Biodiversity of Anguilliform Leptocephali in the Central Indonesian Seas

BULLETIN OF MARINE SCIENCE, 77(2): 209–223, 2005

BIODIVERSITY OF ANGUILLIFORM LEPTOCEPHALI IN THE CENTRAL INDONESIAN SEAS

Sam Wouthuyzen, Michael J. Miller, Jun Aoyama, Gen Minagawa, H. Yulia Sugeha, Sasanti R. Suharti, Tadashi Inagaki, and Katsumi Tsukamoto

ABSTRACT A sampling survey for leptocephali around Sulawesi Island in the central Indo- nesian Seas region during May 2001 collected more than 136 species of 11 families of the order Anguilliformes at 25 stations. This high biodiversity of eel species and the wide range of sizes of leptocephali of all families indicated that many species had been spawning during recent months in the region. Leptocephali of the Con- gridae, Muraenidae, Ophichthidae, Chlopsidae, and Nemichthyidae were the most abundant. All families were widely distributed and there was high species richness and diversity in many areas, suggesting that most taxa of eels were widely distributed throughout the Indonesian Seas. The highest species richness was found in the semi-enclosed Tomini Bay of eastern Sulawesi Island where species diversity was also high at some stations. Anguilla celebesensis Kaup had been spawning in To- mini Bay, but marine eels appeared to have been spawning in most areas. The catch rates of leptocephali varied among areas, with the highest catch rates occurring in Makassar Strait or in Tomini Bay. This ﬁrst study of the biodiversity of leptocephali in the central Indonesian Seas suggests that many species live in this part of the Indo-Paciﬁc and that eels may be ecologically important components of these high biodiversity ecosystems.

The Indonesian archipelago has a high biodiversity of marine ﬁshes and corals that is apparently the result of its unique geological and evolutionary history in combi- nation with the wide variety of habitats associated with its many islands (Randall, 1998; Briggs, 1999; Edinger et al., 2000; Hughes et al., 2002; Allen and Adrim, 2003). These islands have a variety of coral reef areas, mangrove habitats, sea grass beds, and sandy or rocky coasts, which are adjacent to the deep-water basins of the region. Therefore, these areas have a large amount of coastal habitat that can be used by shallow water marine eels, or “shelf” eels, and the islands have freshwater habitats that are inhabited by at least ﬁve species of tropical anguillid eels (genus Anguilla), which are catadromous species. All of these islands, excuding those in the Java Sea, are surrounded by deep-water basins, 1000–5000 m deep, which extend close to the islands and provide habitats for “slope eels” that live on the outer continental shelf or slope, or in deep ocean benthic areas. Away from the islands there is open ocean deep-water habitat suitable for “oceanic” eels that live entirely at various depths in the mesopelagic and bathypelagic environment. This diversity of marine habitats in the Indonesian Seas region probably supports a high biodiversity of eels, because a wide range of eels from at least 12 families are known to commonly inhabit these various types of habitats in other locations (Castle, 1984; Böhlke, 1989a; Smith, 1999). Each of the marine eel families can be grouped into one of the three general categories based on the types of habitats used by the majority of their species. The shallow-water habitats are used by many species of shelf eels such as the false morays, congers and garden eels, spaghetti eels, morays,

and snake eels (Chlopsidae, Congridae, Moringuidae, Muraenidae, and Ophichthi- dae, respectively), and as many as 118 species of these families have recently been reported from coral reef habitats in Indonesian waters (Allen and Adrim, 2003). In addition, the outer shelf, slope, and deep benthic areas are used by duckbilled eels and synaphobranchids (Nettastomatidae and Synaphobranchidae), and the open ocean deep pelagic areas are used by the oceanic longneck, snipe, and sawtooth eels of the Derichthyidae, Nemichthyidae, Serrivomeridae, respectively. Despite this wide range of juvenile and adult habitats, eel larvae are found almost exclusively in the upper few hundred meters of the ocean (Castonguay and Mc- Cleave, 1987) and can all be collected together offshore (Miller and McCleave, 1994). Although the juveniles and adults have a variety of eel-like body forms and inhabit an incredibly diverse range of habitats, all eels and other fishes of the superorder Elopomorpha (Albuliformes including the notacanthids, Elopiformes, Anguillifor- mes, Saccopharyngiformes) have a leptocephalus larvae (Nelson, 1994; Inoue et al., 2004), which is one of the most distinctive types of fish larvae because they have an elongate, transparent, and highly laterally compressed body filled with gelatinous material (Castle, 1984; Smith, 1989a). The relatively long duration of the leptocephalus stage, that may last 3–10 mo in some anguillid eels (Arai et al., 2001; Marui et al., 2001), makes surveys of leptocephali an useful method of examining the biodiversity and reproductive ecology of eels in a particular region. This study describes the biodiversity and distribution of leptocephali collected in the central Indonesian Seas and provides new information about the general taxonomic composition and relative abundance of marine eels that were spawning in different areas in the region. The collections were made during May 2001 at 25 stations located around Sulawesi Island in seven areas of the Indonesian Seas (Fig. 1). Sulawesi Island is unique in that it is surrounded on all sides by the deep-water basins of the Indonesian Seas. The Celebes Sea (or Sulawesi Sea) is on the north side of Sulawesi Island, Tomini Bay is on the northeast side of the island, the Molucca (or Maluku) and Banda Seas are to the east, the Flores Sea is to the south, the Java Sea is to the southwest, and Makassar Strait is to the west. A previous paper used the data from this survey to compare the overall species richness, diversity, and abundance of the whole collection of leptocephali to a similar sample of leptocephali collected in the East China Sea (Minagawa et al., 2004). In this paper we describe the regional taxonomic composition, size ranges, species richness and diversity, and catch rates of the various taxa of leptocephali that were collected in each specific area, to show that there is high biodiversity of eels throughout the region around Sulawesi Island, but that there may be differences in the spawning activity of some taxa of eels in the different regions. These data are discussed in relation to the ecology and life history of the high biodiversity of eels found in the region.

MATERIALS AND METHODS

Leptocephali were collected from 13 to 26 May 2001 during a cruise of the R/V BARUNA JAYA VII of the Research Center for Oceanography of the Indonesian Institute of Sciences. Sampling occurred at 25 stations in the waters around Sulawesi Island in areas including the Java Sea, Makassar Strait, Celebes Sea, Molucca Sea, Tomini Bay, Banda Sea, and Flores Sea (Fig. 1). Sampling for leptocephali at each station consisted of two tows of a large pelagic trawl, the Isaacs Kidd Midwater Trawl (IKMT) with a net opening of 8.7 m2 and 0.5 mm mesh size, and a surface tow of a 1 m diameter MTD plankton net. All sampling was done at night WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 211

Figure 1. Map showing the sampling locations during the BJ-01-1 cruise of the Baruna Jaya VII in the Indonesian Seas around Sulawesi Island from 13–26 May 2001. except for two stations in Tomini Bay. At each station a 30 min oblique IKMT tow to a depth of 200 m was made, along with a 60–80 min step IKMT tow, which entailed towing horizontally for 10 min at five depths of around 30, 60, 90, 120, and 150 m. The MTD net was towed horizontally just below the sea surface next to the ship for 10 min. Profiles of temperature and salinity (CTD) were also made at each station to a depth of 500 m. All stations were located in areas with water depths > 1000 m. For regional comparisons, stations (Stn.) were separated into the Java Sea (Stn. 1–2), Makassar Strait (Stn. 3–6), Celebes Sea (Stn. 7–10), Molucca Sea (Stn. 11–12), Tomini Bay (Stn. 13–23), Banda Sea (Stn. 24), and Flores Sea (Stn. 25). Only leptocephali caught in the IKMT tows were used to calculate the catch rate and species diversity values, and the catch rates were based on the amount of water filtered by the net during each tow as indicated by a flowmeter suspended in the center of the mouth of the net. The leptocephali were sorted fresh from the plankton samples, identified using Tabeta and Mochioka (1988), Böhlke (1989b), and Castle (1997) before being preserved in a 10% formalin- seawater solution or in 95% ethanol. Identifications were made to the lowest possible level and separated into different species or types. However, much more research is needed to enable leptocephali to be matched with the many adult species that are known from the western Pa- cific Ocean (e.g., Asano et al., 1984; Myers, 1999; Smith, 1999; Hatooka, 2000), so the species 212 BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 2, 2005

level identities of most of the leptocephali that were collected will not be presented here. The phrase “number of species” will be used loosely even though in some cases the leptocephali of groups such as the family Muraenidae were not satisfactorily separated into individual species due to time constraints and the general diﬃculty in separating the leptocephali of this group (see Smith, 1989b). The species richness in each region and the species diversity of leptocephali at each station was calculated using the number of diﬀerent species or types that could be separated in the samples from the 2 IKMT tows at each station, even if their actual identity (an adult species) was not known.

RESULTS

TAXONOMIC COMPOSITION.—In total, 2575 anguilliform leptocephali of 11 families were collected at 25 stations throughout the study area (Table 1). Leptocephali of the family Congridae (n = 1144) were the most abundant, with the taxa of Ariosoma, Conger, Uroconger, and Congrinae being abundant in some areas. Leptocephali of the Muraenidae (n = 315), Ophichthidae (n = 284), Chlopsidae (n = 265), and Nemichthy- idae (n = 219) were also relatively abundant, and except for the latter family, included many different taxa. The Anguillidae (n = 53), Derichthyidae (n = 12), Moringuidae (n = 62), Nettastomatidae (n = 26), Serrivomeridae (n = 163), and Synaphobranchidae (n = 32) were widespread at lower abundances, but included relatively few taxa and were not collected in some areas. The genera and species of leptocephali that overlap with western North Atlan- tic species (Böhlke, 1989b) and those around Japan (Tabeta and Mochioka, 1988) could be identified using their morphological features, but the anguillid leptocephali had to be identified using molecular genetics. The marine eel species or genera included various cosmopolitan taxa of chlopsids, congrids, derichthyids, moringuids, nemichthyids, and nettastomatids (genera listed in Table 1). Species such as Kaupi- chthys hyoproroides Strömman, Robinsia catherinae Böhlke and Smith, Derichthys serpentinus Gill, Nessorhamphus danae Schmidt, Avocettina infans Günther, and Nemichthys scolopaceous Richardson are present in many areas of the Atlantic and Pacific oceans (Böhlke, 1989a,b; Smith, 1999) and were collected around Sulawesi Is- land. TheAriosoma species 1–8 and Chlopsidae species 1–7 of Tabeta and Mochioka (1988) were also collected. The two taxa listed in Table 1 that are rare or absent in the western North Atlantic are Neenchelys, which has overlapping morphological characteristics with both subfamilies of the Ophichthidae (Castle, 1980; Leiby, 1984, 1989), and Thallassenchelys, which was initially thought to be a chlopsid (Castle and Raju, 1975), but appears to be a separate family based on genetic research (Ober- miller and Pfeiler, 2003). The anguillid leptocephali and one glass eel that were collected included 47 longfin and five shortfin specimens (see Jespersen, 1942; Miller et al., 2002a). The details of the catch data of these leptocephali that were identified to species using the mitochondrial 16S ribosomal RNA gene (see Aoyama et al., 1999) are described else- where (Aoyama et al., 2003), but briefly, there were 38 Anguilla celebesensis, eight Anguilla marmorata Quoy and Gaimard, four Anguilla bicolor Schmidt, one An- guilla borneensis Popta, and one Anguilla interioris Whitley. Most of the anguillid leptocephali were collected in the northern part of the study area, with some being collected in the Java Sea (n = 1), Makassar Strait (n = 5), Celebes Sea (n = 6), Molucca Sea (n = 2), and Tomini Bay (n = 38), but none were collected in the limited amount of sampling in the southern areas of the Flores and Banda Seas. WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 213

Table 1. The number of leptocephali, size range, and the number of species of the various taxa of the families of eels that were collected in the seven areas of the Indonesian Seas around Sulawesi Island in May 2001. The number of species or types of each of the taxa is shown in parentheses.

Java Makassar Celebes Molucca Tomini Banda Flores Total Size range Sea Strait Sea Sea Bay Sea Sea (mm) Anguillidae Anguilla spp. (5) 1 7 4 2 39 53 13–51 Chlopsidae Chlopsis spp. (3) 2 9 2 37 4 2 56 9–55 Kaupichthys spp. (3) 3 20 6 1 45 13 11 99 20–73 Robinsia sp. 1 1 2 4 32–49 Chlopsidae spp. (8) 1 20 5 3 68 6 2 105 17–68 Thallassenchelys sp.* 1 1 53 Congridae Ariosoma spp. (9) 145 298 83 29 77 32 55 719 15–387 Conger spp. (4) 6 36 9 45 3 9 108 14–87 Gnathophis spp. (4) 2 6 5 3 11 3 9 39 19–85 Gorgasia spp. (5) 2 11 8 8 6 1 36 11–53 Heteroconger spp. (3) 2 5 3 5 2 17 10–69 Uroconger sp. 29 52 3 15 1 100 10–143 Congrinae spp. (4) 7 4 8 24 63 7 7 120 10–131 Congridae (4) 1 2 2 5 25–131 Derichthyidae Derichthys sp. 6 2 1 9 20–37 Nessorhamphus sp. 2 1 3 42–48 Moringuidae Moringua spp. (3) 3 6 3 1 47 2 62 11–55 Muraenidae Uropteryginae spp. (> 3) 1 8 2 8 2 1 22 27–56 Muraenidae spp. (> 12) 39 73 27 39 70 23 22 293 8–75 Nemichthyidae Avocettina sp. 19 7 2 2 30 16–166 Nemichthys spp. (2) 37 18 13 60 41 20 189 13–250 Nettastomatidae Nettastoma sp. 1 1 88 Nettenchelys sp. 1 2 1 5 2 11 14–94 Saurenchelys spp. (2) 10 2 1 13 18–94 Nettastomatidae 1 1 37 Ophichthidae Neenchelys spp. (4) 88 39 15 7 20 3 7 179 16–80 Ophichthinae spp. (27) 2 3 6 9 3 23 12–134 Myrophinae spp. (9) 10 33 9 2 17 3 8 82 15–89 Serrivomeridae Serrivomeridae spp. (2) 10 6 144 2 1 163 10–54 Synaphobranchidae Ilyophinae spp. (8) 2 1 13 2 1 19 17–76 Synaphobranchinae spp. (3) 3 1 3 4 2 13 21–74 Total number of specimens 359 710 227 134 821 155 169 2,575 Total number of taxa 35 48 39 19 62 33 37 136 Number of IKMT tows 4 8 8 4 18 2 2 46 *Thallassenchelys is probably not a true member of the Chlopsidae as originally thought, but is included for convenience (see Castle and Raju, 1975; Obermiller and Pfeiler, 2003). 214 BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 2, 2005

Figure 2. Length frequency distributions of eight families of anguilliform leptocephali collected in May 2001 in the Indonesian Seas around Sulawesi Island. SIZE OF LEPTOCEPHALI.—There was a wide range of total lengths of each family collected during the cruise, including relatively small leptocephali (< 15 mm) of most families (Table 1, Fig. 2, 3). Muraenids appeared to be the most abundant small leptocephali, indicating recent spawning activity relatively near the sampling stations, but a wide range of sizes up to their maximum lengths was also collected. Various taxa of leptocephali reach diﬀerent maximum lengths (see Böhlke, 1989b), with taxa such as anguillids, moringuids, and serrivomerids reaching about < 60 mm, and others like Ariosoma and Nemichthys reaching > 200 mm. There were leptocephali close to the typical maximum size of almost all taxa collected around Sulawesi Island (Table 1, Fig. 2, 3). The majority of the anguillid leptocephali collected during this cruise were relatively large in all sampling areas (mostly > 30 mm), except at the series of stations in the southern half of Tomini Bay (Stn. 19–21) where two size classes of A. celebesensis leptocephali were collected, indicating that Tomini Bay was a spawning area of that species. Bimodal length frequency distributions were observed for the Anguillidae and for the shelf eel families Congridae, Chlopsidae, Moringuidae, and Muraenidae. These size ranges, and the wide range of sizes of leptocephali of all families, indicated that spawning had occurred over several months prior to the cruise. WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 215

Figure 3. Length frequency distribution of the leptocephali of two taxa of the family Congridae (Ariosoma and the subfamily Congrinae) and Nemichthyidae (Avocettina and Nemichthys) collected in May 2001 in the Indonesian Seas around Sulawesi Island.

REGIONAL SPECIES RICHNESS AND DIVERSITY.—As many as 136 species of 11 families of eels were collected during the cruise, with five families having more than 10 species. The families Ophichthidae (≤ 40 species), Congridae (~35 species), and Chlopsidae (≤ 16 species) appeared to be the most diverse. However, if more characters were available to distinguish muraenid leptocephali, possibly as many as 20 or more additional species could have been identified. However, the pigment patterns of the different sizes of leptocephali of the same species of families such as the Chlo- psidae and Ophichthidae are not yet documented in the Pacific Ocean region, so these numbers of species could possibly be slight overestimates. There were far fewer taxa of slope and oceanic families, which is typical of these families of eels (Castle, 1984). Most taxa were present in almost all the different areas and there were at least 19–62 species collected in the various areas (Table 1, Fig. 4). Stations 11 and 12 in the Molucca Sea close to the mouth of Tomini Bay had the lowest number of species, due in part to the complete absence of several families such as Nettastomatidae, Synaphobranchidae, Derichthyidae, and Serrivovmeridae, but with a few exceptions, leptocephali of all the major families were present in each sea area. There were more than 20 shelf species collected in each area, with more than 60 collected in Tomini Bay. The Congridae and Ophichthidae consistently showed the highest number of taxa throughout the study area, but muraenids were also common in all areas. The slope and oceanic taxa were also widely distributed with a much lower number of species, but these taxa appeared to be rare or absent at the two stations in the Java and Molucca Seas (Fig. 4). The Shannon-Wiener index of species diversity (H) for the two night tows at each station ranged from 2.3 to 3.3 throughout the study area (Fig. 5). The highest species diversities were at stations in the Java Sea, Makassar Strait, two stations in Tomini Bay and the Flores Sea, and there were moderately high values at some stations in most regions of the study area. The lowest values were at Stn. 1 close to the shelf of the Java Sea where the leptocephali of the three oceanic families were absent, and 216 BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 2, 2005

Figure 4. The minimum number of species leptocephali of shelf, slope, and oceanic species of eels collected in each of the seven Indonesian Seas or areas around Sulawesi Island. The number of stations in each area is in parenthesis. at Stn. 11 in the Molucca Sea where the leptocephali of two oceanic and two slope families were absent. The species diversity was not calculated for the two tows made during the day in Tomini Bay. RELATIVE ABUNDANCE OF LEPTOCEPHALI.—The catch rates of leptocephali were higher for various taxa in areas such as the western and southeastern sides of Su- lawesi Island. Leptocephali of the congrid genus Ariosoma were typically the most abundant throughout the region (Table 1), and they had high catch rates in Makas- sar Strait and the Java Sea (Figs. 6,7). Ophichthids were also more abundant in these two areas and in the Flores Sea than at other stations, and the highest catch rate of nettastomatids also occurred at the Java Sea stations. The two stations in the eastern Java Sea area are surrounded by coral reef areas on all sides (Fig. 7), and these reefs and the associated shallow water or slope habitats should be appropriate habitats for shelf eels such as Ariosoma and ophichthids and the typically deeper water species WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 217

Figure 5. The Shannon-Wiener Species Diversity Index (H´) of the leptocephali collected at each station during the BJ-01-1 cruise in May 2001 in the Indonesian Seas around Sulawesi Island.

of the Nettastomatidae. The other stations with relatively high catch rates were in the Banda and Flores Seas where nemichthyids were most abundant, and shelf taxa such as chlopsids and muraenids were also relatively abundant. The catch rates of most taxa were somewhat lower in the Celebes and Molucca Sea stations and in some parts of Tomini Bay. However, the highest catch rates of serrivomerid leptocephali occurred in Tomini Bay, which even though it is a semi-enclosed bay, is deeper than 1000 m in most areas.

DISCUSSION

Our results indicate that there is a high biodiversity of anguilliform leptocephali in the central Indonesian Seas, and that many eel species with diﬀerent life histories had been spawning there recently. As many as 136 species of eels of 11 anguilliform families had been spawning in the region during the months prior to the cruise, and a new spawning area of A. celebesensis was discovered. These collections around Sulawesi Island showed that there was an especially high species richness of the leptocephali of marine eels such as chlopsids, congrids, muraenids, ophichthids, and synaphobranchids in the region. However, our separation of only 15 diﬀerent types of muraenid leptocephali was likely a considerable underestimate of the number of species that were collected because Allen and Adrim (2003) have reported that there are 61 species of moray eels found in the coral reef habitats of Indonesian waters. Alternatively, we distinguished more species of congrids (35) and ophichthids (40) than the 15 and 25, respectively, that Allen and Adrim (2003) reported from coral reef areas in Indonesia. This is not unexpected though, as many congrid and ophichthid species are found in a much wider range of habitats and depths than just around coral reefs (Böhlke, 1989a). The biodiversity of leptocephali observed in the Indonesian Seas during this study was much higher than has been observed during comparable surveys for leptocephali in other regions. Miller and McCleave (1994) reported the collection of about 50 species of 11 families of anguilliform leptocephali during the winter and spring season 218 BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 2, 2005

Figure 6. Catch rates of each major family of leptocephali of shelf, slope, and oceanic species of eels collected in each of the seven Indonesian Seas or areas around Sulawesi Island.

using the IKMT in offshore regions of the Sargasso Sea in the western North Atlan- tic. This number of species is probably not representative of the number of shelf eels living to the south around the Bahama Islands, however, because many more species have been reported from the region as adults and leptocephali (Böhlke, 1989a,b), and some species such as ophichthids may be more frequently collected close to or over continental shelf areas (Fahay and Obenchain, 1978; Leiby, 1989) than in offshore areas (Miller, 1995). To the southeast near Barbados, Richardson and Cowen (2004) collected at least 68 species of leptocephali. Only 20 species were collected in the eastern Gulf of Mexico in offshore sampling near the edge of the continental shelf with other types of sampling gear (Crabtree et al., 1992). Blache (1977) reported collections of more than 10,000 leptocephali made over about a 10 yr period in the Gulf of Guinea of East Africa, but only about 68 species of leptocephali of seven families appeared to be present in that region. In a survey for leptocephali using the IKMT that sampled across the shelf break along the boundary of the Kuroshio Current and East China Sea to the south of Japan, a similarly low number of at least 45 species of WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 219 , and (left) (right) at each station during thecruise. BJ-01-1 The distribution of coral reef habitats in the Ariosoma leptocephali (family Congridae), all other leptocephali of the family Congridae, Muraenidae, and Ophichthidae Chlopsidae, Moringuidae, Nemichthyidae, and Serrivomeridae using sensingimagerysatellitefromremoteplotted detected by was Thiscoralreefs distribution dots. of lines or black by shown is Island aroundSulawesi study Maps obtainedthe were sensor. SeaWiFS from the ReefBase project (http://www.reefbase.org; see and Stumpf NOAA; NASA et al. 1999). Figure Catch 7. rates of 220 BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 2, 2005

10 families were collected (Miller et al., 2002b). A direct comparison of the species assemblages of leptocephali in the East China Sea and our survey around Sulawesi Island showed that there was a much greater overall species richness and diversity in the Indonesian Seas region, but there was a higher overall catch rate of leptocephali in the East China Sea (Minagawa et al., 2004). This higher catch rate was due to the recent spawning activity by species of Dysomma and Gnathophis of the families Synaphobranchidae and Congridae, respectively, which were both spawning near the shelf break along the edge of the Kuroshio Current (Miller et al., 2002b). The collection of far fewer leptocephali species with the IKMT or other gear during previous surveys than during our study suggests that there may be a much higher biodiversity of eels in the tropical waters of the Indonesian Seas than in most other regions. The wide range of shallow water habitats and coral reefs found around Su- lawesi and nearby islands probably provide suitable habitat for a high diversity of marine eels, which are known to use many different types of marine habitats (Böhl- ke, 1989a). The widespread distribution of many types of leptocephali of shelf eels around Sulawesi Island can be explained simply based on the distribution of coral reef areas in the region. These coral reefs and associated shallow water habitats are typically inhabited by many species of chlopsids, congrids, muraenids, moringuids, and ophichthids, as was found by Allen and Adrim (2003), and these families of eels appear to be widespread in the region based on the larval distributions we observed. Relatively high species diversity was found in many areas around Sulawesi Island and all of these areas have coral reefs in the adjacent shallow water habitats. Some of the highest species diversities of leptocephali were observed at stations in Tomini Bay that were relatively close to the Togian Islands (the large group of islands in Tomini Bay), which have many coral reef areas and an unusually high biodiversity of corals (Wallace, 1999) as well as some endemic species of fishes (Allen and Adrim, 2003). Another factor contributing to the high biodiversity observed during this study is that the leptocephali of eels with different life histories, such as the freshwater eels and open ocean and slope species, were present in the region. All of the areas around Sulawesi Island have deep-water basins that provide habitat for the oceanic species of the Derichthyidae, Nemichthyidae, and Serrivomeridae, and the outer continental shelf and slope areas around the island provide habitat for slope species such as nettastomatids and synaphobranchids, which are found at many different depths (Böhlke, 1989a). In addition to the wide range of leptocephali of marine eels that were collected, the leptocephali of five species of catadromous anguillid eels also were collected (Aoyama et al., 2003). The genus Anguilla may have originated in the area around Sulawesi Island (Aoyama et al., 2001), so this region probably has the highest number of anguillid species, but it is presently unclear if it has a greater diversity of marine eels than other tropical regions such as around New Guinea or in the western South Pacific. The marine eels present around Sulawesi Island appeared to have been spawning in many areas and over several months because a wide size range of most taxa of leptocephali was collected over a broad geographic area. Most marine eels appear to spawn relatively close to their adult habitats (Moyer and Zaiser, 1982; Ferraris, 1985; Miller, 1995; Miller et al., 2002b), as do some species of tropical anguillids (Jespers- en, 1942; Aoyama et al, 2003), even though anguillids that recruit to higher latitudes make much longer spawning migrations (Tsukamoto, 1992; McCleave, 1993; Miller et al., 2002a). Most of the sampling stations during this cruise were not close to the WOUTHUYZEN ET AL.: LEPTOCEPHALI IN THE INDONESIAN SEAS 221

shelf break, which may be one reason why a larger proportion of small leptocephali was not collected. The geographic variation in catch rate during this study suggests that there were some spatial or temporal differences in spawning time or location among the various taxa of eels. Each family appeared to show differing patterns of abundance at the various stations, with species like the serrivomerids and chlopsids being more abundant in Tomini Bay than most other areas, and other taxa such as Ariosoma and ophichthids being the only taxa that were abundant close to the shelf at the south- ernmost station in the Java Sea. The distributions of catch rates and size of these leptocephali in relation to the locations of coral reef areas, tidal currents (Hatayama et al., 1996), and larger scale circulation features in this region (Wyrtki, 1961; Miyama et al., 1995) will be the subject of future studies. Our survey of leptocephali around Sulawesi Island suggests the possibility that a higher biodiversity of marine eels lives and spawns in the central Indonesian Seas than in most other areas of the world. However, this hypothesis needs to be tested using similar surveys for leptocephali in other regions with diverse coral reef and other types of tropical habitats. The collection of so many species during one relatively short survey such as ours also indicates that eels are probably important ecological components of both the marine and freshwater ecosystems of the region. Future studies of leptocephali in different seasons will improve our understanding of the biodiversity, spawning ecology, and recruitment mechanisms of the many species of marine and freshwater eels that inhabit the Indonesian Seas region.

ACKNOWLEGEMENTS

We thank the captain, crew, and technicians of the R/V BARUNA JAYA VII for their help in making this cruise successful. This work was supported in part by Grants-in-Aid numbers 07306022, 07556046, 08041139, 08456094, 10460081, and 11691177 from the Ministry of Education, Science, Sports and Culture, Japan, and by grant Numbers JSPS-RFTF 97L00901 from the “Research for the Future Program” of the Japan Society for the Promotion of Science. K.T. was supported by the Research Foundation “Touwa Shokuhin Shinkoukai” and the Eel Research Foundation “Noborikai”.

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DATE SUBMITTED: 4 January, 2005. DATE ACCEPTED: 15 March, 2005.

ADDRESSES: (S.W.) Research Center for Oceanography, Indonesian Institute of Sciences, Jl. Pa- sir Putih 1, Ancol Timur, Jakarta 11480, Indonesia. (M.J.M., J.A., H.Y.S., T.I., K.T.) Ocean Re- search Institute, Th e University of Tokyo, 1-15-1 Minamidai Nakano, Tokyo, 164-8639, Japan. CORRESPONDING AUTHOR: (M.J.M.) Telephone: 03-5351-6879, Fax: 03-5351-6514, E-mail: .