Distribution and early life history of Kaupichthys leptocephali (family Chlopsidae) in the central Indonesian Seas

RESEARCH ARTICLE

Distribution and early life history of Kaupichthys leptocephali(family Chlopsidae) in the central Indonesian Seas

Tae Won Lee Æ Michael J. Miller Æ Hak Bin Hwang ÆSam Wouthuyzen Æ Katsumi Tsukamoto

Received: 28 March 2007 / Accepted: 23 August 2007 / Published online: 10 October 2007

� Springer-Verlag 2007

Abstract Leptocephali of the widely distributed tropical

marine eels of the genus Kaupichthys (family Chlopsidae)

were collected around Sulawesi Island during a sampling

survey in the Indonesian Seas in late September and early

October 2002, and the otolith microstructure of 24 of the

59 specimens captured was examined to learn about the

larval growth rates and spawning times of these small sized

eels. Leptocephali ranging in size from 25 to 60 mm were

collected in Makassar Strait and the Celebes Sea, but they

were most abundant in the semi-enclosed Tomini Bay of

northeast Sulawesi Island. The Kaupichthys leptocephali

examined had 39–161 otolith growth increments. Their

back-calculated hatching dates indicated that five age

groups were present and each group appeared to have been

spawned around the full moon of previous months. Aver-

age growth rate estimates of the first two age groups were

0.65 and 0.54 mm/day for the 27.4–30.4 and 37.6–

45.6 mm age classes. The growth rates of the oldest three

age groups (52.0–60.8 mm) appeared to have slowed down

after they reached their approximate maximum size.

An increase in increment widths at the outer margin of

the otoliths of those larger than 53 mm suggested that

the process of metamorphosis had begun even though

there were few external morphological changes indicating

metamorphosis. It is hypothesized that chlopsid lepto-

cephali have an unusually short gut that may not need to

move forward during early metamorphosis. The presence

of four age classes in Tomini Bay suggests that the Togian

Islands region may be productive habitats for Kaupichthys

juveniles and adults.

Introduction

The false morays of the family Chlopsidae are found in

shallow water areas in tropical regions worldwide and are

one of the most poorly known families of the Anguilli-

formes. These eels are much smaller in size than most

marine eels because they only reach maximum sizes of

about 250 mm (Smith 1989a). They probably hide in holes

or crevices primarily in coral reef areas or sea grass beds

and very little is known about their reproductive ecology or

spawning areas because they are rarely observed or col-

lected (Matsubara and Asano 1959; Smith 1969, 1989a).

Some information about their life histories can be inferred

from the distribution and size of their leptocephali that

suggest they do not migrate very far offshore to spawn

(Smith 1989b; Miller 1995; Miller and McCleave 2007).

Some of the most common chlopsid eels seem to be

those of the genus Kaupichthys, which includes about six

species worldwide. Kaupichthys hyoproroides appears to

be widely distributed in tropical areas of the western North

Atlantic and also has been considered to be present in the

Pacific and Indian oceans (Smith 1989a). However, outside

Communicated by S. Nishida.

T. W. Lee � H. B. Hwang

Department of Oceanography,

Chungnam National University,

Daejeon 305-764, Korea

M. J. Miller (&) � K. Tsukamoto

Ocean Research Institute, The University of Tokyo,

1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan

e-mail: [email protected]

S. Wouthuyzen

Research Center for Oceanography,

Indonesian Institute of Sciences, Jl. Pasir Putih 1,

Ancol Timur, Jakarta 11480, Indonesia

123

Mar Biol (2008) 153:285–295

DOI 10.1007/s00227-007-0804-z

of the Atlantic, this species is now considered to be a

complex of cryptic species that include K. japonicus in the

Indonesia region and K. diodontus in the central Pacific

region, which appear to be the more common species in the

tropical Indo-Pacific (Froese and Pauly 2007; K. Tighe pers

comm). These eels are found primarily in and around coral

reefs and are rarely collected without the use of ichthyo-

cides (Smith 1989a). Females can reach sexual maturity by

at least a size of 150 mm (Smith 1989a) and K. hyopr-

oroides appears to be one of the more common chlopsid

eels based on the abundance of their leptocephali (Smith

1989b; Miller 1995; Miller and McCleave 2007). Smith

(1989b) reported that K. hyoproroides leptocephali were

collected throughout the year in the western North Atlantic.

The leptocephali of this genus also have been described

from the western North Pacific (Tabeta and Mochioka

1988), however, four species of Kaupichthys appear to be

present in the Indo-Pacific (K. astronasus, K. brachychirus,

K. diodontus, K. japonicus) based on adult specimens

(Matsubara and Asano 1959; Allen and Adrim 2003;

Froese and Pauly 2007). More research is needed on the

morphology and identification of Kaupichthys adults and

leptocephali in the Indonesian Seas region to facilitate

studies on the life histories of these poorly known fishes.

Because aspects of the life history of fishes are recorded

chronologically in otoliths, analysis of otolith microstruc-

ture provides valuable information about the previous

growth history of a species when some life stages are not

easy to study in their native habitats. Although the otolith

microstructure of Kaupichthys or other chlopsid lepto-

cephali have not been previously examined, there have

been studies on the otoliths of leptocephali of anguillid and

a few families of marine eels. The otolith microstructure

and microchemistry of several species of temperate and

tropical anguillid leptocephali (Castonguay 1987; Arai

et al. 2001a; Ishikawa et al. 2001; Kuroki et al. 2005, 2006)

and glass eels have been studied (e.g. Tsukamoto 1990;

Otake et al. 1994; Wang and Tzeng 2000; Arai et al. 1997,

2001b; Marui et al. 2001). There also have been studies on

the otolith microstructure of leptocephali of congrid eels

such as Conger (e.g. Lee and Byun 1996; Otake et al. 1997;

Correia et al. 2002, 2004), Ariosoma, and Paraconger

(Bishop et al. 2000). Other leptocephali of marine eels of

the families Muraenidae and Ophichthidae (Bishop et al.

2000) and Nettatomatidae and Synaphobranchidae (Ma

et al. 2005) also have been aged using their otolith

microstructure. These studies have been based on the

assumption of daily deposition of growth increments in

otoliths after hatching, which has been validated in the

glass eel or elver stages of Anguilla japonica (Tsukamoto

1989), Anguilla rostrata (Cieri and McCleave 2001), and

tropical anguillids (Arai et al. 2000; Sugeha et al. 2001).

Evidence of daily deposition during the leptocephalus stage

also has been found using A. japonica larvae hatched and

reared in the laboratory (Shinoda et al. 2004) and a meta-

morphosing ophichthid (Powles et al. 2006).

Studies on the otolith microstructure of leptocephali and

glass eels can be especially useful because leptocephali

undergo drastic changes in morphology when they meta-

morphose into the glass eel stage, which is reflected in their

otoliths (Otake 2003). During metamorphosis, the end of

the gut moves forward, the larval teeth are absorbed, the

body thickens, and there is an increase in head length

(Castle 1970; Asano et al. 1978; Smith 1989c; Lee and

Byun 1996; Bell et al. 2003; Miller and Tsukamoto 2004).

Otolith studies found that during metamorphosis there is an

increase in the otolith increment widths in anguillid and

congrid leptocephali, which is also accompanied by chan-

ges in the Sr:Ca ratios in the otoliths (Otake et al. 1994,

1997; Arai et al. 1997). Leptocephali differ significantly

from other fish larvae however, because the body is

transparent and is filled with an energy storage material

that is used to form new tissues during metamorphosis

(Pfeiler 1999), but the physiological processes that occur

when the body of leptocephali is transformed into the eel-

like body of glass eels are poorly understood.

This study was designed to provide the first information

about the early life history and spawning times of chlopsid

eels by describing the larval distribution and size of the

Kaupichthys leptocephali collected around Sulawesi Island

in the central Indonesian Seas and by examining their

otolith microstructure. The specific objectives were to use

otolith microstructure to determine the ages, larval growth

rates, and hatching dates using a wide range of sizes of

leptocephali that were collected in various different areas

during a sampling survey that targeted leptocephali.

Materials and methods

Leptocephali were collected in September and October of

2002 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 34 stations

in the Java Sea, Makassar Strait, Celebes Sea, Molucca

(Maluku) Sea, and Tomini Bay (Fig. 1). The oceano-

graphic characteristics of this region have been overviewed

recently by Gordon (2005), Miller et al. (2006) and Susanto

et al. (2006). Sampling for leptocephali at each station

usually consisted of a single tow of the large pelagic trawl,

the Isaacs Kidd Midwater Trawl (IKMT) with a net

opening of 8.7 m2 and 0.5 mm mesh size (Isaacs and Kidd

1953). All sampling was done at nighttime (except for two

stations in Tomini Bay), and each tow consisted of an

approximately 30 min oblique IKMT tow to a depth of

about 200 m in most cases except in the Java Sea, or a

286 Mar Biol (2008) 153:285–295

123

60–80 min IKMT step tow, which towed horizontally for

10 min at five depths of around 30, 60, 90, 120 and 150 m.

Both an oblique and a step tow were made at the same

station (Stn) on two occasions (Stn 9, 31). Stations were

numbered sequentially as sampling occurred along the

cruise track from the Java Sea through Makassar Strait, the

southern Celebes Sea, around the northern tip of Suluawesi

Island, through the Molucca Sea, and into Tomini Bay

where there were 11 stations. The same cruise track was

followed on the return trip back through the Celebes Sea,

Makassar Strait, and the over the continental shelf of the

Java Sea. Except for the stations in the Java Sea (Stn 1, 31,

32, 33, 34) all stations were located over water about

1,000–4,000 m deep.

Specimens were sorted fresh from the plankton, their

lengths measured to the nearest 0.1 mm (total length TL,

predorsal length PDL, preanal length PAL). Among the 59

individuals collected, 24 specimens representative of entire

size range of leptocephali were subsampled for otolith

analysis and they were preserved in 99% ethanol; the other

specimens were preserved in a 10% formalin–seawater

solution. The body shape and distinctive pigment spots

all over the body make Kaupichthys leptocephali easy to

identify (Smith 1969; Tabeta and Mochioka 1988; Smith

1989b), so time constraints resulted in the number of

myomeres (total myomeres TM, predorsal myomyeres

PDM, preanal myomeres PAM) being obtained from only a

subsample of the specimens that were collected (N = 21),

and these counts ranged from 107 to 126. This range is

similar to the overall range of number of vertebrae of the

juveniles and adults of the K. hyoproroides species complex

in the western Atlantic, western Pacific, and Indian oceans,

which was found to be 109–126 (Smith 1989a). The

leptocephali collected around Sulawesi Island appear to be

the K. hyoproroides type, so they may mostly be the larvae

of K. japonicus in the Indonesian Seas region, but there is

presently not enough published information to allow their

identification due to the overlapping ranges of vertebrae

and myomeres of the Indo-Pacific species (Smith 1969).

Therefore, because of the present lack of information about

the morphology or genetic differences in the Indo-Pacific

species of this genus, the species identity of the Kaupichthys

leptocephali in present study were not determined.

The otoliths of 24 Kaupichthys leptocephali were pre-

pared for examination of their microstructure according to

Lee and Byun (1996). Briefly, the otoliths were embedded

in polyester resin, ground to the sagittal plane with a series

of graded silicon carbide papers (600, 800 and 1,000 grit),

and polished with 1 lm alumina powder. Grinding and

polishing was continued until the growth increments were

clearly visible. All specimens were observed under the

scanning electron microscope (SEM). For viewing under

the SEM, ground surfaces of otoliths were etched with

0.3% HCl for 3–5 s. These samples were coated with gold

for 5 min and examined under the SEM.

Total radius (R) was measured along the longest axis

from the core to the anterior margin using a light micro-

scope when the core was clearly visible during grinding.

The ground surface viewed under the SEM did not always

show the exact sagittal plane through the core, so the radii

and the incremental widths measured under the SEM

photographs were calibrated using the radii measured

Tomini Bay

South ChinaSea

Celebes Sea

Borneo

Java

SulawesiIsland

125°E120°E115°E110°E

Flores Sea

Banda SeaJava Sea

MoluccaSea

0°

5°S

5°N

tiartS rassaka

M

1

2

3

45

6 78 92425

2627

28

2930

3132

3334

10 11

12

131415

Fig. 1 Map of the stations in

the Indonesian Seas around

Sulawesi Island, Indonesia that

were sampled from 27

September to 16 October 2002

showing the locations where

Kaupichthys leptocephali were

collected. Specimens used for

otolith analyses are shown with

black squares, other

Kaupichthys leptocephali with

black circles, and stations where

no Kaupichthys leptocephali

were collected with whitecircles. Stations are labeled

1–34, but stations 16–23 in

Tomini Bay are not labeled

Mar Biol (2008) 153:285–295 287

123

under the light microscope. Since daily deposition of

growth increments in fish otoliths has been generally

accepted, and the microstructure of Kaupichthys otoliths

was similar to that of the other anguilliform otoliths for

which the daily deposition has been validated, the age was

estimated from the number of growth increments from the

core, assuming that the growth increments were deposited

daily from hatching.

The growth rates of the leptocephali based on the

examination of their otolith microstructure was determined

using their age and TL data. A growth curve was fitted to

these data that was calculated using the Von Bertalanffy

growth model. For comparison to the growth rates in other

previous studies on leptocephali, the individual growth

rates were calculated for each specimen by first subtracting

an estimated 3 mm for the size at hatching as has been

done in other studies (Arai et al. 2001b; Ma et al. 2005;

Kuroki et al. 2006), and calculating growth as, growth

rate = TL–3/age. The mean individual growth rates for

each age group found by back-calculating their hatching

dates were also calculated.

Results

Distribution and size of leptocephali

Kaupichthys leptocephali were present in all of the general

regions that were sampled except for the Java Sea and the

Molucca Sea and were most abundant in Tomini Bay of

northwest Sulawesi Island (Fig. 1). They were collected

at all but one of the 11 tows in Tomini Bay, and the catch

rates at the positive stations in the bay ranged from

2.9 to 36.7 ind./105 m3 of water filtered (mean ± SD:

13.6 ± 13.1). Kaupichthys leptocephali were caught in nine

of the 20 tows outside of Tomini Bay, and the catch rates at

these positive stations ranged from 2.4 to 15.1 ind./105 m3

(mean 5.5 ± 4.0). The 59 leptocephali collected during the

survey ranged in size from 25.7 to 60.8 mm, but Tomini Bay

was the only region where a wide range of sizes were

collected (Fig. 2). The various size classes were widely

distributed at the sampling stations in Tomini Bay at sizes

ranging from 25.7 to 59.0 mm. Based on the finding of

different age groups using the back calculated hatching dates

described below, four age groups could be roughly seen in

the length frequency plot of the Tomimi Bay specimens

(Fig. 3). In contrast to in Tomini Bay, relatively large sized

leptocephali ([40 mm) were collected in the Celebes Sea,

but both large and small sized individuals were collected

during the two sampling periods in Makassar Strait (Fig. 2).

Morphology of leptocephali

Leptocephali of the family Chlopsidae differ from most

other species of leptocephali that have been studied during

metamorphosis because they have a very short gut, and a

deep body (Fig. 4). Because the smaller sized leptocephali

have a slightly longer relative gut length than the larger

sizes, the PAL/TL ratio of the Kaupichthys leptocephali

examined for the otolith study tended to decrease as the

body size increased (Fig. 4). The mean ± SD PAL/TL of

the premetamorphic specimens 37 mm and larger was

0.43 ± 0.02, and those that were found to have apparently

begun the process of metamorphosis as described below

had a mean of 0.44 ± 0.01. Therefore, there was no clear

forward movement of the gut associated with early meta-

morphosis, which is typically observed during the

metamorphic process of leptocephali. All specimens also

still had the characteristic pattern of small spots all over the

body, and still had small teeth, both of which (lateral

pigment and teeth) are often lost during metamorphosis in

Julian day272 274 276 278 280 282 284 286 288

30 Sept 14 Oct

)m

m( htgnel latoT

20

30

40

50

60

70Makassar

StraitCelebes

SeaTomini Bay Celebes

SeaMakassar

Strait

Fig. 2 The total lengths of the individual Kaupichthys leptocephali

that were collected at each station around Sulawesi Island plotted by

date of sampling (Julian day of year) and showing the five different

age groups indicated by their back-calculated hatching dates. The 40

(circle), 70 (downward triangle), 101 (diamond), 129 (square), and

161 (upward triangle) day old age groups are shown with blacksymbols along with Kaupichthys leptocephali whose otoliths were not

examined (white circles)

288 Mar Biol (2008) 153:285–295

123

other species of leptocephali. However, the largest speci-

men (60.8 mm) was noted at the time of examination

before preservation as being at the metamorphosing stage

because of its thicker head and enlarged olfactory rosette.

Otolith microstructure

The otolith microstructure of the 24 Kaupichthys lepto-

cephali that were examined was similar to that of other

anguilliform leptocephali such as Anguilla spp. and Conger

spp. (Otake et al. 1994; Lee and Byun 1996; Otake et al.

1997; Correia et al. 2002, 2004, Kuroki et al. 2006). The

core of each otolith was located in the posterior half of the

otolith, and under the SEM it appeared as a round black

depression with no apparent growth increments visible

(Fig. 5). The core was delimited by a hatching check, and

outside of the core was a thick ring in which about ten

barely discernible narrow increments were deposited. This

thick ring has been known to be deposited during yolk

absorption in larval fishes. Outside of the first feeding

check (e.g. Geffen 1992), the growth increments were

concentrically deposited and had a peak in widths at about

the twentieth increment (Fig. 6). After this peak, the

increment widths diminished gradually and maintained low

values until the outer margin in the specimens that were

smaller than 53 mm. For the specimens larger than 53 mm,

a prominent check was observed at the 94th to 111th

increment, which may have been a metamorphosis check

(Lee and Byun 1996). The otolith increment widths sharply

increased from the prominent check in three individuals

among the six showing the prominent check, and slightly

increased in the other three (Fig. 6). This indicated that the

individuals larger than 53 mm may have begun the process

of metamorphosis based on similar rapid increases in the

otolith increment widths during metamorphosis in Conger

and Anguilla leptocephali (Otake et al. 1994, 1997; Lee and

Byun 1996; Arai et al. 1997; Correia et al. 2002, 2004;

Kuroki et al. 2005).

The increase in increment width in the specimens larger

than 53 mm was not associated with an increase in somatic

growth rate, because the radius of the otoliths of some of

these specimens increased markedly without much increase

in total length (Fig. 7). The increase in otolith radius in

relation to increase in length changed after the size of about

53 mm and could be divided into two segments, which may

correspond to the leptocephalus and metamorphic stages.

Age, growth, and hatching date

The ages of the Kaupichthys leptocephali ranging in size

from 27.4 to 60.8 mm were from 39 to 161 days (Table 1).

The plot of length versus age indicated that there were five

apparent age groups with clearly separated ages, but with

partially overlapping sizes (Fig. 8). The five groups had

mean ± SD age and length compositions of 40.3 ± 1.1 days

(29.2 ± 1.6 mm, n = 3), 70.2 ± 3.1 days (40.8 ± 2.5 mm,

n = 11), 101.0 ± 1.8 days (49.9 ± 2.3 mm, n = 4), 129.8 ±

2.9 days (56.0 ± 1.8 mm, n = 5) and 161 days (60.8 mm,

n = 1). Based on their mean ages, the five groups will be

referred to as the 40 day age group, for the youngest group,

and the 70, 101, 129, and 161 day age groups for the larger

KaupichthysTomini Bay

N = 46

Total length (mm)70

ilahpecotpel fo rebmu

N

0

1

2

3

4

5

6

1 2 3 4

20 30 40 50 60

Fig. 3 Length frequency distribution of the Kaupichthys leptocephali

collected in Tomini Bay of Sulawesi Island showing the sizes of the

specimens belonging to four of the age groups (labeled 1–4)

determined using their otolith microstructure (black bars), and the

Kaupichthys leptocephali whose otoliths were not examined (whitebars)

Total length (mm)20 30 40 50 60 70

PA

L/T

L

0.55

0.50

0.45

0.40

0.35

y = -0.0017x + 0.519R2 = 0.45

N = 24

TL

PAL

PDL

Fig. 4 The relationship between total length (TL) and preanal length

(PAL) plotted using their PAL/TL ratios in relation to size of the

Kaupichthys leptocephali that were used in the otolith analyses. The

leptocephali that may have begun the process of metamorphosis are

shown with black circles. The leptocephalus is from Smith (1989b)

Mar Biol (2008) 153:285–295 289

123

sizes. The 129 and 161 day age groups consisted entirely of

leptocephali that had increased increment widths in the

outer edge of their otoliths and may have begun the process

of metamorphosis.

The growth rates of the larger sized Kaupichthys

leptocephali appeared to slow down after they reached a

size of about 40 mm and an age of about 70 days as

indicated by both the growth curve (Fig. 8) and the indi-

vidual growth rates calculated using the age and TL

(Table 1). The leptocephali of the smallest sized 40 day

age group had the fastest mean ± SD individual growth

rate of 0.65 ± 0.02 mm/day and the mean growth rates

decreased steadily in each of the older age groups from

0.54 ± 0.03 mm/day in the 70 day group, to 0.36 mm/day

in the 161-day-old specimen. The growth in total length

(Lt) versus age (t) of the Kaupichthys leptocephali was

expressed by the Von Bertalanffy growth curve (Fig. 8) as,

Lt ¼ 73:24 1� e�0:0105 tþ7:73ð Þh i

; r2 ¼ 0:96� �

:

The shape of the curve indicated that the growth rate

was fastest in the younger leptocephali and then slowed

down considerably in the larger sized individuals, as was

reflected in the average growth rate calculations.

Assuming that the otolith growth increments were

deposited daily after hatching, the back-calculated hatching

dates ranged from May to August 2002 and showed a

periodic pattern with peaks near the full moon (Fig. 9). The

three small sized specimens of the 40 day age group were

collected in Tomini Bay and were hatched on 29 August

after the full moon on 23 August (Figs. 2, 8, 9). The largest

number of specimens was in the 70 day age group that was

mostly collected in Tomini Bay and the Celebes Sea, and

their back-calculated hatching dates ranged from just

before full moon of late July to about the last quarter. The

101 and 129 day age groups were also hatched close to the

full moon periods of June and late May, respectively,

except for one specimen on 19 June before full moon that

was caught at Stn 2 near the southern end of Makassar

Strait (Figs. 1, 9). The 161-day-old specimen collected at

Stn 29 in Makassar Strait calculated back to 5 May after

full moon. Based on these five groups identified by the

Fig. 5 SEM photographs of the otolith microstructure of 43.0 mm

TL (upper) and 57.5 mm TL (lower) Kaupichthys leptocephali from

the Indonesian Seas. Scale bars = 10 lm. The first feeding checks

(FFC) in both specimens and the metamorphosis (M) check in the

larger specimen are indicated with arrows

)mµ( htdi

w tneme rcnI

Age (days after hatching)

0

1

2

3

4

5

1400 160

N = 24

20 40 60 10080 120

Fig. 6 The mean otolith increment widths along the length of the

otoliths of the Kaupichthys specimens. The bars show the standard

deviations

Total length (mm)

300

250

200

150

100

50

03020 40 50 60 70

y = 17.02x - 810R2 = 0.52)

mµ( suidar htilotO

y = 2.09x - 19.4R2 = 0.69

N = 24

Fig. 7 The otolith radius and total length of Kaupichthys leptoceph-

ali, with the leptocephali that may have begun the process of

metamorphosis based on their otolith increment widths shown with

black circles

290 Mar Biol (2008) 153:285–295

123

otolith back-calculations and the sizes of the other speci-

mens, there appeared to be four age groups of Kaupichthys

leptocephali collected in Makassar Strait, at least two in the

Celebes Sea, and four in Tomini Bay (Fig. 2).

Discussion

Distribution of leptocephali

The sampling survey around Sulawesi Island found that the

leptocephali of Kaupichthys were present in a number of

different areas throughout the region. They were present in

Makassar Strait, the Celebes Sea, and in Tomini Bay, but

except for the latter area, they were only collected in small

numbers. The same pattern of wide distribution was

observed during a similar survey around Sulawesi Island in

May of 2001, with the largest numbers of Kaupichthys

leptocephali being collected in Makassar Strait and Tomini

Bay; they were also at stations in the Banda and Flores seas

on the southeast side of Sulawesi Island in areas not

sampled in the 2002 survey (Wouthuyzen et al. 2005). The

leptocephali of a congrid eel, Ariosoma scheelei, were also

widespread in the 2001 survey around Sulawesi Island

(Miller et al. 2006), as were various other taxa of lepto-

cephali (Wouthuyzen et al. 2005). These findings suggest

that Kaupichthys and other marine eels are probably widely

distributed in the central Indonesian Seas and that spawn-

ing may occur in areas closer to shore than the locations

of the sampling stations, because the smallest Kaupichthys

leptocephali collected during the two surveys were

20.0 mm in 2001 (Wouthuyzen et al. 2005) and 25.7 mm

in 2002 (this study). Surveys for leptocephali in the western

North Atlantic indicate chlopsids do not migrate very far

from shore to spawn (Miller 1995; Miller and McCleave

2007), so it is likely that spawning by Kaupichthys occurs

somewhere over the shelf or relatively close to the shelf

break. If this is the case, the predominantly larger sized

individuals collected in most areas had been transported

offshore by currents.

Tomini Bay may have a substantial population of

Kaupichthys and other chlopsid eels because the survey

for leptocephali around Sulawesi Island the previous year

found higher catch rates of chlopsids in Tomini Bay than in

most other areas (Wouthuyzen et al. 2005). The Togian

Table 1 Means and ranges of the total lengths, number of otolith increments, growth rates and hatching dates of the five age groups of

Kaupichthys leptocephali that were detected based on their ages and back-calculated hatching dates

Age group No. of specimens Total length (mm) No. of increments Growth rate (mm/day) Hatch date

Mean Range Mean Range Mean Range

1 3 29.2 27.4–30.4 40.3 39–41 0.65 0.64–0.67 27 August

2 11 40.8 37.6–45.6 70.2 65–76 0.54 0.49–0.59 23 July–1 August

3 4 49.9 46.7–52.0 101.0 99–103 0.46 0.43–0.48 19–27 June

4 5 56.0 53.2–57.5 129.8 126–133 0.41 0.38–0.43 26–29 May

5 1 60.8 – 161.0 – 0.36 – 5 May

)m

m( htgnel latoT

Age (days after hatching)

20

10

00

30

40

50

50 100 150 200

60

70

TL = 73.24 x (1 - e-0.0105 (t + 7.73))

N = 24

R2 = 0.96

Fig. 8 The relationship between total length and age of the

Kaupichthys leptocephali whose otolith microstructure was examined,

with the leptocephali that may have begun the process of metamor-

phosis based on their otolith increment widths shown with blackcircles. The Von Bertalanffy’s growth curve that was fitted to the data

is shown

N = 24

Hatching date

120 140 160 180 200 220 240slaudividni .o

N0

1

2

3

4

18-Aug29-Jul9-Jul19-Jun10-May 30-May

Fig. 9 The back-calculated hatching dates of the Kaupichthysleptocephali whose otolith microstructure was examined, showing

the dates of the full moon with open circles and new moon with blackcircles

Mar Biol (2008) 153:285–295 291

123

Islands are the large group of coral reef islands that can be

seen in Tomini Bay in Fig. 1, and they support a rich coral

reef fauna that includes an unusually high diversity of

corals and some endemic fish species (Wallace 1999; Allen

and Adrim 2003). These coral reef and other habitats may

also support many chlopsid eels, and Allen and Adrim

(2003) reported that both K. brachychirus, K. diodontus

(possibly K. japonicus) were collected in the Togian

Islands. The leptocephali spawned near these islands and

other reef habitats would likely remain within the bay due

to the potentially limited amount of water exchange with

outside areas (Hatayama et al. 1996). Tidal currents and

eddies appear to have caused the leptocephali of four dif-

ferent spawning groups to mix in Tomini Bay where they

were collected at sizes ranging from 25.7 to 59.0 mm.

Coral reef areas are widespread around Sulawesi Island

(Wouthuyzen et al. 2005; Miller et al. 2006) so there may

be suitable habitat for Kaupichthys juveniles and adults

throughout the region.

Otolith microstructure and growth of leptocephali

The otolith microstructure of Kaupichthys leptocephali

consisted of a series of concentric rings from the core to the

edge of the otolith (Fig. 5) that was essentially the same as

other species of leptocephali that have been observed. Each

otolith had a central core, an area deposited during yolk

absorption, and concentric rings extending out to the edge

of the otolith. These same characteristics have also been

observed in the otoliths of the leptocephali of both tem-

perate (Castonguay 1987; Otake et al. 1994; Arai et al.

1997) and tropical (Kuroki et al. 2006) anguillids, species

of Conger (Lee and Byun 1996; Otake et al. 1997; Correia

et al. 2002, 2004, 2006), and nettastomatid and synapho-

branchid species (Ma et al. 2005). Based on the total

number of increments, the ages of the Kaupichthys lepto-

cephali (27.4–60.8 mm) that were examined ranged from

39 to 161 days old (Table 1).

The growth rates of the Kaupichthys leptocephali stea-

dily decreased as the larvae grew older based on the growth

curve of their body sizes and ages. Their mean individual

growth rates varied from 0.65 mm/day in the youngest age

group, to 0.36 mm/day in the oldest. The mean individual

growth rate of the 70 day age group (37.6–45.6 mm) was

0.54 mm/day, which is similar to estimates of the mean

growth rates (0.44–0.56 mm/day) calculated the same way

for four species of anguillid leptocephali (8.0–54.1 mm)

from the Indo-Pacific region including the Indonesian Seas

(Kuroki et al. 2006). Similar individual growth rates of

0.43–0.83 mm mm/day for Sarenchelys stylura leptoceph-

ali (10.0–48.6 mm) and 0.20–0.53 mm/day for Dysomma

sp. leptocephali (8.4–33.5 mm) were found in specimens

from the East China Sea (Ma et al. 2005). Faster growth

rates for species of the Congridae, Muraenidae, or Oph-

ichthidae that were suggested to be greater than 1.0 mm/day

(Bishop et al. 2000), but these faster growth rates have yet

to be confirmed in other samples of leptocephali.

The otolith increment width and otolith radius of

Kaupichthys leptocephali grew slowly before increasing

abruptly from the age of 94–111 days in the six oldest

specimens. This rapid increase in increment width has been

considered to occur during metamorphosis from the lep-

tocephalus stage to the glass eel stage (Otake et al. 1994,

1997; Arai et al. 1997, 2001; Wang and Tzeng 2000; Marui

et al. 2001; Correia et al. 2006). Further support for this

hypothesis was recently found in Anguilla marmorata in a

study that included leptocephali, metamorphosing lepto-

cephali, oceanic glass eels and glass eels collected after

recruitment to coastal areas (Kuroki et al. 2005). The rapid

increase in increment widths was observed to have begun

in the metamorphosing leptocephali and glass eels, but not

in the premetamorphic leptocephali. An increase in otolith

increment widths was also observed to occur during

metamorphosis in tarpon leptocephali (Chen and Tzeng

2006).

Onset of metamorphosis

During the transition from larvae to juveniles, fish larvae

undergo various morphological and osteological modifi-

cations related to changes in swimming and feeding

function. During the metamorphosis of leptocephali the

head thickens, the teeth are lost, the body length is reduced,

and the anus, and the anterior base of the dorsal and anal

fins usually move forward (Smith 1989c; Otake 2003;

Miller and Tsukamoto 2004). These changes in morphol-

ogy during metamorphosis of leptocephali have been

documented in a variety of species and families of eels

(Castle 1970; Raju 1974; Asano et al. 1978; Lieby 1979;

Bell et al. 2003). Interestingly, five of the six largest

Kaupichthys specimens that were examined in this study

showed no obvious external morphological evidence of

metamorphosis, but they showed an increase in the incre-

ment widths at the outer edge of their otoliths, which

suggested the onset of metamorphosis was occurring.

The forward movement of the gut as measured by an

abrupt decrease of the PAL/TL or PAM/TM ratios has been

used as a criterion for defining the onset of metamorphosis

of conger eel leptocephali, because it is difficult to deter-

mine the relative stage of metamorphosis based on other

morphometric characteristics (Tanaka et al. 1987; Lee

and Byun 1996; Otake et al. 1997). The leptocephali of

Anguilla, Ariosoma and Conger have long guts at the onset

of metamorphosis, so their PAL/TL ratios decrease during

292 Mar Biol (2008) 153:285–295

123

metamorphosis, because it is necessary for the gut to move

forward to the eventual position of the anus in the glass eel

and juvenile eel stage (Asano et al. 1978; Lee and Byun

1996; Bell et al. 2003; Otake 2003; Miller et al. 2006).

However, the PAL/TL ratio of Kaupichthys leptocephali

had not changed in the specimens whose otolith increment

widths showed abrupt increases. The obvious possible

reason for this lack of a decrease in the PAL/TL ratios of

the largest Kaupichthys leptocephali is that the position of

the end of the gut in chlopsid leptocephali is located much

farther forward than most other taxa of leptocephali

(Fig. 4; Tabeta and Mochioka 1988; Smith 1989b; Miller

and Tsukamoto 2004). Therefore, because of this anterior

position, the gut does not have to move much to be in its

final position at the end of metamorphosis. Some species of

ophichthid leptocephali, such as Myrophis puntatus (Lieby

1979; Powles et al. 2006) and M. platyrhynchus (Lieby

1989), also have very short guts, which may not move very

much more forward during metamorphosis.

The present study suggests that in some species the rapid

increase in otolith increment widths may occur before there

are major changes in external morphology. It is possible

the rapid increase in otolith increment widths may be

associated with physiological changes linked to the meta-

morphic process, such as breaking down the transparent

internal glycosaminoglycan (GAG) material for use in

building new tissues in the head and body. The oldest

Kaupichthys specimen examined here was 28 days older

than the next oldest specimen, and it showed clear changes

in the morphology of its head, with a thickening of the

tissue and an enlargement of the olfactory rosette. Smith

(1969) described a glass eel and a metamorphosing lepto-

cephalus of Kaupichthys hyoproroides from near the

northern Bahamas in which the gut had moved forward, so

it is likely that as metamorphosis progresses further, the gut

eventually moves forward in chlopsid leptocephali. The

body length of leptocephali also decreases markedly during

metamorphosis from the leptocephalus stage to the glass

eel stage, but the Kaupichthys leptocephali examined here

were possibly not at enough of an advanced stage of

metamorphosis to show any size decrease however. Further

research is needed to determine if the process of meta-

morphosis proceeds differently in chlopsid leptocephali by

examining a greater number of large sized specimens

including those that show clear external evidence of

metamorphosis.

Spawning periodicity

The back-calculated hatching dates of the Kaupichthys

leptocephali examined during this study were mostly

around one of the five full moons from early May to late

August of 2002. This finding suggested that this genus of

marine eels has a lunar cycle of reproduction and spawn

during or shortly after full moon periods around Sulawesi

Island. Four of these spawning groups appeared to be

collected in more than one sea area based on the otolith

analyses or the distinctiveness of the smallest size class

of leptocephali. This suggested that synchronous lunar

spawning may have been occurring in many areas, and so

this could be a life history characteristic of Kaupichthys

eels in the central Indonesian Seas region.

Lunar periodicity has not been reported in marine eels,

but their reproductive ecologies are diverse and very poorly

known (Thresher 1984; Fishelson 1992, 1994). Two ripe

Kaupichthys females (238, 239 mm TL) with full-grown

ova were collected from a shallow coral head in the Amami

Islands near Okinawa Japan during the new moon of

July 1958 (Matsubara and Asano 1959), but it is unclear

when they would have eventually spawned. However, the

catadromous anguillid eel, A. japonica, appears to spawn

during new moon periods in its offshore spawning area in

the western North Pacific (Ishikawa et al. 2001; Tsukamoto

et al. 2003; Tsukamoto 2006). Analyses of the otolith

microstructure of A. japonica leptocephali collected near

the spawning area during several different years have

shown that their back-calculated hatching dates were all

centered on the new moon periods of previous months,

suggesting that this species synchronizes its spawning with

the lunar cycle.

Various other species of teleost fishes such as groupers,

snappers, rabbitfishes and other coral reef fishes also have

lunar spawning periodicities that serve to synchronize their

spawning activities (Thresher 1984). This subject has been

reviewed recently (Takemura et al. 2004) and spawning

associated with either full or new moon has been reported

in a wide variety of families of marine fishes (Rhodes

and Sadovy 2002; Heyman et al. 2005; Johannes 1978;

Domeier and Colin 1997). A primary purpose of this

behavior appears to be to synchronize the formation of

spawning aggregations in a particular location with all

participants becoming ripe at the same time for successful

fertilization of eggs. Other possible functions of lunar

synchronization include predator avoidance, defense of

demersal egg clutches from nocturnal predators, or the

release of eggs during periods of strong tidal flow to

facilitate transport of eggs offshore away from the reef

(Takemura et al. 2004).

Very little is known about the reproductive ecology of

chlopsid and other marine eels however, so the function of

full moon spawning is difficult to determine. Kaupichthys

eels have polycyclic ovaries (Fishelson 1994), but it is

unknown if they spawn multiple times per year as is possible

with this type of ovary, or if they have any form of a spawning

aggregation or migration. Garden eels (Congridae) and some

Mar Biol (2008) 153:285–295 293

123

species of moray eels (Muraenidae) spawn within their

shallow water habitats (Moyer and Zaiser 1982; Thresher

1984; Ferraris 1985), whereas some species of congrids

migrate offshore to spawn (McCleave and Miller 1994;

Miller 2002). Various species of reproductively mature

ophichthids have been observed at the surface at night

(Ross and Rohde 2003) or to make spawning migrations

towards the edge of the shelf (Cohen and Dean 1970). The

only reported observation of spawning related behavior by

chlopsid eels was by a fisherman who observed many small

eels swarming around his light at night over about 900 m of

water (Smith 1989a). The eels had enlarged abdomens and

the one specimen that was collected was a ripe female. This

species was given the name Powellichthys ventriosus, but it

has never been collected again. If Kaupichthys eels also form

spawning aggregations, then spawning during full moon

could allow them to use visual cues to locate mates at night,

or it could serve to synchronize spawning during a period of

strong tides that could transport their eggs and larvae further

offshore.

This finding of apparent spawning during full moon

around Sulawesi Island should be confirmed using larger

sample sizes, and research on the back-calculated hatching

dates of Kaupichthys leptocephali in different seasons and

in other tropical areas is needed to determine if lunar

spawning during full moon periods is characteristic of the

eels of this genus. Other chlopsids in the tropical areas of

the Indonesian Seas also should be examined to see if this

type of spawning strategy is used by other species of the

family.

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