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RESEARCH ARTICLE Michael J. Miller Sam Wouthuyzen Gen Minagawa Jun Aoyama Katsumi Tsukamoto Distribution and ecology of leptocephali of the congrid eel, Ariosoma scheelei, around Sulawesi Island, Indonesia Received: 25 May 2005 / Accepted: 6 October 2005 / Published online: 11 November 2005 Ó Springer-Verlag 2005 Abstract A survey for leptocephali around Sulawesi Is- land in the central Indonesian Seas during May 2001 found that the leptocephali of the congrid eel, Ariosoma scheelei, were present in all seven areas that were sam- pled. A total of 551 leptocephali (22–166 mm TL) were collected, and A. scheelei was by far the most abundant species of leptocephali collected during the survey. The wide range of sizes in most areas indicated that spawning had occurred during a period of several months in many different areas, although the exact spawning locations were not determined. The larger size classes were more abundant in all areas except in To- mini Bay on the northeast side of Sulawesi Island. The highest catch rates were observed at the eastern edge of the Java Sea and to the north in the Celebes Sea near Makassar Strait. Premetamorphic leptocephali were also collected in surface samples at 11 stations (N=62), but metamorphosing leptocephali (N=86) were only caught in IKMT tows that fished from the surface to about 200 m. Metamorphosing leptocephali were col- lected primarily at two stations in the Java Sea and Makassar Strait where a surface layer of lower-salinity water was detected. Their total lengths (105.3– 153.3 mm) and the largest premetamorphic individuals suggested that this species can reach maximum sizes of about 165 mm before beginning to metamorphose. It is hypothesized that this species may be abundant in the Indonesian Seas region and that it has ecological traits such as large size at recruitment and a small size at reproduction that have made it successful in many regions of the Indo-Pacific. Introduction Ariosoma scheelei is a small marine eel of the family Congridae that appears to be abundant and widespread in the western Pacific region based on the presence of its leptocephali in many areas. The juvenile and adult eels of the genus Ariosoma are all relatively small compared to many other species of the Anguilliformes (Bo¨hlke 1989a), and A. scheelei appears to reach maturity at sizes less than 200 mm (Castle 1963). Their leptocephali have been reported from areas ranging across about 60 de- grees of latitude from south of New Caledonia all the way northward to Japan (Castle 1964; Mochioka et al. 1991). A. scheelei may be widespread in the Indian Ocean (Castle 1963; Castle 1986) and also lives in the Indonesian Seas region based on the presence of their adults (Allen and Adrim 2003) and leptocephali there (Castle 1964; Mochioka et al. 1991). The Indonesian Seas region has many islands with shallow-water coastal areas that provide diverse habitats for marine fishes such as the eels of the genus Ariosoma. This region is generally considered to have the highest biodiversity of marine fishes in the world (Randall 1998; Allen and Adrim 2003), but relatively little is known about the wide variety of species of marine eels that live there. Many species of eels that are associated with coral reefs have been reported in Indonesian waters (Allen and Adrim 2003), and a recent survey for leptocephali around Sulawesi Island in the central Indonesian Seas confirmed that there is a very high biodiversity of all different types of marine and freshwater eels in the re- gion (Aoyama et al. 2003; Minagawa et al. 2004; Wou- thuyzen et al. 2005). This survey collected more than 136 species of leptocephali, but the leptocephali of the con- grid genus Ariosoma were considerably more abundant than any other taxa of leptocephali (Wouthuyzen et al. Communicated by S. Nishida, Tokyo M. J. Miller (&) G. Minagawa J. Aoyama K. Tsukamoto Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, 164-8639 Tokyo, Japan E-mail: [email protected] Tel.: +3-5351-6879 Fax: +3-5351-6514 S. Wouthuyzen Research Center for Oceanography, Indonesian Institute of Sciences, Jl. Pasir Putih 1, Ancol Timur, 11480 Jakarta, Indonesia Marine Biology (2006) 148: 1101–1111 DOI 10.1007/s00227-005-0144-9

Distribution and ecology of leptocephali of the congrid eel, Ariosoma scheelei , around Sulawesi Island, Indonesia

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RESEARCH ARTICLE

Michael J. Miller Æ Sam Wouthuyzen Æ Gen Minagawa

Jun Aoyama Æ Katsumi Tsukamoto

Distribution and ecology of leptocephali of the congrid eel, Ariosomascheelei, around Sulawesi Island, Indonesia

Received: 25 May 2005 / Accepted: 6 October 2005 / Published online: 11 November 2005� Springer-Verlag 2005

Abstract A survey for leptocephali around Sulawesi Is-land in the central Indonesian Seas during May 2001found that the leptocephali of the congrid eel, Ariosomascheelei, were present in all seven areas that were sam-pled. A total of 551 leptocephali (22–166 mm TL) werecollected, and A. scheelei was by far the most abundantspecies of leptocephali collected during the survey. Thewide range of sizes in most areas indicated thatspawning had occurred during a period of severalmonths in many different areas, although the exactspawning locations were not determined. The larger sizeclasses were more abundant in all areas except in To-mini Bay on the northeast side of Sulawesi Island. Thehighest catch rates were observed at the eastern edge ofthe Java Sea and to the north in the Celebes Sea nearMakassar Strait. Premetamorphic leptocephali werealso collected in surface samples at 11 stations (N=62),but metamorphosing leptocephali (N=86) were onlycaught in IKMT tows that fished from the surface toabout 200 m. Metamorphosing leptocephali were col-lected primarily at two stations in the Java Sea andMakassar Strait where a surface layer of lower-salinitywater was detected. Their total lengths (105.3–153.3 mm) and the largest premetamorphic individualssuggested that this species can reach maximum sizes ofabout 165 mm before beginning to metamorphose. It ishypothesized that this species may be abundant in theIndonesian Seas region and that it has ecological traitssuch as large size at recruitment and a small size at

reproduction that have made it successful in manyregions of the Indo-Pacific.

Introduction

Ariosoma scheelei is a small marine eel of the familyCongridae that appears to be abundant and widespreadin the western Pacific region based on the presence of itsleptocephali in many areas. The juvenile and adult eelsof the genus Ariosoma are all relatively small comparedto many other species of the Anguilliformes (Bohlke1989a), and A. scheelei appears to reach maturity at sizesless than 200 mm (Castle 1963). Their leptocephali havebeen reported from areas ranging across about 60 de-grees of latitude from south of New Caledonia all theway northward to Japan (Castle 1964; Mochioka et al.1991). A. scheelei may be widespread in the IndianOcean (Castle 1963; Castle 1986) and also lives in theIndonesian Seas region based on the presence of theiradults (Allen and Adrim 2003) and leptocephali there(Castle 1964; Mochioka et al. 1991).

The Indonesian Seas region has many islands withshallow-water coastal areas that provide diverse habitatsfor marine fishes such as the eels of the genus Ariosoma.This region is generally considered to have the highestbiodiversity of marine fishes in the world (Randall 1998;Allen and Adrim 2003), but relatively little is knownabout the wide variety of species of marine eels that livethere. Many species of eels that are associated with coralreefs have been reported in Indonesian waters (Allen andAdrim 2003), and a recent survey for leptocephaliaround Sulawesi Island in the central Indonesian Seasconfirmed that there is a very high biodiversity of alldifferent types of marine and freshwater eels in the re-gion (Aoyama et al. 2003; Minagawa et al. 2004; Wou-thuyzen et al. 2005). This survey collected more than 136species of leptocephali, but the leptocephali of the con-grid genus Ariosoma were considerably more abundantthan any other taxa of leptocephali (Wouthuyzen et al.

Communicated by S. Nishida, Tokyo

M. J. Miller (&) Æ G. Minagawa Æ J. Aoyama Æ K. TsukamotoOcean Research Institute, The University of Tokyo,1-15-1 Minamidai, Nakano, 164-8639 Tokyo, JapanE-mail: [email protected].: +3-5351-6879Fax: +3-5351-6514

S. WouthuyzenResearch Center for Oceanography,Indonesian Institute of Sciences, Jl. Pasir Putih 1,Ancol Timur, 11480 Jakarta, Indonesia

Marine Biology (2006) 148: 1101–1111DOI 10.1007/s00227-005-0144-9

2005). However, A. scheelei, accounted for most of theabundance of Ariosoma leptocephali, because it was byfar the most frequently collected species during thesurvey.

The markedly greater abundance of the leptocephaliof A. scheelei is similar to observations about theabundance of the leptocephali of Ariosoma balearicum inthe Sargasso Sea region of the western North Atlantic,which have been found to be consistently one of themost abundant species among the families of eels whoseadults live in shallow water (Smith 1989a, b; Miller andMcCleave 1994; Miller 1995, 2002). However, little isknown about the ecology of these small eels, and whytheir larvae are so much more abundant than most othertaxa. It is also unclear where these eels spawn in relationto their adult habitats and whether they have distinctseasonal patterns of spawning.

In this paper we analyze the collections of A. scheeleileptocephali that were made during a sampling surveytargeting anguillid and marine eel leptocephali aroundSulawesi Island, Indonesia in May 2001. The catches ofanguillid (Aoyama et al. 2003) and the major taxa ofmarine eel leptocephali (Wouthuyzen et al. 2005), andtheir assemblage structure (Minagawa et al. 2004) havebeen described from this survey. The objective of thepresent study was to learn about the reproductive ecol-

ogy and early life history of this apparently abundantmarine eel species by examining its larval distributionsand size ranges in a variety of different areas sampledduring the 2001 survey. These data are also used toevaluate the size at metamorphosis of A. scheelei lepto-cephali, the potential triggers of metamorphosis, and thepossible spawning areas and seasonality of spawning oftheir adults in the Indonesian Seas region.

Methods and materials

Study area

The Indonesian Seas around Sulawesi Island consist ofdeep basins that are about 1,000–4,000 m deep. Thesebasins have steep slopes that lead up to very narrowareas of continental shelf adjacent to the coastlines, ex-cept in the Java Sea, which is relatively shallow (mostly<200 m). The Celebes Sea is on the north side of Su-lawesi Island, Tomini Bay is on the northeast side of theisland, the Molucca (or Maluku) and Banda seas are tothe east, the Flores Sea is to the south, the Java Sea is tothe southwest, and Makassar Strait is to the west(Fig. 1). This region has a high biodiversity of marinefishes and other marine organisms such as corals, which

Fig. 1 Map showing thesampling locations during theBJ-01-1 cruise of the BarunaJaya VII in the Indonesian Seasaround Sulawesi Island,Indonesia, from 12 to 26 May2001. Stations 18–22 insouthern Tomini Bay are notlabeled, but were sequentialfrom south to north and then tothe east

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is apparently the result of its unique geological andevolutionary history in combination with the widevariety of habitats associated with its many islands ofvarious sizes (Randall 1998; Briggs 1999; Edinger et al.2000; Hughes et al. 2002; Allen and Adrim 2003).

The small-scale surface circulation of the seas inmuch of the region is probably influenced by wind shiftsassociated with the seasonal monsoons (Wyrtki 1961),and tidal currents (Hatayama et al. 1996), but there arealso some larger-scale persistent patterns of currents insome areas. The Celebes Sea has inflow of water fromthe Mindanao Current (Lukas et al. 1991; Wijffels et al.1995), which is the southward flowing branch of theNorth Equatorial Current (Toole et al. 1990; Qu andLukas 2003). At least some of this water from the wes-tern North Pacific then flows south through MakassarStrait and then into the Indian Ocean (Wyrtki 1961;Miyama et al. 1995; Vranes et al. 2002). This persistentflow is referred to as the Indonesian Throughflow and isthe primary pathway for water from the Pacific to theIndian Ocean (Godfrey 1996). Not all of the water thatenters the Celebes Sea is thought to go south through

Makassar Strait, however, as the Celebes Sea appears tohave large eddies (Kashino et al. 2001; Masumoto et al.2001), and some water probably flows back out into thewestern North Pacific and into the North EquatorialCountercurrent (Lukas et al. 1991; Wijffels et al. 1995).The surface circulation of other regions such as theMolucca, Banda, and Flores Seas may vary dependingon the monsoon winds (Wyrtki 1961; Moore et al. 2003),and the surface waters of Tomini Bay may be somewhatisolated from the other deeper basins (Hatayama et al.1996).

The salinity and temperature conditions of the studyarea varied among the seven different areas that weresampled during May 2001. The temperature and salinityplots (TS diagrams) showed that both these character-istics differed among several of the basins (Fig. 2). Thetemperature in the upper 100 m ranged between 24 and30�C, with the highest surface temperatures being inTomini Bay. The salinity structure was more variablethroughout the study area, with some stations havinglower salinities near the surface or a mixed layer ofsalinity down to 20–55 m depths.

Fig. 2 Temperature–salinityplots of the CTD data at eachsampling station aroundSulawesi Island during May2001 separated by region (toppanels), and the temperatureand salinity profiles at threestations where most of themetamorphosing leptocephaliwere collected. The boxeswithin the upper panels areincluded to provide a frame ofreference for comparing amongstations

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Collection of leptocephali

Leptocephali were collected from 13 to 26 May 2001during a cruise of the R/V Baruna Jaya VII of the Re-search Center for Oceanography of the IndonesianInstitute of Sciences. Sampling occurred at 25 stations inthe waters around Sulawesi Island in areas including theJava Sea (Stns. 1–2), Makassar Strait (Stns. 3–6), CelebesSea (Stns. 7–10), Molucca Sea (Stns. 11–12), Tomini Bay(Stns. 13–23), Banda Sea (Stn. 24), or Flores Sea (Stn. 25)in areas with water depths >1,000 m (Fig. 1). Samplingfor leptocephali at each station consisted of two tows ofthe large pelagic trawl, the Isaacs Kidd Midwater Trawl(IKMT) with a net opening of 8.7 m2 and 0.5 mm meshsize (Isaacs and Kidd 1953), and a surface tow of a 0.8 mdiameter MTD plankton net with a 0.33 mm mesh size(Motoda 1971).All samplingwas done at night (except fortwo stations in Tomini Bay), and at each station a 30 minoblique IKMT tow to a depth of 200 m was made, alongwith a 60–80 min step IKMT tow, which towed hori-zontally for 10 min at five depths of around 30, 60, 90, 120and 150 m. The depth of the IKMT was estimated bymeasuring the wire angle and the meters of wire out. TheMTD net was towed horizontally just below the sea sur-face next to the ship for 10 min. Only leptocephali caughtin the IKMT tows were used to calculate the catch rate ateach station, which were based on the amount of waterfiltered by the net during each tow as indicated by a flowmeter suspended in the center of the mouth of the net.Profiles of temperature and salinity (CTD)were alsomadeat each station to a depth of 500 m.

Identification of leptocephali

The leptocephali of A. scheelei were identified based ontheir low range of total myomeres (TM) and the myo-mere count of the position of their last vertical blood

vessel (LVBV), which are lower than any other type ofAriosoma leptocephali in the western Pacific (TM: 108–128, LVBV: 53–63, Mochioka et al. 1991). This specieswas listed as Ariosoma sp. 5 by Tabeta and Mochioka(1988a), and as Type I by Mochioka et al. (1991), butboth were suggested to be A. scheelei. Castle (1963) alsonoted that this species has a very low number vertebrae/myomeres for congrid eels. Therefore, because no otherAriosoma species has such a low range of myomeres, thespecies identification of these low myomere-count le-ptocephali as A. scheelei seems certain. All leptocephaliwere identified and measured to the nearest 0.1 mm totallength (TL) on board the ship before being preserved in10% formalin seawater.

The LVBV was used as the primary means of iden-tification during this study because no other Ariosomaspecies has such a low range of LVBV counts. Timeconstraints prevented all specimens from being countedat a few high-catch stations, so similarly sized specimenswith the same morphological features (pigmentation, nobranched LVBV) were subsampled for their LVBVcounts to confirm that they were A. scheelei. Our countsduring this study ranged from 51 to 61 (mean ± SD:54.1±2.1, N=356). Other similar species of Ariosomahave either a branched LVBV, or multiple vertical bloodvessels near the LVBV, in addition to their higher rangesof myomeres (Mochioka et al. 1991), so this method ofexamination and subsampling of myomere countsshould have been effective in distinguishing A. scheeleifrom other species.

Results

Size of leptocephali

A total of 551 leptocephali of A. scheelei were collectedin the various areas that were sampled around Sulawesi

Fig. 3 Ariosoma scheelei. Thetotal lengths of leptocephalicollected at each station by theIsaacs Kidd Midwater Trawl(IKMT) and MTD surface net,plotted by the Julian Date(sampling occurred from 12 to26 May, 2001) on which theywere collected in the seven areasthat were sampled aroundSulawesi Island. Leptocephalithat were undergoingmetamorphosis are shown withtriangles

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Island. These leptocephali had lengths of 22.4–166.0 mm(mean ± SD: 107.0±26.9), with 83.3% of the lepto-cephali being in the 60–150 mm size range (Fig. 3). Awide size range of leptocephali were collected in mostareas, and at least a few smaller leptocephali (20–50 mm) were collected in all areas except for at theCelebes and Banda Sea stations. The largest number ofsmall specimens was collected at the stations in TominiBay at sizes between 25 and 50 mm (Figs. 3, 4). TominiBay was the only region where the small leptocephaliwere more abundant than the larger size classes. At Stn.6 in the southwest Celebes Sea near the northern end ofMakassar Strait, where the biggest catch of premeta-morphic leptocephali occurred, most individuals were95–145 mm in length (Fig. 4). The lengths of these le-ptocephali and those of the big catch of metamorphos-ing leptocephali in the Java Sea formed approximatelynormal distributions. The distributions of sizes of le-ptocephali at the other stations were more spread out.Statistical comparisons of the lengths of premetamor-phic leptocephali among all the areas (single stations orgroups of stations) in Fig. 4 (N=26–193), except Stn. 5,found significant differences among these stations

(P<0.001, Kruskal–Wallis Test). The pairwise testsfound differences between Stn. 6 and four of the otherareas (Stn. 1, Tomini Bay, Stn. 24, 25), between Stn. 7and Tomini Bay, and between Stn. 25 and Tomini Bay(P<0.05, Dunn’s Test).

Metamorphosing leptocephali

There were 86 A. scheelei leptocephali that were under-going the process of metamorphosis from the lepto-cephalus to the glass eel stage. These leptocephali rangedin size from 105.3 to 153.3 mm and had a mean length of122.6±8.6 (Figs. 3, 4). They had all lost their teeth andthe lateral pigment on the myosepta along the midline ofthe body had disappeared, but they were still clearlyleptocephali and were not close to the glass eel stage.The position of the anus in most of these specimens hadmoved anteriorly compared to the position in premeta-morphic specimens (Fig. 5). The ratio of PAL to TLchanged from 0.89–0.98 (mean ± SD: 0.95±0.01) inpremetamorphic individuals, to 0.53–0.93 (mean±SD:= 0.75±0.07) in those undergoing metamorphosis.Most of the metamorphosing leptocephali were collectedat Stn. 1 (N=55, range: 107.0–142.0 mm, mean:123.1±7.1 mm) in the Java Sea and Stn. 5 (N=13,108.2–135.2 mm, 118.6±8.1 mm) at the northern end ofMakassar Strait (Figs. 3, 4). There were also five meta-morphosing leptocephali at Stn. 2, two at Stn. 6, and oneat Stn. 14 in Tomini Bay (Fig. 3). The maximum size ofthe metamorphosing leptocephali was 153.3 mm, but allthe rest were less than 145 mm. There were only tenpremetamorphic leptocephali collected that were largerthan 145 mm, so metamorphosis may have been occur-ring in A. scheelei leptocephali at lengths between about145 and 165 mm around Sulawesi Island.

Fig. 4 Ariosoma scheelei. Length frequency plots of leptocephalicollected with the IKMT at several stations around SulawesiIsland. Leptocephali that were undergoing metamorphosis aredistinguished from the others

Fig. 5 Ariosoma scheelei. Plot of the total and preanal lengths ofleptocephali before starting to metamorphose (premetamorphic)and of metamorphosing leptocephali, showing a decrease in totallength and anterior movement of the anus during metamorphosis

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What causes metamorphosis to begin in leptocephaliis not known, but the largest catches of metamorphosingA. scheelei around Sulawesi Island coincided with thepresence of a mixed layer of low-salinity water. Thelargest catch of metamorphosing leptocephali occurredat Stn. 1 (Fig. 4) where there was a mixed layer in theupper 55 m that had a low salinity of about 32.8 (Fig. 2).At station 2, where fewer metamorphosing leptocephaliwere collected, there was a mixed salinity layer of 32.6 inthe upper 20 m. The second largest catch of metamor-phosing leptocephali occurred at Stn. 5 where there was asalinity-mixed layer of 32.9 in the upper 30 m. Therewere fairly low-salinity values detected at some stationsin Tomini Bay, and some mixed layers of higher salinitiesnear the surface at some other stations, but the mixedlayer of salinities lower than 33.0 was not observed at anyother stations (not shown) except for Stn. 1, 2 and 5(Fig. 2, lower panels) where all but three of the meta-morphosing leptocephali were collected.

Distribution and abundance

Both premetamorphic and metamorphosing leptocephaliwere collected in the oblique and step tows of the IKMT,but only premetamorphic individuals were collected inthe MTD net tows at the surface. A total of 62 pre-metamorphic leptocephali were collected in the MTDtows at 11 stations. The biggest catch was at Stn. 1(N=20), and from 1 to 8 were collected at Stns. 2–8, 11,12, 21, 25. A slightly narrower size range was collected inthe MTD tows (range: 50.7–141.0 mm, mean:95.5±19.5 mm) compared to the oblique (range: 30.4–166.0 mm, mean: 96.6±29.4 mm) and step (range: 22.4–156.3 mm, mean: 106.8±27.2 mm) tows (Fig. 6). The

TL of the leptocephali in these three types of tows weresignificantly different (P<0.001, Kruskal-Wallis Test).The pairwise tests found differences between the TL ofleptocephali collected in the step andMTD tows, and thestep and oblique tows (P<0.05, Dunn’s Test), but therewas no difference between the oblique and MTD tows.

The catch rates of the leptocephali of A. scheelei inthe IKMT tows at each station suggested that there werehigher densities present in some of the areas that weresampled than in others. The overall catch rates in boththe oblique and step tows was highest at Stn. 6 (241 ind./105 m3of water filtered) at the northern end of MakassarStrait (Fig. 7) where all but two of the individuals werepremetamorphic (Fig. 4). The next highest catch rate ofleptocephali during the study was at Stn. 1 in the JavaSea (140 ind./105 m3) where 64% of the leptocephaliwere metamorphosing. This station was located rela-tively near the shelf break of the Java Sea and thereappear to be shallow water coral reef areas on both sidesof the station (Fig. 7). There were also high catch ratesat Stn. 7 (67 ind./105 m3) in the Celebes Sea and Stn. 25(57 ind./105 m3) in the Flores Sea.

These higher catch rates at a few of the stations ap-pear to be reflecting higher densities in these areas basedon comparisons of the catches in the step and obliquetows of the IKMT at each station. The mean catch rate(± SD) in the step tows (37.8±66.8 ind./105 m3, range:0–308.5 ind./105 m3) at each station was higher than inthe oblique tows (27.0±36.6 ind./105 m3; range: 0–129.3ind./105 m3), but these differences were not significant(P=0.19, U-test). The higher mean catch rate of the steptows was due to a much higher catch rate in the step towthan in the oblique tow at Stn. 6 (Fig. 8). The catch ratesin the two types of tows were much more similar at theother stations, and the oblique tows had higher catchrates than the step tows at six of the stations. However,at all the stations that had higher overall catch rates,both types of tows showed higher catch rates than at thelow catch stations. This suggests that these catches werethe result of higher densities of leptocephali in theseareas and were not just the result of a random chanceencounter of a higher-density patch in a local area or ata particular depth during a single tow.

Discussion

Spawning ecology and larval distribution

The leptocephali of A. scheelei were present at a widerange of sizes in all the seven areas around SulawesiIsland that were sampled during May 2001. They werecollected at each of the 23 night stations, and there werehigh catch rates in several different areas. Most of theleptocephali were large in size, although a smaller-sizeclass of leptocephali between about 20 and 50 mm waspresent in most areas. This suggests that juveniles andadults of this species were widespread in the

Fig. 6 Ariosoma scheelei. Length frequency plots of leptocephalicollected in the oblique and step tows of the IKMT at 23 stationsand in the MTD surface net at 11 stations around Sulawesi Island

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shallow-water habitats around Sulawesi Island and inthe surrounding areas.

Without the collection of small leptocephali <10 mmduring the survey, it is difficult to predict the exact typeof locations where A. scheelei spawns, because thespawning areas of various species of marine eels appearto vary widely. If spawning occurs in isolated local areas,such as relatively close to the shelf break, the samplingstations during this survey may have been located toofar offshore. However, based on the geography of theregion, the widespread distribution of leptocephali, andthe likely patterns of surface currents, a spawning area

must have been located in Tomini Bay, and spawningalso must have occurred in other areas. This type ofspawning ecology with multiple spawning areas may besimilar to that of the tropical freshwater eel, Anguillacelebesensis, which appears to spawn in at least twolocations in the region (Celebes Sea and Tomini Bay)after making relatively short local migrations (Aoyamaet al. 2003). Other anguillid eels make much longerspawning migrations (see Tsukamoto 1992; Tsukamotoet al. 2002), and some moray eels and garden eels mayspawn after no migration (Moyer and Zaiser 1982;Thresher 1984; Ferraris 1985), so the spawning locationsand migrations of anguilliform eels can vary widely.

Available evidence suggests that Ariosoma and othertaxa of congrid eels also use various types of spawninglocations, which may be determined by the geography oftheir adult habitats and the ocean currents in the region.A few small leptocephali of Ariosoma have been col-lected over the outer edge of the continental shelf of theEast China Sea (Miller et al. 2002), and Blache (1977)suggested that spawning by the widespread species in theAtlantic Ocean, A. balearicum, occurred over depths of500–2,000 m in the Gulf of Guinea of West Africa. Inaddition, two apparent subpopulations of A. balearicumappear to have different spawning locations in the wes-tern Sargasso Sea region, with one group spawning lo-cally in the Northern Bahamas, and the other migratingto spawn offshore in the western Sargasso Sea (Miller2002). The latter migration is similar to that of Congeroceanicus, which also appears to spawn in the SargassoSea (McCleave and Miller 1994). Other congrid eels ofthe genus Gnathophis may spawn near the shelf break orover the slope in several different regions of the world

Fig. 7 Ariosoma scheelei.Combined catch rates ofleptocephali in both the obliqueand step tows of the IKMT at23 stations around SulawesiIsland. The numbers within thelarge catch stations are theactual catch rate values. Theapparent distribution of coralreef habitats in the region areshown by short black lines ordots. This distribution of coralreefs was created from imagerygathered by satellite remotesensing using the SeaWiFSsensor. The maps used to showthe distribution of coral reefs inthis region were obtained fromthe ReefBase Project (http://www.reefbase.org; NASA andNOAA, USA; see Stumpf et al.1999). The thin lines show the500 m isobath in most areas(adapted from Gordon et al.1994), but this isobath is notshown in some areas where itwas very close to the coastline,small islands, or reefs

Fig. 8 Ariosoma scheelei. Plots of the catch rates of leptocephalicollected in the oblique and step tows of the IKMT at 23 stations(2 day tows excluded) around Sulawesi Island

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(Castle 1968; Castle and Robertson 1974; Miller et al.2002; Kimura et al. In press).

The wide size range A. scheelei leptocephali that werepresent around Sulawesi Island indicated that spawninghad occurred over several months, but it is unclear ifspawning occurs throughout the year. Some Ariosoma,Conger and Gnathophis species have been suggested tospawn seasonally (Castle and Robertson 1974; Blache1977; Smith 1989b; Ishii et al. 2003; Utoh et al. 2005),but studies on marine eels are lacking in the tropicalregion of the Indonesian Seas. Another possibility is thatspawning occurs monthly at a specific period of the lu-nar cycle, such as close to new moon, as has been indi-cated for the Japanese eel, Anguilla japonica (Ishikawaet al. 2001; Tsukamoto et al. 2003). The presence of asmall-size class of leptocephali in most areas aroundSulawesi Island, suggested the possibility that spawningmay have been synchronous in several different areasbefore the cruise, but further research on the spawningtimes and locations of A. scheelei that utilizes otolithgrowth increment analyses of leptocephali is needed totest this hypothesis.

Surface catches of leptocephali

The 62 premetamorphic A. scheelei leptocephali thatwere collected at the surface alongside the ship in theMTD tows at 11 stations raise questions about whythese individuals were distributed in such shallow water.The biggest catch was of 20 individuals at Stn. 1 andfrom 1 to 8 were collected at ten other stations. Theleptocephali collected at the surface had a slightly nar-rower size range than those collected in the IKMT tows,and no metamorphosing individuals were collected atthe surface in the MTD tows. The reason why theseleptocephali were distributed in the upper meter of theocean is impossible to determine, especially since thefeeding ecology of leptocephali in general is so poorlyunderstood (Pfeiler 1999; Miller and Tsukamoto 2004).Leptocephali have been hypothesized to feed on detritalmaterial such as marine snow or discarded larvaceanhouses (Otake et al. 1993; Mochioka and Iwamizu1996), so a visually based feeding mechanism is mostlikely used by leptocephali. This makes it questionablewhether there is enough light at the surface of the oceanat night to feed on particulate matter. It is possible thatsome individuals come to the surface at night to reside inthe warmest water, which might facilitate faster growthwhile digesting the food consumed during the day, orthat some individuals show vertical migrations thatbring them to the surface temporarily. Most leptocephaliincluding Ariosoma may reside in the upper 100 m of theocean at night (Castonguay and McCleave 1987), butsome Ariosoma and other taxa of leptocephali have beenfrequently caught at the surface or in the upper 10 m ofthe ocean (Tabeta and Mochioka 1988b; Mochiokaet al. 1991; Miller et al. 2004)

Metamorphosis of leptocephali

Although the reproductive ecology and larval behaviorof A. scheelei cannot be fully understood yet, the find-ings of the present study provided useful data about themetamorphosis of the leptocephali of this species. Themetamorphosing A. scheelei leptocephali ranged in sizefrom 105.3 to 153.3 mm, which is about the same sizerange as the metamorphosing leptocephali of A. bal-earicum that were collected in the Florida Currentadjacent to the Sargasso Sea (Miller 2002). In the pres-ent study, the fact that there were only ten premeta-morphic leptocephali collected that were 145–166 mm,at a time when metamorphosis was occurring in someareas, indicated that A. scheelei leptocephali probablybegin to metamorphose at lengths between about 145and 165 mm around Sulawesi Island.

The metamorphosing leptocephali of A. scheeleishowed the same loss of teeth that has been observed inspecies of Anguilla, Congridae, Muraenidae and Serr-ivomeridae (Miller and Tsukamoto 2004) and is char-acteristic of all taxa of leptocephali (Smith 1989c). Thegut moved forward during metamorphosis, as also oc-curs in other eel species (Otake 2003). The ratio of PALto TL changed from 0.89–0.98 in premetamorphicindividuals, to 0.53–0.93 in metamorphosing specimensof A. scheelei, indicating that there were individuals atvarious different stages of metamorphosis that werecollected. The stimuli that trigger metamorphosis arenot known for any species of leptocephali (Smith 1989c;Otake 2003), although it is possible that cues associatedwith the shallow water coastal areas to which manyspecies of leptocephali eventually recruit, may trigger theprocess of metamorphosis in some taxa.

The occurrence of almost all of the metamorphosingspecimens of A. scheelei at stations with a low-salinitymixed layer near the surface is suggestive that this typeof water may be associated with some kind of cue thattriggers metamorphosis in this species. The largest catchof metamorphosing leptocephali occurred at Stn. 1,which had shallow shelf areas with coral reefs relativelyclose by both to the east and west. The low salinitiesdown to a depth of 55 m at this station was unique andmay have been water that originated over the conti-nental shelf of the Java Sea, because there appears to bean eastward flow of water through at least parts of theJava Sea from October to April (Wyrtki 1961). The low-salinity layer at Stns. 1 and 2 (32.6–32.9) also generallycorrespond to the average surface salinities in the JavaSea during that time of year (Wyrtki 1961; Miyama et al.1996). Even if low salinity itself is not an actual trigger,water from a large shelf area such as in the Java Seacould contain olfactory cues that trigger metamorphosisin leptocephali that have reached their fully grown size.Stations 2 and 5 where most of the other metamor-phosing leptocephali were caught had mixed layers oflow salinity less than 33.0 down to depths of 20 and30 m, respectively. The origin of the low-salinity waterat Stn. 5 is unclear however, because this station was not

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particularly close to the large rivers located on the eastside of Borneo (Kalimantan Island).

Previous reports have shown that metamorphosingA. scheelei (Mochioka et al. 1991), A. balearicum (Miller2002) and Gnathophis capensis (Castle 1968) were mostlycaught relatively close to coastal areas, but the meta-morphosing leptocephali of other Ariosoma-type specieshave been occasionally collected far offshore (Mochiokaet al. 1991). More intensive surveys with collectionscloser to and over the shelf in combination with moredetailed hydrographic data are needed to study thepossible cues triggering metamorphosis in this and otherspecies of leptocephali.

Abundance of A. scheelei

Another interesting finding during the survey aroundSulawesi Island was that A. scheelei was collected atevery night station and was by far the most abundantspecies that was collected. This one species comprised21% of the 2,575 leptocephali of more than 136 speciesof 11 families of eels that were collected (Wouthuyzenet al. 2005). A. scheelei was still the most abundantspecies during the survey even if the two largest catchesat Stns. 1 and 6 were not included. In comparison, onlyabout 100 leptocephali of the other seven species of theAriosoma-type were collected, indicating that this speciesmay be either much more abundant than the otherAriosoma species in the Indonesian Seas region, or thatthey had been spawning more in the months before thesurvey.

The leptocephali of A. scheelei also appear to berelatively abundant in other areas of the western Pacificcompared with different species of Ariosoma. They werereported to be the most abundant species in the westernPacific region and comprised 71% of 3,492 nonexteril-lium Ariosoma leptocephali that were collected (Moc-hioka et al. 1991). It was also the most abundantAriosoma species reported in collections in the westernSouth Pacific in the region near New Caledonia (Castle1966). Ariosoma-type leptocephali, with an exterilliumgut that extends outside of the body, also appear to bemuch less abundant than A. scheelei in the western Pa-cific (Mochioka et al. 1982). However, A. scheelei maynot be the most abundant species in all regions of thePacific and Indian oceans, because the leptocephali ofthe nonexterillium species, A. mauritianum, appear tohave been more abundant than A. scheelei off westernAustralia (Castle 1969) and in the western North Pacificto the south of Japan (Mochioka et al. 1991).

In the Atlantic Ocean, a distinctly greater abundanceof leptocephali similar to that of A. scheelei in theIndonesian Seas has been observed for A. balearicum.This species also has a very wide distribution and isfound in the Atlantic Ocean, the Mediterranean Sea andthe Red Sea (Smith 1989a). Its leptocephali have beenfound to be among the most abundant species of eellarvae collected during surveys for leptocephali in the

Sargasso Sea and Gulf Stream regions (Miller andMcCleave 1994; Miller 1995, 2002) and in the Gulf ofMexico (Smith 1989b). Their leptocephali have also beencollected in the Gulf of Guinea off western Africa(Blache 1977), and they have been reported from manyother areas of the Atlantic (see Smith 1989b; Miller2002). The leptocephali of A. scheelei and A. balearicumappear to be almost morphologically identical except forhaving slightly different, but overlapping, ranges ofmyomeres. Their adult body forms also appear to besimilar (Castle 1963; Smith 1989a), so they may be fairlyclosely related species with similar ecological traits.

The reason for the greater abundance of the lepto-cephali of these two species in some areas is not known,but the adults of A. balearicum are relatively small(<340 mm) and appear to be most abundant on sandybottoms in less than 100 m of water (Smith 1989a).Several other species of the genus also are found inshallow water less than 100 m (Bohlke 1989a), but thereis little evidence of other Atlantic species of Ariosomabeing similarly abundant based on the presence of theirleptocephali. A. scheelei may grow to about the samesize as A. balearicum and has been reported to reachsexual maturity at sizes less than 200 mm (Castle 1963).This small size at reproductive maturity may be onereason why their leptocephali are more abundant thanother taxa. In addition, their leptocephali reach rela-tively large sizes of up to 165 mm, so even aftershrinkage during metamorphosis, they would recruit totheir juvenile habitats at relatively large sizes comparedto the likely size at recruitment of the larvae of familiessuch as the Chlopsidae, Moringuidae, Muraenidae andOphichthidae, which have shorter maximum larval sizes(Bohlke 1989b). Interestingly, however, the leptocephaliof both A. scheelei and A. balearicum do not get as largeas most other species of Ariosoma-type leptocephali,which reach sizes considerably greater than 200 mm(Castle 1969; Mochioka et al. 1982, 1991; Smith 1989b;Miller 2002). Metamorphosing sooner than other Ario-soma species could reduce transportation offshore awayfrom their juvenile habitats. These reproductive andrecruitment characteristics in combination with the fastlarval growth rates that have been suggested by otolithanalyses of A. balearicum leptocephali (Bishop et al.2000) may be part of the reason why A. scheelei and A.balearicum appear to be very successful and widely dis-tributed species of marine eels.

If the larval abundance of A. scheelei during thepresent study is a direct reflection of the abundance oftheir juveniles and adults in the Indonesian Seas, thisspecies may be a very important ecological componentof the high biodiversity shallow water marine ecosystemsof the Indonesian Seas and other regions of the Indo-Pacific and Indian Ocean. They may be important notonly as predators on other marine organisms, but iflarge numbers of their larvae recruit to coastal areasthey also could be an important food source for manyother types of fishes. More research is needed on thedistribution and life history traits of A. scheelei

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leptocephali in the Indonesian Seas, and studies shouldbe initiated to learn about the ecology of their juvenilesand adults in this and other parts of its range to betterunderstand its importance in marine ecosystems.

Acknowledgements We are grateful to the captain, crew and tech-nicians of the R/V Baruna Jaya VII for their help in carrying outthe sampling survey around Sulawesi Island. This work was sup-ported in part by Grants-in-Aid numbers 1299346, 11691177 and12NP0201 from the Ministry of Education, Science, Sports andCulture, Japan, and by grant Numbers JSPS-RFTF 97L00901 fromthe ‘‘Research for the Future Program’’ of the Japan Society for thePromotion of Science. KT was supported by the Research Foun-dation ‘‘Touwa Shokuhin Shinkoukai’’ and the Eel ResearchFoundation ‘‘Noborikai’’.

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