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Aquaculture 243 (2005) 229 – 239

Control of reproduction in Nile tilapia Oreochromis niloticus (L.)

by photoperiod manipulation
Amal K. Biswas, Tetsuro Morita, Goro Yoshizaki, Masashi Maita, Toshio Takeuchi*
Department of Marine Science, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan
Received 14 July 2004; received in revised form 1 October 2004; accepted 4 October 2004


A major problem in tilapia aquaculture is the frequent reproduction of female fish, leading to increased competition for
supplemented food and stunted somatic growth. The feasibility of using photoperiod manipulation to arrest the reproductive
performance of tilapia Oreochromis niloticus was therefore examined. Newly hatched O. niloticus were reared in the laboratory
under 12L:12D photoperiod at 28 8C. Fish (230–340 g) were maintained under 6L:6D, 12L:12D and 14L:10D photoperiod at
28 8C during the course of this study. Effect of photoperiod manipulation on reproductive parameters of fecundity, gamete
quality, offspring viability and overall reproductive success were evaluated. Steroid levels (estradiol-17h, E2; testosterone, T)
during the spawning cycles of fish were analyzed on days 1 and 3 postspawning and at 3-day intervals thereafter. A total of 72
female fish from each photoperiod treatment were investigated the changing pattern of E2, T and GSI with fish that have
spawned once, twice and three times. Fish exposed to 12L:12D and 14L:10D photoperiod spawned successfully throughout the
study. Whereas the spawning of fish exposed to 6L:6D photoperiod was arrested after three to four spawning cycles. The
arrestment of spawning in fish exposed to 6L:6D photoperiod was paralleled by a significant decrease in plasma levels of E2
( Pb0.05). By contrast, there was no major difference in T levels among the treatments. These findings suggest that photoperiod
manipulation can be used to arrest the spawning in tilapia O. niloticus. The utility of this in controlling the problem of
overcrowding due to excess offspring in tilapia aquaculture is applicable.
D 2004 Elsevier B.V. All rights reserved.

Keywords: Photoperiod manipulation; Oreochromis niloticus; Reproductive performance; Steroids

1. Introduction istics, the ease with which they can be bred in captivity
and the wide variety of water conditions in which they
Nile tilapia Oreochromis niloticus is one of the most will grow. However, these traits can also create
important food fishes in the world and is prized as an problems. Survival of young is high and grow-out
aquaculture species because of, among other character- ponds can reach too high a stocking density and fish
become stunted, as the supply of food becomes
* Corresponding author. Tel./fax: +81 3 5463 0545. insufficient. Most of these problems can be overcome
E-mail address: (T. Takeuchi). if a technique can be developed to arrest the spawning.
0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
230 A.K. Biswas et al. / Aquaculture 243 (2005) 229–239

A lot of research has been undertaken to examine niloticus. Therefore, the aim of this study was to
potential methods to control the reproduction and investigate the effect of photoperiod manipulation on
growth of tilapia in the last decades. Most of the reproductive parameters such as fecundity, gamete
emphasis has been given to producing monosex male quality, offspring viability and overall reproductive
populations. Several commercially applicable techni- success. And particularly, to determine the feasibility of
ques are used to produce progeny with a high using photoperiod manipulation to arrest the reproduc-
percentage of males: hand sexing (Chervinsky and tive performance of tilapia O. niloticus.
Rothbard, 1982), hormonal sex reversal using andro-
gen (Vera-Cruz and Mair, 1994; Gale et al., 1999),
interspecific hybridization (Mair et al., 1991), produc- 2. Materials and methods
tion of a YY super male line in O. niloticus (Beardmore
et al., 2001). However, there are some limitations in the 2.1. Test animals and rearing conditions
techniques involved such as: being labor intensive,
broodstock contamination, vigilance required in selec- Newly hatched O. niloticus were reared in the
tion and maintenance of broodstock, requirements of laboratory under 12L:12D photoperiod at 28 8C until
high level of control and the consumer acceptance of they reached an appropriate size (200–300 g). We used
hormonally sex reversed fish can be limited even in a recirculating system with covered chambered com-
countries where hormonal applications to food fish are partments for tanks and a mini-computer (Omron,
accepted practice. Kyoto, Japan) was used to manipulate photoperiod.
Finding an effective photoperiod to arrest the The physical structure of the system and control of
incidence of reproduction would solve both the different photoperiod regimes are described elsewhere
problems of consumer acceptance and overcrowding (Biswas and Takeuchi, 2003). Three types of photo-
in culture. The photoperiod is generally accepted as the periods viz. 6L:6D, 12L:12D and 14L:10D were used.
most important factor synchronizing sexual maturation All fish were acclimatized to the photoperiod regimes
and reproduction in fish (Bromage et al., 2001). Use of for 1 month before the sampling commenced. Fish
photoperiod manipulation to alter the incidence of were fed ad libitum once daily with a commercial diet
sexual maturation and the time of spawning has been (crude protein 50.7%, crude lipid 9.3%, Nippon
reported for a number of species (Duston and Bromage, Formula MFG, Yokohama, Japan), 6 days/week.
1988; Randall et al., 1998; Bromage et al., 2001;
Duston et al., 2003; Imsland et al., 2003). However, 2.2. Manual stripping and hatching performance
photoperiod manipulations that have been undertaken
so far to control reproduction were carried out over 24- A total of 12 fish were maintained in 30-l
h cycles of variable light/dark periodicities. There is no aquarium at the ratio of 3 females to 1 male for each
information to control reproduction using a 6-h cycle treatment. The hatching performance was investigated
(3L:3D) and 12-h cycle (6L:6D). Moreover, photo- over three consecutive spawning cycles. Fish were
period manipulations have not yet been practiced to checked every day for signs of reproductive activity
arrest the excessive reproductive activities of O. including turgid papilla, which indicates imminent
niloticus. Attempts to investigate the effect of several spawning. Before stripping the females, males were
photoperiod cycles (3L:3D, 6L:6D, 12L:12D and anesthetized, wiped free of excess water with moist
24L:24D) on metabolism and growth in O. niloticus paper towels and sperm was collected in petri dishes.
were made (Biswas and Takeuchi, 2003). These Artificial seminal fluid (Tris 2.42 g, glycine 3.75 g,
showed a higher growth rate in fish exposed to NaCl 5.52 g, KCl 2.00 g) was added to the sperm and
6L:6D photoperiod (12-h cycle) than those exposed put on ice until use (Müller-Belecke and Hörstgen-
to 3L:3D (6-h cycle), 12L:12D (24-h cycle) and Schwark, 1995). Eggs were stripped into a petri dish
24L:24D (48-h cycle) photoperiod regimes. This by applying gentle pressure on the abdomen in an
higher growth rate was assumed, in part, due to the anterior to posterior direction and were immediately
arrestment of reproduction. If this assumption is true, it fertilized with sperm. Eggs and sperm were mixed by
will give a simple way of controlling reproduction in O. gently rotating the dish and the mixture was left for 5
A.K. Biswas et al. / Aquaculture 243 (2005) 229–239 231

min to allow for fertilization. Sperm used for all Each fish was then stocked individually in an acrylic
treatments was collected from male fish that are aquarium (20 l), after thorough checking to ensure
maintained under 12L:12D photoperiod. the removal of all residual eggs from the mouth. For
Initially, 30 eggs were weighed and 30 more each treatment, fish were sampled on days 1 and 3
subsampled for determination of egg diameters from postspawning (D1 and D3) and then at 3-day
each fish. For diameter, long and short axes of eggs intervals up to D15. At each time point, fish were
were measured using a microscope with a calibrated anaesthetized in 100-ppm 4-ethyl-aminobenzoate
eyepiece graticule. Mean egg diameter was calculated (Wako, Osaka, Japan) and the total body length
for each spawn as follows: mean egg diameter and body weights were measured to the nearest 0.1
(Am)=(length of long axis+length of short axis)/2. cm and 0.01 g, respectively. Approximately 1 ml of
One hundred eggs were placed in each of three blood was collected from the caudal vein using a
eggcups. Eggs in one cup were used to check heparinized syringe equipped with a 25-guage needle
fertilization rate, percentage of eyed larvae and and maintained on ice until centrifugation. Plasma
percentage of hatching larvae. Eggs in the other two was separated by centrifugation at 3000 rpm at 4 8C
cups were used to count the percentage of swim-up for 15 min and stored at 80 8C for subsequent
larvae and the number of gross deformities. Hatching analysis of plasma sex steroid levels. At each
performance was investigated over consecutive spawn- sampling point, the ovaries were removed and
ing cycles to check for changes with time course. A weighed for calculation of the GSI (GSI=ovarian
total of seven fish were used for each treatment to check weight100/body weight). All samplings were per-
the hatching performance over three consecutive formed in the morning (around 0900 h). The
spawning cycles. sampling protocol was repeated until a sample size
of four fish at each sampling point for all treatments
2.3. Blood and gonad samples was reached. A total of 72 female fish from each
treatment were sacrificed to investigate the changing
Three 100-l tanks and ten 20-l acrylic aquaria pattern of E2, T and GSI with fish that have spawned
were used for each photoperiod treatment to inves- once, twice and three times.
tigate the changing pattern of estradiol-17h (E2),
testosterone (T) and gonadosomatic index (GSI) over 2.4. Steroid radioimmunoassay (RIA)
three consecutive spawning cycles. Fish were
stocked into 100-l tanks, one tank for fish spawning The steroid RIA was carried out using the method
once, another for fish spawning twice and another of Aida et al. (1984). Briefly, 100 Al of plasma for
for fish spawning three times. Forty fish were either E2 or T was used for steroid extraction with
stocked into each 100-l tank at a ratio of three diethylether. After the ether was evaporated at 40 8C,
females to one male. An initial observation showed the steroid was reconstituted with 200 Al Gel-PBS
that 14 out of 16 fish exposed to 6L:6D photoperiod solution (0.1% gelatin, 10 mM phosphate buffer, 140
spawned up to the 3 reproductive cycles. Only two mM NaCl, pH 7.5). Reconstituted samples were used
cases were noted where fish spawned up to four for the RIA to determine the levels of the steroids.
reproductive cycles. Therefore, the parameters in fish After the 3H-labeled steroid and the diluted antisera
exposed to all treatments were analyzed up to third solution were added, the mixture was incubated at 4
spawning cycle to investigate the changing pattern in 8C overnight. The following day, a dextran-charcoal
E2, T and GSI. solution [phosphate-buffered saline containing 5 g
The presence of incubating females was checked dextran (Sigma) and 0.5 g charcoal (American Norit,
every morning before feeding. The day of spawning USA) per liter] was added to the mixture to separate
was recorded with the appearance of a gular bulge in the free steroid from bound steroids. After 20 min of
the female, indicating that eggs were being brooded incubation at 48C, the mixture was centrifuged at
in the mouth. The fish were then transferred to a 3000 rpm for 15 min at 4 8C. The radioactivity of
bucket of water and forced to keep their mouths the supernatant was measured with a liquid scintilla-
open for a short while, until the eggs were released. tion counter (1600TR; Packard, USA).
232 A.K. Biswas et al. / Aquaculture 243 (2005) 229–239

2.5. Statistics postspawning) and the differences among treatments

for the same day were compared using ANOVA.
All results shown are the meanFS.D. The results When the ANOVA showed significant differences,
within each group (expressed as a function of days data within each group and among treatments for the

Fig. 1. Mean percentages of fertilization rate (FE), eyed larvae (EL), hatchability (HL) and swim-up larvae (SL) for eggs stripped from fish
exposed to different photoperiod regimes. The asterisks indicate significant differences between groups of fish ( Pb0.05).
A.K. Biswas et al. / Aquaculture 243 (2005) 229–239 233

same day were compared using Tukey’s test of the presence of multiple lipid droplets, a wrinkled
multiple comparison with a 95% significant level. or dimpled appearance, discoloration or clouding,
Prior to the analysis of data, normality was ensured irregular size.
through the Kolmogorov–Smirnov test and Bartlett’s The mean number of eggs per spawning, mean
test was used to establish homogeneity of variance egg diameter, mean egg weight and percentage of
(Zar, 1974). All statistical analyses were carried out deformed embryos are shown in Table 1. There
using the Statistical Package for the Social Sciences were no significant differences in the mean number
(SPSS) program for Windows (v. 10.0). of eggs spawned among the treatments at the 1st
spawning but the number was significantly lower in
fish exposed to 6L:6D photoperiod at the third
3. Results spawning. Although there was no significant differ-
ence, the mean egg diameter was smaller in the fish
Data for mean percentages of fertilization rate, exposed to 6L:6D photoperiod at the third spawn-
eyed larvae, hatchability and swim-up larvae for ing. A significant decrease in the egg weight in fish
eggs stripped from fish exposed to different treat- exposed to the 6L:6D photoperiod was observed at
ments are presented in Fig. 1. There were no major the third spawning ( F=16.84, P = 0.02). The fish
differences in the mean fertilization rate, percentage exposed to 6L:6D photoperiod also showed a higher
eyed larvae, hatchability and percentage swim-up percentage of deformed embryos when the eggs
larvae among the treatments at the 1st spawning from this fish were hatched than that in fish
time. At the second spawning, the eggs stripped exposed to 12L:12D and 14L:10D photoperiod.
from the fish exposed to 6L:6D photoperiod were The variation in plasma E2 levels among treat-
fertilized at a near 100% level, but the percentage ments at the various spawning cycles is shown in Fig.
of eyed, hatching and swim-up larvae was signifi- 2. Fish exposed to different photoperiod was
cantly lower than fish exposed to 12L:12D and spawned once in 15 days. The plasma levels of E2
14L:10D photoperiod. Although the eggs from the were similar among the treatments on the different
fish exposed to 6L:6D photoperiod were fertilized at sampling days after the 1st spawning cycle. The
the third spawning, no eyed, hatching or swim-up plasma levels of E2 in fish exposed to 12L:12D and
larvae were observed. Most of the embryos were 14L:10D photoperiod were more or less the same
dead 40-h after fertilization. Poor quality of eggs after the second and third spawning cycles. Whereas,
were observed in fish exposed to the 6L:6D the levels in the fish exposed to 6L:6D photoperiod
photoperiod at the third spawning as evidenced by gradually decreased during the second and third

Table 1
Number of eggs per spawning, egg diameter, egg weight and percentage of deformed embryos in O. niloticus exposed to different photoperiod
regimes at different spawnings (n=7)
Spawning Photoperiod Fish length Fish weight Number of Egg diameter Egg weight Deformed
(cm) (g) eggs/spawning (Am) (mg) embryos (%)
1st 14L:10D 19.4F1.2 234.5F50.7 1853.6F124.7a 2315.3F210.3 4.1F0.3a 2.6F0.4a
12L:12D 19.3F1.0 241.3F42.6 1816.4F133.5a 2217.7F196.8 3.9F0.4a 4.3F1.0ab
6L:6D 19.6F1.2 245.7F45.7 1887.7F119.2a 2192.5F240.2 4.0F0.4a 5.4F0.9ab
2nd 14L:10D 19.8F1.2 275.3F48.1 1903.1F135.5a 2356.3F197.6 4.2F0.5a 3.2F0.5a
12L:12D 19.8F1.1 277.2F45.3 1943.2F108.4a 2342.6F153.8 4.1F0.3a 5.2F1.2ab
6L:6D 20.0F1.3 291.2F51.6 1588.5F116.6ab 1822.4F161.9 3.3F0.5ab 7.3F1.3b
3rd 14L:10D 20.5F1.2 321.7F53.0 2081.4F130.3a 2306.9F202.6 4.2F0.4a 2.3F0.3a
12L:12D 20.6F1.1 322.3F47.2 1968.2F112.5a 2252.2F160.2 4.2F0.4a 5.7F1.0ab
6L:6D 20.5F1.2 343.4F45.8 1213.7F105.3b 1748.4F140.2 2.5F0.3b 0*
Means within each column followed by superscripts not sharing a common letter are significantly different ( Pb0.05).
* The egg from fish exposed to 6L:6D photoperiod could not hatch at third spawning. Therefore, the value remains blank.
234 A.K. Biswas et al. / Aquaculture 243 (2005) 229–239

Fig. 2. Changes in plasma levels of estradiol-17h (E2) in the reproductive cycle of tilapia O. niloticus maintained in different photoperiod
regimes as a function of days postspawning. Data are presented as the meanFS.D. for four fish at each sampling point for each treatment. Fish
exposed to 12L:12D and 14L:10D are indicated by the similar letter (a, b and c) since there were no significant differences between the groups.
For each day, mean values with different letters in the same group of fish are significantly different ( Pb0.05). The asterisks indicate significant
differences among groups of fish for the same day.

spawning and showed a significantly lower levels in days in the fish exposed to 6L:6D photoperiod were
all sampling days except D1 after the third spawning progressively lower and the peak activity had almost
cycle ( F=15.55, P=0.001). In all three spawnings, disappeared by the third spawning.
the E2 levels remained low immediately after spawn- In all treatments, the plasma T levels showed a
ing and then increased significantly to reach a peak similar pattern during the reproductive cycle at all
on day 9 in fish exposed to 12L:12D and 14L:10D spawnings (Fig. 3). Although statistically insignificant,
photoperiod. But the E2 levels on different sampling the plasma T levels in fish exposed to the 6L:6D
A.K. Biswas et al. / Aquaculture 243 (2005) 229–239 235

Fig. 3. Changes in plasma levels of testosterone (T) in the reproductive cycle of tilapia O. niloticus maintained in different photoperiod regimes
as a function of days post-spawning. Legends are as in Fig. 2.

photoperiod were higher than those exposed to the sively lower at all sampling days after both the
other treatments. The plasma T levels in all treatments second and third spawning cycles. The mean value at
increased continuously from D3 to D15, despite a days 12 and 15 in fish exposed to 6L:6D photo-
plateau between days 3 and 6 for all three spawning period was significantly lower than the fish exposed
cycles. to 12L:12D and 14L:10D photoperiod for both the
In the first spawning, GSI in all treatments was second and third spawning cycles ( F=28.35,
similar at different sampling days (Fig. 4). Mean GSI P =0.01). In all treatments, GSI appeared to decrease
in fish exposed to 12L:12D and 14L:10D photo- slightly during the first 3 days after spawning.
period was also more or less the same after the Afterwards, the GSI value increased continuously
second and third spawning cycles but the value in until the end of the cycle in all treatments with
fish exposed to 6L:6D photoperiod was progres- significant depressed levels in fish exposed to 6L:6D
236 A.K. Biswas et al. / Aquaculture 243 (2005) 229–239

Fig. 4. Changes in GSI of O. niloticus exposed to different photoperiod regimes during the reproductive cycle. Legends are as in Fig. 2.

photoperiod after the second and third spawning after three to four spawning cycles. Therefore, it
cycles. shows a possible way of controlling frequent
spawning in tilapia O. niloticus. This will help to
solve the problems of overcrowding that has
4. Discussion happened frequently in O. niloticus culture farms.
Photoperiod manipulation is widely used to control
This study showed that the fish exposed to reproduction in a range of fish species. It is
6L:6D photoperiod could not successfully spawn generally accepted as the most important factor
A.K. Biswas et al. / Aquaculture 243 (2005) 229–239 237

synchronizing sexual maturation and reproduction in the cortisol treatment affected the production of E2
fish (Bromage et al., 2001). first and the low level of E2 in turn retarded the
The higher growth in fish exposed to 6L:6D ovarian growth due to reduced vitellogenesis. The
photoperiod in our previous study (Biswas and significantly lower egg weight and smaller egg
Takeuchi, 2003) may be due to the arrestment of diameter in fish exposed to the 6L:6D photoperiod
sexual maturation with a resultant gain in growth. may be due to the lower E2 levels, which in turn
This is supported by the significantly lower GSI and reduce vitellogenin production. Because, the contri-
the inability of fish to spawn after three to four bution of vitellogenin sequestration to oocyte growth
spawning cycles in fish exposed to the 6L:6D photo- is well recognized (Tyler and Sumpter, 1996) as is the
period. The arrestment of gonadal development and role of E2 in stimulating vitellogenesis (Specker and
spawning of fish in the 6L:6D photoperiod treatment Sullivan, 1994).
may also indicate that the energy sources from the In the third spawning cycle, levels of E2 signifi-
feed that would normally be used in the development cantly decline while those of T continue to increase in
of gonad and eggs are shunted into somatic growth fish exposed to the 6L:6D photoperiod possibly
with a resulting added weight gain in fish exposed to indicating a reduction in the aromatase (a mem-
6L:6D photoperiod as shown in Biswas and Takeuchi brane-bound enzyme which is responsible for the
(2003). This is similar to the observations of Kissil et conversion of testosterone to 17h-estradiol) activity
al. (2001) in seabream by photoperiod manipulation. (Lamba et al., 1983; Winkler and Wade, 1998;
A long day photoperiod in European sea bass and Campbell et al., 1976).
gilthead seabream, and continuous light in the This study was designed in indoor tanks. The
Atlantic cod have been used to delay or stop sexual relevance of these results needs to be investigated in
maturation or spawning and enhance growth (Karlsen commercial aquaculture. The photoperiod technique
et al., 1999; Kissil et al., 2001). Bromage et al. (1984) used in this study may also be designed in outdoor
delayed spawning of rainbow trout using constant tanks economically. For example, heavy duty poly-
short days (6L:18D), and in a separate trial with this thene or butyl linings over a single metal, plastic pipe
same photoperiod, demonstrated that they grew better or wooden framework may provide a cheap and
on the same feed ration than constant photoperiod or effective method of blacking out the culture farms.
long day (18L:6D) treated fish. In Atlantic salmon, a In conclusion, the present study showed a simple
30% increased growth and appetite have been way of controlling the spawning in Nile tilapia O.
achieved with a 57% reduction in grilsing (Hansen niloticus by photoperiod manipulation, which could
et al., 1992; Taranger et al., 1999; Porter et al., 1999) be possibly used to control overcrowding. Recently,
due to photoperiod control. Desprez et al. (2003) produced monosex male using
The arrestment of reproduction within three to four natural androgen as an alternative to use synthetic
spawning cycles after onset of photoperiod in fish hormone. However, this may still affect the consumer
exposed to the 6L:6D photoperiod is due to the acceptance since exogenic hormone is involved.
depressed levels of E2. Low levels of plasma E2 have Biswas and Takeuchi (2003) showed higher growth
also been measured during the regressed stages of the rates in fish exposed to 6L:6D photoperiod and, in
sexual cycle of striped mullet, Mugil cephalus (Dindo addition, this study showed the arrestment of repro-
and MacGregor, 1981), Tilapia aurea (Terkatin- duction in fish exposed to 6L:6D photoperiod.
Shimony and Yaron, 1978), brown trout, Salmo trutta Therefore, by manipulation of the photoperiod,
(Billard et al., 1978), rainbow trout, Salmo gairdneri enhanced growth and arrestment of reproduction of
(Van Bohemen and Lambert, 1981), and Atlantic Nile tilapia can be achieved.
salmon, Salmo salar (Taranger et al., 1999). Plasma
E2 plays a dominant role in the reproductive process.
In teleosts, the induction of vitellogenin synthesis by Acknowledgements
the liver is a function already ascribed to E2 (Van
Bohemen et al., 1982). In tilapia Oreochromis The expenses of the present study were defrayed
mossambicus, Foo and Lam (1993) postulated that in part by a Grant-in-Aid for Scientific Research
238 A.K. Biswas et al. / Aquaculture 243 (2005) 229–239

(No. 13460145) from the Ministry of Education, mossambicus, by cortisol implantation. Aquaculture 115,
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