002–2005 by the local government unit of Parang, Maguindanao assisted by the BFAR- Autonomous Region of Muslim Mindanao (ARMM). The 1,200-ha MPA in Sultan Kudarat was established in the barangays of Paril and Sangay, municipality of Kalamansig also in 2002–2005, with the assistance of the DENR. Both MPAs consist of coral reef, mangroves and seagrass beds and are co-managed by the local government units and local communities. The species of seagrass and mangrove in these two MPAs and in unprotected sites in southern Mindanao listed in Tables 1 and 2 are common throughout the country. Reef and reef-associated fish. The reef and reef-associated fish species in southern Mindanao are listed in Appendix 1, based on the 2002–2005 monitoring reports on the two MPAs in Sultan Kudarat and Maguindanao (MRDP-CMBC Annual Impact Assessment 2005, Nillos et al. 2005a, 2005b) and from rapid-survey assessments made at few selected sites in Sarangani Bay, Davao Gulf and Malalag Bay (Calumpong et al. 1997a, 1997b; Mindanao State University 1995). A total of about 350 species in 33 Families has been identified in underwater visual surveys. This is only a rough estimate of the total number of species found in the area as visual surveys generally underestimate the true numbers. The majority of the species in the list belonged to the category of small, indicator species, and only about 111 species in 13 Families were food or target species. The 13 Families to which the food fishes belong were Acanthuridae (surgeonfishes), Caesionidae (fusiliers), Carangidae (jacks), Eppiphidae (bat fishes), Haemulidae (sweetlips), Holocentridae (soldier fishes), Lethrinidae (emperor breams), Lutjanidae (snappers), Mullidae (goat fishes), Nemipteridae (breams), Scaridae (parrotfishes), Serranidae (groupers) and Siganidae (rabbitfishes). The acanthurids consisted of 27 species, followed by scarids with 16 species, serranids

Alcala et al.: Biodiversity of Southern Philippine Seas 17

with 15 species, and caesionids, lutjanids, mullids, and siganids with eight species each. The rest of the Families were represented by two to five species. Carangidae, which comprises top predators, was represented by only three species. No reef and reef-associated species were unique to southern Philippines. The two MPAs in Sultan Kudarat and Maguindanao had the highest mean species richness, >100 species, while unprotected sites in Sarangani, Malalag, and Davao Gulf had fewer species, indicating the role of protection in maintaining species richness (Fig. 9). The most noteworthy fish species found in these MPAs were the several large bumphead parrotfish (Bolbometopon muricatum) and the aquarium fish, blue tang (Paracanthurus hepatus). The former was found in the two MPAs, while the latter was limited to Paril-Sangay, Sultan Kudarat. There was a wide range in the estimates of mean fish density in the various sites in southern Mindanao. The highest estimate was in Sarangani Bay (9,075 individuals per 500 m2), followed by Davao Gulf (1,929 individuals/500m2), and was lowest in Malalag Bay (Fig. 10). It is difficult to make a generalization on the basis of the data, but it is obvious that the estimate for Sarangani Bay is an outlier. The mean biomass of target fish species (Fig. 11) was highest in Maguindanao (an MPA), 7.8 kg/500 m2 or 15.6 tons/km2. Davao Gulf, a non-MPA, was second, with a biomass of 5.2 kg/500 m2 or 10.4 tons/km2. The rest were lower than 10 tons/km2. These estimates are in the lower end of the scale for fully protected MPAs (e.g., Alcala 2001). Mean number of species of macro-invertebrates. There were only few macro-invertebrates such as giant clams, sea urchins, sea cucumbers, and shells observed in southern Philippines. The mean number of species ranged from 0 to 13.16 (Fig. 12), indicating their depleted status. There have been reports of rare gastropod species but documentation is lacking. Mean density of holothurians and giant clams in Maguindanao and Sultan Kudarat MPAs (Bongo Island and Paril-Sangay). The data for three years on density of these two macro-invertebrate groups in the two MPAs are shown in Fig. 13 for holothurians and Fig. 14 for giant clams. The giant clams belong to two common species, Tridacna squamosa and T. maxima. The effect of protection on giant clam density is obvious, density being higher after a period of protection. However, the density of holothurians was higher in take zones.

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Figure 9. Fish species richness in southern Mindanao. Figure in parenthesis indicates number of stations surveyed. Year indicates time of survey. (Sources: MRDP-CMBC Annual Impact Assessment 2005; Mindanao State University- Naawan 1995; Calumpong et al. 1997a; Calumpong et al.1997b)

Figure 10. Southern Mindanao Mean Fish Density compared to Density in and South China Sea. Figure in parenthesis indicates number of stations. Year indicates time of survey. (Sources: MRDP-CMBC Annual Impact Assessment 2005; Mindanao State University-Naawan 1995; Calumpong et al. 1997a; Calumpong et al. 1997b)

Alcala et al.: Biodiversity of Southern Philippine Seas 19

Figure 11. Southern Mindanao target fish biomass by locality compared with those in Bohol Sea and South China Sea. Figure in parenthesis indicates number of stations. Year indicates time of survey. (Sources: MRDP-CMBC Annual Impact Assessment 2005; Mindanao State University-Naawan, 1995; Calumpong et al. 1997a; Calumpong et al.1997b)

Figure 12. Southern Mindanao mean macro-invertebrate species richness. Figure in parenthesis indicates number of stations. Year indicates time of survey. (Sources: MRDP-CMBC Annual Impact Assessment 2005; Mindanao State University-Naawan 1995; Calumpong et al. 1997a; Calumpong et al. 1997b)

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Figure 13. Mean holothurian density at the two MPAs in Maguindanao and Sultan Kudarat in 2003–2005. TZ - take (fishing) zones; NTZ - No Take Zones. (Source: MRDP-CMBC 2003 Baseline Survey Report)

Figure 14. Density of two common species of Tridacna in the two MPAs in Maguindanao and Sultan Kudarat in 2003–2005. TZ - take (fishing) zones; NTZ - no take zones. (Source: MRDP-CMBC 2003 Baseline Survey Report)

Alcala et al.: Biodiversity of Southern Philippine Seas 21

Diversity of Fishery Species

It is estimated that there are about 2,500 fish species in the Sulu- Sulawesi Sea (e.g., DeVantier et al. 2004). The fishery species in this sea is not known. A BFAR poster “Marine Fishes of the Philippines” shows pictures of about 81 commercial species in 47 Families of cartilaginous and bony fishes that are widely consumed throughout the country. The top four specious Families in this poster in the order of abundance are Carangidae, Serranidae, Scombridae, and Clupeidae, the first two being reef-associated and the last two pelagic. The number of species in this poster is definitely an underestimate. In a 30-year study of coral reef fishes associated with MPAs in central Philippines, Alcala & Russ (2002) estimated about 100 species of food fishes. This number is also probably an underestimation.

Diversity of Species in Tuna Fisheries

Tuna fisheries mostly in southern Philippines and Sulawesi Sea increased in landings from 10,000 tons in 1971 to over 200,000 tons in 1981 according to Ruben Ganaden of BFAR. Another report (Chee 1996) provides data on tuna landings, 325,000 tons in 1989 and 1990 and 300,000 tons in 1991. Langley et al. (2004) puts the 2002 total tuna landings at 209,771 tons (146,436 tons commercial and 63,335 municipal). According to Noel Barut of the National Fisheries Research and Development Institute (NFRDI), the total landed catch for all tunas is more than 500,000 tons. For 2005, Regions 11 and 12 (Davao and Cotabato provinces) produced 293,000 tons of fish (assumed to be mainly tunas), and exported 84,288 tons in 2003, 77,356 tons in 2004, and 54,708 tons in 2005 (Fisheries Statistics of the Philippines 2003– 2005). Species landed were yellowfin (Thunnus albacares), skipjack (Katsuwonus pelamis), frigate (Auxis thazard), bullet (Auxis rochei), longtail (Thunnus tonggol) and bigeye (Thunnus obesus), the latter two being relatively insignificant (Report of the Workshop on Philippines and Indonesia research activities. Indo-Pacific Tuna Development and Management Program 1983). Aprieto (1982) considers yellowfin, skipjack, frigate and eastern little tuna (Euthynnus affinis) as the four important tuna species. She pointed out that tuna migration (usually understood as the physical movements of tunas in oceans around the world) does not stop at capture but continues to move over long distances

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in the form of canned products. Rasalan (1977) and Montilla & Bunag (1957) mention the blue bonito (Euthynnus yaito) as a commercial tuna species. Aside from the tuna species, non-tuna species caught off southern Mindanao include blue marlin (Makaira mazara), sailfish (Istiophorus platypterus), black marlin (Makaira indica), and swordfish (Langley et al. 2004). The southern Philippine seas appear to have the largest number and volume of large fishery species in the country. The tuna species for export are the yellowfin and bigeye, for canneries the skipjack, and for the local market the frigate, bullet and the eastern little tuna. Major importers of chilled fresh tuna in 2002 were Japan, USA, and Hongkong, and Canada, Germany, and Singapore for canned tuna (Langley et al. 2004). Tuna handline boats numbered ca 10,000 in 2002, but licenses issued were less. General Santos had 2,000 vessels for handliners. Ring net fleet in General Santos was about 500 vessels; about 41 (in Davao) and 40 (in General Santos) were purse seiners. Tuna Migrations. Movements to and from the Philippines of tagged yellowfins, skipjacks, and bigeyes through the Sulawesi and other seas in the Philippines, Indonesia, New Guinea and other islands in the western Pacific have been summarized in maps in the WWF Philippines biophysical assessment (2003). These maps are reproduced in this report (Figs. 15–18). The impression is that “tuna highways” exist in these seas. Comparison of Present and Past Fisheries. A reliable observer (A. Ong) who has had wide and long experience on tuna fishing recalls that tuna fishing was a year-round activity in the area in the 1970s–1980s when tuna species were abundant in Sarangani Bay and environs. At those times yellow fin tuna and skipjack were the common commercial fishes in the area. The skipjack trapped in fish corrals was easily caught by hand. In Sarangani Bay, it was not unusual to catch 80 tons of skipjack in one day in the 1980s. This fish at those times grew to large sizes, 10–15 kg, in contrast to their rarity and small size (1 kg) these days (A. Ong, pers comm). The yellow fin tuna has been over-fished in the seas of southern Philippines and the adjacent Sulawesi Sea. Tuna long-liners and hand- liners now fish far out into the Indonesian Sulawesi reaching the Halmahera and Taliabu Islands to as far as New Guinea in order to catch sufficient fish volume for the export market estimated at US$33M per year for the 3,000 hand-liners and US$50-60M for long-liners and other gears catching yellow fins and other species (R. Lim, pers comm).

Alcala et al.: Biodiversity of Southern Philippine Seas 23

Movements of tuna released in the Philippines and recaptured Movements of tuna recaptured in the Philippines from outside Philippine waters (Shipjack – solid lines, yellowfin – releases outside Philippine waters (Shipjack – solid lines, dashed lines, PRIMEX-SPC, 1993) yellowfin – dashed lines, PRIMEX-SPC, 1993)

Figure 15. Movement of Skipjack and Yellowfin Tuna to and from the Philippines (Source: WWF-Philippines 2003)

Figure 16. Movement of Skipjack Tuna from Sulu, Sulawesi, and Philippine Seas. (Source: WWF- Philippines 2003)

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Figure 17. Movement of Yellow-fin Tuna Sulawesi, Philippine, Sulu and Seas (Source: WWF-Philippines 2003)

Figure 18. Movement of Big-eye Tuna from Philippine, Sulawesi, Sulu and Seas (Source: WWF-Philippines 2003)

Alcala et al.: Biodiversity of Southern Philippine Seas 25

Conservation Strategies. Some tuna fishers recommend the exclusive use of hand-lines and the exclusion of other gears in catching tuna because they claim that hand-lines are selective for large-size fish. Use of hand-lines also makes it possible for small unskilled fishers to participate in fishing, thus giving them an opportunity to improve their lives. However, it is claimed that hand-lines catch more sexually mature tunas, implying reduction of spawners. There is reason to believe that tuna depletion has also been caused by the use of small mesh-size ring nets (sinsoro) and baby seines that catch juvenile tuna. Taking small fish reduces the value of the catch. Floyd and Pauly (1984) and Aprieto (1982) have presented evidence on the possible role of fish aggregating devices (payaos) in facilitating the capture of juvenile fish in and around these devices. There are at present about 20 such fish aggregating devices in Sarangani Bay. The practice of catching both large mature fish and juveniles should be controlled to achieve sustainability. There is evidence from length-frequency data that Philippine tuna fishers catch a large proportion of juveniles. The median for tuna catch by ring net is 25 cm, that for US purse seiners is 50–100 cm, and that for Japanese long-liners is 120 cm (Sakagawa 1996). Mullen et al. (1996) give the median of length frequency distribution of yellowfin caught by purse seine as 25–30 cm (range 15–195 cm). Miyabe et al. (1996) confirmed the identification of these small juvenile yellowfins and skipjacks caught in shallow waters off General Santos with the use of mitochondrial DNA. . Fishery Species in Davao Gulf and their Conservation Status

For non-tuna fish species in Davao Gulf, Armada (2004) has shown that catching of juveniles is a threat to sustainable fisheries. He listed eight species of fish with their population parameters, one of which is their extraction rates (E). All of these species appear to have high E’s, all exceeding 0.50 (0.58–0.70) due to overexploitation at the juvenile and adult stages. These species belonging to Families Carangidae, Menidae, Scombridae and Siganidae are Selar crumenophthalmus, Rastrelliger brachysoma, R. kanagurta, Mene maculata, Auxis thazard, A. rochei, and Siganus canaliculatus. The last-named species has the highest E due to extremely high rate of exploitation occurring not only in Davao Gulf but also all over the country. Armada’s study should be repeated for other fishery species.

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The fishery yields for five groups of fish in Davao Gulf and Moro Gulf caught by various gears in 1982 are shown in Fig. 19. Davao Gulf has greater fishery production (0.1–1.0 ton/km2) compared with Moro Gulf (0.1–0.2 ton/km2). These figures indicate a higher fishery productivity for Davao Gulf.

Figure 19. Yields of pelagic fish species in Davao and Moro Gulfs in 1983. (Source: Yesaki 1982)

Billfishes (Family Istiophoridae)

No study, published or unpublished, appears to have been made on this group of commercially important pelagic species in the marine waters under review. Interviews with two tuna fishers (A. Ong and R. Lim) indicated their presence in the Sulawesi Sea. These species certainly pass through the southern Mindanao seas and the Sulawesi Sea because they migrate in the Indo-Pacific region based on the account by Nakamura (2001). Our informants stated that these fishes are strictly of local commercial importance and there is no international market for them. The reason is the fear of foreign buyers that these species accumulate high concentrations of heavy metals.

Alcala et al.: Biodiversity of Southern Philippine Seas 27

Two species of billfishes have been identified by an undated Fisheries Resource Management Project, BFAR poster “Marine Fishes of the Philippines.” These two species are the Black Marlin (Makaira indica) and Indo-Pacific Sailfish (Istiophorus platypterus). Both species are widely distributed in the tropical and subtropical waters of the Indo- Pacific and sometimes extending to temperate waters (Nakamura 2001).

Cetaceans (Whales and Dolphins)

Thus far only one study has been made partly on the cetaceans of Sulawesi Sea (Dolar & Perrin 1996). They reported six species, namely, Stenella longirostris, S. attenuata, Lagenodelphis hosei, Grampus griseus, Globicephala macrorhynchus, and Physeter macrocephalus. Bautista and Tan (in manuscript) report nine sighting of four species of cetaceans Kogia sima, Stenella longirostris, Grampus griseus, and Tursiops aduncus. Dolar (1999), Perrin et al. (2002) and Dolar et al. (2006) have reported on the marine mammals of the adjoining Sulu Sea. Because of the large size of the Sulawesi Sea, it is almost certain that the number of whales and dolphins will exceed that known for the Philippines (27 species). The Longmann’s beaked whale was reported from Matina, Davao City in 2003. It is obvious that studies on the cetaceans of southern Philippines need to be conducted (D. Torres, pers comm). Dolar (pers comm, unpubl list) recently reported a total of 27 marine mammal species in the Philippines, 26 species of cetaceans (Order Cetacea) composed of 21 toothed whales and dolphins and five species of baleen whales and one species of the Order Sirenia, the dugong. Kreb & Budiono (2005) suggest that “the Indonesian through- flow… (passes) east of Kalimantan, through the Sulu-Sulawesi Seas and Makassar Strait carrying larvae and plankton from the Pacific Ocean to the Indian Ocean. Similarly, these seas most likely provide a migratory pathway for whales and dolphins.” These authors have reported 12 species listed in Table 3 in the marine waters east of Kalimantan. These listed species are also probably found in the southern Philippine marine waters under review. Whales and dolphins are threatened by fishing nets (ring nets, gill nets, drift nets). Dolphins are often caught as fisheries by-catch from the Sulu Sea (Dolar 1999, pers comm).

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Table 3. Cetacean species list.

Species 1. Tursiops truncatus 2. Stenella attenuata 3. Stenella longirostris 4. Stenella longirostris, sp. (with short beak) 5. Orcaella brevirostris 6. Stenella l. roseiventris 7. Tursiops sp. 8. Pseudorca crassidens 9. Peponocephala electra 10. Globicephala macrorhynchus 11. Tursiops aduncus 12. Neophocaena phocaenoides

In the Sulawesi Sea, our informant reported that tuna fishers are heavily penalized if caught capturing whales and dolphins. A certification process is in effect which denies access of tuna products to tuna exporters violating the ban on these endangered species (A. Ong, pers comm).

Dugong

The dugong is definitely present in the southern part of the Davao Gulf. Several sightings have been made by R. Lucero and colleagues off New Argao, Malita, Davao del Sur in 2005 (R. Lucero, pers comm). This endangered mammal was observed to swim singly or as a group of three individuals, including a calf. Apparently, these animals were used to the presence of boats about 50 m away. The animals probably fed in the area where three species of seagrass used as food occur. The population size is not known but it is most likely very small. Reports indicate the presence of dugongs in the Sarangani group of islands, where seagrass beds are present. The third site with confirmed dugong (two adult individuals) is the Paril-Sangay area in Sultan Kudarat, part of the Moro Gulf, in 2005 (MRDP-CMBC Annual Impact

Alcala et al.: Biodiversity of Southern Philippine Seas 29

Assessment Report 2005). These individuals apparently must have fed on seagrass beds outside of the site observed because of the absence of seagrass at the observed site. It is inferred that the animals inhabit the coastline of Sultan Kudarat and Sarangani provinces in western Mindanao. One individual was found dead in Sarangani sometime before 2005. The dugong has been reported in other parts of the Philippines (, Palawan) and is threatened by dynamite blasts and in some cases is directly hunted (Marsh et al. 2002, L. Dolar, pers comm).

Sea Turtles

Only three species of sea turtles (hawksbill, green and leatherback) have thus far been reported in the seas off southern Philippines. Five species have been reported in the Sulu-Sulawesi Sea (DeVantier et al. 2004). In Davao City, the beach of Matina Aplaya has been a nesting site of the hawksbill for some time now and hatchlings have been returned to the sea. In 2003, 512 eggs of the hawksbill hatched; the hatchlings were returned to the sea at this site (Torres et al. 2004, J. Guirjen, pers comm). The area is a protected marine turtle sanctuary through the initiative of Mr. Leo Avila of Davao City, who has been waging a campaign to conserve sea turtles in the area. At , Davao Oriental, hawksbill, green and leatherback turtles have been reported (The Marine Protected Area Management Plan 2005–2009, Municipality of Lupon, Davao Oriental). Up to 30 green turtles per night were observed nesting on Panikian Island, Zamboanga del Sur (D. Torres, pers comm.). Green sea turtles are often released back to Sarangani Bay after capture (newspaper account, Philippine Star, February 15, 2007). In the western coast of Mindanao, the beaches of Klid (sitio of Barangay Paril) and Danauan Island (also in Paril), both in Kalamansig, Sultan Kudarat province have been used by green and hawksbill turtles as nesting sites for several years. Since 2003 the local community has been protecting the nests and the hatchlings were allowed to return to Illana Bay, which is part of Moro Gulf (MRDP-CMBC Impact Report for 2005). Similarly, on the island of Bongo, off Cotabato City, the beach at Barangay Limbayan has been an egg-laying site of the two species. Local communities have protected the nests, and hundreds of hatchlings have been allowed to return to the bay in 2003 and 2005.

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Sea Turtle Migrations in the Sulawesi Sea. Since no tagging of hatchlings in southern Mindanao was done, it is not known where these hatchlings go. But some information exists on turtles tagged outside the Philippines that were reported to reach southern Mindanao. Ramirez de Veyra (1994) reported that a green turtle tagged on Yap Island, Micronesia in 1991 was caught in a fish gear in Glan, South Cotabato on 17 January 1992 and must have traversed the Sulawesi Sea. This animal died before its scheduled release. One (No. 27961) of the four leatherback turtles tagged in Papua was tracked by satellite telemetry from Jamursba Medi Beach to Davao Gulf in 2002, traversing the Sulawesi Sea (Fig. 20) (Dermawan 2004). Thus, data showing that sea turtles hatched in southern Mindanao migrate across the Sulawesi Sea are lacking. However, based on the two examples mentioned above, it is likely that those hatchlings from Davao, Sultan Kudarat and Maguindanao do so.

Figure 20. Route of leatherback turtle from New Guinea to Davao Gulf. (Source: Dermawan 2004)

Alcala et al.: Biodiversity of Southern Philippine Seas 31

Sea Turtle Movements from and within the Philippines. The movements of green sea turtles tagged in the Turtle Islands, Sulu Sea, have been on the whole within the Sulu Sea (Fig. 21), except for one animal recovered dead in the Sulawesi Sea off East Kalimantan (Sagun 2004). The rest of the tagged animals were recovered in the Sulu Archipelago and the Visayan Seas. Torres et al. (2004) included data from reports on green turtles tracked by satellite telemetry from Pulau Redang and Sarawak in Malaysia, from Thailand, and from the Turtle Islands to Balabac Island. In the late 1970s, one of the several hawksbill turtles we tagged in Negros Oriental was caught by a fisherman in Masinloc, Zambales, but the tag was not returned to us. Earlier, Meylan (1982) mentioned a report of a single hawksbill tagged in the Turtle Islands, Sabah that traveled a straight-line distance of 713 km in 40 days to the Philippines. Threats to Sea Turtles. Gill nets and direct hunting remain the major threats to sea turtles. This is particularly true in southwest and western Philippines (including the Spratlys), where fishers (some of whom are local government officials) have been hunting turtles and even trading them with foreigners.

Figure 21. Movements of green sea turtles tagged in the Turtle Islands, Sulu Sea. (Source: Sagun 2004)

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Whale Sharks (Rhincodon typus)

Records of the occurrence and movements of the whale shark through and in the Sulawesi Sea are lacking. One animal was reported in the vicinity of General Santos in 2006. Migration in the Sulu and South China Seas. Whale sharks like tunas and billfishes migrate over long distances across seas belonging to different political jurisdictions. Eckert et al. (2002) monitored the movements of six whale sharks from the Sulu Sea to the South China Sea under the political jurisdiction of the Philippines, Malaysia and Vietnam. Two of the sharks traveled 4,567 and 8,025 km. Because of this migration, conservation of this species requires agreement among these three countries. Whale sharks are now protected in many parts of the country but are still threatened by indiscriminate fishing. From the popular press, it appears that eco-tourism has helped in the conservation of the whale shark especially in Donsol, Sorsogon.

Plankton and Fish Spawning Sites

Three studies on plankton in the Davao Gulf have been brought to our attention: those by Mindanao State University at Naawan (1995), Monteclaro (2002) and Abunal (2000). The Mindanao State University study deals with both phytoplankton and zooplankton but does not specifically refer to fish plankton. Monteclaro reported on the zooplankton of Davao Gulf, which he found equally abundant during the northeast and southwest monsoon months but exhibited more biomass during the southwest monsoon. Abunal (2001) found fish eggs and fish larvae throughout the year but mostly during August. Six fish families (but not including the Scombridae) dominated the fish larval composition. The author concluded that commercial fish species, including tuna and reef fish, spawn and are nursed in Davao Gulf. More detailed studies are needed to identify fish larvae to species before making such a conclusion. Studies on fish eggs and fish plankton, especially those of commercial species, are very important in determining the sources of propagules that maintain fishery species populations. The importance of such studies is enhanced if correlated with ocean currents. Information from Noel Barut of NFRDI indicates that the seas under review are tuna

Alcala et al.: Biodiversity of Southern Philippine Seas 33

spawning grounds. The surface currents in the Sulawesi Sea would transport fish larvae from the Pacific Ocean, where, according to Jose Ordoñez of BFAR (pers comm), tuna also spawns. Because tuna individuals of varying sizes from small juveniles to adults were seen in the Sulu Sea, Moro Gulf and Sulawesi Sea, these seas are likely to be spawning sites. Spawning sites of coral reef fish elsewhere appear to be reef areas where several species of Serranidae (groupers) and other fish groups congregate to form spawning aggregations at favorable times of the year. Practically nothing is known on these aggregations in the Sulawesi area as well as in other Philippine seas. A fish plankton study in the South China Sea was made in April 2004 by two graduate students from the University of the Philippines- Visayas and Silliman University (Floren 2008). Fish larvae of demersal species were taken in the vicinity of coral reefs of northern Palawan and the North Danger Reef (Pugad-Parola Atoll) in contrast to pelagic fish larvae taken in the more oceanic sampling stations in between.

Sea Snakes

No study has been done on the sea snakes in the southern Philippine seas and the Sulawesi Sea. But fishers have reported sea snakes from Sarangani Bay and Sarangani Strait. Sea snakes in the Pacific region have been reviewed by Rasmussen (2001). There is a need to determine the species and their numbers for comparison with the Visayas, which has about a dozen species (Alcala 1986).

Migratory Shore, Sea and Aquatic Birds

There are probably more than 180 species of migratory birds wintering in the Philippines, some of them aquatic, sea, and shore birds (Jensen et al. 2005). Seabirds are good indicators of schools of fish, and their presence in a specific sea area serves as a guide to fishers where to fish. Sea birds follow well-known flyways to various parts of the Southern Hemisphere. McClure (1974) summarized the information as of the early 1970s. Three East Asian migration routes to various parts of Indonesia and Australia pass through the Philippines via the chain of islands, the Sulu Sea and the Sulawesi Sea. The information on ringed birds accumulated by the project Migratory Animal Pathological Survey

34 The Philippine Scientist, Volume 45 (2008)

in the 1960s and 1970s showed recoveries of 25 species on Mindanao, some in Davao, Lanao and Zamboanga provinces. The species consisted of egrets (including the cattle egret Bubulcus ibis), night herons (Gorsachius spp.), and sterns (Sterna spp.). Egrets are birds of swamps and coastal areas throughout the country. Frigate birds (Fregata sp.) ringed from islands in Southeast Pacific have been reported to fly to central Philippines via the Sulawesi Sea. Pelagic sea birds of the Family Diomedeidae (albatrosses) and the Family Procellariidae (shearwaters) probably traverse the Sulawesi Sea in their migrations. The Family Sulidae (boobies) move around and nest on small islands (e.g., Tubbataha islets in the Sulu Sea), and are likely to be found on small islands in the Sulawesi Sea.

Marine Species Unique to the Sulawesi Sea Area

The marine biodiversity in southern Philippine seas have many species common to the rest of the country. This is due to ocean water circulation that distributes marine propagules over a wide area. Because of this, species endemism is low in marine ecosystems. However, some endemic species exist in some areas. For example, some rare species of corals are found only in southern Palawan and South China Sea (Morales et al. 2005) (Fig. 22). In the Sulawesi Sea rare cowries and cone shells are found on Balut Island in the Sarangani Group of Islands (Fig. 23) (http://www.shellhorizons.com/details.asp?ProductID=CT-106&Page=1; http://www.shellauction.net/auction_shell.php?id=115216; http://www. schnr-specimen-shells.com/cervus.jpg). The Sulawesi Sea is the home of a very important fish from the standpoint of evolution, the coelacanth. The second known coelacanth species (Latimeria menadoensis) was caught off North Sulawesi in 1997 (Erdman 1999). Fricke et al. (2000) suggested that the population is very small and requires conservation measures but the probability that the coelacanths of North Sulawesi are derived from a different area and drifted there with oceanic currents, probably from the southern Philippines or remote Pacific islands through the southerly Mindanao current, cannot be eliminated. If this species were to be found in Philippine part of the Sulawesi Sea, the country can be proud to be home to this remarkable fish. Thus far, the search for this species by Conservation International in the Sulawesi Sea has yielded negative results. A group of Filipino divers is reportedly searching for Latimeria in the Sarangani Islands.

Alcala et al.: Biodiversity of Southern Philippine Seas 35

The tunas, billfishes, whales, dolphins, dugong, whale sharks, sea turtles, and pelagic sea birds are generally considered globally significant species because of their ecological and economic impacts. They exhibit migratory behavior and are valued as food and/or tourism species.

Figure 22. Two rare species of Acropora, (top) A. fastigata (bottom) A. multiacuta from southern Palawan. (Photo by Brian Stockwell)

36 The Philippine Scientist, Volume 45 (2008)

Cypraea herasei

Conus thomae Conus cervus Figure 23. Three species of rare shells found in Balut Island, Sarangani Province (Sources: www.shellauction.net, www.shellhorizons.com, www.schnr- specimen-shells.com)

Alcala et al.: Biodiversity of Southern Philippine Seas 37

Offshore MPAs

Thus far, only few shallow-water MPAs have been established in the study area. The way to move forward is not only to establish more shallow-water MPAs but also to establish MPA in areas with deeper waters. Sulawesi Sea, because of its large area, appears to offer opportunities in this direction, as MPAs can be an effective means to conserve large migratory fish stocks (e.g., tuna) as well as other globally important biodiversity. The only example of deep-water (high seas) MPA is the Ligurian Sea Cetacean Sanctuary in the Mediterranean (http://en.wikipedia.org/wiki/Ligurian Sea Cetacean Sanctuary). A major constraint is getting regional and international agreements for management. Areas near island groups between the Philippines and Indonesia (Fig. 4) are ideal for establishing deep-water or high seas MPAs. There already exist international and regional management frameworks for such MPAs such as the United Nations Law of the Sea Convention, the Convention on Biological Diversity, International Maritime Organization and Regional Management Organizations, and Fish Stock Agreements.

MPAs and Tourism

MPAs have been shown to be effective as tools for fishery management and conservation of biodiversity (e.g., Alcala 2001). One good idea is to include, in addition to regular tourism, recreational fishing in the design and planning of MPAs in southern Philippines, where a potential for recreational fishing for large pelagic fish still exists. Fishing for pelagic game species with the intention of returning the captured fish after photographing them could attract tourists interested in recreational fishing. This activity outside of no-take zones could bring in income that could be used for the protection and management of MPAs. The Sarangani group of islands could well be considered for recreational fishing (A. Ong, pers comm). The role of MPAs in tourism is amply demonstrated by successes in the Central Visayas, particularly Bohol and Negros Oriental (Alcala et al. 2006).

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Threats to Marine Biodiversity

Threats to marine biodiversity in other parts of the country also exist in southern Philippines as already discussed above. Some fishing gears (e.g., fish aggregation devices, beach seines) catch or facilitate the capture of adult and juvenile fish. Dolphins and sea turtles are still part of commercial fishing by-catch. Dugongs, whale sharks, turtles and whales are often actively hunted. Target fishes, such as groupers and even dugongs, are still fished using cyanides and/or blasting materials. Many species of target or food fishes, mollusks (e.g., giant clams, cowries, cone shells) and echinoderms (e.g., sea cucumbers) are over- harvested. The only way to address these threats to the biodiversity of southern Philippines is to conduct massive educational and information campaigns with the objective of changing attitudes and behavior of our people and offering them alternative, non-extractive uses of biodiversity such as tourism. These activities are made difficult because of poverty that drives people to engage in destructive fishing, but they can be done. Non-monetary rewards and incentives ideally complement educational and conservation campaigns.

SUMMARY AND CONCLUSIONS

This review of research studies and development projects in southern Philippine seas and the Sulawesi Sea, based on available published and unpublished reports and papers, shows that the shallow- water biodiversity of the area studied does not differ much from those in other similar areas of the country in terms of (1) species composition and (2) ecological/conservation status. Unprotected coastal and marine areas in southern Mindanao are comparable with unprotected areas in other parts of the country. Protected areas in southern Philippines have better biodiversity quality than unprotected ones. Southern Philippine seas have, however, biodiversity and fishery species (primarily tunas) that do not occur in large numbers in other parts of the country, upon which an estimated six million people depend directly for livelihood and income. The marine environment of southern Philippines is more complex than those in other parts of the country because of the bottom topography, oceanography and vastness of the Sulawesi Sea. These

Alcala et al.: Biodiversity of Southern Philippine Seas 39

physical and environmental features are the primary reasons for the enormous marine resource production and development potentials of southern Philippines. These features can account for the uniqueness of the biodiversity of the Sulawesi Sea compared with the other seas surrounding the country. Among the unique species are the tunas and the Manado coelacanth, but there are probably more unique species waiting to be discovered in the depths of this vast ocean. While there are geological processes (e.g., earthquakes and tsunamis) in the southern Philippine seas and the Sulawesi Sea that can cause occasional environmental disturbances, the area appears to be generally stable. The primary role of stakeholders is to eliminate the gaps in our knowledge of the area through more studies, to protect the environment and the marine biodiversity and to manage the marine resources for sustainable development through action programs such as the establishment of shallow-water and deep offshore MPAs and the implementation of measures to stop the exploitation practices leading to resource depletion and environmental degradation.

RECOMMENDATIONS

1. There are many gaps in our knowledge of the oceanography and biodiversity of the seas of southern Philippines and the Sulawesi Sea. More studies to determine the biodiversity of the area and its oceanography are needed. Some of these studies would require sophisticated equipment such as submersibles being proposed by American oceanographers to study inner space speciation in the Sulawesi Sea. 2. Without using sophisticated research equipment, much can be achieved toward understanding biodiversity by establishing more shallow-water MPAs with provisions for regular monitoring over time as well as strengthening the management of existing ones. These MPAs will be useful in bringing back depleted demersal fishery species and can play an important role in attracting tourists for economic development (e.g., recreational fishing). 3. There is a need to establish large, high seas or offshore MPAs encompassing deep areas in the high seas used as migration routes and spawning/nursery grounds of large pelagic and

40 The Philippine Scientist, Volume 45 (2008)

migratory species. The Sarangani and Balut Islands can be part of the high seas or offshore MPAs. 4. In agreement with Indonesia, a large MPA should be established for deep-sea monitoring and studies on unique/rare species (including the coelacanth) and oceanographic processes. 5. Because of the over-exploitation of the yellow fin tuna and other species, conservation and control measures (e.g., regulating/ banning non-selective gears such as payaos, fine-mesh beach seines, superlights) are needed. 6. Information, Education and Communication (IEC) and studies on the large migratory species in the Sulawesi Sea should be conducted by academic institutions in southern Philippines.

ACKNOWLEDGMENTS

The financial support of WWF is gratefully acknowledged. Dr. Louella Dolar Perrin, an authority on marine mammals, kindly supplied copies of papers on marine mammals of the Sulawesi Sea. Roger Lim, Alex Ong, Pinky Ong, our friends in General Santos and Davao City, shared with us their vast knowledge and experience on the tuna fisheries of the Sulawesi, Sarangani Bay and Moro Gulf. Girlie Gumanao of Davao del Norte State College, Dr. Alexander Campaner, the President of Southern Philippines Agribusiness, Marine and Aquatic School of Technology (SPAMAST) and Ruth Lucero a faculty member of this school, kindly gave us lists and abstracts of their research projects. George G. Campeon, DA Regional Director kindly supplied us papers on plankton. Noel Barut, gave us information and copies of published papers on fisheries statistics and status of the tuna fisheries. Dan Torres kindly supplied us information on sea turtle movements. Our assistants at SUAKCREM, Jasper Maypa, Julius Guirjen, Emily Layos, Estrilda Cruz-Am, and Gianani Gloria all assisted in various ways that enabled us to complete this report. Jasper Maypa prepared the illustrations. Finally, we thank the two anonymous referees for their comments and suggestions.

Alcala et al.: Biodiversity of Southern Philippine Seas 41

Appendix 1. List of reef and reef-associated fish species in southern Mindanao. *Include Davao Oriental, Davao del Sur and Samal Island.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Apogonidae Apogon aureus X X X Apogon angustatus X Apogon X bandanensis Apogon compressus X X X X X Apogon sealei X X Apogon sp. X X X Archamia X X zosterophora Cheilodipterus X macrodon Cheilodipterus X X quinquelineatus

Blennidae Escenius midas X Meiacanthus sp. X Meiacanthus X X X atrodorsalis Meiacanthus X X X grammistes Plagiotremus X rhynorhynchus

Chaetodontidae Chaetodon auriga X X X X Chaetodon X X X X X baronessa Chaetodon bennetti X X Chaetodon X citrinellus Chaetodon kleinii X X X X Chaetodon lineatus X Chaetodon lunula X X Chaetodon X X melannotus Chaetodon X X X X mertensii Chaetodon meyeri X Chaetodon X ocellicaudus

42 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Chaetodontidae Chaetodon X X X X octofasciatus Chaetodon X X X ornatissimus Chaetodon X X X X punctatofasciatus Chaetodon raffflesi X Chaetodon X rainfordi Chaetodon sp. X X X X Chaetodon X speculum Chaetodon spinus X Chaetodon X X X trifascialis Chaetodon X X X X X trifasciatus Chaetodon X ulietensis Chaetodon X X X X unimaculatus Chaetodon X X X X X vagabundus Chaetodontoplus X X mesoleucus Forcipiger X X X X flavissimus Forcipiger X X longirostis Forcipiger sp. X Hemitaurichthys X polylepis Heniochus X X acuminatus Heniochus X X X X X chrysostomus Heniochus X diphreutes Heniochus varius X X X X X Hemitaurichthys X X polylepsis Coradion altivelis X X Coradion X X X chrysozonus Corasion sp. X

Alcala et al.: Biodiversity of Southern Philippine Seas 43

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Cirrhitidae Cirrtichthys sp. X Cirrtichthys falco X X X Cirhitichthys apinus X X Paracirrhites X forsteri

Labridae Anampses X X caepoleopunctatus Anampses X X meleagrides Anampses twisti X X X X Bodianus axillaris X Bodianus diana X X X X Bodianus X X X X X mesothorax Bolbometopon X muricatum Cheillio arenatus X Cheillio X bimaculatus Cheillio inermis X X X Cheilinus celebicus X X Cheilinus chlororus X X X Cheilinus X diagrammus Cheilinus fasciatus X X X X Cheilinus trilobatus X Cheilinus undulates X Cirrhilabrus X X X X X cyanopleura Cirrhilabrus X punctatus Cirrhilabrus sp. X X X Coris aygula X Coris batuensis X X Coris dorsomacula X Coris gaimard X X Coris schroedi X X

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Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Labridae Diproctacanthus X X xanthurus Dischistodus X X melanotus Epibulus insidiator X Gomphosus varius X X Halichoeres chrysus X X Halichoeres X X X X hortulanus Halichoeres X margaritaceus Halichoeres X marginatus Halichoeres X X melanurus Halichoeres X X melapterus Halichoeres X X X X X prosopeion Halichoeres X X X richmondi Halichoeres X X X X scapularis Halichoeres sp. X X X Hemigymnus X X X X melapterus Hologymnosus X X annulatus Hologymnosus X X doliatus Labrid sp. X Labrichthys X X unilineatus Labroides bicolor X X Labroides X X X X X dimidiatus Labroides X pectoralis Labropsis australis X X Macropharyngodon X negrosensis

Novaculichthys X taeniorus

Alcala et al.: Biodiversity of Southern Philippine Seas 45

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Labridae Oxycheilinus X X digrammus Oxycheilinus X unifasciatus Pseudocheilinus X octotaenia Pseudanthias X huchtii Pseudanthias sp. X Oxymonocanthus X longirostris Stethojulis sp. X X X Thalassoma X X X X X hardwicke Thalassoma lunare X X X X X Thalassoma X X X lutescens Thalassoma X purpureum Thalassoma X quinquevittatum Xyrichtys pavo X X Cheilodipterus X X artus Cheilodipterus X X quenquelineatus Cheilodipterus sp. X Choerodon X anchorago

Pomacanthidae Apolemichthys X trimaculatus Centropyge bicolor X X X X Centropyge X X X bispinosus Centropyge nox X X Centriopyge tibicen X X Centropyge vrolikii X X X X X Chaetodontoplus X mesoleucus Genicanthus X lamarck

46 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Pomacanthidae Pomacanthus X imperator Pomacanthus X navarchus Pygoplites X X X X diacanthus

Pomacentridae Abudefduf X X X X X vaigiensis Abudefduf X sexfasciatus Acanthochromis X X polyacanthus Amblyglyphidodon X X X X X aureus Amblyglyphidon X X X X X curacao Amblyglyphidodon X leucogaster

Amphiprion clarkii X X X X X Amphiprion X occelaris Amphiprion percula X X X Amphiprion X X peridareion Amphiprion X X frenatus Amphiprion X X perideraion Amblyglyphidodon X X X leucogaster

Chromis acares X Chromis X X X amboinensis Chromis analis X X X X Chromis atripes X X X X X Chromis caudalis X X Chromis X X X X margaritifer Chromis nitida X Chromis X X X X X retrofasciata

Alcala et al.: Biodiversity of Southern Philippine Seas 47

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Pomacentridae Chromis sp. X X X X Chromis ternatensis X X X X Chromis viridis X X X X X Chromis weberi X X Chromis xanthura X X X Chryseptera X X brownriggii Chryseptera X X caeroleolineata Chryseptera cyanea X X X X Chrysiptera X X leucopoma Chryseptera X parasema Chryseptera X X X rollandi Chryseptera sp. X Chryspetera starcki X Chryseptera talboti X X X Cirrhilabrus sp. X Dascyllus aruanus X X X X X Dascyllus X melanurus Dascyllus X X X X X reticulatus Dascyllus X X X X X trimaculatus Lepidozygus sp. X Paraglyphipodon X X melas Paraglyphipodon X nigroris Pomacentrus X X alexanderae Pomacentrus X X X X X amboinensis Pomacentrus X bankanensis Pomacentrus X X boroughi Pomacentrus X X X X brachialis

48 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Pomacentridae Pomacentrus X cuadalis Pomacentrus X X X coelestis Pomacentrus X X lepidogenys Pomacentrus X X X X molluccensis Pomacentrus reidi X X X X Pomacentrus sp. X X X X Pomacentrus vaiuli X X Pomachromis X rollandi Neoglyphidodon X X X X melas Neoglyphidodon X X X nigroris Neopomacentrus X X X azysron Neopomacentrus sp. X X X Stegastes X fasciolatus Stegastes nigricans X X Stegastes sp. X X X

Zanclidae Zanclus cornutus X X X X X

TOTAL 8 196 129 188 81 80 84

TARGET SPECIES Acanthuridae Acanthurus bleekeri X X Acanthurus X caudalis Acanthurus X dussumieri Acanthurus mata X X Acanthurus lineatus X X Acanthurus X lituratus Acanthurus X X nigricans

Alcala et al.: Biodiversity of Southern Philippine Seas 49

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Acanthuridae Acanthurus nigroris X Acanthurus X X nigricauada Acanthurus X nigrofiscus Acanthurus X olivaceus Acanthurus X X X X pyroferus Acanthurus sp. X X Acanthurus X X thompsonii Ctenochaetus X X X X binotatus Ctenochaetus X X X X X striatus Ctenochaetus X strigosus Ctenochaetus X X tominiensis Naso annulatus X X Naso hexacanthus X X Naso lituratus X X X X Naso lopezi X Naso minor X Naso unicornis X X Paracanthurus X hepatus Zebrasoma scopoas X X X X X Zebrasoma X X verifellum

Aulostomidae Aulostomus X X X X X chinensis

Caesionidae Caesio X X caerulaureus Caesio cuning X X X X Caesio lunare X Caesio teres X X

50 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Caesionidae Pterocaesio X lativittata Pterocaesio marri X Pterocaesio pisang X X X X Pterocaesio tile X X

Carangidae Selaroides X leptolepis Megalaspis cordyla X Seriola sp. X

Eppiphidae Platax pinnatus X Platax tiera X X X

Haemulidae Plectorhinchus X X X X chaetodonoides Plectorhinchus X goldmanni Plectorhinchus X X lineatus Plectorhinchus X X lessonii

Holocentridae Myripristis sp. X X X X Sargocentron X caudimamaculatum

Sargocentron X punctatissimum Sargocentron sp. X

Lethrinidae Gnathodentex X X X aureolineatus Letthrinus lentjan X X Monotaxis X grandoculis

Lutjanidae Lutjanus bohar X X Lutjanus biguttatus X

Alcala et al.: Biodiversity of Southern Philippine Seas 51

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Lutjanidae Lutjanus decussates X X X Lutjanus fulvus X X X Lutjanus lutjanus X X Lutjanus sp. X X Macolor niger X X Aphareus furca X

Mullidae Mulloidichthys X X vanicolensis Parupeneus X X barberinoides Parupeneus X X X X X barberinus Parupeneus X X X X bifasciatus Parupeneus X cyclostomus Parupeneus indicus X X X X Parupeneus X X X X X multifasciatus Upeneus tragula X X X

Nemipteridae Monotaxis X grandoculis Pentapodus sp. X X X X Scolopsis bilineatus X X X X X Scolopsis lineatus X X X X Scolopsis ciliatus X

Scaridae Cetoscarus bicolor X Chlorurus sp. X X Scarus bleekeri X Scarus dimidiatus X X Scarus forstenii X X Scarus frenatus X X Scarus ghobban X X X Scarus globiceps X X X

52 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Scaridae Scarus microrhinos X X X Scarus lepidus X Scarus niger X X X Scarus psittacus X Scarus scaber X Scarus sordidus X X X Scarus tricolor X X Scarus sp. X X X X

Serranidae Cephalopholis X X miniata Cephalopholis X argus Cephalopholis X X X sexmaculatus Cephalopholis X X urodeta Cephalopholis X X boenak Cephalopholis sp. X Diploprion X bifasciatum Epinephelus X X fasciatus Epinephelus mera X X Epinephelus sp. X X Plectropomus X X leopardus Pseudanthias X X X huchtii Pseudanthias tuka X X Pseudanthias X ventralis Variola louti X

Siganidae Siganus X atripectoralis Siganus X X X canaliculatus Siganus corralinus X X

Alcala et al.: Biodiversity of Southern Philippine Seas 53

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Siganidae Siganus guttatus X Siganus X X punctatissimus Siganus spinus X X X Siganus puellus X X Siganus vulpinus X X

TOTAL 14 112 69 60 35 46 30

OTHERS SPECIES Balistidae Balistoides X X conspicillum Balistapus X X X X undulatus Balistapus sp. X Melichthys vidua X X Sufflamen bursa X X X Sufflamen X chrysoptera Sufflamen frenatus X Pseudobalistes X X flavimarginatus

Ostraciidae Ostracion cubicus X X X Ostracion meleagris X X Ostracion sp. X X

Monacanthidae Monacanthus X longirostris Unidentified X X monocanthid

Centriscidae Aeoliscus strigatus X X X X X Aeoliscus chinensis X

54 The Philippine Scientist, Volume 45 (2008)

Appendix 1. continued.

FISH INDICATOR Paril- Bongo Sarang- Davao Malalag FAMILIES SPECIES Sangay Is. ani Bay Gulf * Bay

Tetraodontidae Canthigaster X amboinensis Canthigaster X coronata Canthigaster papua X X Canthigaster sp. X X X Canthigaster X X solandri Canthigaster X X X valentinii Arothron X X nigropunctatus

Microdesmidae Nemateleotris X magnifica

Pinguipedidae Parapercis X X X cylindrica Parapercis X clathrata

Callionymidae Ptereleotris evides X X

Scorpaenidae Pterois volitans X X X Pterois antennata X Pterois radiata X Scoraenopsis sp. X

Synodontidae Saurida gracilis X X X Synodus sp. X X X

Plotosidae Plotosus lineatus X TOTAL 11 33 19 17 6 15 9

Alcala et al.: Biodiversity of Southern Philippine Seas 55

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About the Authors Angel C. Alcala is the principal Filipino scientist in a research program on land vertebrates and marine biodiversity regarded as an outstanding contribution to Philippine biological sciences. The studies deal with ecology, taxonomy, and conservation biology based in Silliman University, Dumaguete City, spanning 1955 through the present. Alcala’s fieldwork from 1954 to 1999 resulted in the addition of 50 new species of amphibians and reptiles, with comprehensive studies on these Philippine species and minor contributions on birds and mammals. Alcala also pioneered the use of the concept of no-take marine reserves to conserve marine biodiversity in 1974 in collaboration with local communities and government units. He has established a dozen marine reserves in the central Philippines, some of them highly successful in preserving marine biodiversity, promoting marine biological and oceanographic research, and encouraging environment-friendly, tourism-related activities that have improved incomes of local communities. Presently a Professor Emeritus of Biological Sciences and the Director of the Silliman University– Angelo King Center for Research and Environmental Management (SUAKCREM), Dr. Alcala is concurrently the Director of the Commission on Higher Education Zonal Research Center at Silliman University.

Jose A. Ingles is a senior fisheries specialist with extensive experience in fisheries stock assessment and coastal resource assessment studies in major fishing grounds throughout the Philippines. Equipped with academic degrees in zoology, marine biology, and natural science and special training in tropical fisheries resource assessment, he has carried out research activities in the fields of fisheries resource assessments, coastal resource management, and biology of commercially important invertebrates, particularly crabs. As a professional biologist, Ingles served at the Institute of Marine Fisheries and Oceanology of the University of the Philippines in the Visayas (UPV) where he became Full Professor in 2000. In 2002, he joined WWF Philippines to lead the Ecoregion Conservation Program of the Sulu Sulawesi Marine Ecoregion Program. Since 2007, he became the Tuna Strategy Leader of the Coral Triangle Network Initiative of WWF, working with the private sector and utilizing markets and trade to put tuna in the coral triangle countries on its path to sustainability.

Abner A. Bucol holds a degree in Biology and has worked with various terrestrial and marine conservation projects, serving as field and research assistant. He is presently a researcher at the SUAKCREM, and co-author of an upcoming book Directory of Marine Reserves in the Visayas with Dr. Angel C. Alcala and P. Nillos-Kleiven.