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Editor-in-Chief
Dan Mires
Editorial Board
Sheenan Harpaz Agricultural Research Organization
Beit Dagan, Israel
Zvi Yaron Dept. of Zoology
Tel Aviv University
Tel Aviv, Israel
Angelo Colorni National Center for Mariculture, IOLR
Eilat, Israel
Rina Chakrabarti Aqua Research Lab
Dept. of Zoology
University of Delhi
Ingrid Lupatsch Swansea University
Singleton Park, Swansea, UK
Jaap van Rijn The Hebrew University
Faculty of Agriculture
Israel
Spencer Malecha Dept. of Human Nutrition, Food
and Animal Sciences
University of Hawaii
Daniel Golani The Hebrew University of Jerusalem
Jerusalem, Israel
Emilio Tibaldi Udine University
Udine, Italy
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Israeli Journal of Aquaculture - BAMIGDEH.
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The Israeli Journal of Aquaculture – Bamidgeh 57(1), 2005, 19-24. 19
EFFECT OF PHOTOPERIOD ON PLASMA THYROXINE HORMONE
LEVEL OF MIRROR CARP (CYPRINUS CARPIO) RAISED AT A
LOW WATER TEMPERATURE IN A CONTROLLED ENVIRONMENT
Sükriye Aras Hisar1, Birsen Kirim1, Serdar Bektas1, Konca Altinkaynak2, Olcay Hisar1*
and Telat Yanik1
1Atatürk University, Agriculture Faculty, Department of Aquaculture, Erzurum, Turkey
2Atatürk University, Medical Faculty, Department of Biochemistry, Erzurum, Turkey
(Received 7.5.04, Accepted 18.10.04)
Key words: mirror carp, photoperiod, thyroxin hormone, weight gain
Abstract
The objective of this study was to examine the effects of various lighting regimes on the plasma
thyroxin hormone (T4) level of mirror carp (Cyprinus carpio). The carp were kept at the low tem-
perature of 9°C to eliminate any influence of water temperature on feed intake, growth, and the
hormone level. Treatments were 8 h light:16 h dark, 12 h light:12 h dark, and 16 h light:8 h dark.
Plasma thyroxin levels were measured every four weeks for 12 weeks. The levels were signifi-
cantly higher (p<0.05) in the groups exposed to 8 or 12 h light than in the group exposed to 16
h. The T4levels significantly dropped with time in all photoperiods.
Introduction
Thyroid hormones play important roles in the
physiology of teleost fishes, i.e., in the regula-
tion of metabolism (Gupta and Thapliyal,
1991; MacKenzie et al., 1998), growth and
development (Power et al., 2001; Gavlik et al.,
2002), energy utilization (Leatherland, 1994),
sexual maturation (Monteverdi and Di Giulio,
2000; Mercure et al., 2001), breeding cycle
(Volkoff et al., 1999), migration (Matty, 1985),
and electrolyte and water metabolism (Peter
et al., 2000).
Physiological and morphological charac-
teristics of fish continually adjust to the ever-
changing aquatic environment. The circannu-
* Corresponding author.
Tel: +90-442-2313482; fax: +90-442-2360948; e-mail: ohisar@atauni.edu.tr
20
al rhythms of hormones seem to be closely
associated with circannual variations in ambi-
ent temperature, day length, and gonadal
steroids (Pavlidis et al., 2000).
Developmental and maturational events
are dominated and coordinated by seasonal
changes in photoperiod, temperature, food
supplies, rainfall, etc. (Porter et al., 1998;
Sánchez–Vázquez et al., 2000). Photoperiod
and temperature are generally considered the
most important factors. Recent data suggest
that genotype, hormones, and physiological
conditions are equally important endogenous
regulators of growth (Dutta, 1994).
Fish growth and food conversion are
improved by increasing the photoperiod
(Gross et al., 1965). Water temperature is
also correlated to food intake, being high in
the spring and summer and relatively lower
during the winter (Larsen et al., 2001).
Changes in temperature and food consump-
tion cause dynamic changes in the seasonal
profiles of many physiological parameters,
including growth rate and plasma thyroxin (T4;
Tiitu and Vornanen, 2003).
In Atlantic salmon, thyroid hormone pro-
duction reaches a maximum in summer when
the long period of light stimulates growth and
plasma T4levels without affecting T3
(McCormick et al., 1987). Low levels of thyroid
hormones are found in fish during winter when
the light period is short (Samejima et al.,
2000). On the other hand, Brown (1988)
reported that a short day length or complete
darkness stimulated the thyroid gland in fresh-
water and euryhaline species.
Most of the above studies were concerned
with seasonal fluctuations in growth or thyroid
hormones while some dealt with the optimum
temperature for growth or thyroid hormones.
We investigated whether different photoperi-
ods affect the plasma T4level of mirror carp at
a constant low temperature (9°C).
Materials and Methods
Animals. The study was conducted in the
Central Laboratory at the Aquarium Fish
Rearing Facility of the Fisheries Department
of the Agricultural Faculty at Atatürk
University with mirror carp obtained from the
Research and Extension Center of the
Fisheries Department.
Photoperiod experiments. The carp were
randomly sorted into three 70-l circular fiber-
glass tanks (45 x 45 cm) with a constant water
flow of 1.5 l/min of aerated dechlorinated tap
water at a density of 10 fish per tank. Three
photoperiods were tested in triplicate for a
total of nine tanks, i.e., 30 fish in each regime.
Mean weights were 63.06±3.83 g, 62.40±3.54
g, and 61.96±3.49 g, respectively for the three
regimes.
Fish were acclimated for one week at 12 h
light:12 h dark. Then the photoperiods were
switched to short (8 h light:16 h dark, lights on
at 09:00), medium (12 h light:12 h dark, lights
on at 06:00), or long (16 h light:8 h dark, lights
on at 04:00) for 12 weeks at a constant water
temperature of 9°C.
The fish were fed a daily ration at 1% of
their live body weight. Feeding times were
centered in the middle of the light period.
Growth was expressed as mean weight over
the duration of the study and as mean weight
gain (% of the initial weight).
Blood sampling. Every four weeks, the fish
were captured, anesthetized in MS-222 (200
mg/l) during the scotophase, and individually
weighed. At the same time, blood samples
were obtained from the caudal vasculature of
each carp with a heparinized syringe. The
blood samples were kept on ice for up to 30
min until the plasma was separated by cen-
trifugation. Plasma samples were stored at
–80°C until analysis. Plasma T4 concentra-
tions were determined according to the
method of Dickhoff et al. (1982).
Statistics. All data were subjected to a
one-way analysis of variance followed by
Duncan’s multiple-range test to determine sig-
nificant differences among the regimes at the
0.05 level. Results are presented as means ±
standard deviation.
Results
There were no significant differences in weight
gain among treatments (Fig. 1). Plasma T
4
levels were significantly higher in the groups
exposed to 8 or 12 hours of light than in the
group exposed to 16 (Fig. 2). Plasma T
4
levels
Hisar et al.
21Effect of photoperiod on plasma thyroxine hormone level of mirror carp
significantly dropped with time in all three pho-
toperiods. At 12 weeks, weight gain dropped
4.78±5.11%, 7.57±1.51%, and 8.72±1.37%
while plasma T
4
dropped 12.1%, 15.8%, and
66.9% in the 8:16, 12:12, and 16:8 photoperi-
ods, respectively.
Discussion
Despite the fact that the fish were fed at a ratio
of 1% of their body weight daily, they did not
grow at the low temperature of 9°C. Reduced
growth at this temperature is expected, due to
bioenergetic considerations (Hepher, 1988).
Fig. 2. Plasma thyroxin hormone (T4) of mirror carp kept at 8 h light:16 h dark, 12 h light:12 h dark, or
16 h light:8 h dark for twelve weeks at a low water temperature (9°C).
Fig. 1. Growth of mirror carp kept at 8 h light:16 h dark, 12 h light:12 h dark, or 16 h light:8 h dark for
twelve weeks at a low water temperature (9°C).
70
65
60
55
50 4812
8:16 LD 12:12 LD 16:8 LD
1.5
1.2
0.9
0.6
0.3 4812
8:16 LD 12:12 LD 16:8 LD
Week
Week
Body wt (g)
Thyroxin (ng/dl)
22
Similar to our findings, reduction in growth was
reported in trout kept at a low water tempera-
ture of 2.5°C (Larsen et al., 2001).
Although no significant differences were
observed in the present study with respect to
weight gain, it has been reported that photope-
riod and temperature affect growth in some
species. Boehlert (1981) showed that 16 h
light:8 h dark enhanced growth in Sebastes
diploproa compared to 12:12, and is probably
related to a lower metabolic rate. Gilthead
seabream raised in longer light periods (in an
experiment testing 8:16, 12:12, 16:8, 24:0, and
natural
photoperiods
) grew better (Silva-
Garcia, 1996). Boeuf and Le Bail (1999) report-
ed that water temperature ranges from less
than 10°C (December-February) to as high as
20°C (June-August); thus, the fluctuation in
temperature also affects the growth rate.
Multiple mechanisms undoubtedly are involved
in promoting tolerance to low temperatures. In
goldfish, for example, acclimation to tempera-
tures below 10°C evokes a highly regulated
reduction in the metabolic rate, membrane
phospholipid reorganization, and alterations in
enzyme-substrate affinity relative to warm-
acclimated individuals (Ganim et al., 1998).
In fish, the secretion of thyroid hormones
is influenced by photoperiod, temperature,
and food intake (Cyr et al., 1998; Tiitu and
Vornanen, 2003). Food intake depends on
temperature and is high in spring and summer
when light effects better food conversion effi-
ciency and, thus, better growth (Boeuf and Le
Bail, 1999). Contrary to the effects on growth,
it is difficult to distinguish how photoperiod
affects the thyroid hormone level. We raised
the carp in a low water temperature to assure
that any fluctuation in thyroid level could not
be attributed to an increased feed intake
resulting from a warmer environment.
Differences in T4 level could result only from
differences in the photoperiod. Indeed, we
found that T4levels were significantly reduced
by a longer period of light throughout the
study period.
Similarly, Larsen et al. (2001) reported
that during the winter, when day lengths are
short and temperature is low, T4levels are rel-
atively unaffected by manipulations in feeding
and temperature compared with insulin or
insulin-like growth factor-I (IGF-I) and sug-
gested that photoperiod has a more signifi-
cant effect on the plasma profile of T4than
temperature or ration. However, the 8:16 and
12:12 treatments significantly differed from
the 16:8 treatment, showing that low water
temperature had a lesser impact on T4in a
short photoperiod than in a long photoperiod.
In other words if the water temperature had
been optimum, fish exposed to longer periods
of light would have grown better (Silva-Garcia,
1996; Boehlert, 1981) and thyroxin secretion
would have increased. Similarly, Brown and
Stetson (1985) showed that 14 h light
increased and 8 h light decreased the nega-
tive feedback sensitivity of the hypothala-
mus–pituitary axis to TH in killifish Fundulus
heteroclitus. They proposed that such a pho-
toperiod-induced change could aid in the
year-round maintenance of thyroxin levels
necessary for seasonal adaptation and sur-
vival. Eales and Fletcher (1982) also
observed seasonal changes in plasma TH
levels in laboratory and wild fish while Osborn
and Simpson (1978) obtained seasonal varia-
tions in plasma circulating T3and T4, with
maxima reached in winter and summer.
Obviously, these changes, even if related to
light as in the present study, can also be
linked to temperature changes as mentioned
in the above studies.
There were no significant differences in
growth while the T4value was much lower at
16:8. These results suggest that future aqua-
culture studies, especially off-season studies,
should not be based on a photoperiod of 16
light:8 dark. Further studies should be con-
ducted at optimum and high temperatures to
test various photoperiods in other fish
species.
References
Boehlert G.W., 1981. The effects of photope-
riod and temperature on laboratory growth of
juvenile Sebastes diploproa and a comparison
with growth in the field. Fish. Bull., 79:789-
794.
Boeuf G. and P-Y. Le Bail, 1999. Does light
have an influence on fish growth? Aquaculture,
Hisar et al.
177:129-152.
Brown C.L., 1988. Photoperiod effects on thy-
roid function in fish. pp. 1-17. In: M.H. Stetson
(ed.). Processing of Environmental
Information in Vertebrates. Springer, New
York.
Brown C.L. and M.H. Stetson, 1985.
Photoperiod-dependent negative feedback
effects of thyroid hormones in Fundulus hete-
roclitus. Gen. Comp. Endocrinol., 58:186-191.
Cyr D.G., Idler D.R., Audet C., McLeese
J.M. and J.G. Eales, 1998. Effects of long-
term temperature acclimation on thyroid hor-
mone deiodinase function, plasma thyroid
hormone levels, growth, and reproductive sta-
tus of male Atlantic cod, Gadus morhua. Gen.
Comp. Endocrinol., 109:24-36.
Dickhoff W.W., Folmar L.C., Mighell J.L.
and C.V.W. Mahnken, 1982. Plasma thyroid
hormones during smoltification of yearling and
underyearling coho salmon and yearling
Chinook salmon and steelhead trout.
Aquaculture, 28:39-48.
Dutta H., 1994. Growth in fishes. Geronto-
logy, 40:97-112.
Eales J.G. and G.L. Fletcher, 1982.
Circannual cycles of thyroid hormones in plas-
ma of winter flounder Pseudopleuronectes
americanus Walbaum. Can. J. Zool., 60:304-
309.
Ganim R.B., Peckol E.L., Larkin J.,
Ruchhoeft M.L. and J.S. Cameron, 1998.
ATP-sensitive K+channels in cardiac muscle
from cold-acclimated goldfish: characteriza-
tion and altered response to ATP. Comp.
Biochem. Physiol., 119A(1):395-401.
Gavlik S., Albino M. and J.L. Specker,
2002. Metamorphosis in summer flounder:
manipulation of thyroid status to synchronize
settling behavior, growth, and development.
Aquacul-ture, 203:359-373.
Gross W.L., Roelofs E.W. and P.O. Fromm,
1965. Influence of photoperiod on growth of
green sunfish, Lepomis cyanellus. J. Fish.
Res. Board Can., 22:1379-1386.
Gupta B.B.P. and J.P. Thapliyal, 1991.
Endocrine regulation of the oxidative metabo-
lism in poikilothermic vertebrates. Zool. Sci.,
8:625-634.
Hepher B., 1988. Nutrition of Pond Fishes.
Cambridge University Press, New York, New
Rochelle, Melbourne Sydney.
Larsen D.A., Beckman B.R. and W.W.
Dickhoff, 2001. The effect of low temperature
and fasting during the winter on metabolic
stores and endocrine physiology (insulin,
insulin-like growth factor-I, and thyroxin) of
coho salmon, Oncorhynchus kisutch. Gen.
Comp. Endocrinol., 123:308-323.
Leatherland J.F., 1994. Reflections on the
thyroidology of fishes: from molecules to
humankind. Guelph Ichthyol. Rev., 2:1-67.
MacKenzie D.S., VanPutte C.M. and K.A.
Leiner, 1998. Nutrient regulation of endocrine
function in fish. Aquaculture, 161:3-25.
Matty A.J., 1985. The thyroid gland. pp. 54-
83. In: A.J. Matty (ed.). Fish Endocrinology.
Croom Helm, London.
McCormick S.D., Saunders R.L., Hender-
son E.B. and P.R. Harmon, 1987.
Photoperiod control of parr-smolt transforma-
tion in Atlantic salmon (Salmo salar): changes
in salinity tolerance, gill Na
+
, K
+
-ATPase activ-
ity, and plasma thyroid hormones. Can. J.
Fish. Aquat. Sci., 44:1462-1468.
Mercure F., Holloway A.C., Tocher D.R.,
Sheridan M.A., Van der Kraak G. and J.F.
Leatherland, 2001. Influence of plasma lipid
changes in response to 17b-oestradiol stimu-
lation on plasma growth hormone, somato-
statin, and thyroid hormone levels in immature
rainbow trout. J. Fish Biol., 59:605-615.
Monteverdi G.H. and R.T. Di Giulio, 2000.
Vitellogenin association and oocytic accumu-
lation of thyroxin and 3,5,3’-triiodothyronine in
gravid Fundulus heteroclitus. Gen. Comp.
Endocrinol., 120:198-211.
Osborn R.H. and T.H. Simpson, 1978.
Seasonal changes in thyroidal status in the
plaice, Pleuronectes platessa L. J. Fish Biol.,
12(6):519-526.
Pavlidis M., Greenwood L., Mourot B.,
Kokkari C., Le Menn F., Divanach P. and
A.P. Scott, 2000. Seasonal variations and
maturity stages in relation to differences in
serum levels of gonadal steroids, vitellogenin,
and thyroid hormones in the common dentex
(Dentex dentex). Gen. Comp. Endocrinol.,
118:14-25.
Peter M.C.S., Lock R.A. and S.E.W. Bonga,
23Effect of photoperiod on plasma thyroxine hormone level of mirror carp
24
2000. Evidence for an osmoregulatory role of
thyroid hormones in the fresh water
Mozambique tilapia, Oreochromis mossambi-
cus. Gen. Comp. Endocrinol., 120:157-167.
Porter M.J.R., Randall C.F., Bromage N.R.
and J.E. Thorpe, 1998. The role of melatonin
and the pineal gland on development and
smoltification of Atlantic salmon (Salmo salar)
parr. Aquaculture, 168:139-155.
Power D.M., Llewellyn L., Faustino M.,
Nowell M.A., Bjornsson B.T., Einarsdottir
I.E., Canario A.V. and G.E. Sweeney, 2001.
Thyroid hormones in growth and development
of fish. Comp. Biochem. Physiol., 130C:447-
459.
Samejima M., Shavali S., Tamotsu S.,
Uchida K., Morita Y. and A. Fukada, 2000.
Light temperature-dependence of the lam-
preys, Lampetra japonica. Jpn. J. Physiol.,
50:437-442.
Sánchez–Vázquez F.J., Iigo M., Madrid J.A.
and M. Tabata, 2000. Pinealectomy does not
affect the entrainment to light nor the genera-
tion of the circadian demand-feeding rhythms
of rainbow trout. Physiol. Behav., 69:455-461.
Silva-Garcia A.J., 1996. Growth of juvenile
gilthead seabream (Sparus aurata L.) reared
under different photoperiod regimes. Israeli J.
Aquacult. – Bamidgeh, 48:84-93.
Tiitu V. and M. Vornanen, 2003. Does differ-
ent thyroid state effect on the contractility of
the cardiac muscle of eurythermal fish
species, rainbow trout (Oncorhynchus mykiss,
Walbaum)? J. Therm. Biol., 28:35-42.
Volkoff H., Wourms J.P., Amsebury E. and
F.F. Snelson, 1999. Structure of the thyroid
gland, serum thyroid hormones, and the
reproductive cycle of the Atlantic stingray,
Dasyatis sabina. J. Exp. Zool., 284:505-516.
Hisar et al.
