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Effects of water temperature on growth and sex

ratio of juvenile Nile Tilapia Oreochromis
niloticus (Linneaus) reared in geothermal
waters in southern Tunisia

Article in Journal of Thermal Biology February 2008

DOI: 10.1016/j.jtherbio.2007.05.007

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 ARTICLE IN PRESS

Journal of Thermal Biology 33 (2008) 98105

www.elsevier.com/locate/jtherbio

Effects of water temperature on growth and sex ratio of juvenile

Nile tilapia Oreochromis niloticus (Linnaeus) reared in geothermal
waters in southern Tunisia
M.S. Azaza, M.N. Dhra ef, M.M. Kra em
National Institute of Marine Sciences and Technologies, 2025 Salammbo, Tunisia
Received 28 March 2007; accepted 21 May 2007

Abstract

Growth of juvenile Nile tilapia, Oreochromis niloticus (Maryut strain) was studied under laboratory conditions. Four thermal regimes
(22, 26, 30, and 34 1C) were tested on 480 20-day-old fry.
Signicant (Po0.05) effects of temperature on growth were observed. Results showed that the nal mean weight was signicantly
higher at 26 and 30 1C than at 22 and 34 1C. Feed conversion ratio (FCR) and daily weight gain (DWG) were better at 26 and 30 1C. At
all temperatures, survival rates were not affected. These results suggest that the best growth and feed utilization of O. niloticus juveniles
may be higher at 26 and 30 1C.
A second experiment was performed to assess the effect of ambient water temperature during the period of sex differentiation on the
sex ratio. Results showed that the high-temperature (almost 36.90 1C) treatments yielded a signicantly higher proportion of males
(64.2080%) with lower survival rates (6081%), whereas the sex ratio of progenies reared at temperature below 36 1C never deviated
signicantly from the balanced sex ratio.
This study provided clear evidence that the exposure of progenies to masculinizing temperature may signicantly decrease the
survival rate of sh.
r 2007 Elsevier Ltd. All rights reserved.

Keywords: Temperature; Growth; Temperature-dependent sex determination; Sex ratio; Survival rate; Thermosensitivity; Geothermal water; Nile tilapia;
Oreochromis niloticus; Maryut strain

1. Introduction Growth of sh is a complex process affected by many

Tilapias are members of the Cichlidae family which are a
group of warm water sh and have become the most
important warmwater aquaculture sh group in the world
(FAO, 2003). In Tunisia, Tilapia was rst introduced in 1999
in order to develop the enormous geothermal water resources
in the south of the country. Their tropical and subtropical
origins are clearly reected in their thermal preferendum;
these sh do not grow well at temperature below 16 1C and
cannot usually survive for more than a few days below 10 1C
(Chervinski, 1982), but they are remarkably tolerant to high
temperatures, up to 40 1C (Azaza, 2004).
Corresponding author. Tel./fax: +216 75 27 25 11.
E-mail address: med.azaza@instm.rnrt.tn (M.S. Azaza).
behavioral, physiological, nutrional, and environmental
factors; however, temperature is recognized as one of the
most important single abiotic factor affecting growth, food
intake, and food conversion of sh (Martinez et al., 1996).
In the natural aquatic systems, sh moves into deeper
water when surface water temperature decreases or
increases beyond their preferred range (Brett, 1979). In
captivity, the determination of optimal environmental
conditions to reach the best growth performance is
essential for the maximization and optimization of its
production. The effects of water temperature on growth
and development of sh have been well documented for
many species (El-Sayed et al., 1996; Van Ham et al., 2003;
Anelli et al., 2004; Campinho et al., 2004; Chatterjee et al.,
2004; Larsson and Berglund, 2005). For Nile tilapia, most

0306-4565/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtherbio.2007.05.007
 ARTICLE IN PRESS
M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105
studies used sh at a late stage of development when
factors other than temperature may have had permanent
effects on growth characteristics (Hauser, 1977; Platt and
Hauser, 1978). No detailed information is available on the
optimum temperature requirement of Nile tilapia fry.
Furthermore, in captivity, it may be possible to control
and maintain optimal rearing temperature according to
species requirements. Temperature control is essential for
optimizing the development of younger stages, as especially
the earlier stages of growth are more sensitive to thermal
conditions than other stages.
In animal kingdom, there are many examples of
temperature-dependent sex determination, principally in
numerous reptilian species (Ewert and Nelson, 2003) or
amphibians (Dournon et al., 1990). In sh species,
temperature sex determination was rst demonstrated by
Conover and Kynard (1981), who found that fry of
Atlantic Silverside Menidia menidia developed as females
at lower temperatures and as males at higher temperatures.
More recent studies provided evidence that water tem-
perature also governed the phenotypic sex of genus
Oreochromis. It was found that high-temperature treatments
during early developmental stage (labile period) cause a
signicant deviation of sex ratio in favor of males in
Oreochromis aureus (Desprez and Melard, 1998; Baras et
al., 2000) and O. niloticus (Baroiller et al., 1996a, b; Baras et
al., 2001). In genus Oreochromis spp., rearing monosex male
is more advantageous for aquaculturists, because males grow
faster than females (Melard, 1986; Toguyeni et al., 1996;
Baras and Melard, 1997), and also increases production by
preventing mating so that the sh allocate higher proportion
of energy toward growth (Oldeld, 2005).
A review of the literature, in previous studies, has shown
that there is a huge variation of thermosensitivity of
progenies of Nile tilapia, which is explained by the
variability of the strains and populations used, as shown
by Baroiller et al. (1996b) in the Bouake strain, by Baras
et al. (2001) in the Menzala strain and by Tessema et al.
(2006) in populations of Lake ManzalaEgypt and Lake
RudolphKenya. However, no study evaluated the
efciency of masculinizing thermal treatments in the
Maryut strain used in Tunisia.
The present study was carried out with two consecutive
experiments and aimed, in the rst experiment, to
determine the effect of ambient water temperature on
growth, feed utilization efciency, and fry survival rates,
and, in the second experiment, to assess the effect of
different temperatures on sex ratio of progenies of Nile
tilapia, Maryut strain, during their early life stages.
2. Material and methods
2.1. Experimental procedures
This study was conducted at the sh-culture research
station of the National Institute of Marine Sciences and
Technologies (INSTM) at Bechima, Gabes, Tunisia.
99
2.1.1. Fish
The sh used in this experiment belonged to the
Maryut strain, which had been introduced in Tunisia
from stock reared in the Marine Center of Tajoura (Libya)
(Turki and Kra em, 2002).
2.1.2. Experiment 1: effect of water temperature on growth
Twenty-day-old Nile tilapia fry, weighing 0.25470.002
(SE) g (n 480), were obtained from one female and were
dispatched in 16 glass aquaria (45-L capacity) at an initial
stocking density of 30 fry per aquarium. Photoperiod was
kept at a constant 12:12 (light:dark) ratio throughout the
study. Each treatment was tested in four replicates
simultaneously. Variations in average weight between
different aquariums were minimized as necessary by
redistribution of sh to ensure a uniform starting weight.
Temperature treatment was carried out in four recirculat-
ing systems, each with a separate temperature regulation
(reservoir tank), biolter (model oase, ltoclear UWC
9/11W), UV-sterilization lamp and four glass aquaria.
A 1 kW immersion thermostatic heater was installed in
each reservoir tank to maintain the preselected water
temperature. Four different temperature regimes were
maintained at 22, 26, 30, and 34 1C.
Fecal matter removal was accomplished with a submerged
ltration in each aquarium (Rena, Filstar). Supplemental
aeration was provided to maintain dissolved oxygen levels
near saturation. In all aquaria, water was constantly replaced
by continuous ow at the rate of 1 L min1 to provide
oxygen and remove excess nitrogenous wastes.
Fish fry were acclimated to experimental system for 1
week prior to the start of experiment. Experimental water
temperatures were attained gradually by heating or cooling
water at 1 1C day1. All sh were hand fed to apparent
satiation six times daily between 08.00 and 18.00 h every
2 h. All sh in each aquarium were anesthetized (MS-222,
50 ppm), to reduce stress and to improve accuracy of the
weighing, then weighed and measured to the nearest 0.001 g
and 0.1 cm, respectively, at the beginning and at the end of
the experiment. Mortality was recorded daily.
Fish were fed on a diet of formulated sh meal, soybean
meal, maize meal, soybean oil, vitamin, and mineral
premix. The feed contained 40% crude protein. The
ingredients were milled and mixed in a food mixer. Next,
water was added gradually until a desirable paste-like
consistency was reached, pelleted through 3 mm holes in a
kitchen meat grinder, and then sun-dried. The dry pieces of
feed were then ground to obtain suitable particle size and
stored in a freezer at 20 1C in polythene bags until
required. Initially sh were fed powder diets to accom-
modate the fry, and as the experiment progressed the size
of pellets was increased.
2.1.3. Experiment 2: effect of water temperature on sex
ratio and survival rates
In the second experiment, we studied the effect of
ambient water temperature on sex ratio during the period
 ARTICLE IN PRESS
100 M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105

of sex differentiation (rst 20 days after yolk sac Table 1

resorption) and was carried out in the same recirculating Mean initial body weights (IBW), total lengths (Lt), coefcient of
variation of initial body weights (CVIBW %), and biomass (Bi) for
system described above. This study was conducted in 16
Oreochromis niloticus at the beginning of the experiment under different
glass aquaria (45 L). Four different temperature regimes levels of temperature treatments
(19, 32, 34, and 36.5 1C) were applied to sibling fry and
each temperature treatment was tested in four replicates Temperature IBW (g) CVIBW (%) Li (cm) Bi (g)
and the fry of the same parent was used as one replicate. (1C)
Water temperature for each aquarium was progressively 22 0.25470.001 4.75670.649 2.11570.013 8.13770.020
cooled or warmed to adjust and maintain the desired level 26 0.25470.002 5.01270.923 2.09270.009 8.12770.013
of temperature (1937 1C) at a rate of 1 1C per 2 h in order 30 0.25370.001 4.53470.768 2.10170.012 8.15070.049
to avoid thermal shock. Experimental temperature was 34 0.25570.002 5.54371.123 2.10370.003 8.10370.037
maintained throughout 28 days (after Baroiller et al., Data are expressed as mean7SEM of four replicate determinationsa.
1996a, b). At the end of the experiment, water temperature IBW: initial body weight; CVIBW (%): coefcient of variation; Li: initial
was adjusted progressively at 28 1C (1 1C per 2 h). From length; Bi: initial biomass.
a
each aquarium, sh were transferred into larger tanks No signicant differences among treatment groups were observed for
any of these parameters (P40.05).
(400 L) and held at 28 1C to promote growth. When
juveniles reached 20 g, they were removed for sexing
(genital papilla). Coefficient of condition : Kc 103 mean weight=length3 :

CV was calculated to determine the extent of assymetry in

2.2. Water chemistry
Water quality parameters from every aquarium were
monitored daily throughout the experimental period.
Water temperature, levels of pH (MP120 METTLER),
and dissolved oxygen were measured twice daily (8:00 and
17:00 h) using an oxythermometer (WTW/OXI 96). Water
analysis for N-NH+ 
4 and N-NO2 were colorimetricaly
determined, twice weekly, with indophenol blue and
sulfanilamide methods. For the rst experiment, water
temperature in each treatment remained nearly constant
throughout the experimental period (ranges: 21.622.5 1C;
25.626.4 1C; 29.530.2 1C, and 33.634.8 1C), dissolved
oxygen ranged between 4.81 and 6.79 mg L1, total
ammonia ranged between 0.08 and 0.84 mg L1, and pH
ranged between 6.98 and 7.41.
2.3. Analytical procedures
Growth performance was analyzed in terms of specic
growth rate (SGR), body weight gain per day (BWG), feed
conversion ratio (FCR), feed intake (FI), coefcient of
condition, and coefcient of variation (CV). The following
formulae were used:
SGR % 100 dt1 Ln FBW=IBW;
where dt is the duration of the experiment in days; FBW
and IBW are the nal body weight and initial body weight,
respectively.
BWG g=day FBW  IBW=dt days;
the size distribution of the batches:
CV standard deviation of weight=mean body weights:
Initial mean body weights, and the CV of IBW,
length, and biomass did not differ signicantly (P40.05,
ANOVA) among treatment groups (Table 1).
2.4. Statistical analysis
Results were subjected to a one-way ANOVA and the
signicance of the difference between means was tested
using Duncans multiple range test. Differences were
deemed to be signicant at Po0.05. The procedure used
was GLM of the software STATISTICAs version 5.1
(Statsoft, Tulsa, USA). Values are expressed as mean7
means standard error. In the case where homogeneity
variances were not found, the non-parametric Mann and
Whitney test (U-test) was performed. The chi-square test
(w2) was used to determine whether the observed sex ratio
differed from the expected 1:1.
3. Results
3.1. Experiment 1: effect of temperature on growth
3.1.1. Diet acceptance
The acceptance response for the diet in the sh varied in
a remarkable way with the experimental temperature. The
sh at 22 1C fed slowly, compared with all other
temperatures.

Relative growth weight RGW; % 100 FBW  IBW=IBW;

3.1.2. Growth performance
The nal body weight, total length, survival rates, weight
FCR g=g dry matter FI=live BWG; gain, nal biomass, SGR, daily weight gain (DWG), FCR,
CV of nal weight, and condition factor for all groups are
FI g=day g dry matter=day; given in Table 2.
 ARTICLE IN PRESS
M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105 101

At the end of the experiment, the mean body weights sexing. The percentage of males reared over the rst 28
ranged 6.4619.16 g among treatments and were signi- days of exogenous feeding at temperatures between 19 and
cantly (Po0.05) greater at 26 and 30 1C than at 22 and 34 1C never deviated signicantly from equilibrated sex
34 1C (Table 2). Final mean lengths ranged 7.299.90 cm ratio. However, the sex ratio was skewed signicantly
among treatments and showed the same trends as observed (Po0.01 and Po0.001) in favor of males in all progenies
for weights. The growth rates over the 60 experimental reared at circa 36.5 1C (6480% of males).
days, expressed as mean DWG and SGR, signicantly
(Po0.05) increased, from a minimum (0.103 g day1 and Table 3
5.38% bw day1, respectively) at 22 1C to a maximum Effects of ambient water temperature on survival rate (SR %) and sex
(0.31 g day1 and 7.18% bw day1) at 30 1C. ratio in 16 groups (100 sh each) of Oreochromis niloticus from 4
Survival rates throughout the experiment ranged progenies, during the rst 28 days of exogenous feeding
8790% among treatments and were similar at the 0.05 Replicate Temperature Survival Males Females Test
level of signicance of all treatments. (1C) (%) (%) (%) w2
Mean7SD 1:1
3.1.3. Feed utilization and feed conversion ratio
M1XF1 19.3870.90 62 43.55 56.45 NS
Highly signicant effects of temperature (Po0.001) on 32.2970.42 98 46.94 53.06 NS
feed consumption were observed. Feed consumption 34.3870.29 74 48.65 51.35 NS
increased with increasing temperature until 30 1C. Food 36.4870.35 81 64.20 35.80 **
conversion ratio differed between groups (Po0.05) and M2XF2 19.1570.87 67 56.72 43.28 NS
decreased from 2.85 at the lowest temperature (22 1C) to 31.9970.55 86 46.51 53.49 NS
1.96 at 30 1C (Table 2). 34.0870.42 66 45.45 54.55 NS
Increasing CV of FBW was observed at all temperatures. 36.5170.41 78 74.36 25.64 ***
But at the end of the experiment a signicant (Po0.01) M3XF3 19.2170.99 74 46.15 53.85 NS
effect was observed between the temperature treatments of 31.9270.71 94 51.06 48.94 NS
30 and 34 1C and the other temperatures (22 and 26 1C, 34.1370.67 79 51.89 48.11 NS
Table 2). Fish reared at 30 and 22 1C had the highest and 36.7070.45 81 74.07 25.93 ***
the lowest condition factor, respectively. The other M4XF4 19.5470.78 72 44.44 55.56 NS
treatments had intermediate and similar (P40.05) condi- 32.0670.63 95 53.68 46.32 NS
tion factors. 34.2270.62 87 45.98 54.02 NS
36.8370.35 60 80.00 20.00 ***

3.2. Experiment 2: effect of temperature on sex ratio and **Po0.01.

survival rates ***Po0.001.
P is the probability of accepting the hypothesis that sex ratio is balanced.
Survival data relate the % of sh surviving after 28-day-temperature
3.2.1. Sex ratio variance treatment.
Table 3 summarizes the survival rates after temperature w2 represents the deviation of sex ratio of the treated progeny from that of
treatment and percentage of males and females after balanced (1:1) sex ratio.

Table 2
Effects of 22, 26, 30, and 34 1C water temperature on mean nal body weight (FBW), mean total length (Lt), survival rate (SR), nal biomass (FBi),
specic growth rate (SGR), daily weight gain (DWG), food conversion ratio (FCR), relative growth rate (RGW), coefcient of variation (CV), feed intake
(FI), and coefcient of condition (Kc) of O. niloticus during the trial period

Variables Temperature (1C)

22 26 30 34
a b c
FBW (g) 6.46370.275 14.08370.318 19.16070.430 10.63070.162d
Lf (cm) 7.29570.122a 9.55670.185b 9.90270.212b 8.54170.049c
SR (%) 87.33372.027a 90.66672.027a 89.66671.333a 87.33372.027a
FBi (kg) 0.18070.060a 0.40870.013b 0.59470.080c 0.29770.092d
SGR (%/day) 5.38370.067a 6.64970.051cd 7.18270.042c 6.22170.028d
DWG (g/day/sh) 0.10370.004a 0.22470.007b 0.31070.007c 0.17370.002d
FCR (g/g) 2.84670.047a 1.96970.034b 1.96070.049b 2.62770.050a
RWG (%/day) 40.74671.856a 90.86472.172b 123.71872.490c 68.35570.856d
CVFBW (%) 41.78772.650a 37.61071.634b 26.05672.081c 26.99372.085c
FI (g/day/sh) 0.30270.012a 0.44170.009b 0.62370.011c 0.45370.005ba
Kc 1.66670.095ac 1.61670.017a 1.97970.083b 1.70670.011c

Data are expressed as mean7SEM of four replicate determinations.Values (means of four trials) in the same line having different letters (a, b, c, and d) are
signicantly different (Po0.05, Duncans multiple range test).
 ARTICLE IN PRESS
102 M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105
Table 4
Effect of temperature treatment on meana survival rates of O. niloticus,
over a 28-day treatment period
Temperature (1C) Survival rate
means7SE (%)
19 60.0077.29a
32 93.2572.56b
34 76.5074.40ab
36.5 75.0075.05a
Means having different letters are signicantly (Po0.05) different (U-test).
a and implies that mobilization of body protein and lipids for
Means of four replications (Mean7SE).
3.5. Survival rates
Table 4 summarizes the mean of survival rates of four
replications for each temperature treatment. The mean
survival rates in the batches reared at 19 and 36.5 1C were
signicantly (Po0.05; U-test) lower than those observed at
30 and 32 1C ( 60.0077.29 and 7575.05 vs 91.7572.25
and 93.2972.56, respectively).
4. Discussion and conclusions
O. niloticus is known to tolerate high temperatures. It
cannot tolerate for a long period water temperature
between 10 and 15 1C (Ballarin and Hatton, 1979), and
does not survive below 10 1C (Chervinski and Lahav,
1976). The optimum temperature for feeding, growth and
reproduction is between 22 and 30 1C (Caulton, 1982),
while good growth was recorded in the upper portion of
this range (Hauser, 1977). Thus, at higher or lower
temperatures, feeding and growth rates are reduced, and
at 20 1C or less, feeding and growth are stopped (Caulton,
1982).
Studies on several sh species have revealed that in the
temperature range tolerated by sh, growth rates increase
with increasing temperature and show a parabolic pattern
(Xiao-Jun and Ruyung, 1992; Watanabe et al., 1993;
Larsson and Berglund, 2005). When experimental tem-
perature reaches the upper extreme of the tolerance range,
performance of growth decreases. This depression of
growth is due to the higher energy cost for maintenance
metabolism and seems to be related mainly to a loss of
appetite. Results of our study show that performance of
growth is better at 34 1C than at 22 1C, which conrms the
thermophilic character of O. niloticus.
In the present study, growth performance of O. niloticus
reared at 22, 26, 30, and 34 1C was temperature dependent.
Generally, growth rate increased with increasing water
temperature and reached its optimal at 30 1C, then declined
signicantly (Po0.05) at 34 1C. The effect of temperature
on growth depends on the interaction between food
consumption and metabolism (Brett, 1979). This is mainly
due to the feeding activity (feed consumption) and
metabolic scope, where a substantial amount of feeding
energy is used to cover maintenance metabolism at the
expense of somatic growth (Brett, 1979). This reexion
supports the results of body composition of O. niloticus
reared at different water temperatures. El-Sayed et al.
(1996) demonstrated that body lipid and protein content
were signicantly decreased in lower water temperature
rearing, suggesting that body protein and lipid content was
directly used as an energy supply to meet the increasing
physiological demands. This is in agreement with the
ndings of Caulton and Burzell (1977) and Caulton (1982),
catabolic processes is linked, in a large amount to
deterioration of environmental rearing conditions. On the
other hand, it is noticeable that sh fed at low temperatures
have a lower daily food intake than those fed at higher
temperatures. This may be explained by the fact that sh
maintained at higher temperatures present a greater
efciency of assimilation, as demonstrated by Caulton
(1978). According to this author, the mean energy content
of the feces of Tilapia rendalli followed the expected trend,
with a greater energy residue being voided by sh fed at
lower temperature and, as a corollary, assimilation less
efcient, suggesting that digestibility and assimilation
efciency are, thus, temperature dependent through enzy-
matic kinetics. Watanabe et al. (1996) reported 25 1C to be
the optimum temperature for nutrient digestibility in
tilapia, O. niloticus (L.) and carp, C. carpio. Shrable et al.
(1969), working on channel catsh, Ictalurus punctatus
(Ranesque), reported that digestion is more rapid between
26.6 and 29.4 1C than between 21.1 and 23.9 1C. In catsh,
Heteropneustes fossilis (Bloch), digestibility was reported to
be better at 28 1C than at 18 1C (Usmani and Jafri, 2002).
This may have occurred in sh at low water temperature,
thereby resulting in poor growth performance in the sh.
The reduced growth performance at 34 1C could be
attributed to the high rate of gastric evacuation, as
reported by Elliot (1972), who observed a positive
correlation between water temperature and the rate of
gastric evacuation in sh. It has been suggested that higher
temperature accelerates the rate of passing digesta through
the intestinal tract, thus reducing the digestibility and
assimilation of nutrients, signifying that at high tempera-
ture, physiological processes associated with digestion and
nitrogen retention function are less efcient in sh.
In the present experiment, we observe maximum growth
of O. niloticus at 30 1C in relation with maximum feed
consumption and better FCR as shown in Table 2. This
temperature value also produced more homogeneous
batches indicated by lower coefcients of variation of nal
body weights. Although, initially they showed the same
CVs with other groups, batches reared at 30 and 34 1C
presented the lowest CVs at the end of the experiment. The
lower CV of batch reared at 30 1C was also observed by
Watanabe et al. (1993) on juvenile sex-reversed male
Florida red tilapia at 22, 27, and 32 1C temperatures with
CVs 58.2%, 46%, and 44.1%, respectively. In contrast to
our ndings, Saclauso (1984) demonstrated that CVs of the
 ARTICLE IN PRESS
M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105
nal body weight of Tilapia zilli were signicantly higher at
30 1C than at 27 and 25 1C. Therefore, it seems that optimal
temperature for rearing tilapia not only enhances growth of
this sh but also produces more uniform growth batches.
In natural aquatic systems, sh live in deeper water
during the cold season and migrate to shallower water
when the temperature increases (Caulton, 1975). The
vertical migration and inshoreoffshore movements of
tilapia in response to water temperature have been well
documented (Caulton and Hill, 1975). This behavior was
observed for many species of tilapias. El-Sayed et al. (1996)
demonstrated better growth rates of O. niloticus in ponds
that were 300 cm deep than in ponds that were 200 cm
deep, indicating that sh avoided lower water temperature
during cold season by moving to the bottom. Similar
results were also obtained by Van someren and Whitehead
(1954) in Tilapia nigra, Caulton (1975) in Tilapia rendalli,
and Bruton and Boltt (1975) in Tilapia mossambica. These
studies demonstrated much greater variation in tempera-
ture of shallow ponds than in the deeper ones. Conclu-
sively, sh move into deeper water when the surface water
temperature decreases beyond their optimal range, a
behavioral component of a physiological adaptation
leading to the enhancement of growth by selection of the
habitat that is most suitable for their physiological
requirements. Such movements have an important impact
on the growth of sh and represent a response which
was attributed to the activitytemperature relationship
expected in poikilotherms.
Overall, it is possible to conclude that a temperature near
30 1C is the optimum for growth of O. niloticus fry; lower
temperature (22 1C) results in slow growth. Similar
temperature optima have been noted in other members of
the cichlidae family. For example, O. mossambicus has an
optimum temperature of growth at 30 1C and Tilapia zilli
has an optimum feeding temperature between 28.8 and
31.4 1C (Stickney, 1986).
In addition to the effect of temperature on growth, we
studied its effect on the sex ratio during the early stage of
development. We noticed that ambient water temperature
during the period of sex differentiation of fry strongly
inuences sex ratio in Nile tilapia (O. niloticus), as shown
by Baroiller et al. (1995, 1996a) on O. niloticus (strain
Bouake), Baroiller et al. (1996b) on Florida red tilapia,
Baras et al. (2001) on O. niloticus (strain Manzala), and
Desprez and Melard (1998) on O. aureus, that high
temperatures skewed the sex ratio in favor of males. On
the other hand, we found that low rearing temperatures
(19 1C) did not affect the sex ratio of progenies, conrming
results obtained for other strains and species of tilapia.
However, feminizing effect at low temperatures rearing
was observed in several non-cichlid sh species, like,
M. menidia (Conover and Kynard, 1981), Odonthestes
argentinensis (Strussmann et al., 1996), and Hoplosternum
littorale (Hostache et al., 1995).
Since both Bouake strain and Manzala strain produce
almost 78100% monosex male progenies at 36.5 1C, with
103
lower mortality during the treatment (Baras et al., 2001), it
seems that these strains appear to be more thermosensitive
than the Maryut strain used in this study. Indeed, our
results show that the best rate of masculizing is 80% and
was obtained after exposure to 36.83 1C, but with lower
survival rates during treatment (60%).
According to the results of this study, we notice a large
variance in the sex ratio between groups treated at the same
temperature, which may be explained by differing tem-
perature sensitivities in individual sh. These differences
may have originated from parental inuence according to
the ndings of Baroiller et al. (1996a, b) in O. niloticus,
suggesting that thermosensitivity would be inuenced by
parental traits. Moreover, Baras et al. (2001) attributed
these differences to the heterogeneity of the strain, which
may be a mixture of two or more populations. This
explanation supports the ndings of Conover and Kynard
(1981) on the effects of temperatures on sex differentiation
in M. menidia. These authors demonstrated different sex
ratio responses to temperature in different populations of
this species, which may be explained by the variation in
patterns of thermosensitivity related to the geographic
origin of these strains. Indeed, according to Conover
and Heins (1987) cited by Desprez and Melard (1998), in
M. menidia the magnitude of thermosensitivity decreases
with increasing latitudes.
As indicated by Baroiller et al. (1995, 1996a), the
sensitivity of environmental effects on sex ratio depends
on genotypes. Desprez and Melard (1998) demonstrated
that thermosensitivity is as important in Oreochromis
species with ZW chromosomal sex determinism (O. aureus)
as it is in O. niloticus, which has an XY chromosomal
system. In fact in O. aureus, these authors showed higher
survival rates at masculinizing temperatures which do not
exceed 35 1C (3435 1C), but in O. niloticus, masculinizing
temperatures close, almost, the upper incipient lethal
temperature (UILT; Melard, 1986).
The physiological action of the high-temperature treat-
ments may have an effect on the structure or action of
hormone or hormones acting during sex differentiation
(Hunter and Donaldson, 1983) and involves the thermo-
sensitivity of gene P450 aro, which codes for the aromatase,
which normally transforms androstenedione into estrone,
or testosterone into 17 beta-estradiol (Guigen et al., 1988).
In conclusion, this last experiment shows the possibility
of producing higher male sex ratio populations of Nile
tilapia of the Maryut strain by thermal sex reversal. Owing
to the proximity of the UILT and masculinizing tempera-
tures and to the long duration of thermal treatment (28
days), which signicantly affect the survival and growth
rates, future investigations should aim at (i) selecting the
most thermosensitive breeders, (ii) studying the possibility
of reducing the duration of the treatment while preserving
similar sex ratio, and (iii) evaluating the loss of production
(mortality) incurred during the masculinizing treatment
and whether this loss is compensated after this treatment
by faster growth of male.
 ARTICLE IN PRESS
104 M.S. Azaza et al. / Journal of Thermal Biology 33 (2008) 98105
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