Biodiversity of Marine Zooplankton in Southeast Asia (Project-3: Plankton Group)

Chapter 5

Biodiversity of marine zooplankton in Southeast Asia (Project-3: Plankton Group)

Shuhei Nishida and Jun Nishikawa

Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa 277-8564, Japan

Introduction Fleminger 1986). A large body of knowledge has accu- The ocean occupies more than 95% of the mulated on the high species diversity of volume of biosphere on Earth. There is a marine fauna in this region. To pick up a wealth of diversity in ocean life, but we few: there are more than 550 species of know only a small portion of it. Among pelagic copepods known in this small re- others, zooplankton are distributed in any gion, accounting for one fourth of those pelagic habitats in the sea, from coasts to known in the world; the MUSORSTOM offshore waters, and from the sea surface Expedition, which aimed at re-discovering to the abyssal depths. Many of them are the primitive decapods “Neoglyhphaea”, known to play important roles in marine resulted in records of >600 species of ecosystems, including those in the food macrobenthos and demersal fishes as a chain and matter transfer, but there are also biproduct, including discovery of more many species whose distribution and ecol- than 80 new species from the very narrow ogy are mostly unknown. shelf in the northeastern Sulu Sea (e.g. Southeast Asia is known as the center Forest 1989); more recently, there was also of marine biodiversity in the world, and the famous discovery of the coelacanth this is referable to several unique settings Latimeria menadoensis from near Manado, of this region. First, the area has the Sulawesi in 1998 (Pouyaud et al. 1999). Tethyan origin, which dates back to ca. 200 All these indicate the ancient nature of the million years ago. It also has complex geo- fauna, the extremely high species diver- logic history, including eustatic sea-level sity in this area, and potential diversity of changes during the glacial- and inter-gla- species still waiting for our investigation. cial periods, and frequent continental fu- However, the area has also been iden- sion and fission events through its geologic tified as a serious hotspot of biodiversity history. These resulted in the presence of crisis owing to various human activities, many island chains and marginal seas, such as: eutrophication, pollution by haz- some of which have semi-enclosed deep ardous chemicals, destruction of habitats basins, such as Sulu and Celebes Seas (e.g. such as coral reefs, mangrove forests, and

S. Nishida, M. D. Fortes and N. Miyazaki, eds. Coastal Marine Science in Southeast Asia —Synthesis Report of the Core University Program of the Japan Society for the Promotion of Science: Coastal Marine Science (2001–2010), pp. 59–71. © by TERRAPUB 2011. 60 S. NISHIDA AND J. NISHIKAWA

Table 1. List of members of the Plankton Group.

Country Name Affiliation Indonesia Mulyadi Research Center for Biology, Indonesian Institute of Sciences Indonesia Inneke FM Rumengan Sam Raturangi University Japan Susumu Ohtsuka Hiroshima University Japan Nozomu Iwasaki Kochi University Japan Tomohiko Kikuchi Yokohama National University Japan Shozo Sawamoto Tokai University Japan Hideo Sekiguchi Mie University Japan Shuhei Nishida The University of Tokyo Japan Jun Nishikawa The University of Tokyo Japan Makoto Terazaki The University of Tokyo Japan Tatsuki Toda Soka University Malaysia BH Ross Othman Universiti Kebangsaan Malaysia Malaysia Fatimah Md Yusoff Universiti Putra Malaysia Philippines Wilfredo L Campos University of the Philippines Visayas Philippines Lourdes V Castillo* University of the Philippines Los Baños Philippines Ephrime B Metillo Mindanao State University Thailand Khwanruan Srinui (Pinkaew) Burapha University Thailand Ajcharaporn Piunsumboon Chulalongkorn University Thailand Suree Satapoomin Phuket Marine Biological Center Vietnam Nguyen Cho Institute of Oceanography, Nha Trang Vietnam Nguyen Thi Thu Institute of Marine Environment and Resources

*Deceased

seagrass beds, and overfishing. laborating countries. It was agreed that Under this circumstance, we have con- Plankton-Group comprises two core mem- ducted researches into the biodiversity of bers from each Southeast Asian country, zooplankton in Southeast Asia, as one of as a general rule, and Japanese collabora- the field research projects of the Japan tors specializing in major zooplankton Society for the Promotion of Science taxa, resulting in the collaborators as listed (JSPS) on Coastal Marine Science during in Table 1 (see Appendix-1 for details). the years 2001–2010. We have also coop- The objectives of our research were: erated with the Census of Marine establishing past- and present status of Zooplankton (CMarZ), a field project of zooplankton communities; elucidating the Census of Marine Life (CoML). This mechanisms of generation/maintenance of is being done with the multilateral coop- biodiversity; elucidating functional role of eration of Japan and five countries in this biodiversity; and predicting the future of region: Thailand, Malaysia, Indonesia, the marine ecosystems in this region. We Philippines, and Vietnam. have approached the last objective through: utilization of historical sample Research Planning collections; training courses on methods of ecology and identification; fulfilling The research on zooplankton in the present basic knowledge of biodiversity at species/ program was initially planned during the community levels; utilization of genetic “Workshop on the Biodiversity Studies in tools for biodiversity analysis; and estab- the Coastal Waters of the East and South- lishing databases. east Asia” held at Lankawi Island, Octo- The sites for general and/or specific ber 2002, following preparatory commu- field researches are indicated in Fig. 1, in- nication among researchers in the six col- cluding sites for general assessment of Biodiversity of marine zooplankton in Southeast Asia 61

Fig. 1. Research sites of the Plankton Group in the JSPS-CMS Program.

zooplankton abundance and species com- expertise, needs of countries, and funding position, and those for taxonomic and circumstances. This led to our basic strat- faunal studies with a larger geographic egy to put some flexibility in research plan- coverage. There are also sites for trophic- ning in each country, in terms of, e.g., se- structure studies of coral and seagrass lection of research sites and seasons, sam- communities, including zooplankton, and pling gears, and focal taxonomic groups, deep marginal basins such as the Sulu, which appears to have been a good choice Celebes, and South China Seas. for realistic collaboration. As an essential strategic aspect, the core members were encouraged to seek and Discovery of New Species obtain research funds from their domestic sources for practical field research and Particular efforts have been paid to areas analysis, since the support from the present that we call “the hotspots”, where there project has been limited mainly to travel have been few studies due to logistical and/ and meeting expenses. This appears to or technical difficulties. Hence, a compre- have been relatively well done, resulting hensive research has been conducted in in collaboration with various field projects, major biodiversity hotspots such as either domestic or bilateral-type, as re- embayed waters, coastal areas and mar- ferred to in the following sections. It was ginal-seas of Southeast Asia, which have also essential to consider differences very complicated geography and geologic among collaborating countries in research history. This resulted in the discovery of 62 S. NISHIDA AND J. NISHIKAWA

Table 2. List of new species of copepods, amphipods, and isopods described during the JSPS- CMS Program by project members and collaborators. Sampling localities are also shown. “n. gen.” and “n. fam.” in parentheses indicate that the species also represent new genus and new family, respectively.

Copepoda (holoplankton): 30 spp. (16 papers) Macandrewella stygiana Ohtsuka, Nishida & Nakaguchi, 2002; Okinawa Macandrewella omorii Ohtsuka, Nishida & Nakaguchi, 2002; Okinawa Macandrewella serratipes Ohtsuka, Nishida & Nakaguchi, 2002; Okinawa Pontella bonei Mulyadi, 2003; Indonesia Pontella kleini Mulyadi, 2003; Indonesia Pontella vervoorti Mulyadi, 2003; Indonesia Neoscolecithrix japonica Ohtsuka, Boxshall & Fosshagen, 2003; Okinawa Scutogerulus boettgerschnacken Ohtsuka & Boxshall, 2004; Okinawa Pseudodiaptomus sulawesiensis Nishida & Rumengan, 2005; Sulawesi Tortanus vietnamicus Nishida & Cho, 2005; Vietnam Metacalanalis hakuhoae Ohtsuka, Nishida & Machida, 2005; Sulu Sea (n. gen.) Protoparamisophria biforaminis Ohtsuka, Nishida & Machida, 2005; Sulu Sea (n. gen.) Paraugaptiloides mirandipes Ohtsuka, Nishida & Machida, 2005; Sulu Sea Sarsarietellus suluensis Ohtsuka, Nishida & Machida, 2005; Sulu Sea Bradyetes pacificus Ohtsuka, Boxshall & Shimomura, 2005; Nansei Is. Lutamator paradiseus Ohtsuka, Boxshall & Shimomura, 2005; Nansei Is. Paracomantenna goi Ohtsuka, Boxshall & Shimomura, 2005; Nansei Is. Centropages maigo Ohtsuka, Itoh & Mizushima, 2005; Japan Tortanus magnonyx Ohtsuka & Conway, 2005; Seychelles Acartia (Odontacartia) ohtsukai Ueda & Bucklin, 2006; Japan Pseudodiaptomus terazakii Walter, Ohtsuka & Castillo, 2006; Philippine Apocyclops ramkhamhaengi Chullasorn, Kangtia, Pinkaew & Ferrari, 2008; Thailand Kelleria indonesiana Mulyadi, 2009; Indonesia Kelleria javaensis Mulyadi, 2009; Indonesia Halicyclops ariakensis Ueda & Nagai, 2009; Japan Halicyclops continentalis Ueda & Nagai, 2009; Japan Halicyclops uncus Ueda & Nagai, 2009; Japan Three un-described species of Pontellopsis from Indonesia to be published in 2011

Copepoda (meroplankton/parasite): 16 spp. (10 papers) Hemicyclops tanakai Itoh & Nishida, 2002; Japan Hemicyclops javaensis Mulyadi, 2005; Indonesia Hemicyclops minutus Mulyadi, 2005; Indonesia Neomysidion rahotsu Ohtsuka, Boxshall & Harada, 2005; Japan (n. gen.) Umazuracola elongatus Ho, Ohtsuka & Nakadachi, 2006; Japan (n. fam.) Dactylopusioides malleus Shimono, Iwasaki & Kawai, 2007; Japan Maemonstrilla hyottoko Grygier & Ohtsuka, 2008; Okinawa (n. gen.) Maemonstrilla okame Grygier & Ohtsuka, 2008; Okinawa Maemonstrilla polka Grygier & Ohtsuka, 2008; Okinawa Maemonstrilla simplex Grygier & Ohtsuka, 2008; Okinawa Maemonstrilla spinicoxa Grygier & Ohtsuka, 2008; Okinawa Thysanote chalermwati Piasecki, Ohtsuka & Yoshizaki, 2008; Thailand Kensakia aiiroa Harris & Iwasaki, 2009; Malaysia Kensakia shimodensis Harris & Iwasaki, 2009; Japan Thalestris hokkaidoensis Takemori & Iwasaki, 2009; Japan Parenterognathus troglodytes Ohtsuka, Kitazawa & Boxshall, 2010; Japan (n. gen.)

Amphipoda: 4 spp. (3 papers) Talorchestia morinoi Othman & Azman, 2007; Malaysia Listriella longipalma Othman & Morino, 2006; Malaysia Ceradocus mizani Lim, Azman & Othman, 2010; Malaysia Victoriopisa tinggiensis Lim, Azman & Othman, 2010; Malaysia

Isopoda Metaphrixus setouchiensis Shimomura, Ohtsuka & Sakakihara, 2006; Japan Prodajus curviabdominalis Shimomura, Ohtsuka & Naito, 2005; Japan Biodiversity of marine zooplankton in Southeast Asia 63

Fig. 2. The copepod Tortanus vietnamicus, collected from a coral reef area in the middle of Vietnam during a nighttime sampling. It is thought that this species has escaped from conven- tional sampling, since they hide behind corals in the daytime (modified from Nishida and Cho 2005). many species new to science. This was papers during the project. In addition, more more-or-less predicted in the earliest stage than 50 undescribed species are still wait- of the research, since taxonomic knowl- ing for our analysis and description. Many edge in this region had been largely based of these species have been found from spe- on the results from historical expeditions, cific habitats that had been poorly investi- and there were many types of habitats that gated, such as estuaries, benthopelagic had received little attention in previous zones, coral reefs and marginal basins, and researchers. many of them are by no means “rare spe- Through cooperation from members cies”, sometimes comprising major com- and taxonomy experts who collaborated ponents of zooplankton. with the project through our taxonomic As an example, Tortanus (Atortus) network, 29 planktonic copepods and 16 vietnamicus is a copepod discovered from mero-planktonic or non-planktonic a coral reef area in the middle of Vietnam copepods, 4 amphipods, and 2 isopods (Fig. 2; Nishida and Cho 2005). They mea- have been described as new to science (Ta- sure ca. 2 mm in total lengths, and are rela- ble 2, see Appendix-2 for references). In tively large in size for copepods. They addition, 37 species of mysids have been were collected by towing a small net from described as new from Southeast Asia and a pier at night. The copepods of this group, Japanese waters by experts collaborating from the subgenus Atortus, are known to with the present project and CMarZ, both inhabit clear water and close to bottom from new field sampling and examination substrates or structures, such as corals, in of sample collections from previous re- the daytime, and emerge up in the water search cruises. Accordingly, a total of ca. column at night. So, it is very important to 90 new species have been described in 51 know the ecology and behavior of diverse 64 S. NISHIDA AND J. NISHIKAWA groups of zooplankton for a full coverage nomic literature on mysids, one of the most of the fauna. A review of the geographic species-rich groups of zooplankton in distribution of this group indicated pres- Southeast Asia, have been fully catalogued ence of more than 10 species in the Indo- (Sawamoto and Fukuoka 2005) with a to- Pacific Region (Nishida and Cho 2005). tal of 191 species reported from this re- They show a highly allopatric pattern of gion. As a matter of particular attention, geographic distribution, suggesting an integrative, multidisciplinary research speciation through isolation of populations on coral reef ecosystems has been con- that might have been enhanced by the ducted in cooperation with the bilateral eustatic sea level changes during the gla- project between JSPS and VCC (Vice cial-interglacial periods, which may have Counselor’s Committee), Malaysia. This resulted in the repeated emergence of both was the first comprehensive research on land and deep-ocean barriers. Discovery the coral reef systems in Malaysia, encom- of many more species is expected through passing islands and coasts in both eastern finer geographic coverage of sampling. and western sides of Peninsular Malaysia, These copepods would also be a good resulting in a number of papers, e.g., the model of allopatric speciation in coastal stable-isotope study on food-web structure areas (see, e.g. Fleminger 1986). (e.g. Iwasaki et al. 2004), the community structure and health condition of coral Coastal Habitats reefs (Toda et al. 2007), abundance, composition and spatio-temporal variability of The coastal waters in Southeast Asia are zooplankton (e.g. Nakajima et al. 2009a), characterized by the presence of highly and potential importance of coral mucus diverse habitats such as coral reefs, man- and dissolved organic matter (e.g. grove forests, seagrass beds, and sandy Nakajima et al. 2009b). beaches. To obtain basic information on the current status of zooplankton communities, Marginal Basins: their abundance and composition were Sulu, Celebes and South China Seas studied in these representative habitats in the member countries (Fig. 1). These in- Comprising another set of habitats in clude the coastal waters in Vietnam (e.g. Southeast Asia where research had been Thu 2005, Cho and Trinh 2006, 2008), the wanting, we investigated the Sulu and Straits of Malacca (e.g. Rezai et al. 2005, Celebes Seas, which have highly contrast- 2009, Yoshida et al. 2006), the Gulf of ing geographic features. Both basins are Thailand (e.g. Pinkaew 2003, Srinui 2007), fairly deep with depths of more than 5000 the Philippine waters (e.g. copepods, fish m; the Sulu Sea is semi-enclosed with sur- larvae, and chaetognaths: Noblezada et al. rounding sills less than 420 m deep, mostly 2004, Campos and Santillan 2005, shallower than 200 m, hence the water Noblezada and Campos 2008), and the In- exchange with outside is mostly limited to donesian waters (e.g. calanoid copepods: the epipelagic zone, while the Celebes Sea Mulyadi 2004, 2006). These data have is less enclosed and with more typical been assessed for quality by expert mem- open-oceanic conditions. The most strik- bers and incorporated into the database of ing oceanographic feature in the Sulu Sea the project (CMarZ-Asia Database, Fig. 4) is its highly homogenous water structure for integration in the assessment of the in meso- and bathypelagic zones, with high current status of zooplankton biodiversity. temperature of ca. 10°C from ca. 600 m Although the inventory of zooplankton through to the sea bottom of ca. 5000 m. species are still in preparation, the taxo- Similar conditions of homogenous, high- Biodiversity of marine zooplankton in Southeast Asia 65 temperature deep water have also been presence of species endemic to the Sulu known in the Mediterranean and the Red Sea, inviting further research into the sur- Sea (e.g. Scotto di Carlo et al. 1984). We rounding waters. investigated these seas during the two In summary, the zooplankton diversity cruises of the R/V Hakuho Maru, and com- in these marginal seas are characterized by: pared the species diversity and community (1) high species richness in the Celebes structure of meso-zooplankton between Sea; (2) reduced species richness in the them, using a MOCNESS-1 as a main sam- Sulu Sea; and (3) different community pling device (Johnson et al. 2006, structure in the deep water between the Nishikawa et al. 2007, Matsuura et al. seas. We hypothesize that semi-enclosed 2010, Machida and Nishida 2010). marginal basins are other sites of Contrary to our expectation, there were speciation; the stable environmental gra- no significant differences between the ver- dients in the mesopelagic layer in the tical patterns either in the total zooplankton Celebes Sea may be an important factor abundance and biomass and in composi- for the observed high species richness; the tion at higher taxonomic levels, such as semi-enclosed, warm, homogenous deep copepods, chaetognaths, and cnidarians. water in the Sulu Sea might have elimi- Focusing on copepods, the most dominant nated many species, allowed endemic spe- group of zooplankton, the calanoids domi- cies to evolve, and fewer species occupied nated in both seas, which is a general fea- broader niches as compared to the Celebes ture in pelagic communities, and again Sea. These views will give insights into our there was no significant difference in the understanding of the mechanisms of order-level community structure between speciation and species co-existence in the the seas. However, analyses at the fami- pelagic habitats. lies/species level revealed totally different features (Nishikawa et al. 2007, Nishikawa Jellyfish Fisheries and Jellyfish Fauna unpublished data). First, a total of 359 spe- in Southeast Asia cies were identified from the seas. This accounts for >15% of all known pelagic Jellyfish are one of the rare marine copepods, indicating fairly high species zooplankton that have been commercially richness in this narrow area. Second, com- exploited by humans for food. According pared to the 314 species from the Celebes to the FAO statistics, global jellyfish catch Sea, only 217 species were found from the increased from 1970 to 2000, and it Sulu Sea, accounting for 2/3 of the former. reached 3–5 × 105 Mt after 2000. At least The vertical patterns of species richness 8 species of jellyfishes belonging to the clearly indicate that the reduction in the order Rhizostomeae, class Scyphozoa, are Sulu Sea is due to those in the mesopelagic known to be harvested in Southeast Asia. zone. An analysis of the community struc- However, detailed information, such as ture at the species level also indicated target species, collection and processing marked differences in the mesopelagic methods, and the derived income of fish- zone between the two seas as compared ermen and the processing company, is not with the epipelagic zone. It is also noted well known in most of the fishing grounds. that the Sulu Sea is another source of spe- Moreover, biological and ecological as- cies discovery. So far a total of 10 new or pects of those large jellyfish are rarely undescribed species have been found from studied in spite of their quantitative im- the mesopelagic or benthopelagic zones portance in the local coastal marine eco- only of the Sulu Sea (Ohtsuka et al. 2005, systems. Nishikawa, unpublished data), suggesting Since 2005, we have started the inves- 66 S. NISHIDA AND J. NISHIKAWA

THAILAND

A B

Fig. 3. A: Locations of the studied area for Jellyfish fisheries in Southeast Asia: Thanh Hoa in Vietnam, Bagan Datoh in Malaysia, and Kebumen in Indonesia, Ang Sila and Sri Racha in Thai- land (modified from Nishikawa et al. 2008). B: Fishing boat full of jellyfish; inset, targeted species Rhopilema hispidum (modified from Nishikawa et al. 2007). tigations on the jellyfish fisheries (JF) at were identified. This species number is several fishery grounds in Southeast Asian more than two times higher than those pre- countries, such as Vietnam, Indonesia, viously known in Vietnam (9 species). Malaysia, and Thailand, with the coopera- In Central Java, Indonesia, main fish- tion of local fishermen and fishery office ing season of jellyfish is from August to staff (Fig. 3). Information was gathered November. Main target species is from interview (with the owner of a jelly- Crambionella sp. that appears to be new fish processing factory (JPF) and fisher- to science. In Malaysia and unlike in most men), sampling animals and other ecosys- of the fishery grounds, the JF is carried out tem constituents, and through reports of all year round at the Perak River estuary fishery statistics. Here we outline the re- in Bagan Datoh, Malaysia. The fishermen sults of our JF research, parts of which set their fishing nets at the beginning of have been published in Nishikawa et al. both low and high tides, usually once or (2008, 2009). twice a day. By utilizing the tidal current In northern Vietnam, the harvesting that transports jellyfish into the nets, they season begins in April and ends in May. catch the jellyfish without towing them. Two species, Rhopilema hispidum and R. The main harvested species is Acromitus esculentum are confirmed as commercially hardenbergi, which is rarely collected in exploited, with the former species being other areas and its biology is little known. caught in much higher abundance than the Interestingly, Acromitus occurs abundantly latter (Fig. 3B). Cyanea, Chrysaora, only in this river, not in neighboring riv- Sanderia, and Aequorea were also caught, ers, and it appears to prefer brackish wa- but not used for processing. The number ter environments. To understand the fac- of Rhopilema jellyfish collected by fish- tors controlling its mass occurrence only ermen is estimated at 800,000–1,200,000 in the Perak River, research on its popula- individuals per fishery season, suggesting tion dynamics, food habits, and trophic that the fishery can have an impact on jel- structure is now ongoing. lyfish populations in the area. In Vietnam, Jellyfish fishery is also active in the 19 species belonging to 12 genera, 7 fami- eastern Gulf of Thailand. High season for lies and 3 orders of the class Scyphozoa the fishery corresponds to the SW Biodiversity of marine zooplankton in Southeast Asia 67 monsoon season, which probably transport or accumulate jellyfish to the eastern coastal area of the country. The gears used

)

1 for catching jellyfish are dip-nets and − hooks. The main harvested species is Rhopilema hispidum.

(USD kg Comparison of some aspects of the JF in five sites in Southeast Asia is shown in Table 3. It is interesting that the selling price of processed jellyfish is very similar between the fishery sites, 1.1–1.4 USD, although the price of commodities in gen-

eral are different between the countries. Hypochlorite unknown

processing Selling price to dealer* We also investigated the symbionts on jellyfish (Ohtsuka et al. 2009).

(Soda) 1.1 Scyphozoan jellyfishes harbored a wide Soda 1.2 variety of invertebrates and fishes. Juve-

Alum 1.4 niles of benthic organisms such as crabs Alum 1.4 and ophiuroids appear to be hitchhikers for

Chemicals used for

Salt,

Salt, Alum,

Salt,

Salt, Alum, dispersal, while juvenile fish utilize jellyfish as refugia against visual predators.

Since edible jellyfish are associated with (rare) many kinds of symbionts, the JF possibly

(main), hinder recruitment of symbionts. (rare),

(main),

(?) (rare) Anthropogenic Pollutants in Coastal-

(rare)

Lobonemoides and Deep-Sea Ecosystems sp. Salt, Alum, Calcium

or To assess the present status of the impact of anthropogenic pollutants on ecosystems,

Target species

Rhopilema hispidum R. esculentum Acromitus hardenbergi Rhopilema esculentum Lobonema smithii Rhopilema hispidum Crambionella Rhopilema hispidum we investigated the coastal waters and Lobonema marginal seas of Southeast Asia and the equatorial Pacific in collaboration with a project supported by the JSPS Grant-in-aid

December for Scientific Research (2004-06). The lev- season

May

August

−

− els of pollutants were analyzed for vari- Comparison of jellyfish in Southeast methods fisheries in three sites and processing ous ecosystem components, including

Fishing

April

All year

All year August− June pelagic- and benthic organisms, marine

Table 3. Table snow, and bottom sediments with special Asia. reference to the ecological properties of the Sila organisms, such as their vertical distribu- tions and trophic levels. Datoh Analysis of organotin compounds,

Kukup organochlorines and polybrominated Sri Racha, Ang diphenyl ethers in the Sulu Sea revealed, for the first time, that these compounds are accumulated in the deep-sea animals in the

Country Area

Vietnam Than Hoa

Malaysia Bagan

Malaysia Indonesia Kebumen area, while their levels are lower than in Thailand

*Most popular price of the most popular products, i.e. swimming bell of most popular species. Currency conversions are 1 USD = 3.47 RM, 17800 VND and 33.3 are popular species. Currency conversions i.e. swimming bell of most popular price of the most popular products, *Most THB, respectively. 68 S. NISHIDA AND J. NISHIKAWA the other, more northern areas of the west- phological taxonomy of copepods and ern Pacific (Ramu et al. 2006). An analy- chaetognaths by using molecular markers sis of trace elements (TE) and stable iso- (Machida and Nishida 2010, Miyamoto et tope ratios of micronekton and fish in the al. 2010). Of particular importance in the Sulu Sea and the adjacent Celebes and ecosystem functioning in the Asian Region Philippine Seas indicated high concentra- has been the identification of Calanus spe- tions of Zn, Cu and Ag in non-migrant fish cies by molecular markers (Nonomura et in deep-water, in contrast to high Rb lev- al. 2008), as summarized below. els in fish which migrate up to the The copepods of the genus Calanus are epipelagic zone, probably resulting from among the most important animals both in differences in background levels of these abundance and biomass in zooplankton TEs in each water environment or func- communities and play important roles in tion of adaptation to deep-water by migrant marine food chains and matter cycling. In and non-migrant species. Arsenic level in the East Asian waters including the coastal fish in the Sulu Sea was positively corre- waters of China and Japan, three species lated with δ15N indicating are distributed: C. sinicus, C. pacificus, biomagnification of the element (Asante and C. jashnovi. They are very similar in et al. 2010). shape, and identification of younger stages In an attempt to obtain basic informa- of these species is almost impossible us- tion necessary to apply zooplankton as in- ing morphology alone. For a better under- dicators of impact of anthropogenic pol- standing of their life history, we applied lutants, a series of experiments was con- molecular markers to identify these ducted in collaboration with the Pollution younger stages. By using three genetic re- Group. It was indicated that the copepod gions as markers, we were able to distin- Apocyclops sp. from Sulawesi, Indonesia, guish the adults and immature copepodids is highly sensitive to acute toxicity of of these species. As a result, it was revealed tributyltin, suggesting its potential useful- that the smaller and larger fifth copepodid ness in environmental assessment stages (CVs) of Calanus that are abundant (Rumengan et al. 2009). in the mesopelagic layer of Sagami Bay correspond to C. sinicus and C. jashnovi, Use of Genetic Markers in respectively. The CVs of C. sinicus showed Biodiversity Research a bimodal distribution, and the deep population was very abundant, which is com- Genes, as well as morphology, provide parable to its epipelagic population. This important information in understanding the and other life-history analyses with wider biodiversity of zooplankton. In addition to seasonal and geographic coverage indi- the analyses of the relationships between cated that the CV of C. sinicus is a species and infra-specific genetic struc- diapausing stage and very widely distrib- ture, genetic information is used in practi- uted in the mesopelagic waters as south as cal identification of species, such as those the continental slope in the East China Sea in immature and/or damaged specimens. during the seasons when the epipelagic In the present project, research was water is too hot for their survival. conducted on the genetic aspects of zooplankton biodiversity. We contributed CMarZ-Asia Database barcode data of ca. 120 species of copepods and chaetognaths from the Asian Finally we introduce CMarZ-Asia Data- Region. There have also been much ad- base (http://www.cmarz-asia.org/db/ vancements in the re-evaluation of mor- index.html), which is a database estab- Biodiversity of marine zooplankton in Southeast Asia 69

Fig. 4. An example of the species search using the CMarZ-Asia Database (http://www.cmarz- asia.org/db/index.html), a comprehensive database on zooplankton information focusing on the Asian Region, containing a search system from species names and sea areas to distribution, sampling data, taxonomic illustrations, images, literature, and gene sequences. It also contains a search system of gene-sequence database (BLAST) to identify species from sequenced data of unidentified specimens.

lished during the present project in col- Conclusion laboration with the Census of Marine Zooplankton (Fig. 4). This includes data The present project has considerably in- sets of sample collection and species increased our knowledge on the status of formation, including taxonomic, distribu- zooplankton biodiversity in East and tional, and gene sequence (barcode) infor- Southeast Asia. However, much still re- mation, photographic images and taxo- main to be addressed. The continuous dis- nomic illustrations for species identifica- covery of many new species indicates high tion. The ecological data (distribution, potential biodiversity of the region, ne- abundance, biomass, diversity, etc.) col- cessitating continued research wherein lected/analyzed from different areas and/ communication and collaboration with or zooplankton-groups by the project taxonomic experts are essential, including members have been uploaded to this data- education of experts in the collaborating base with the metadata for the sample col- countries themselves. On the other hand, lection (dates, gears, depths, analysts, en- the present research indicates that South- vironmental data, etc.). east Asian water represents excellent habi- 70 S. NISHIDA AND J. NISHIKAWA tats in elucidating the mechanisms gener- Acknowledgements ating and maintaining species diversity in the pelagic realm. This will invite further We thank the Japan Society for the Promotion of research on pelagic biodiversity through Science (JSPS) for supporting the Multilateral Core integrated morphological, genetic, and University Program: Coastal Marine Science. Thanks are also due to all members of the Plankton Group biogeographic studies. As for evaluation for their collaboration throughout the project. Spe- of the present status and future prediction cial thanks are due to staff members and students of of ecosystems, quantitative information on collaborating universities and institutes for their variability of zooplankton communities in great help in the field and laboratory. On behalf of space and time is still very limited. Com- the Plankton-Group members, we dedicate this report to the memory of our good friend and colleague bination of data rescue and mining, use of Lourdes V. Castillo, who died unexpectedly in April historical samples, and expanding database 2008. should be an inexpensive, promising strat- egy.

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