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Effect of starvation and re‐feeding on growth performance and content of

plasma lipids, glucose and insulin in cultured juvenile Persian sturgeon
(Acipenser persicus Borodin, 1897)

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 Journal of
Applied Ichthyology
J. Appl. Ichthyol. 28 (2012), 692–696 Received: June 27, 2011
 2012 Blackwell Verlag, Berlin Accepted: January 30, 2012
ISSN 0175–8659 doi: 10.1111/j.1439-0426.2012.01969.x

Effect of starvation and re-feeding on growth performance and content of plasma

lipids, glucose and insulin in cultured juvenile Persian sturgeon (Acipenser persicus
Borodin, 1897)
By M. Yarmohammadi1, A. Shabani1, M. Pourkazemi2, H. Soltanloo3 and M. R. Imanpour1
1
Department of Fishery, College of Fishery and Environment, Gorgan University of Agricultural Sciences and Natural Resources,
Gorgan, Iran; 2International Sturgeon Research Institute, Rasht, Iran; and; 3Department of Biotechnology and breeding, College of
Plant production, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

Summary
The effect of starvation and subsequent re-feeding to satiation
on compensatory growth performance, insulin and blood
serum values were investigated in juvenile Persian sturgeon
(Acipencer persicus) with an average weight 108.04 ± 0.28 g
(mean ± SEM) and in the same rearing condition over an
8-week period. Sturgeons were allocated to one of five feeding
treatments: controls (C, continuous feeding), W1 (1 week
starvation), W2 (2 weeks starvation), W3 (3 weeks starvation)
and W4 (4 weeks starvation), followed by a single 4 weeks of
re-feeding to satiation. Changes in growth performance and
blood serum indices were examined at the end of weeks 4 and
8. Body weight, specific growth rate (SGR), condition factor
(CF) and weight gain were determined to have significantly
decreased during starvation. Fish starved for 1 week reached
the same weight as the control fish after re-feeding for
4 weeks, indicating that complete compensatory growth
occurred. Although the specific growth rate in W2, W3 and
W4 fish was greater than that in the control fish after re-
feeding, W2, W3 and W4 fish did not reach the same body
weight as control fish at the end of re-feeding period, and
showed partial compensation only. Blood plasma, glucose
and insulin concentrations did not change significantly during
starvation and re-feeding (P > 0.05). This suggests that
sturgeon are able to maintain glycaemia during starvation,
probably due to their non-carbohydrate dietary source.
Plasma total lipid and triglyceride levels increased in starva-
tion treatments, whereas the increases were significant only in
W3 treatment (P < 0.05). After a 4-week re-feeding period,
their levels decreased in comparison to the starvation periods.
Increases in plasma total lipid and triglyceride levels appear
to be due to their roles as preferred nutrients for mobilization
in Persian sturgeon and the magnitude and duration of
compensatory growth depended on the length of food
deprivation.
Introduction
Food restriction for many aquatic animals, including fishes is a
natural occurrence in the wild due to limitations in the forage
base, weather events and certain phases of their reproductive
cycles (Davis and Gaylord, 2011). Moreover, in aquaculture,
food restrictions or deprivation for short periods may be part
of a feeding strategy to solve water quality problems, reduce
negative effects of stress due to handling (Davis and Gaylord,
2011), reduce mortality due to diseases, or save feed in order to
increase farm profits (Gaylord and Gatlin, 2000; Wang et al.,
2000; Caruso et al., 2011).
During starvation, animals employ various behavioral,
physiological, and structural mechanisms to cover their
metabolic needs using their energy reserves (Navarro and
Gutierrez, 1995). When re-feeding resumes, starved fish exhibit
a period of compensatory growth (Jobling et al., 1994; Sahin
et al., 2000; Ali et al., 2003). This phenomena may be due to
hyperfagia (increase in appetite) (Saether and Jobling, 1999;
Chatakondi and Yante, 2001; Ali et al., 2003; Nikki et al.,
2004), protein synthesis (Quinton and Blake, 1990), and
replenishment of energy reserve (Alvarez and Nicieza, 2005).
Fish species vary in their growth responses to food limitation.
Compensatory growth can be classified into three types related
to the degree of recovery: over-compensation, complete
compensation, and partial compensation (see Ali et al.,
2003). If over or complete compensatory growth occurs, there
could be an opportunity to reduce the cost of feeding the fish
by starving them and making up for lost growth when feeding
resumes. Therefore, compensatory growth can be used to
increase profits of aquaculture operations (Chatakondi and
Yante, 2001).
Several studies have used periods of food deprivation and
re-feeding to examine compensatory growth in several major
aquaculture finfish species, e.g. salmonids (Jobling and Koskela,
1996; Boujard et al., 2000), Atlantic halibut (Hippoglossus
hippoglossus L.) (Heide et al., 2006), gibel carp (Carassius
auratus gibelio) (Qin et al., 2000; Xie et al., 2001), channel
catfish (Ictalurus punctatus) (Kim and Lovell, 1995; Gaylord
and Gatlin, 2000; Chatakondi and Yante, 2001), Chinese
sturgeon (Acipenser sinensis) (Liu et al., 2011), and European
sea bass (Dicentrachus labrax) (Chatzifotis et al., 2011). These
studies have shown that some blood indices are strongly
affected by nutrition and that they can provide a useful tool to
monitor nutritional status and growth performance (Navarro
and Gutierrez, 1995; Power et al., 2000; Montserrat et al.,
2007a,b). Focusing on these features is especially important
when dealing with non-teleost aquaculture species, like Persian
sturgeon, Acipenser persicus Borodin, 1897, due to the lack of
knowledge of its metabolic traits.
Persian sturgeon is endemic to the southern Caspian Sea and
is being considered as an aquaculture species in Iran (Pourkaz-
emi, 2006). Although this species has a lower growth rate in
comparison with the beluga sturgeon (Huso huso), it matures at
an earlier age, around 6–7 years, raising the possibility of obtaining
more frequent harvests of caviar (Hosseini et al., 2009).

U.S. Copyright Clearance Centre Code Statement: 0175–8659/2012/2805–0692$15.00/0

Effect of starvation and re-feeding on growth
Because of the long rearing time, and consequent rearing
costs, physiological data on this species could provide a basis
for improved rearing and feeding protocols, with possible
reductions in production costs. In the present study we
examined growth performance and physiological parameters
(i.e. variations in levels of glucose, total lipid, triglyceride and
insulin in the plasma) in Persian sturgeon exposed to different
starvation periods and tested compensatory growth at
subsequent re-feeding. The work ascertains the extent of
compensatory growth in juvenile Persian sturgeon and its
relevance for cost-saving in large-scale aquaculture.
Materials and methods
Test specimens and experimental conditions
Three hundred and 75 juvenile (7-month-old) Persian sturgeon
with a mean initial weight 108 ± 0.63 g and length 31.73
± 0.28 cm were acclimated to rearing conditions at the Shahid
Beheshti Sturgeon Propagation Complex, located in Rasht,
Iran. To study the effects of re-feeding after starvation for
different periods, we used the experimental design previously
described by Montserrat et al. (2007a,b) with some modifica-
tions. Briefly, fish were randomly distributed in 15 circular
1000-L outdoor tanks that were allocated to one of five
treatments (W1, W2, W3, W4, and C). Each treatment was
replicated in three tanks with 25 individuals in each. There
were no significant differences in fish weight among treatments
at the commencement of the experiment.
The experiment was conducted in two phases over an 8-week
period between October and December 2009. In the first phase,
four starvation conditions were induced through food restric-
tion: 1 week (W1), 2 weeks (W2), 3 weeks (W3) and 4 weeks
(W4), while controls (C) were fed until satiety. In the second
phase of the trial the starved (W) treatments were fed to
satiation three times per day for the remaining 4-week period
of the experiment. The timing of food deprivation was such
that all groups finished their fasting period at the same time
and were re-fed simultaneously during the final 4 weeks.
Water quality in experimental tanks was monitored daily
using (Multi-parameter WTW 34O, Weilheim, Germany)
throughout both fasting and re-feeding periods. The water
quality parameters, i.e. dissolved oxygen (6–8 mg L)1), pH (7.5–
8.5) and temperature (16.5–18.5C) during experiment period
did not differ significantly between treatments. The sturgeons
were fed a commercial formulated feed (BIOMAR, INICIO Plus
868, Nersac, France) containing: 48% crude protein, 22% crude
fat, three times per day (08:00, 13:00 and 18:00).
Sample collection
All fish were weighed individually to the nearest 0.01 g at the
start and, after starvation, at the end of the experiment. The
fish were starved 12 h prior to weighing and during sampling
when the fish were anaesthetized moderately (clove powder,
0.5 gl)1). Blood samples were taken from the caudal vessels in
fifteen fish per treatment (five individuals per tank chosen
randomly) with heparinized needles. Plasma samples were
obtained after blood centrifugation (3000 g, 10 min, 4C) then
stored at )20C for subsequent analyses. Standard length (cm)
and body weight (g) were determined. Specific growth rates
(SGR) were calculated for fish in the different treatments
according to the commonly used formula described by Houde
and Schekter (1981) as:
693
SGR (SGR, %g day)1) = 100 · ln (w2)w1) ⁄ t,
where w2 = weight after fasting or re-feeding and w1 = weight
before feeding (g), t = is the interval (days) between weighings.
Condition factor (CF – an indicator of body shape)
(Montserrat et al., 2007a,b) and percentage weight gain
(Eroldogan et al., 2006) were calculated using the formulae:
CF = (body weight, g) ⁄ (body length, cm)3 · 100
Weight gain (%) = 100 · (w2)w1) ⁄ w1
where, w2 = weight after fasting or re-feeding and w1 was
weight before feeding.
Biochemical analyses of plasma parameters
All biochemical assays were carried out using commercial
diagnostic kits. Plasma glucose concentration was determined
by a kit based on a colorimetric glucose oxidase – peroxidase
reaction (Pars azmoon, Karaj, Iran) and Auto analyzer system
(Technicon, NY). Plasma insulin levels were measured by
immunoradiometric assay (IRMA) (Biosource INS-IRMA kit,
Biosource, Europe, SA, Nivelles, Belgium) using a Gama
counter (LKB, Turku, Finland). Total lipid and triglycerides
were determined using an enzymatic method (Pars Azmoon,
Karaj, Iran) in conjunction with an Auto analyzer (Thomas,
1998).
Statistical methods
Data are reported as mean values ± standard error of mean
(SEM). All statistical analyses were conducted using SPSS
statistical software, version 17 (IBM, Chicago, IL). Each tank
was considered an experimental unit in this study. Therefore,
tank means were used to test the treatment effect on each
variable. A Kolmogorov–Smirnov test was used to assess for
normality of distribution and data were examined using
LevenÕs test for homogeneity of variances. The starva-
tion ⁄ re-feeding effects were analyzed with one-way ANOVA
followed by DuncanÕs test where variances were homogeneous.
The differences were regarded as significant when P < 0.05.
Results
Growth performance and compensatory growth
Initial weights of fish did not significantly differ between
experimental treatments (P < 0.05). Throughout the experi-
ment, fish survival was 100%.
Mean final body weight of juveniles was significantly
impacted by the length of the fasting period (Table 1).
Starvation caused weight loss, with the mean weight of fish
subjected to the three different deprivation regimes, W2
(108.94 ± 1.18 g), W3 (100.36 ± 1.8 g) and W4 (99.68
± 2.3 g) being significantly lower than that of the control
group (139.08 ± 2.27 g) (P < 0.05). After 4 weeks re-feeding,
only the W1 treatment (125.02 ± 5.06 g) was not significantly
lighter than the final weight of the control group.
In addition, specific growth rate (SGR) was significantly
higher in the control group (0.88) than in W2 (0.025), W3
()2.28) and W4 ()0.26) treatments (P < 0.05), while W1
(0.47) did not differ from control fish (P > 0.05). Following
4 weeks re-feeding, SGR in all four groups, W1 (2.01%), W2
(2.01%), W3 (2.07%) and W4 (2.32%) were significantly
higher than in the control group (C) (1.61%) (P < 0.05).
694 M. Yarmohammadi et al.

Table 1
Growth performance after different starvation periods and subsequent re-feeding of Persian sturgeon (Acipenser persicus)

C W1 W2 W3 W4

Initial weight (g) 108.65 ± 1.35 109.18 ± 0.37 108.94 ± 1.16 106.96 ± 0.34 107.944 ± 2.88
Fasting weight (g) 139.08 ± 2.27b 125.02 ± 5.06b 108.15 ± 1.18a 100.36 ± 1.80a 99.68 ± 2.30a
Re-feeding weight (g) 218.56 ± 8.11b 219.33 ± 2.76b 190.23 ± 3.01a 179.6 ± 5.2a 191.01 ± 2.01a
SGR (%day)1) after fasting 0.88 ± 0.09b 0.47 ± 0.15b )0.025 ± 0.05a )2.28 ± 0.05a )0.26 ± 0.02a
SGR (%day)1) after re-feeding 1.61 ± 0.12a 2.01 ± 0.10b 2.01 ± 0.02b 2.07 ± 0.04b 2.32 ± 0.07b
Weight gain (%) after fasting 28.09 ± 3.52c 14.53 ± 4.97b )0.7 ± 1.46a )6.16 ± 1.51a )7.25 ± 0.62a
Weight gain (%) after re-feeding 57.16 ± 5.56a 75.84 ± 5.09b 75.86 ± 1.14b 78.87 ± 2-21b 91.81 ± 4.04b
CF (%) after fasting 0.31b 0.31b 0.28a 0.28a 0.27a
CF (%) after re-feeding 0.35c 0.35b,c 0.34a 0.33a, b 0.33a

SGR, Specific Growth Rate, CF, Condition Factor.

Values are means ± SEM. Different superscripts in same row = significant (P < 0.05) difference between groups. C (control treatment), W1
(1 week starvation), W2 (2 weeks starvation), W3 (3 weeks starvation) and W4 (4 weeks starvation). Calculated based on end of starvation and
end of re-feeding.

Percentage weight gains (WG %) during fasting in the four (a) Glucose
80 b b
treatments (W1, W2, W3 and W4) were 14.53, )0.7, )6.16 and b a
a

Glucose (mg dl–1)

)7.25%, respectively, and were significantly lower than control 60
fish (28.09%). After the re-feeding period, WG% in all four
groups (CF = 75.84, 75.86, 78.87 and 91.81 in W1, W2, W3 40

and W4 respectively) was significantly higher than in the C 20

group (57.16) (P < 0.05). This demonstrates clear evidence for
a compensatory growth response of these food-restricted 0
groups. The condition factor (CF) during fasting periods was Fasting Refeeding
significantly higher in C and W1 groups (0.31%) than in the
W2 (0.28%), W3 (0.28%) and W4 (0.27%) groups. Interest- (b) 7
Insulin
Insulin (micIU ml–1)

ingly though, after the re-feeding period, the fish in three 6

treatments (CF = W1, W2 and W3 were 0.35, 0.34 and 0.34, 5
respectively) were not statistically different from that of 4
the control group (CF = 0.35) in their condition factor 3
(P > 0.05), but the W4 (0.33) treatment was statistically 2
1
different from control group (P < 0.05).
0
Fasting Refeeding
Effects of fasting and re-feeding on plasma metabolites and insulin
(c) c
Lipid
2500
Different starvation treatments did not affect plasma glucose b,c
levels significantly (P > 0.05) (Fig. 1a). Moreover, after the 2000 a,b
Lipid (mg dl–1)

a a
re-feeding period, the level of plasma glucose significantly
1500
increased from that of the starvation period (P < 0.05), but its
level was similar across groups. 1000
Different starvation periods likewise did not have a signif-
500
icant effect on plasma insulin (Fig. 1b). After re-feeding
periods (1 month), treatment (W) groups had similar insulin 0
levels as the starvation as well as control fish (P > 0.05). Fasting Re-feeding
Plasma total lipid and triglyceride levels increased during
starvation, and in the W3 treatment were significantly higher (d) Triglyceride
Tryglycerid (mg dl–1)

1800 b
than in the other treatments. Following 4 weeks re-feeding, 1600 b
total lipid and triglyceride concentrations were significantly 1400 a,b
a a
1200
lower compared with starvation treatments, and showed similar 1000
800
levels between experimental treatments (P > 0.05) (Fig. 1c,d). 600
400
200
0
Discussion Fasting Re-feeding
Starvation and re-feeding are known to have strong effects on
1W 2W 3W 4W C
the physiology and muscle growth of fish (Navarro and
Gutierrez, 1995). In this study we examined whether compen- Fig. 1. Changes in circulation level of blood glucose (a), lipid (b),
satory growth by re-feeding modulates growth, plasma triglyceride (c) and insulin of Persian sturgeon (Acipenser persicus) in
controls (C), and starved fish for 1 (W1), 2 (W2), 3 (W3) and 4 (W4)
metabolites, and insulin in juvenile A. persicus. For this weeks and after 4 weeks re-feeding period. Data present mean ± -
purpose, we imposed 1, 2, 3 or 4 weeks of starvation and then SEM. Differences between subscripts indicate significantly different
fed ad lib. for 1 month. means at P < 0.05. (n = 15 sample size, from three replicates)
Effect of starvation and re-feeding on growth
There are several indicators of the effectiveness of compen-
satory growth (Jobling et al., 1994). As expected, fasting for 2,
3 and 4 weeks resulted in significant reductions in body weight,
specific growth rate (SGR) and condition factor in the juvenile
Persian sturgeon. After re-feeding for 1 month ad lib., the W1
group achieved the same weight as C and also showed higher
SGR, indicating full compensation in W1 group. However,
while W2, W3 and W4 showed higher SGR and WG after
re-feeding, their final weights were less than that of C,
suggesting partial compensation of growth. The increase in
SGR and WG in W groups after re-feeding indicates that the
fish had the tendency to recover their initial weight and growth
trajectories. The findings of the current experiment were
similar to that for trout (Oncorhynchus mykiss) where full
compensation after 1 week of starvation and partial compen-
sation after 2 or 3 weeks starvation was observed after fasting
(Montserrat et al., 2007a). Similar findings have also been
observed in barramundi (Lates calcalifer) (Tian and Qin, 2003)
and in hybrid tilapia, Oreochromis mossambicus and O. niloti-
cus (Wang et al., 2000) and Atlantic cod (Gadus morhua)
(Jobling et al., 1994).
Numerous fish species experience long periods of starvation
and then recover after re-feeding (Navarro and Gutierrez,
1995). Responses of plasma glucose levels during starvation
are variable in fish. The maintenance of blood glucose
concentration during food deprivation indicates an active
gluconeogenic process in the liver. Since glucose is an
essential fuel for a number of tissues, it is particularly
important that glucose levels be maintained throughout
starvation (Gillis and Ballantyne, 1996). In the present study,
the glucose plasma levels for juvenile Persian sturgeon
remained relatively stable over the 4 weeks of food depriva-
tion. Consistent with the results of Hung (1991), the
maintenance of the plasma glucose of sturgeon during
4 weeks of starvation suggests that sturgeon prefer to use a
dietary non-carbohydrates source instead of mobilizing their
muscle protein for gluconeogenesis. The ability of Persian
sturgeon to maintain plasma glucose levels in the fasting state
is consistent with results for lake sturgeon (A. fulvescens), in
which a glycaemia maintenance over 60 days of starvation
was evident (Gillis and Ballantyne, 1996). In contrast to the
present study, white sturgeon (A. transmontanus) showed a
significant reduction in plasma glucose levels during 8 weeks
of starvation (Hung et al., 1997). The maintenance of
glycaemia during starvation has been observed in many
species of teleost (Hochachka and Sinclair, 1962; Zammit and
Newsholme, 1979; Davis and Gaylod, 2011; Wood et al.,
2010; Chatzifotis et al., 2011). However, many other teleost
species are unable to maintain plasma glucose levels for
extended starvation periods (Peterson and Small, 2004;
Montserrat et al., 2007a,b).
Insulin is an anabolic hormone that induces glucose uptake
in liver and muscle (Machado et al., 1988). Insulin plasma
levels throughout our experiment showed a decrease in W
groups. The insulin plasma levels of the W4 group were the
least; however, no significant differences between the W groups
and control (P > 0.05) were evident. After re-feeding, insulin
plasma levels did not appear to change. Stability of insulin
levels during fasting is consistent with that of plasma glucose.
In contrast to our study, reduced plasma insulin levels
following starvation and complete recovery after re-feeding
are commonly observed in other species of teleost, including
cod and rainbow trout (Navarro and Gutierrez, 1995; Larsen
et al., 2001).
695
During starvation, fat stores are known to become mobilized
in response to food deprivation. Glycerol and free fatty acids
(FFAs) are produced as a result of the fat mobilization. In the
current research, total plasma lipid (FFAs) and triglyceride
increased during the fasting period so that its level in W3 was
significantly greater than in other groups. Increases in plasma
lipid and triglyceride levels suggested that the lipids were the
preferred nutrients for mobilization in juvenile Persian sturgeon
during starvation periods. These observations are inconsistent
with findings in sub-yearling white sturgeon, in which lipid was
the preferred nutrient for mobilization during starvation (Hung
et al., 1997). However, in lake sturgeon (A. fulvescens), starved
fish had an ability to metabolize amino acids to produce energy
(Gillis and Ballantyne, 1996). Other studies of finfish reported
increases in FFAs in fasting groups (Albata et al., 2005;
Montserrat et al., 2007a,b; Perez-Jimenez et al., 2007), and
decreases after re-feeding. Furthermore, in Persian sturgeon, re-
feeding after fasting restores total lipids (FFAs) and triglyce-
rides to the levels observed in control fish, indicating that lipid
mobilization had ended (Potlinger et al., 2003).
In conclusion, the compensatory growth in Persian sturgeon
depended on the length of food deprivation, although 1 week
starvation and 4 weeks subsequent re-feeding appears to be the
best regime to recover weight. Our data clearly indicate that fat
stores are mobilized during fasting in order to assume metab-
olism. It is also concluded that a periodic short-term starvation
in Persian sturgeon does not sacrifice fish weight gain.
Acknowledgements
This research has been supported by the Agricultural Sciences
and Natural Resources University of Gorgan and the Iranian
Fisheries Research Organization. We wish to thank Mr.
Abbasalizadeh, Deputy of Shahid Beheshti Sturgeon Propa-
gation Complex, for his assistance with this research. We are
also highly indebted to Dr. Dean Jerry from James Cook
University, Australia for proofreading the article.
References
Albata, A.; Gomez-Requeni, P.; Rojas, P.; Medale, F.; Kaushik, S.;
Vianen, G. J.; Van den Thillart, G.; Gutierrez, J.; Preze-Sanchez,
J.; Navarro, I., 2005: Nutritional and hormonal control of
lipolysis in isolated gilthead seabream (Sparus aurata) adipocytes.
Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, 259–265.
Ali, M.; Nicieza, A.; Wootton, R. J., 2003: Compensatory growth in
fishes: a response to growth depression. Fish Fish. 4, 147–190.
Alvarez, D.; Nicieza, A. G., 2005: Compensatory response ‘‘defends’’
energy levels but not growth trajectories in brown trout, Salmo
trutta L., Proc. R. Soc. B. 272, 610–607.
Boujard, T.; Burel, C.; Medale, F.; Haylor, G.; Moisan, A., 2000:
Effects of past nutritional history and fasting on feed intake and
growth in rainbow trout Onchorhynchus mykiss. Aquat. Liv. Res.
13, 129–137.
Caruso, G.; Denaro, M. G.; Caruso, R.; Mancari, F.; Genovese, L.;
Maricchiolo, G., 2011: Response to short term starvation of
growth, haematological, biochemical and non-specific immune
parameters in European sea bass (Dicentrachus labrax) and
blackspot sea bream (Pagellus bogaraveo). Mar. Environ. Res.
72, 46–52.
Chatakondi, N. G.; Yante, R. D., 2001: Application of compensatory
growth to enhance production in channel catfish Ictalurus
punctatus. J. World Aquacult. Soc. 32, 278–285.
Chatzifotis, S.; Papadaki, M.; Despsoti, S.; Roufidou, C.; Antonop-
oulou, E., 2011: Effects of starvation and re-feeding on repro-
ductive indices, body weight, plasma metabolites and oxidative
enzymes of sea bass (Dicentrachus labrax). Aquaculture 316,
53–59.
696
Davis, K. B.; Gaylord, T. G., 2011: Effect of fasting on body
composition and responses to stress in sunshine bass. Comp.
Biochem. Physiol. A. 158, 30–36.
Eroldogan, O. T.; Kumlu, M.; Kiris, G. A.; Sezer, B., 2006:
Compensatory growth response of Sparus aurata following
different starvation and refeeding protocols. Aquacult. Nutr. 12,
203–210.
Gaylord, T. G.; Gatlin, D. M., 2000: Dietary protein and energy
modifications to maximize compensatory growth of channel
catfish (Ictalurus punctatus). Aquaculture 194, 337–348.
Gillis, T. E.; Ballantyne, J. S., 1996: The effects of starvation on plasma
free amino acid and glucose concentrations in lake sturgeon.
J. Fish Biol. 49, 1306–1316.
Heide, A.; Foss, A.; Stefansson, S. O.; Mayer, I.; Norberg, B.; Roth,
B.; Jenssen, M. D.; Nortvedt, R.; Imsland, A., 2006: Compensa-
tory growth and fillet crude composition in juvenile Atlantic
halibut: effect of short term starvation periods and subsequent
feeding. Aquaculture 261, 109–117.
Hochachka, P. W.; Sinclair, A. C., 1962: Glycogen stores in trout
tissues before and after stream planting. J. Fish. Res. Board Can.
19, 127–136.
Hosseini, M. R.; Mohseni, M.; Zahedifar, M.; Pourali, H.; Alizadeh,
M.; Shahifar, R., 2011: Determining nutritional requirement in
Persian sturgeon (Acipenser persicus) in fingerling and grow out
stages. Iranian Fish. Res. Organ. pp. 91.
Houde, E. D.; Schekter, R. C., 1981: Growth rates and cohort
consumption of marine fish larvae in relation to prey concentra-
tions. Rapp. P.V. Reuncons. Int. Explor. Mer. 178, 441–453.
Hung, S. S. O., 1991: Carbohydrate utilization by white sturgeon as
assessed by oral administration tests. J. Nat. 121, 1600–1605.
Hung, S.S.O.; Liu, W.; Li, H.B.; Storebakken, T.; Cui, Y.B., 1997:
Effects of starvation on some morphological and biochemical
parameters in white sturgeon, Acipenser transmontanus. Aquacul-
ture 151, 357–363.
Jobling, M.; Koskela, J., 1996: Interindividual variations in feeding
and growth in rainbow trout during restricted feeding and in a
subsequent period of compensatory growth. J. Fish Biol. 49, 658–
667.
Jobling, M.; Meloy, O. H.; Dos Santos, J.; Christiansen, B., 1994: The
compensatory growth response of the Atlantic cod: elects of
nutritional history. Aquacult. Internat. 2, 75–90.
Kim, M. K.; Lovell, R. T., 1995: Effect of restricted feeding regimens
on compensatory weight gain and body tissue changes in channel
catfish Ictalurus punctatus in ponds. Aquaculture 135, 285–293.
Larsen, D. A.; Beckman, B. R.; Dickhoff, W. W., 2001: The effect of
low temperature and fasting during the winter on metabolic stores
and endocrine physiology (insulin, insulin-like growth factor-I
and thyroxine) of coho salmon, Oncorhynchus kisutch. Gen.
Comp. Endocrinol. 123, 308–323.
Liu, W.; Wei, Q. W.; Wen, H.; Jiang, M.; Wu, F.; Shi, Y., 2011:
Compensatory growth in juvenile Chinese sturgeon (Acipenser
sinensis): effects of starvation and subsequent feeding on growth
and body composition. J. Appl. Ichthyol. 27, 749–754.
Machado, C. R.; Garofalo, M. A. R.; Roselino, J. E. S.; Kettelhut, I.
C.; Migliorini, R. H., 1988: Effects of starvation, refeeding, and
insulin on energy-linked metabolic processes in catfish (Rhamdia
hilarii) adapted to a carbohydrate-rich diet. Gen. Comp. Endo-
crinol. 71, 429–437.
Montserrat, N.; Gabillard, J. C.; Capilla, E.; Navarro, M. I.;
Gutierrez, J., 2007a: Role of Insulin, insulin-like growth factors,
and muscle regulatory factors in the compensatory growth of the
trout (Onchorhynchus mykiss). Gen. Comp. Endocr. 150, 462–427.
Montserrat, N.; Gomez-Requeni, P.; Bellini, G.; Capilla, E.; Prez-
Sanchez, J.; Navarro, I.; Gutierrez, J., 2007b: Distinct role of
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M. Yarmohammadi et al.
insulin and IGF-I and its receptors in white skeletal muscle during
the compensatory growth of gilthead sea bream (Sparus aurata).
Aquaculture 267, 188–198.
Navarro, I.; Gutierrez, J., 1995: Fasting and starvation. In: Biochem.
Mol. Biol. Fishes, vol. 4. P.W. Hochachka, T. P. Mommsen (Eds).
Elsevier Science, BV, pp. 393–434.
Nikki, J.; Pirhonen, J.; Jobling, M.; Karjalainen, J., 2004: Compen-
satory growth in juvenile Oncorhynchus mykiss (Walbaum), held
individually. Aquaculture 235, 285–296.
Perez-Jimenez, A.; Guedes, M. J.; Morales, A. E.; Oliva-Teles, A.,
2007: Metabolic responses to short starvation and re-feeding in
Dicentrachus labrax. Effects of dietary composition. Aquaculture
265, 325–335.
Peterson, B. C.; Small, B. C., 2004: Effects of fasting on circulating
IGF-binding proteins, glucose, and cortisol in channel catfish
(Ictalurus punctatus). Dom. Endocrinol. 26, 231–240.
Potlinger, T. G.; Rand-Weaver, M.; Sumpter, J. P., 2003: Overwinter
fasting and re-feeding in rainbow trout: plasma growth hormone
and cortisol levels in relation to energy mobilization. Comp.
Biochem. Physiol. Biochem. Mol. Biol. 136, 403–417.
Pourkazemi, M., 2006: Caspian Sea sturgeon conservation and
fisheries: past, present and future. J. Appl. Ichthyol. 22, 12–16.
Power, D. M.; Melo, J.; Santos, C. R., 2000: The effect of food
deprivation and refeeding on the liver, thyroid hormones and
transthyretin in sea bream. J. Fish Biol. 56, 374–384.
Qin, X.; Cui, Y.; Xiong, B.; Yang, Y., 2000: Compensatory growth,
feed utilization and activity in gibel carp, following feed depriva-
tion. J. Fish Biol. 56, 228–232.
Quinton, J. C.; Blake, R. W., 1990: The effect of feed cycling and
ration level on the compensatory growth-response in rainbow
trout, Oncorhynchus mykiss. J. Fish Biol. 37, 33–41.
Saether, B. S.; Jobling, M., 1999: The effect of ration level on feed intake
and growth, and compensatory growth after restricted feeding, in
turbot Scophthalmus maximus. Aquacult. Res. 30, 647–653.
Sahin, T.; Akbulut, B.; Aksungur, M., 2000: Compensatory growth in
sea bass (Dicentrarchus labrax), sea bream (Sparus aurata) and
rainbow trout (Onchorhynchus mykiss). Turk. J. Zool. 24, 81–86.
Thomas, L., 1998: Clinical laboratory diagnostics, 1st edn. TH-Books
Verlagsgesellschaft, Frankfurt, pp. 131–137.
Tian, X.; Qin, J. G., 2003: A single phase of food deprivation provoked
compensatory growth in barramundi Lates calcarifer. Aquacul-
ture 224, 169–179.
Wang, Y.; Cui, Y.; Yang, Y. X.; Cai, F. S., 2000: Compensatory
growth in hybrid tilapia, Oreochromis mossambicus and O.
niloticus, reared in seawater. Aquaculture 189, 101–108.
Wood, C. M.; Walsh, P. J.; Kajimura, M.; McClelland, G. B.; Chew,
S. F., 2010: The influence of feeding and fasting on plasma
metabolites in the dogfish shark (Squalus acanthias). Comp.
Biochem. Physiol. Part A. 155, 435–444.
Xie, S.; Zhu, X.; Cui, Y.; Wootton, R. J.; Lei, W.; Yang, Y., 2001:
Compensatory growth in gibel carp following feed deprivation:
temporal pattern in growth, nutrient deposition, feed intake and
body composition. J. Fish Biol. 58, 999–1009.
Zammit, V. A.; Newsholme, E. A., 1979: Activities of enzymes of fat
and ketone - body metabolism and effects of starvation on blood
concentrations of glucose and fat fuels in teleost and elasmo-
branch fish. Biochem. J. 184, 313–322.
AuthorÕs address: Mahtab Yarmohammadi, Department of Fishery,
College of Fishery and Environment, Gorgan
University of Agricultural Sciences and Natural
Resources, Gorgan, 49138-15739, Iran.
E-mail: mahtabyarmohammadi@gmail.com