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The life history of the tropical shad Tenualosa toli from Sarawak: First
evidence of protandry in the Clupeiformes?

Article in Environmental Biology of Fishes · July 1996

DOI: 10.1007/BF00004998

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Environmental Biology of Fishes 46: 225242.1996.
0 1996 Kluwer Academic Publishers. Printed in the Netherlands.

The life history of the tropical shad Tenuahsa toli from Sarawak:
first evidence of protandry in the Clupeiformes?

Stephen J.M. Blaber’, David A. Milton’, Josephine Pang’, Philip Wang’, Ong Boon-Teck*, Lolin Nyigo3 &
David Lubim3
’ CSIRO Division of Fisheries, Marine Laboratories, I? 0. Box 120, Cleveland, Queensland 4163, Australia
’ Inland Fisheries Branch, Ministry of Agriculture & Community Development, Kompleks Negeri, JI Simpang
Tiga, 93632, Kuching, Sarawak, Malaysia
’ PPES Santubong (Sdn Bhd), SEDC, PO. Box 400, 93902 Kuching, Sarawak, Malaysia

Received 8.9.1994 Accepted 28.8.1995

Key words: Estuaries, Ecology, Hermaphroditism, Diet, Age, Growth, Distribution

Synopsis

Sharp declines in catches prompted a detailed study of the commercially and culturally important ‘terubok’
Tenualosa toli, which lives in the fast-flowing, turbid estuariesand adjacent shallow coastal waters of Sarawak.
Its reproduction, diet, age and growth were investigated. An absenceof small females and large males, togeth-
er with histological data showing transitional gonads, suggest that 7: toli is a protandrous hermaphrodite.
Ageing based on otoliths indicates that individuals may not live more than about two years. Male fish spawn
towards the end of their first year, change sex (transitional gonads were recorded in fish from 14 to 31 cm SL)
and spawn as females in their secondyear. Spawning takes place in the middle reachesof estuariesand females
deposit all their eggsat once. Fecundity is linearly related to fish length but shows significant seasonaland site
variations. Hermaphroditism is discussedin relation to possible environmental and isolating mechanisms. i?
toli is a zooplanktivore eating mainly calanoid copepods. Laser-ablation inductively-coupled plasma mass
spectroscopy of trace elements across otoliths revealed that the speciesdoes not move into full seawater or
freshwater, but completes its life cycle in estuarine and adjacent coastal waters. Therefore 7: toli populations
in each estuary and adjacent coastal waters may be relatively isolated from one another, and hence particular-
ly susceptible to overfishing.

Introduction known and most studied tropical shad Tenualosa il-

The Alosinae (shads) are a subfamily of the Clupei-
dae (Nelson 1984)which occur throughout temper-
ate and tropical regions in marine, estuarine and
fresh waters. The largest concentration of speciesis
in the genus Alosa, which occurs in Europe and
eastern North America. Several species form the
basis of important fisheries (Whitehead 1985).
Many are anadromous, amongst them the best
isha, the target of the large ‘hilsa’fisheries of India
and Bangladesh (McDowell 1988, Pillay 1967).
Other Tenualosa specieshave a narrower distribu-
tion, and most are probably anadromous, but the
extent of anadromy in tropical clupeoids is difficult
to assess(Whitehead 1985)becausetheir life histo-
ries are largely unknown (McDowell 1988).
Tenualosa toli (Valenciennes,1847) the ‘terubok’
of Sarawak, is the most commercially and culturally
226

a 30’ N

1’3O‘N

1110 E

Fig. I. The Batang Lassa (Site A) and Batang Lupar (Site B) estuaries of Sarawak showing sampling stations and marine coastal areas
where fish were collected (C).

important estuarine fish of Sarawak. The fishery
there lasts from April to October, with peak catches
early in the season (Willman et al.).’ However,
catches have been declining since the 1980sand in
recent years have fallen to historically low levels
(Willman et al. 1989). This prompted the Sarawak
Government to initiate, in collaboration with CSI-
RO, Australia, a detailed scientific study of the spe-
cies. Little was known of the life history, biology or
ecology of Tenualosa toli, although Whitehead
(1985) thought it was ‘perhaps anadromous’.
The objectives of the present study were, firstly,
to describe the reproduction, diet, age and growth
of ‘I: toli and secondly, to define its life cycle with
particular reference to movements between, and
dependence on, marine, estuarine and freshwater
habitats.
Methods
Study areas. - Samples were collected during three
intensive surveys (May-June, July-August and Oc-
tober) in 1993 from the only two large estuaries of
Sarawak where there is still any significant com-
mercial fishing for 7: toli: the Batang Lupar and the
Batang Lassa (Fig. 1). Fish were also collected from
the Batang Lassa in November-December 1993
and from the Batang Lupar in August 1994.In addi-
tion, samples were collected from coastal marine
areas of Sarawak (Maludam, Kabong, Mukah, Bin-
tulu, Sibuti and Miri) in August 1994 and from Sib-
uti and Miri in March 1995. The location of sam-
pling stations is shown in Fig. 1.
Field methods. - 7: toli were obtained from each of
the study areas during each sampling period in
three ways: (1) By hiring local fishermen to fish for
set periods with their own gill nets (75 mm and
100 mm stretch mesh monofilament), (2) by using
research gill nets (25, 50, 75, 100, 125 and 150 mm
stretch mesh monofilament), and (3) by purchasing
’Willman, R., G. Melvin, S. Jiram, R. Hadil, A.H. Yong & L.
Gabriel. 1989. Proposal for the management of the Tenualosa to/i
fishery in Sarawak. Technical Cooperation Programme FAO-
Malaysia, FAO-UN, Rome, Fl: TCP/MAL/675(1).
227
freshly caught fish of known origin from markets or
directly from fishermen at Lingga (Batang Lupar),
Daro (Batang Lassa), Maludam (sea), Kabong
(sea), Mukah (sea), Bintulu (sea), Sibuti (sea) and
Miri (sea).
The collection of fish during January and Febru-
ary was not possible as all fishing in the estuaries
and sea ceasesat this time due to the rough condi-
tions during the NE monsoon.
The standard length (SL) and weight (g) of all
fish were recorded. Their stomachs and gonads
were removed and preserved in 10% formalin for
analyses in the CSIRO laboratory in Australia.
Otoliths to be used for ageing and chemical analys-
es at CSIRO were removed and stored in 70% etha-
nol.
ir: toli larvae and plankton were caught with a
square frame (50 x 50 cm) plankton net of 500 mi-
cron mesh. This was deployed either passively (be-
causeof high current speeds) for 15 min or 30 min in
conjunction with an Ott current meter both at the
water surface and approximately 1 m from the bot-
tom, or towed at about 3 km h-’for 15 min. Most
plankton samples were taken during the three in-
tensive surveys of the Batang Lassa and Batang Lu-
par. All plankton samples were stored in 70% etha-
nol for subsequent analyses at CSIRO.
Several physical variables were measured at each
site in May-June and in October 1993: salinity was
measured with an optical salinometer, temperature
with a standard thermometer, turbidity (as NTU -
nephelometric turbidity units) with a Hach neph-
elometer (model 2100) and current speeds with an
Ott current meter.
Laboratory methods. -The reproductive condition,
diet and age of every 7: toli collected were exam-
ined.
Reproduction
The gonads of both sexeswere weighed in the lab-
oratory (+ 0.001 g) and subsamples from each go-
nad from all fish placed in cassettesfor histological
processing.
228

The Gonadosomatic Index (GSI) was calculated as sons of fecundity between the two rivers and be-
follows: tween sampling periods were made by analysis of
covariance. This enabled the effects of differences
gonad weight
GSI = x 100. in fish size between samples to be taken into ac-
fish weight (minus gonad weight)
count when comparing the other factors. Similarly,
any potential relationship between fish size and egg
The histological sampleswere dehydrated, infiltrat-
weight was also taken into account when making
ed with wax and sectioned at 9 urn. The sections
seasonalor temporal comparisons of egg weight.
were stained with haematoxylin and eosin. In order
to assessany differential development of the go-
nads three transversesectionswere examined from
Diet
along the length of each gonad. The proportion (by
area) of each development stage in all histological
The diet was identified from intact and broken
sections (male, female and transitional) was record-
items found in the stomachsof fish examined under
ed using the following criteria (Cyrus & Blaber
a microscope.The numbers of each food type were
1984).
recorded and their contribution to the diet ex-
pressed as a percentage. The number of fish in
Oogenesis
which each item occurred was also noted and ex-
Stage 1 = oogonia; stage II = pre-vitellogenic oo-
pressed as percentage frequency of occurrence.
cytes; stageIII to V = vitellogenesis; stageIII = yolk
precursor; stage IV = non-staining yolk; stage V =
red-staining yolk; stage VI = completion of devel-
Age and growth
opment; stage VII = atresion.
In the laboratory, the otolith sagitta was dried and
Spermatogenesis
excess tissue removed. Otoliths were weighed
StageI = primary germ cells (stem spermatogonia);
(+ 0.0001g), embedded onto microscope slideswith
stage II = spermatogonia; stage III = primary sper-
thermoplastic cement, and then polished with wet
matocytes; stage IV = secondary spermatocytes;
and dry sandpaper (800 grit) until the midplane was
stage V = spermatids; stage VI = spermatozoa.
reached. The otoliths were viewed under immer-
Transitional gonads were defined as those con-
sion oil at 400 x to 1000x on a video screenattached
taining both degenerating testicular tissue and oo-
to a microscope.Daily rings were counted along the
cytes at various stagesof development.
longitudinal axis towards the posterior of the oto-
Gonads that were shown by histology to be from
liths, as this was the axis where rings were most eas-
pre-spawning females were subsampled. The sub-
ily distinguished. No annuli were visible in either
samples (1.0 g) were weighed (+ 0.001g) and their
one or two year old fish.
number of ripe eggscounted under a microscope.In
A von Bertalanffy growth curve (Milton et al.
order to compare egg weights from different sites
1991)was fitted separately to the data from each riv-
and seasons the eggs in the subsamples were
er system. The curve was of the form defined by
grouped in fives, dried in the oven at 60” C and then
Francis (1988) which provides uncorrelated growth
weighed on a fine-scale balance (accuracy f
parameters that can be directly compared (e.g. Mil-
0.00001g). Annual fecundity was estimated by the
ton et al. 1991,1993).
formula:
To validate that the growth rings on the otoliths
are laid down daily, eggs of T to/i were collected
F = ovary wet weight x subsampleegg count/sub-
with a plankton net from the known spawning
sample wet weight.
ground at Pulau Seduku (LA) in the Batang Lupar
(Fig. 1) between 10:00 and 11:OO h. These embryos
As fecundity is usually related to fish size,compari-
hatched in aquaria the following morning (8:OOh).
 229

Three free embryos were immediately preserved in
70% alcohol, while the remaining six were kept and
fed mixed phytoplankton from tows in the adjacent
estuary. Larvae were killed after 5 days and pre-
served in 70% alcohol. In the laboratory the larvae
were measured (& 0.1 mm) and their sagittae were
removed and examined at 1000 x with a video-en-
hanced microscope. The rings were legible on all
sagittae and were counted on two separate occa-
sions by at least two readers with 9.5to 100% con-
cordance. Larger fish could not be captured live for
use in validation experiments and hence we have
assumedthat the above validation applied to the ol-
der age groups.
Movement
It is assumed that otoliths of fish take up chemicals
from the water and that levels of strontium (usually
expressed as strontium/calcium ratios), for exam-
ple, may be valuable in determining the salinity of
the water in which the fish has lived (Radtke 1989,
Radtke et al. 1990).
Seasonal changes in the trace-element composi-
tion of the otoliths were used to detect possible
movement of fish out of the Batang Lassa estuary.
The otoliths of 9 fish that had been aged were
mounted on small blocks in polyester resin. The
blocks were then polished with successively finer
grades of sandpaper and diamond pastes (down to
1 urn). The trace-elements were determined by la-
ser-ablation inductively-coupled plasma massspec-
trometry at the British Geological Survey (BGS),
Nottingham, United Kingdom. The BGS laser abla-
tion microprobe consists of a Spectron laser oper-
ating in the far-UV (266 nm), linked to a high qual-
ity Leitz microscope. A VG plasmaquad 2 + spec-
trometer, with a modified sample introduction sys-
tem was used in peak jumping mode to achieve the

Table I. Summary of physical measurements in the Batang Lassa and Batang Lupar in October 1993 (for location of station numbers refer
to Fig. 1: - = no data).

River Station Position Depth Tide Salinity Turbidity Current

(ml (%) (NTU + s.e.) (m s-l)

Batang Lassa Sl (sea) 1 km off mouth surface high 22 34-163 (range) -

s4 centre surface low 4 192+41 -
S6 west side surface rising 0 417 f 8 0.92
14.5 rising 0 - 0.76
surface ebbing 4 263 It: 2 0.54
14.5 ebbing 4 - 0.47
SlO centre surface high 1 321 f6 0
ebbing 1 346 t 1
s12 centre surface high 0 62 * 0.7 0
ebbing 1 58 i 0.4 -
s13 centre surface ebbing 0 40 k 0.6 -
s14 centre surface low 0 22 * 0.3 0
S16 centre surface low 0 9 rk 0.2 0
Batang Lupar Ll centre surface low 13 68 k 2 -
west side surface low 14 38 + 3 -
L2 centre surface low 13 68 IL 2 -
west side surface low 14 38 + 3 -
L2 centre surface low 13 184 -
L3 east side surface low 12 167?21 0
centre surface low 9 134 3~8 0
east side surface high 11 131 ?r49
centre surface high 11 52 t 5
L4 west side surface ehbing 90 > 1000 0.91
230

May - June 1993 trometer. For all otoliths except one, five ablations
were made across the otolith from the origin to the
g,,-;;L j:k,,; edge; the remaining otolith had 33 ablations.
The elements examined were strontium, barium,
zinc, copper, magnesium and sodium. In other spe-
0 10 20 30 40 0 10 20 30 40 cies, the relative differences in calcium content
across an otolith have varied less than 2% (e.g. Sa-
July - August 1993
dovy & Severin 1994). The absolute amount of oto-
lith material ablated may vary by up to 10% because
of changes in the crystalline matrix (S. Chenery per-
sonal communication). Calcium was therefore as-
sumed to comprise 40% of otolith weight in this
study, and this value was used as an internal stan-
September - October 1993 dard. Hence changes in strontium/calcium ratios
LLlSStl Lupar
would mirror, and not differ significantly from, the

-bL
2 40
N=SS
40
N=105
absolute concentrations of strontium. After the
5 30 30
g 20 20
10 10
L 0 0L Maludam - Kabong August 1994
0 10 20 30 40 0 10 20 30 40
Length (cm) Length (cm) 12
2 10 N=21
November - December 1993
S a
gi?! 6
12 Lassa LL 4
6 10 N=19
Cl male 2
5 8 0
s 6 n transitional
e 4 10 20 30 40
2 n female
0 male
Lt. 0 L
0 10 20 30 40 Mukah eastwards August 1994 1 transitional
Length (cm)
14 H female

Fig. 2. Length frequency distributions of samples of 7: roll col- 8 12

5 10 N=38
lected in 1993 from the Batang Lassa and Batang Lupar. Males a
s
(white bars), females (black bars) and transitional fish (grey ?? 6
bars) are shown. Ll- 4
2
0
0 10 20 30 40
best detection limits on a transient signal. The BGS
laser ablation microprobe has a number of key fea-
tures which are not available in commercial sys- Sibuti - Miri March 1995
tems. Firstly, the laser operates in the ultra-violet
(266 nm), instead of the infra-red (1064 nm), hence a
’ c N=15
it is able to achieve a very small beam diameter, pro- 6
s
duce craters with a diameter of less than 5 ym and z
E
4
IL
can couple efficiently with a wide variety of materi- 2
als. Secondly the high quality microscope used in 0
0 10 20 30 40
the system allows accurate positioning of the sam-
ples across the otolith. Length (cm)

A laser beam shot at the surface of the otolith Fig. 3. Length frequency distributions of samples of 7: toli col-
atomises a small point of the surface (crater); the lected from coastal marine areas of Sarawak. Males (white bars),
chemicals released are detected with the mass spec- females (black bars) and transitional fish (grey bars) are shown.
 231

analyses,the otoliths were re-examined to estimate
the age at which each ablation was made.
Results
though over 1000 NTU was recorded around Pulau
Seduku (L4) in the Batang Lupar. The highest cur-
rent speeds, of between 0.9 and 1.0 m s-‘, were re-
corded on the rising tide in both estuaries.

Physical conditions Fish

Physical variables were measured only in the mid-
dle reaches (station S6) of the Batang Lassa and the
Batang Lupar (station L3) in May-June, but in Oc-
tober a series of measurements along each estuary
was taken over 48 h periods.
Both estuaries are very turbid and fast flowing,
with a large tidal range (maximum of 5.3 m). Their
salinity regimes are slightly different. Salinities over
much of the Batang Lassa are less than those of the
Batang Lupar. During May and June, salinities at
station S6 in the middle reaches of the Batang Lassa
varied from 0 to 7 ppt according to the state of the
tide, whereas at L3 in the Batang Lupar they ranged
from 4 to 11 ppt. The Batang Lassa had a similar
pattern to the Batang Lupar but with lower salin-
ities in October (Table l), which suggests that its
freshwater inflow may be higher than that into the
Batang Lupar. The water temperatures of both es-
tuaries were between 28 and 29 “C. Turbidities in
the middle reaches of both estuaries in May and
June were similar and varied with the tide: in the
Batang Lassa they ranged from 119to 627 NTU, and
in the Batang Lupar from 105 to 664 NTU. In Octo-
ber turbidities were somewhat lower (Table l), al-
Totals of 289 Tenualosa tofi from the Batang Lupar
and 289 from the Batang Lassa were analysed in
1993.In August 1994 a further 15 fish were obtained
from the Batang Lupar and 74 fish were collected
from the sea in August 1994 and March 1995. The
length-frequency distributions of the estuary sam-
ples are clearly bimodal, with the exception of No-
vember-December 1993 when only males were
caught (Fig. 2). The presence of junveniles in the
estuaries is also indicated in Fig. 2. Fish from the
coastal marine environment in August 1994 also
consisted mainly of two size groups but by the end
of the monsoon (March) only one group was found
(Fig. 3).
Reproduction
The reproductive condition of T toli collected dur-
ing the sampling periods is shown in Table 2. The
species has a long spawning period, from at least
May to October. It spawns in the estuaries. All fe-
males from marine coastal areas (Fig. 3) were de-
veloping (stages II-IV) and none had ripe or spent

Table 2. Reproductive data from Ten&osa foli collected during 1993 (se. = standard error, N = number of fish).

River Period Sex GSI f se. N % Spawning

Lassa May-June Female 18.8 f 0.6 37 66.1

Male 0.8 k 0.06 16 20.1
July-August Female 15.8 + 1.8 26 81.2
Male 3.6 F 2.8 123 29.3
Sept-Ott Female 18.1 + 2.0 3 100.0
Male 0.7 + 0.1 49 18.4
Lupar May-June Female 20.1 + 1.1 16 94.1
Male 0.8 + 0.04 55 23.1
July-Aug Female 15.7 + 1.3 28 86.4
Male 0.6 + 0.05 32 25.0
Sept-Ott Female 17.2 + 1.2 22 95.1
Male 0.9 * 0.03 100 33.0
232

Lassa Lupar
3o -May - June l
l l

‘;i a-
@

B
10 -

0
0, . , f@$JQ, - l , 3
0 100 200 300 400

30 July - August

1
3o 1 July - August

:
*a l l
20 -
Q$y .

l l l
10 - l

0
0 0 I a I ’ , -
0 100 200 300 400 0 100 200 300 400

30 September - October 3o September - October

1
a
l

01-“”
0 100 200 300 400
Length (mm) Length (mm)

Fig. 4. Gonadosomatic indices (GSI) of male @) and female (-) T. toli from the Batang Lassa and Batang Lupar.

gonads (stagesV-VII) based on histological oocyte
stages.
Gonadosomatic indices plotted against fish
length for all fish from the Batang Lupar and Ba-
tang Lassa at three different times of year are com-
pared in Fig. 4. All ripe females during May-June
were over 30 cm SL and the smallest female was
23 cm. The smallest size at which females were ripe
decreased later in the year, when spawning females
of 20 to 2.5cm were recorded. Spent females (deter-
 233

mined histologically, usually with post-ovulatory 0 Female st 4 lm Female st 1

follicles) had GSI’s of less than 2 and were uncom- q Female st 3 n male

mon. Ripe males had a low GSI, as did nearly all Female st 2

males of all sizes at all times. The largest recorded (4)(4)(2)

100
male was 27 cm (November-December 1993,Fig. 2)
and the smallest recorded female in the estuaries
90
was 19.5 cm (July-August 1993,Fig. 2) and in the sea
16 cm (August 1994,Fig. 3). 80
Histology of the gonads of all ripe and spent fe-
males showed that individuals of i? toli release all
their eggsat once.The ovaries of all females, includ-
ing ripe females, consistedalmost entirely of eggsof
a uniform size and at the same stage of develop-
ment. Spent ovaries contained a few atretic eggs of
various stages and degenerating ovarian tissue.
Hence there was no evidence of multiple or batch
spawning.
The indications from histology are that Tenualo-
sa toli changes sex. It is apparently a protandrous
hermaphrodite (changing from male to female).
Transitional gonads were found in two individuals
(18 cm and 23 cm SL) in the May-June 1993 sam-
ples, in 11 individuals (13-31 cm SL) from coastal
marine areas in August 1994,and in March 1995 in 21314151617181920212223242526272829303132
15 individuals (17-22 cm SL) also from the sea.The
Standard length (cm)
proportions of testicular and various stagesof ovar-
ian tissue in transitional gonads in relation to fish
Fig. 5. Proportions of male (black bars) and female (st = various
length are shown in Fig. 5. No fish of lessthan 13 cm gonad stages) tissue in fish with transitional gonads. All refer to
contained any oocytes. Transitional fish less than single fish with the exception of those of 18,19 and 20 cm where
about 23 cm contained predominantly degenerat- numbers are shown in parentheses and the values are means.
ing testicular tissue, whereas larger fish contained
mainly ovarian tissue and smaller amounts of de- The fecundity of 7: toli ranged between 100 000
generating male tissue. Histological sections of the and 1.2million eggs(Table 3) and was linearly relat-
transitional gonad of an 18 cm individual are shown ed to fish size in both the Batang Lassa and the Ba-
in Fig. 6; they show small eggs (stagesI and II) and tang Lupar (Fig. 7). The relationship for the Batang
testicular tissue with spermatocytes and sperma- Lassa was F = 3900 x length (mm)-884,709, r2 =
tids, as well as degenerating male tissue. All males 0.40; p < 0.001and for the Batang Lupar F = 3005 x
in Fig. 5 exhibited degenerating spermatozoa and length-567,560, r* = 0.60; p < 0.001. Although the
testicular tissue. relationship was similar in the two river systems,fe-
The GSI and histological data indicate that the cundity was significantly different among the three
speciesundergoes a functional sex change relative- sampling periods when the effects of fish size were
ly rapidly, although traces of degenerating testicu- removed. Fecundity was higher among fish collect-
lar tissue were recorded in some fish from 26 to ed during May-June 1993 than at other times
31 cm SL (Fig. 5). The smaller ripe females found (F2,,oz= 40.17,p < 0.001). Egg weight based on the
late in the season(Fig. 4) may represent the smaller dried eggswas similar in the rivers and in the three
sizeclassesthat had either changedsex earlier in the sampling periods (Table 3). There was no relation-
year or had been born later in the previous season.
234

Fig. 6. Histological sections 125 x of transitional gonad of 18 cm SL 7: toli (Dg sp = degenerating spermatids, Sp = spermatids, St2 = eggsal
early stage of development (stage II)).
 235

ship between fish size and egg size for 7: toli in 1200000 - a
either river. 1000000 -

800000-
.z?
Diet 23 600000 -
2
400000 -
The compositions of the diets of fish 12-20,20-29
and > 30 cm SL collected in 1993 are shown in Table 200000 -

4. All food items were from the zooplankton. The 01~,~,.,~,~,.,~/~,~,

0 50 100 150 200 250 300 350 400 450
most important items in May-June were unidenti-
Length (mm)
fied eggs (mainly calanoid copepod and other crus-
tacean), calanoid copepods and cyclopoid cope-
pods. The diets of small (mainly male) and large (fe-
male) fish were similar, although the small fish ate 1200000 .
b
more smaller organisms such as cyclopoid cope-
1000000 i
pods, bivalve and gastropod veligers and copepo-
dids. The larger fish ate markedly more eggs. In Ju- 800000-
.%?
ly-August 1993 over 90% of the food items in the -0
5 600000 -
diet of all three groups were calanoid copepods. L0
The remaining 16 food items were not numerous 400000-
and contributed relatively little to the diet, although 200000 -
some, such as bivalve and gastropod veligers oc-
01 ' I ' I - I ' / 1 7 I
curred relatively often (Table 4). In September-Oc- 0 50 100 150 200 250 300 350 400 450
tober 1993 the food of the three groups was again Length (mm)
dominated by calanoid copepods, although as in
May-June, eggs were important in the larger size Fig. 7. Relationships between fish length and fecundity for 7: toli
group. It is evident that on all three sampling occa- from the Batang Lassa (a) and Batang Lupar (b).
sions the diet consisted entirely of zooplankton cap-
tured by filter feeding. Calanoid copepods are the ble 5. They had also eaten exclusively zooplankton
most important food of all size groups above a but, unlike the larger fish, ate mainly smaller orga-
length of 12 cm SL. nisms, particularly bivalve and gastropod larvae,
A small number of larvae (11-32 mm) were col- and relatively few calanoid copepods.
lected during October 1993 in plankton samples
from the Batang Lassa. Their diets are shown in Ta-

Table 3. Mean fecundity (+ standard error) and egg dry weight (mg) (k standard error) of Tenualosa foli from the Batang Lassa and
Batang Lupar during 1993.

River Period Fecundity Egg dry wt Sample size

Lassa May-June 494.286+ 13.118 0.13 + 0.002 34

July-August 284.409 k 13,919 0.13 f 0.002 17
Sept-October 307.642 2~25.563 0. I I f 0.007 3
Overall 417,845 + 16.588 0.13 * 0.002 54
Lupar May-June 59 1.775 + 45,350 0.11 f 0.002 17
July-August 374.149 ?c42,760 0.12 + 0.002 ?I
Sept-October 379.669 k 33,774 0.12~0.002 17
Overall 451.266 k 26,333 0. I I ck0.001 54
236

Table 4. Diet of 7: roll in the Batang Lupar and Batang Lassa at three sampling times during 1993 (%N = percentage by numbers, %F =
percentage frequency of occurrence).

Standard length May-June July-August September-October

(cm)
<20 20-29 > 30 <20 20-29 7 30 <20 20-29 7 30

Prey items %N %F %N %F %N %F %N %F %N %F %N %F %N %F %N %F %N %F

Mysidacea - - - - - - - - 0.1 8.3 <O.l 4.7 < 0.1 1.4 - - - -

Cumacea - - - <O.l 0.8 <O.l 8.3 - - <O.l 0.7 - - - -
Calanoida 26.7 20.6 10.3 8.7 17.0 18.2 81.3 10.6 90.7 62.5 96.8 46.5 96.3 27.7 97.4 40.0 46.4 68.8
Cyclopoida 21.7 4.8 6.9 8.7 7.5 6.1 0.7 3.0 0.2 18.8 0.3 9.3 0.3 5.0 0.3 6.7 - -
Harpacticoida 1.7 1.6 3.4 4.3 0.9 1.5 co.1 0.8 <O.l 10.4 - - <O.l 1.4 - - - -
Amphipoda - - 6.9 8.7 0.9 1.5 <O.l 0.8 co.1 14.6 0.1 7.0 <O.l 1.4 - - - -
Ostracoda 1.7 1.6 17.2 13.0 0.9 1.5 - - <O.l 2.1 - - < 0.1 0.7 - - - -
Natant zoea - - - - - - <O.l 0.8 <O.l 2.1 - - - - - - - -
mysis - - - - < 0.1 2.1 <O.l 2.3 <O.l 0.7 - - - -
Brachyura zoea 1.7 1.6 - - - - <O.l 1.5 c 0.1 10.4 <O.l 2.3 < 0.1 0.7 - - - -
megalopa - - - - - - - - co.1 2.1 - - - - - - - -
Gastropoda 15.0 7.9 6.9 8.7 3.8 3.0 6.8 17.4 0.3 33.3 <O.l 4.7 co.1 1.4 - - - -
Bivalvia 15.0 6.3 6.9 4.3 6.6 7.6 5.2 18.9 < 0.1 50.0 1.2 11.6 0.3 12.0 - - 3.6 5.3
Chaetognatha - - - - - - <O.l 1.6 - - - - <O.l 0.7 - - - -
Unid. eggs 5.0 4.8 3.4 4.3 62.2 31.8 - - - - 0.5 11.6 <O.l 2.1 0.8 6.7 50.0 21.1
No. stomachs 63 23 66 132 48 43 141 15 19

Age and growth
Ageing 50 fish from both sites showed that i? toli
live for at least two years (Fig. 8). Males (up to
23 cm) are about 1 year old and females (up to
40 cm) appear to be up to 2 years old. No single
growth curve has been drawn through the entire da-
ta as it appears that growth is not continuous
throughout the life cycle.
Samples of i? tofi larvae (11-32 mm) collected
from SlO in the upper reaches of the Batang Lassa
were aged at up to 100 days old (Fig. 9). Their
growth was linear and quite slow for a tropical fish
species (Milton et al. 1993). Extrapolating from the
growth curve back to where it cuts the y-axis gives
an estimate of the length at hatching: 5.5 mm. This
is consistent with earlier results obtained from eggs
500,

Table5 Diet of 13 young (16-34 mm SL) of Tenualosa roli collect-

ed in plankton samples from the Batang Lassa in October 1993
analysed by numerical percentage (% N) and frequency of oc-
currence of food items (% F).

Prey item %N %F
04
0 100 200 300 400 500 600 700 800 900
Bivalve veligers 16.0 46.2
Age (Increments)
Gastropod veligers 76.1 69.2
Calanoid copepods 3.5 23.1
Copepodids 3.5 15.4 Fig. 8. Age in days (otolith increments) versus fish length for T
Natant zoae 0.3 7.7 toli from the Batang Lassa and Batang Lupar combined. The
Natant mysis 0.6 15.4 curves represent the relationships that best fit the data for the
Number of stomachs 13 juvenile (linear) and adult periods e = females, 0 = males, fish
less than 30 mm could not be sexed).
 237

50
3 6/ -1
(a) growth rate = 0.4Of: 0.01 mm.d
40
(b) growth rate = 0.24f 0.01 mm.d-’
01 I ’ I ’ I I * I
0 20 40 60 80 100
Number of increments
Fig. 9. Growth of 7: toli larvae and juveniles collected from the
Batang Lupar (Ott-Nov 1993) (a) and Batang Lassa (Ott 1993)
@I.
hatched by Sarawak Inland Fisheries staff (Sara-
wak Inland Fisheries Branch unpublished report).
Samples of juvenile 7: toli (32-47 mm) collected
from Pulau Seduku in the Batang Lupar in October
and November 1993 were aged at up to 110 days
(Fig. 9). Their growth rate was significantly greater
than that of the smaller larvae in the Batang Lassa.
The combined ageing data for larvae and adults
suggests that there are at least two phases in the
growth of 7: toli. As we did not collect any fish be-
tween 110 and 250 days old, the growth curves
shown in Fig. 8 are an extrapolation. More data
from intermediate-sized fish will be required to tell
at what age terubok change from linear growth (ju-
venile period) to asymptotic growth (adult period).
From the adult data (SL above 130 mm), it appears
this speciesgrows according to the von Bertalanffy
growth equation with the following parameters:
maximum length (Lm) = 460 mm, growth constant
(K) = 1.28 yr’ and t, = 0.43 yr. There was no differ-
ence in the overall growth rate of fish from either
0
estuary despite the differences shown by the larvae
and small juveniles.
Age validation with embryos hatched in aquaria
showed that otolith increments were formed daily.
Fish removed shortly after hatching had developed
sagittae with no identifiable increments, but six lar-
vae (mean length 6.8 mm, SE 0.3) that were exam-
ined after five days had five increments in their oto-
liths.
’ I
120
Movement and distribution
Nine fish from the Batang Lassa (180-557 days old)
were used for trace-element analysis. The mean re-
sults of the analysis, using five ablations on otoliths
from fish during their first year of life are summar-
ised in Table 6. Only the results for strontium, bari-
um, magnesium and sodium are shown; the other
elements examined (copper and zinc) had low or
variable concentrations. The results show some in-
dividual differences in the composition. Strontium
levels (overall range 1160-2400ppm) declined as
the fish grew: they had higher concentrations at
hatching and at 3 months than at 9 and 12months of
age. The differences between ages are statistically
significant (t test, p < 0.05). Magnesium concentra-
tions showed the opposite trend: it was lowest at
hatching and highest at 12 months of age although
the differences were not significant.
For the 18-month-old fish (380 mm SL) that was
analysed in detail, 33 ablations were made between
the origin and the outer edge of the otolith. At each
point, strontium, magnesium, barium and sodium
were measured (Fig. 10). The results show signifi-
cant differences in the concentration of the ele-
ments from the origin towards the edge of the oto-
lith. Barium showed an annual cycle in concentra-

Table 6. Mean trace-element concentration (in ppm) of 7: roli otoliths from Batang Lassa during the first year of life.

Element Birth 3 months 6 months 9 months 12 months

Sr 2030 k.56 2046 +49 1727 2~108 1564 k53 1690 k 92

Ba 7.0 f 1.4 7.5 * 2.0 7.0 XL2.0 6.9 f 1.8 6.1 lt2.1
Mg 18.4 i. 1.8 20.6 f 1.6 25.2 k 3.0 27.0 k 1.7 78.6 k 23.7
Na 2612 k 120 2580 +197 2737 k 168 2768 f 150 3219 + 168
Sample size 9 8 9 8 0
238

35001 (a) Discussion

The food of juvenile and adult T toli collected in

this study consisted entirely of zooplankton. In this
respect it is similar to 7: ilisha (Halder 1971,Rajya-
lakshmi 1973,De & Datta 1990)in India, but where-
as adults of the latter speciesalso take benthic prey,
no benthic organisms,detritus or sand were record-
ed in the diet of 7: foli. The only ontogenetic change
2 4 6 6 IO 12 14 16 18 20
in the diet of 7: roli is an increase in the size of the
zooplankton prey. It is therefore probable that all
life intervals of is tofi feed in the water column.
Most other alosids,such asAlosa aestivalisin North
America (Creed 1985) and Ethmalosa fimbriatu in

25

0 2 4 6 8 10 12 14 16 18 20
Age(months)

0
1 2 3 4 5 6 7 6 9 10111213141516
Fig. 10. Trace-element concentration (ppm) across the otolith of
an 18 month old 7: toli collected in May 1993 from the Batang
60
Lassa. The last data point on each plot represents element con-
centration at capture.

tion that was positively related to the strontium

content (r* = 0.33; p < 0.001).The concentrations of
strontium and barium were negatively related to
the magnesium content (r* = 0.19 and r2 = 0.14; p < 0
123456 7 6 9 10111213141516
0.05, respectively). Only the magnesiumconcentra-
tion was correlated with the sodium content (r* =
0.21;p < 0.01). 350 -25
300
The distribution of T toli in the Batang Lassa -20
during the study period is shown in Fig. 11. Males
were distributed throughout the estuary,with larger
numbers congregating in the upper reaches where
salinities are low and turbidities high. Femaleswere
caught mainly in the middle and lower reaches.Nei-
ther adults nor larvae were caught in freshwater. 1 2 3 4 5 6 7 6 910111213141516
site
During May-June, larvae and juveniles were found
in the middle reaches, but by September-October
they had moved to the upper reaches. Insufficient Fig. II. Distribution of male (black) and female (shaded) Z toli in
the Batang Lassa from the river mouth (1) to the upper reaches
information was available to plot the seasonaldis- (16) during the three sampling periods. ‘Ibrbidity (NTU) shown
tribution of the sexesin the Batang Lupar. by solid circles and salinity by open circles. Arrows indicate con-
centrations of young.

West Africa (Charles-Dominique 1982) are plank-
tivorous, although Alosa fallax in Europe take
larger prey such as fish and shrimps (Assis et al.
1992)
7: toli spawns in both the Batang Lupar and Ba-
tang Lassa over an extended period, but each fe-
male spawns only once. Individual T ilisha in India,
also spawn only once in a season(De 1980) but tem-
perate Alosa species are usually fractional spawn-
ers (Nigro & Ney 1982,Creed 1985).The fecundities
for T toli are very similar to those reported for 7:
ilisha (De 1980, Pillay & Rao 1962): between about
200000 and 1.5 million. In both species fecundity is
linearly related to fish length. Although the changes
in fecundity through the year might suggest that 7:
toli is a fractional spawner, the histological evidence
strongly indicates a single spawning; there is no evi-
dence of batch spawning. The reasons for the sea-
sonal differences in fecundity are obscure, but in
other Clupeidae may be related to seasonal differ-
ences in food supply (Alheit 1988, Jennings & Be-
verton 1991).
Eggs, embryos and larvae of ir: toli were collected
from the Pulau Seduku area of the Batang Lupar,
and larvae were collected from the upper reaches of
the Batang Lassa. These catches, together with the
catch distribution of females, suggest that spawning
takes place in the middle reaches of the estuaries.
No larvae, juveniles or adults were recorded in
freshwaters beyond the limits of the estuaries. In
this respect 7: toli differs from the anadromous T.
ilisha of India and Bangladesh, which moves into
freshwater to spawn, after which the embryos and
larvae make their way downstream to the sea
(McDowall 1988, Moula et al. 1991). Most other
Alosinae also spawn in freshwater (McDowall
1988).
1: toli were believed to migrate to the sea at the
end of the spawning season (October-November)
(Willman et al. 1989, Pang 1991) as does the closely
related Indian species 7: ilisha (McDowall 1988).
However, there is no evidence of a single migration,
rather it appears that there is a general movement
of fish that have spawned towards coastal marine
areas, with many not leaving the vicinity of the estu-
ary. Age and growth information from the present
study suggest that T. toli does not live longer than
239
about two years. It is therefore probable that the
females die after spawning in their second year of
life, unlike T. ilisha, which lives for at least six years
(De & Datta 1990) or most temperate alosids, some
of which reach 13 years of age (McDowalll988).
The results of this study indicate that T. toli is
probably a protandrous hermaphrodite. Persist-
ence of non-functional pre-vitellogenic oocytes in
males, or differential growth rates of males and fe-
males are possible alternative interpretations of the
data. It is not possible to completely rule out differ-
ential growth rates of males and females as an ex-
planation but the absence of small females and
large males in all habitats and all seasonsprecludes
any valid comparisons of male and female growth
rates. This, together with (a) the markedly bimodal
sex length frequency distributions, and (b) the age-
ing data with males up to one year old and females
from not less than one to at least two years old, and
(c) the histology of the gonads (with evidence of a
rapid decline in testicular tissue and progressive de-
velopment of ovarian tissue) favour the sex change
hypothesis. This would be the first recorded in-
stance of sex change in a clupeid fish and it has im-
portant implications, both for interpreting the life
history, and for the fisheries management and con-
servation of the species. Sex change has not been
recorded in the closely related 7: ilisha, where both
large and small individuals of both sexes are com-
mon. It is noteworthy, however, that the sex ratio of
7: ilisha varies considerably (Jones & Menon 1951)
with females predominant in the larger size classes
and males in the smaller size classes(Rajyalakshmi
1973). This phenomenon has also been reported in
Alosa alosa (Mennesson-Boisneau et al. 1986) and
A. macedonica (Sinis & Kattoulas 1986).
We could find no record of sex reversal in Clupei-
formes in the literature but it is very widespread in
teleosts (Chan & Yeung 1983,Yamamoto 1969) and
exists in a variety of forms controlled by both ex-
trinsic and intrinsic factors (Ross 1990, Reinboth
1980). Diagnosis of sex reversal can pose problems,
but Sadovy & Shapiro (1987) state in their review
that ‘the strongest indicators of protandry are tran-
sitional individuals whose gonads contain degener-
ating testicular tissue and developing ovarian tis-
sue’. If this is supported by bimodal age and length
240
distributions, then sex reversal can be reasonably
inferred. These conditions were met for 7: toli. Sa-
dovy & Shapiro (1987) report that transitional indi-
viduals are relatively uncommon in field collec-
tions, Only 28 transitional gonads were found
among the 667 T. toli examined, but sex change
may be rapid and in protandry there is usually no
persistence of male features in the final female go-
nads (Sadovy & Shapiro 1987). Transitional fish
were found in May-June, August and March sug-
gesting that sex reversal begins after spawning
which may be at any time between May and Octo-
ber. These data also support the view that the spe-
cies is semelparous; if it exhibited iteroparity the
sex reversal would be more likely to occur only to-
wards the end of the spawning season.
There has been much discussion of the adaptive
significance and evolution of sex change in teleosts
(Warner 1988,Ghiselin 1969) and a number of mod-
els have been proposed to predict its occurrence.
Many of these involve behaviour and social orga-
nisation, particularly in sedentary coral reef species
(Ross 1990). For 7: tori, which inhabits a highly
‘physically controlled’ environment (Dutrieux
1991) with extremes of salinity, turbidity and cur-
rent speed, the size advantage and gene dispersal
models of Ghiselin (1969) may be relevant. The for-
mer predicts protandry where the younger stages
must hunt for a suitable environment, but if repro-
ducing when small could do so better if male rather
than female, the situation pertaining to 7: toli which
only has a two year life span. The latter predicts se-
quential hermaphroditism when a change in ecol-
ogy reduces gene flow between populations of a
species, and the isolated populations could suffer
the deleterious effects of genetic drift. This is partic-
ularly relevant to ir: toli whose populations in the
two large Sarawak estuaries appear to be relatively
isolated from each other. Although sex reversal has
not previously been recorded in clupeids, females
of a number of tropical clupeids, e.g. Herklotsich-
thys quadrimaculutus (Williams & Clarke 1983) and
Amblyguster sirm (Conand 1991)reach a larger size
than males. Fecundity is related to body size in most
fishes and hence one advantage of larger body size
is increased fecundity. Kawasaki (1980) has postu-
lated that as a larger body size may decrease the
rate of intrinsic population increase (r) because of
greater age at maturity, one way to compensate for
this would be to increase growth rates and increase
the body size and GSI of females, while keeping
males small with low GSI values. The sex reversal
employed by i? toli may be one way of achieving
this goal, another would be differential growth rates
of males and females.
Estuaries and rivers have lower concentrations of
strontium than marine ecosystems(Ingram & Sloan
1992). If T toli did migrate once a year, as had been
thought, two-year-old fish would have had two peri-
ods in higher salinity. The otolith ablation results
show relatively low, declining strontium levels
(equivalent in this case to strontium/calcium ratios)
during life. Strontium/calcium ratios have recently
been inversely correlated with growth rates (Kalish
1989,Sadovy & Severin 1994). Hence, they could be
expected to increase in a stable environment with
age. There was no regular cycle in Sr in 7: toli that
indicated a seasonal movement into seawater (cf.
Kalish 1990) and the strontium concentrations
(1160-2400 ppm) were similar to those found in
other estuarine species (Edmonds et al. 1992). This
indicates that 7: toli remains in low-salinity water
and does not spend any time in higher salinities.
This does not exclude them from the sea outside
larger Sarawak estuaries, as the marine salinities
are low for several km offshore (Table 1: 15-22 ppt,
see also Lai).*
Our results therefore indicate that T toli may
spend most or all their lives in or adjacent to a single
estuary system. If we are correct, their life cycle
(Fig. 12) would have the following characteristics:
(1) Larvae and juveniles move to the upper reaches
of estuaries, but not freshwater, and grow into
males; (2) during the spawning season (May-Octo-
ber) these males spread through the estuary; (3) af-
ter spawning male fish move to the middle and low-
er reaches and adjacent coast and change to fe-
males. They spawn the following seasonin the mid-
dle reaches of the estuary. It is possible that males
2 Lai. H.C. 1973.A preliminary report on the hydrobiology of the
Sungai Sibu estuary in Sarawak, Malaysia. Pacific Science Asso-
ciation Marine Science Symposium, Hong Kong 1973: 13-16.

Fig. 12. Schematic diagram of the life cycle of 7: toli
that spawn early in the season (April-May) may al-
so spawn late in the season as females; (4) the fe-
males that have spawned die or otherwise disap-
pear.
If this scenario is correct then 7: toli populations
in each estuary and adjacent coastal areas may be
relatively isolated, with little exchange between es-
tuaries. This is important from a conservation and
management point of view becauseit means that in-
dividual estuaries could be overfished and would
not re-stock easily from other estuaries. This theory
is consistent with the fact that 7: tofi are now only
common in a few of the larger estuaries of Sarawak
and have disappeared from the smaller ones (Sara-
wak Inland Fisheries Branch unpublished data).
Acknowledgements
This project was funded by the Ministry of Agricul-
ture and Community Development, Sarawak Gov-
ernment and PPES Aqua (Santubong) Sdn Bhd
(SEDC). The project participants are very grateful
to Datuk Amar Alfred Jabu anak Numpang for his
interest and support; to Leonard Martin Uning,
Henry Jantum and Hang Tuah Merawin for their
support; to William Chang for assistanceand sup-
port. We are also grateful to Tonya Van der Velde
and Margaret Farmer for assistancein the laborato-
ry in Australia and to Simon Chenery and col-
241
leagues at the British Geological Survey, Notting-
ham for carrying out the laser-ablation.
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