Journal of Thermal Biology 45 (2014) 6268

Contents lists available at ScienceDirect

Journal of Thermal Biology

journal homepage: www.elsevier.com/locate/jtherbio

Effect of temperature on the effectiveness of articial reproduction of

dace [Cyprinidae (Leuciscus leuciscus (L.))] under laboratory and eld
conditions
Joanna Nowosad a, Katarzyna Targoska a, Rafa Chwaluczyk b, Rafa Kaszubowski c,
Dariusz Kucharczyk a,n
a

Department of Lake and River Fisheries, University of Warmia and Mazury in Olsztyn, Poland

Czarci Jar Fish Farm, Poland

Janowo Fish Farm, Poland

arti cl e i n fo

abs tract

Article history:
Received 13 March 2014
Received in revised form
19 July 2014
Accepted 31 July 2014
Available online 7 August 2014

This study sought to determine the effect of water temperature on the effectiveness of articial
reproduction of dace brooders under laboratory and eld conditions. Three temperatures were tested
in the laboratory: 9.5, 12 and 14.5 C ( 70.1 C). The water temperature under eld conditions was
11.07 0.3 C (Czarci Jar Fish Farm) and 13.27 1.4 C (Janowo Fish Farm). The study showed that articial
reproduction of dace is possible in all the temperature ranges under study and an embryo survival rate of
over 87% can be achieved. Dace has also been found to be very sensitive to rapid temperature changes,
even within the temperature ranges optimal for the species. Such changes have an adverse effect on the
outcome of the reproduction process, such as a decrease in the percentage of reproducing females, a
decrease in the pseudo-gonado-somatic index (PGSI) and a decrease in the embryo survival rate.
& 2014 Elsevier Ltd. All rights reserved.

Keywords:
Temperature uctuations
Dace
Reproduction
Spawning effectiveness

1. Introduction
Temperature is one of the most important environmental

are in danger of extinction due to global warming (McGrath, 2012).

Water warming and seasonal temperature uctuations signifactors affecting life processes in organisms. Poikilotherms, which

include sh, are especially sensitive to temperature and its

uctuations (Burt et al., 2011; Targoska et al., 2014). The
tem-perature of their bodies depends closely on the
environment in which they live. Temperature changes accelerate
or delay gamete maturation (Vikingstad et al., 2008) and may
affect the time and course of spawning (Hilder and Pankhurst,
2003), the quality and size of eggs (Gillet et al., 1996; Pankhurst
et al., 1996; King et al., 2003; Kucharczyk et al., 2014; Nowosad et
al., 2014) as well as the larvae growth, development and survival
rates (Kucharczyk et al., 1997; 1998; Kujawa et al., 1997;
Kupren et al., 2010, 2011). Moreover, the temperature in sh
is responsible for the period of nal gamete maturation (FOM)
and can even inhibit the reproduc-tion process or reduce the
larvae survival rate to 0% (Bromage et al., 2001; Davies and
Bromage, 2002; Kupren et al., 2011). Weather anomalies,
including the temperature uctuations ob-served in recent
years, pose a serious threat to global biodiversity (Morrongiello et
al., 2011). It is estimated that 24% of sh species
n

Corresponding author. Tel.: 48 895234215; fax: 48 895233969.

E-mail address: dariusz.kucharczyk@uwm.edu.pl (D. Kucharczyk).

http://dx.doi.org/10.1016/j.jtherbio.2014.07.011
0306-4565/& 2014 Elsevier Ltd. All rights reserved.

cantly affect reproduction and sh size (Pankhurst and Munday,

2011; McGrath, 2012). The ndings of the study conducted with
common bream (Abramis brama) under controlled and eld conditions are an example of the adverse effect of water temperature
and its uctuations on the effectiveness of sh reproduction
(Targoska et al., 2014). The deteriorating condition of the natural
environment, climate and other changes: for example, regulation
of rivers, deterioration of natural habitats and spawning grounds
of rivers, all reduce the abundance of aquatic species (Daufresne
et al., 2004; Kujawa and Gliska-Lewczuk, 2011, McGrath, 2012;
Comte et al., 2013). Because of the rapid decrease in the size of
populations of rheophilic cyprinids in rivers, these species have
become objects of scientic interest (e.g. Penczak and Kruk, 2000;
Copp et al., 2007; Kupren et al., 2008; 2010; arski et al., 2009).
Populations of rheophilic sh can be restored, but this requires
developing or perfecting reproduction techniques. One of the most
important elements of reproduction biotechnology is to establish
the optimum thermal conditions during the nal gamete maturation as well as ovulation and spermiation (Cejko et al., 2010;
Targoska et al., 2010, 2011; arski et al., 2010; Nowosad et
al., 2014). It is only a combination of the proper stimulation
with environmental (especially thermal) conditions and the
administration of the appropriate hormonal agents that can guarantee

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

biotechnological success (e.g. Kucharczyk et al., 2005, 2008;

Kujawa et al., 2011). Dace (Leuciscus leuciscus (L.)) is one of the
least-known rheophilic cyprinids (Cyprinidae), but it is an important element of European ichthyofauna (Mann and Mills, 1986;
Penczak and Kruk, 2000; Copp et al., 2007; Kucharczyk et al.,
2008; Cejko et al., 2012; Kirtiklis et al., 2013). It occurs mainly in
upper and middle parts of rivers, without vegetation. These sh
prefer deeper water, with a stronger current and a bottom covered
with pebbles, gravel or sand (Mills, 1981; Mann and Mills, 1986;
Tadajewska, 1986; Kucharczyk et al., 2008). According to
Tadajewska (1986), reproduction of dace in the natural environment takes place from April to May at a water temperature of 10
12 C, whereas according to Mann (1996) it occurs from February
to April at a temperature between 5 C and 12 C. The narrow
range of the optimum temperature for reproduction of dace (10
12 C) has made it a species endangered with extinction due to
climate change. Although dace is regarded as being relatively
resistant to environmental changes, detailed studies of the populations of lotic waters have shown a signicant reduction in
population sizes (Penczak et al., 2004; Augustyn, 2004; Copp
et al., 2007). The climate changes may make this situation worse.
In the case of the dace population from the Sawica and Marzka
Rivers (North Poland), dace females with resorbing eggs were
collected during the spawning season at water temperatures
between 11 C and 15 C. On the other hand, the same information
was obtained from eld hatcheries located in this area. This
indicates that the temperature during dace spawning season is
too high for normal ovary and oocyte development or the
temperature changes might be too rapid. In northern Poland, the
temperature has increased rapidly (over 23 C per day) during
the spring over the last few years. For this reason, it was decided to
reproduce dace spawners under three constant temperatures:
9.5 C, 12.0 C and 14.5 C, which represent the temperature
regimes registered last years for dace spawning under natural
and hatchery-eld conditions as well as dace reproduced in two
eld hatcheries located in the spring-water of the Drwca River
(with an approximately constant and cold temperature) and lake
surface water of the Sawica River (uctuating and hot temperatures). Both rivers are located in the same area at a distance of
about 25 km. The aim of the study was to determine the effect of
temperature on the effectiveness of articial reproduction of dace
under laboratory and eld conditions.

63

2. Materials and methods

2.1. Brood-stock handling and management
Dace spawners were obtained from the Marzka River in the
autumn period (November). After capturing, all individuals were
transported and kept in at ponds at Czarci Jar Fish Farm (northeast Poland) until mid-February. When the water temperature
reached 6 C the sh were transported to the hatchery. The weight
of spawners was between 91 to 326 g. During all manipulations,
the spawners were anaesthetised with 2-phenoxyethanol in a tank
3

at a concentration of 0.4 cm dm . All sh were individually

marked using oy-tags and then weighed and the oocytes were
obtained by means of a catheter and placed in Serra's solution
(prepared with 70% ethanol, 40% formaldehyde and 99.5% acetic
acid in proportions of 6:3:1, respectively) for clarication of the
cytoplasm. After 5 min, the position of the oocyte nucleus (germinal vesicle) was determined using a 4-stage scale (Brzuska 1979):
germinal vesicle in central position (CGV, stage 1),
early migration of germinal vesicle (less than half of the radius
MGV, stage 2),
late migration of germinal vesicle (more than half of the radius
PGV, stage 3), and
peripheral germinal vesicle or germinal vesicle breakdown
(GVBD, stage 4).
Further experiments were done only on females with oocytes
at stages 23. Marked females and males were kept separately in
1000 dm3 aerated basins (Kujawa et al., 1999). The water temperature was raised from 5 C to 9.5 C during 6 days.
2.2. Hormonal stimulation and temperature
Two separate experiments were performed in the present
study. In both, Ovopel was used as a spawning agent. Hormones
were injected intraperitoneally under the ventral n. Two different
doses were used: 0.2 and 1.0 pellet kg 1. One Ovopel pellet
(average weight about 25 mg) contains 1820 g mammalian
6
9
9
GnRH analogue (D-Ala , Pro NetPro NEt-mGnRHa) and 810 mg
of dopamine antagonist (metoclopramide) (Horvath et al., 1997).
The pellets were pulverised and then dissolved in saline solutions
(0.9% sterile NaCl). The time between the initial and resolving
injection was 24 h (Targoska et al., 2010).

Fig. 1. Temperature distribution during the dace reproduction process under laboratory (A) and eld conditions on the Czarci Jar Fish Farm and the Janowo Fish Farm (B).

64

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

2.2.1. Experiment I: the reproduction of dace at three constant

temperatures
Fish were divided into three temperature groups: 9.5 C, 12.0 C
and 14.5 C ( 7 0.1 C) (called group T9.5, group T12.0 and group
T14.5). The temperature in each experimental group was established (from 9.5 C) over 24 h. On the next day, the sh were
injected with hormones. The schema of the temperature during
the experiment is presented on Fig. 1A.
2.2.2. Experiment II: the reproduction of dace at uctuated
temperatures
For this experiment, sh were transferred to two sh farms: the
Czarci Jar Fish Farm (spring-water of the Drwca River with an
approximately constant temperature) and the Janowo Fish Farm
(lake surface water of Sawica River with uctuating temperature)
with natural water conditions. When the water temperature rose
to 9.5 C, the sh received the hormonal injections as described
earlier. The temperature water regimes from both sh farms are
presented in Fig. 1B.
In both experiments, males and females were kept separately
3
in 1000 dm tanks. Several parameters were noted and calculated:
BWI body weight increase (in females only) actual body
weight (BW)n100%/initial body weight (BW);
Percentage of ovulation number of ovulated femalesn100%/
number of all females in the group;
PGSI pseudo-gonado-somatic index (in females only)
weight of collected eggsn100%/weight of female body (BW);
Embryo survival rate number of live embryos in eyed-eggstagen100%/number of all embryos in the sample;
Survival of spawners number of live sh at the end of the
experiment n100%/number of sh at the beginning of the
experiment.

2.3. Obtaining the gametes and incubation

The milt was collected 2472 h after hormonal stimulation
using syringes. It was kept chilled at 4 C until the total volume
was recorded. The motility of spermatozoa was determined in a
0.5% solution of NaCl under a microscope (magnication 500x)
within 30 min of collection. The milt was collected at the same
time that mass ovulation was observed from the females.
Ovulation was examined every 4 h, from 2472 h after the
second injection. The eggs from each female were placed separately into plastic bowls and then 100150 eggs, in triplicate, from
each female were placed on separate Petri dishes for the fertilisation test. Only sperm samples with a milt motility higher than 60%
were used to fertilise the eggs. Samples of fertilised eggs were

3. Results
3.1. Experiment I
Present studies have shown that if water temperature is slowly
increased before hormonal stimulation in dace (Fig. 1A), the sh
can reproduce at temperatures of 9.5 C, 12 C and 14.5 C. The
latency time was related to the water temperature in which the
spawners were kept and was 3648 h, 4260 h and 4872 h in
T14.5, T12.0 and T9.5 groups, respectively (Table 1; Fig. 2A). The
percentage of ovulating females was high (over 89%) in all groups.
The highest percentage of ovulating females was found in group
T14.5 (100%) and the lowest (89%) was in group T12.0 (Table 1).
The highest percentage of ovulating females in all groups was
found between 19 and 26 degree-days (DD) (Fig. 2B). No signicant differences were found in the pseudo-gonado-somatic index
(P o0.05) (Fig. 3). The highest embryo survival rate (over 92%) was
recorded in the group T12.0 in females showing a latency time of
48 h (Fig. 4A). Converted to degree-days, the highest embryo
survival rate was recorded in all female groups in which the
latency time was 2326 DD (Fig. 4B). In each of the temperature
variants, the spawns of females ovulating between 28 and 30
degree-days showed both kind of oocytes: normal green-grey
coloured and some white coloured (dead oocytes).

3.2. Experiment II
Spawning was successful both at Czarci Jar Fish Farm and at
Janowo Fish Farm, where dace brooders were kept at different
temperatures. The average water temperature (mean 7 SD) on the
farms was 11.07 0.3 and 13.2 7 1.4 C, respectively, but it
in-creased and uctuated both before and after the
hormonal stimulation (Fig. 1B). At Czarci Jar, 100% of females
ovulated within 2642 h after the second injection. In Janowo
(where the tem-perature uctuated more), only 75% of females
ovulated and the latency time was 3660 h (Table 2, Fig. 5A).
Converted to degree-days, the latency time in both farms
was 1933 degree-days (Fig. 5B). The value of PGSI (mean7 SD)
and the embryo survival rate were signicantly higher (P o 0.05)
in the females at Czarci Jar (Table 2) than at the Janowo Fish
Farm. Additionally, the correla-tion between female weight and
PGSI was found for female spawn at Czarci Jar, which was
contrary to the sh spawn in the second farm (Fig. 6A and B).
Signicant differences between both farms were observed for
the embryo survival to the eyed-egg-stage when the latency
time was evaluated in hours and degree days (Fig. 7) The
survival of females during the both experiments was excellent.

incubated to the eyed-egg-stage in 100 dm basins placed in a

recirculating system up to 12 C ( 7 0.1) which was found to be the
optimal temperature for dace embryo development (Kupren et al.,
2010, 2011).

Table 1
The outcome of dace reproduction under laboratory conditions at three temperao

tures: 9.5 C, 12.0 C and 14.5 C. The data are presented as a mean 7 SD. The data
denoted with different letters were statistically different (Po 0.05).

2.4. Statistical analysis

The data expressed as percentages were log-transformed
before calculations. ANOVA was used to test the effect temperature
on milt quantity and quality as well as on embryo survival to the
eyed-egg-stage. The signicance of differences between groups
was estimated using a post-hoc Duncan's multiple range test with
a signicance level of o 0.05.

T9.5
Initial BW [g]
BWI [%]
Ovulating females [%]
Latency time [h]
PGSI [%]
Embryo survival rate to eyed-eggstage [%]

T12.0

120.7 7 48.4 121.7 7 43.3

119.8 7 43.6 102.1 7 1.7
102.1 7 2.7 94 89
4872
4260
17.6 7 2.8
16.7 7 3.8
a
a
92.17 2.6
92.7 7 3.8

T14.5

102.4 7 1.6
100
3648
18.0 7 4.3
b
87.5 76.0

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

65

Fig. 2. The relationship between the percentage of ovulating females kept at three temperature ranges (9.5 C, 12.0 C and 14.5 C) and the latency time in hours (A) and
degree-days (B).

Fig. 3. The gonado-somatic index depending on the latency time, converted to hours (A) and degree-days (B) during the dace reproduction period at three temperatures
(9.5 C, 12.0 C and 14.5 C). The data are presented as a mean 7 SD.

Fig. 4. Embryo survival rate depending on the latency time, in hours (A) and degree-days (B) during the dace reproduction period at three temperatures (9.5 C, 12.0 C and
14.5 C). The data are presented as a mean 7 SD. The data in rows denoted with different letters were statistically different (Po 0.05).

66

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

Table 2
The outcome of dace reproduction under eld conditions in the Czarci Jar Fish Farm
and Janowo Fish Farm. The data are presented as a mean 7SD. The data denoted
with different letters were statistically different (Po 0.05).

Temperature [C]
Initial BW [g]
BWI [%]
Ovulating females [%]
Latency time [h]
PGSI [%]
Embryo survival rate to eyed-eggstage [%]

Czarci Jar Fish Farm

Janowo Fish Farm

11.0 70.3
122.8 721.
1
102.1 7 1.7
100
4260
a
28.0 7 5.5
a
86.2 7 4.2

13.27 1.4
116.0 7 21.
9
101.6 7 1.4
75
3660
b
22.3 7 4.0
b
63.9 7 16.0

4. Discussion
To date, reproduction of dace under controlled condition has
been conducted at 12 C (Kucharczyk et al., 2008; Kupren et al.,
2011; Cejko et al., 2012, Targoska et al., 2013). The spawning
of dace in this experiment was conducted at 9.5 C, 12 C and 14.5
C (experiment I) and the embryo survival rate was high
(above 87.5%) at all temperatures under study after hormonal
treatment. Moreover, the percentage of ovulating females was
the highest at the highest temperature (14.5 C). These results
show
that
dace might
reproduce
successfully
at
temperatures much higher (14.5 C) than previously observed
(1012 C). But this raises the question: is the spawning of dace
really possible at such a high
temperature or is it merely an adaptation to changes in the
environment? Since dace live in a huge area in Eurasia
rate
(Tadajewska, 1986), probably this species might be able to adapt
to the changes in environment if they happen very slowly? During
the rst experiment, no spawning disruption, e.g. egg resorption,
was found in any tested constant temperatures (9.5 C, 12.0 C and
14.5 C). This indicates that the abnormal FOM under natural
conditions in dace observed in Sawica and Marzka River at
temperatures of 1115 C was not only caused by temperature
level. On the other hand, at temperatures of 13.2 71.4 C
(mean 7 SD) on the Janowo Fish Farm, 25% of females did not
ovulate. The difference between the two farms was the uctuating
temperature observed in Janowo. This suggests that rapid temperature uctuations below 14.5 C during FOM might impair
normal gamete development. Manipulating the water temperature
in sh breeding is used in order to precipitate spawning, although
uncontrolled changes in water temperature may cause various
disturbances in the reproductive cycle, or even inhibit spawning,

both in breeding and in the natural environment (Okuzawa et al.,

2003; Targoska et al., 2010, 2014). Epler and Bieniarz
(1979) reported that discharges of cooling water to the
environment from power plants result in increasing the tank
temperature which, in
effect, results in precipitation of spawning and extends the
spawning period in sh. Premature ovulation may cause numerous
developmental anomalies of gonads, resorption of eggs and
hermaphroditism (Epler and Bieniarz, 1979; Luksiene and
Sandstrm, 1994). Among the species with particular sensitivity
to pollutants, including thermal pollution, are rheophilic cyprinids: asp (Aspius aspius), barbel (Barbus barbus), vimba bream
(Vimba vimba), ide (Leuciscus idus), chub (Leuciscus cephalus)
common nase (Chondrostoma nasus) and dace (Daufresne et al.,
2004; Penczak et al., 2004; Kujawa and Gliska-Lewczuk, 2011;
Comte et al., 2013). The effectiveness of actions which aim to
protect endangered species depends on how well the species
biology has been elucidated. Therefore, it is important to determine the optimum temperature ranges and to perfect techniques
of sh reproduction under changing conditions, notably climate
change and environmental pollution.
Kupren et al. (2010) found the range from 7.5 C to 12 C to be
the optimum for the incubation of dace eggs. They also found
that dace embryos were able to tolerate temperatures of up to 23
C, although the survival rate decreased and numerous
deformities appeared. Targoska et al. (2014) observed that
an increase in the water temperature above the optimum
value (20 C) to 23.5 C in bream reproduction resulted in a
decrease in the percentage of ovulating
females and a decrease in the embryo survival rate. On the other
hand,
a temperature increase resulted in a decrease in the spermiation
(80%), sperm quantity and spermatozoa motility in male
bream (Targoska et al., 2014). Such irregularities may have been
caused by an excessively high water temperature, which inhibits
the expression of genes which are responsible for the secretion of
hormones affecting nal gamete maturation and ovulation
(Okuzawa et al., 2003).
It was shown that temperatures and their uctuations during
nal gamete maturation in dace play the most important role from
among environmental factors. Temperature uctuations might
stop ovulation and decrease the quality of oocytes and survival
rates of embryos and spawners. Targoska et al. (2014) observed
that a rapid decrease in water temperature may interrupt bream
spawning. Furthermore, a slight decrease in water temperature for
the ide (L. idus) nal gamete maturation (FOM) did not interrupt
spawning, although it considerably extended the latency time
(Targoska et al., 2011). A worse outcome of the reproduction
process and inhibition of ovulation caused by a sudden increase in

Fig. 5. The relationship between the percentage of ovulating females and the latency time in hours (A) and degree-days (B).

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

67

Fig. 6. The relationship between the pseudo gonado-somatic index and the body weight of a female dace on the Czarci Jar Fish Farm (A) and the Janowo Fish Farm (B).

Fig. 7. Embryo survival rate depending on the latency time, in hours (A) and degree-days (B) during the dace reproduction period at the Czarci Jar Fish Farm and the Janowo
Fish Farm. The data are presented as a mean 7 SD. The data in rows denoted with different letters were statistically different (P o0.05).

temperature was also observed in the asp (Targoska et al., 2010).

Reproduction process and ovulation were inhibited with rapid
temperature a uctuation which was connected with hormonal
activity responsible for reproductive functions (Okuzawa et al.,
2003; Takahara et al., 2011).

Acknowledgements
This study was nanced by Innovations in nsh aquaculture
with special reference to reproduction, Operational Programme
Sustainable Development of the Fisheries Sector and Coastal Fishing Areas 20072013 (OR14-61724-OR1400003/09/10/11).

5. Conclusions
In conclusion, it appears that dace is not as strongly stenothermic (in its reproduction) as previously observed. This study has
shown that it can be reproduced successfully under controlled
conditions not only in the temperature range from 10 C to 12 C,
but also at 14.5 C, with a resulting 100% ovulation and an embryo
survival rate of over 87%. Dace has also been found to be sensitive
to rapid temperature changes, even within the temperature ranges
tested in this study: uctuations in water temperature after the
administration of ovulation-inducing hormones had a negative
effect on reproduction. Such changes adversely affected the
percentage of ovulating females and the quantity and quality of
gametes; thereby, they may affect the natural recruitment. Since
dace is a sh with a short life cycle, any spawning disruption might
strongly inuence the natural population.

References
Augustyn, L., 2004. Restytucja karpiowatych ryb rzecznych w grnym i rodkowym
Dunajcu. Arch. Ryb. Pol 12 (Suppl. 2), 279286 (in Polish).
Bromage, N., Porter, M., Randall, C., 2001. The environmental regulation of
maturation in farmed nsh with special reference to the role of photoperiod
and melatonin. Aquaculture 197, 6398.
Brzuska, E., 1979. The in vivo method of estimating the stages of oocyte maturation
in carp Cyprinus carpio L. Acta Hydrobiol 21, 423433.
Burt, J.M., Hinch, S.G., Patterson, D.A., 2011. The importance of parentage in
assessing temperature effects on sh early life history: a view of the experimental literature. Rev. Fish Biol. Fish. 21, 377406.
Cejko, B.I., Kucharczyk, D., Targoska, K., arski, D., Sarosiek, B., Kowalski, R.K.,
Glogowski, J., 2010. Inuence of temperature on the effectiveness of the
hormonal stimulation of male ide, Leuciscus idus (L.). Arch. Pol. Fish 18, 205
211.
Cejko, B.I., Targoska, K., Kowalski, R.K., arski, D., Sarosiek, B., Kucharczyk, D.,
Glogowski, J., 2012. The effectiveness of hormonal preparations (Ovopel,

68

J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268

Ovaprim, LHRHa, hCG and CPE) in stimulating spermiation in dace Leuciscus

leuciscus (L.). J. Appl. Ichthyol. 28, 873877.
Comte, L., Buisson, L., Daufresne, M., Grenouillet, G.L., 2013. Climate-induced
changes in the distribution of freshwater sh: observed and predicted trends.
Freshw. Biol. 58, 625639.
Copp, G.H., England, J., Tyner, R., Carter, M.G., Stakenas, S., Przybylski, M., Wesley, K.
J., 2007. Growth and condition of dace Leuciscus leuciscus (L. 1758) in the River
Lee (Hertfordshire) relative to selected populations elsewhere in Europe. Lond.
Nat. 86, 7185.
Davies, B., Bromage, N., 2002. The effects of uctuating seasonal and constant water
temperatures on the photoperiodic advancement of reproduction in female
rainbow trout, Oncorhynchus mykiss. Aquaculture 205, 183200.
Daufresne, M., Roger, M.C., Capra, H., Lamouroux, N., 2004. Long-term changes
within the invertebrate and sh communities of the Upper Rhone River: effects
of climatic factors. Glob. Chang. Biol. 10, 124140.
Epler, P., Bieniarz, K., 1979. Sexual maturity of sh in heated water. Pol. Ecol. Stud. 5,
5263.
Gillet, C., Breton, B., Mikoajczyk, T., 1996. Effects of GnRHa and pimozide
treatments on the timing of ovulation and on egg quality in Arctic charr
(Salvelinus apinus) at 5 and 10 C. Aquat. Living Resour. 9, 257260.
Hilder, M.L., Pankhurst, N.W., 2003. Evidence that temperature change cues
reproductive development in the spiny damselsh, Acanthochromis polyacanthus. Environ. Biol. Fishes 66, 187196.
Horvath, L., Szabo, T., Burke, J., 1997. Hatchery testing of GnRH analogue-containing
pellets on ovulation in four cyprinid species. Pol. Arch. Hydrobiol. 44, 281285.
King, H., R., Pankhurst, N.W., Watts, M., Pankhurst, P.M., 2003. Effect of elevated
summer temperatures on gonadal steroid production, vitellogenesis and egg
quality in female Atlantic salmon. J. Fish Biol. 63, 153167.
Kirtiklis, L., Grzymkowska, M., Boro, A., 2013. Characterization of Three Species
from the Subfamily Leuciscinae (Pisces, Cyprinidae) Using the Nuclear ITS-1
rDNA Spacer. Folia Biol. 61, 5357.
Kucharczyk, D., uczyski, M., Kujawa, R., Czerkies, P., 1997. Effect of temperature
on embryonic and larval development of bream (Abramis brama L.). Aquat. Sci.
59, 214224.
Kucharczyk, D., uczyski, M., Kujawa, R., Kamiski, R., Ulikowski, D., Brzuzan, P.,
1998. Inuences of temperature and food on early development of bream
(Abramis brama L.). Arch. Hydrobiol. 141, 243256.
Kucharczyk, D., Kujawa, R., Mamcarz, A., Targoska-Dietrich, K., Wyszomirska, E.,
Glogowski, J., Babiak, I., Szab, T., 2005. Induced spawning in bream (Abramis
brama L.) using pellets containing GnRH. Czech J. Anim. Sci. 50, 8995.
Kucharczyk, D., Mamcarz, A., Kujawa, R., Targoska, K., 2008. Jelec. Mercurius
Kaczmarek Andrzej, Olsztyn.
Kucharczyk, D., arski, D., Targoska, K., uczyski, M.J., Szczerbowski, A., Nowosad,
J., Kujawa, R., Mamcarz, A., 2014. Induced articial androgenesis in common
tench, Tinca tinca (L.), using common carp and common bream eggs. Ital. J
Anim. Sci. 13, 196200.
Kujawa, R., Kucharczyk, D., Mamcarz, A., 1997. Effect of temperature on embryonic
development of asp (Aspius aspius L.). Pol. Arch. Hydrobiol. 44, 139143.
Kujawa, R., Kucharczyk, D., Mamcarz, A., 1999. A model system for keeping
spawners of wild and domestic sh before articial spawning. Aquac. Eng.
20, 8589.
Kujawa, R., Gliska-Lewczuk, K., 2011. The impact of regulation and hydrotechnical
works in river channels on the rheophilic Cyprinidae sh. Contem. Probl.
Manag. Environ. Prot. 7, 233248.
Kujawa, R., Kucharczyk, D., Mamcarz, A., arski, D., Targoska, K., 2011. Articial
spawning of common tench Tinca tinca (Linnaeus, 1758), obtained from wild
and domestic stocks. Aquac. Int. 19, 513521.
Kupren, K., Mamcarz, A., Kucharczyk, D., Prusiska, M., Krejszeff, S., 2008. Inuence
of water temperature on egg incubation time and embryonic development of
sh from genus Leuciscus. Pol. J. Nat. Sci. 23, 461481.
Kupren, K., Mamcarz, A., Kucharczyk, D., 2010. Effects of temperature on survival,
deformation rate and selected parameters of newly-hatched larvae on three
rheophilic cyprinids (Genus Leuciscus). Pol. J. Nat. Sci. 25, 299312.
Kupren, K., Mamcarz, A., Kucharczyk, D., 2011. Effect of variable and constant
thermal conditions on embryonic and early larval development of sh from the
genus Leuciscus (Cyprinidae, Teleostei). Czech J. Anim. Sci. 56, 7080.

Luksiene, D., Sandstrm, O., 1994. Reproductive disturbance in a roach (Rutilus

rutilus) population affected by cooling water discharge. J. Fish Biol. 45, 613625.
Mann, R.H.K., Mills, C.A., 1986. Biological and climatic inuences on the dace
Leuciscus leuciscus in a southern chalk stream. Ann. Rep. F. B. 54, 123136.
Mann, R.H.K., 1996. Environmental requirements of European non-salmonid sh in
rivers. Hydrobiologia 323, 223235.
McGrath, M., 2012. Climate changemay shrink sh. Science Reporter, BBC World
Service. BBS NEWS Science & Environment.
Mills, C.A., 1981. The attachment of dace, Leuciscus leuciscus L., eggs to the
spawning substratum and the inuence of changes in water current on their
survival. J. Fish Biol. 19, 129134.
Morrongiello, J.R., Beatty, S.J., Bennett, J.C., Crook, D.A., Ikedife, D.N.E.N., Kennard,
M.J., Kerezsy, A., Lintermans, M., McNeil, D.G., Pusey, B.J., Rayner, T., 2011.
Climate change and its implications for Australia's freshwater sh. Mar.
Freshw. Res. 62, 10821098.
Nowosad, J., Kucharczyk, D., Liszewski, T., Targoska, K., Kujawa, R., 2014. Comparison of temperature shock timing to induced articial mitotic gynogenesis and
androgenesis in common tench. Aquac. Int., http://dx.doi.org/10.1007/s10499014-9796-0, in press.
Okuzawa, K., Kumakura, N., Gen, K., Yamaguchi, S., Lim, B-S., Kagawa, H., 2003.
Effect of high water temperature on brain-pituitary-gonad axis of the red
seabream during its spawning season. Fish Physiol. Bioch. 28, 439440.
Pankhurst, N.W., Munday, P.L., 2011. Effects of climate change on sh reproduction
and early life history stages. Mar. Freshw. Res. 62, 10151026.
Pankhurst, N.W., Purser, G.J., Van Der Kraak, G., Thomas, P.M., Forteath, G.N.R., 1996.
Effect of holding temperature on ovulation, egg fertility, plasma levels of
reproductive hormones and in vitro ovarian steroidogenesis in the rainbow
trout Oncorhynchus mykiss. Aquaculture 146, 277290.
Penczak, T., Kruk, A., 2000. Threatened obligatory riverine shes in humanmodied Polish rivers. Ecol. Freshw. Fish 9, 109117.
Penczak, T., Galicka, W., Gowacki, ., Koszaliski, H., Kruk, A., Ziba, G., Kostrzewa, J.,
Marsza, L., 2004. Fish assemblage changes relative to environmental factors
and time in the Warta River, Poland, and its oxbow lakes. J. Fish Biol. 64, 483
501.
Tadajewska, M., 1986. Jelec (Leuciscus leuciscus L.). (Dace, Leuciscus leuciscus L.).
In: Brylinska, M. (Ed.), Freshwater Fish in Poland. PWN, Warsaw, pp. 190193.
Takahara, T., Yamanaka, H., Suzuki, A.A., Honjo, M.N., Minamoto, T., Yonekura, R.,
Itayama, T., Kohmatsu, Y., Ito, T., Kawabata, Z., 2011. Stress response to daily
temperature uctuations in common carp, Cyprinus carpio L. Hydrobiologia
675, 6573.
Targoska, K., Kucharczyk, D., Kujawa, R., Mamcarz, A., arski, D., 2010. Controlled
reproduction of asp, Aspius aspius (L.) using luteinizing hormone releasing
hormone (LHRH) analogues with dopamine inhibitors. Aquaculture 306, 407
410.
Targoska, K., Kupren, K., arski, D., Krl, R., Kucharczyk, D., 2011. Inuence of
thermal conditions on successful ide (Leuciscus idus L.) articial reproduction
during spawning season. Ital. J. Anim. Sci. 10 (e50), 209212.
Targoska, K., Paliska-arska, K., Nowosad, J., Kucharczyk, D., 2013. The rst
description of agonistic reproductive behaviour in dace, Leuciscus leuciscus
(L.) males in captivity following hormone treatment. Pensee 75, 198203.
Targoska, K., arski, D., Kupren, K., Paliska-arska, K., Mamcarz, A., Kujawa, R.,
Skrzypczak, A., Furgaa-Selezniow, G., Czarkowski, T.K., Haku-Bakowska, A.,
Kucharczyk, D., 2014. Inuence of temperature during four following spawning
seasons on the spawning effectiveness of common bream, Abramis brama (L.)
under natural and controlled conditions. J. Therm. Biol. 39, 1723.
Vikingstad, E., Andersson, E., Norberg, B., Mayer, I., Klenke, U., Zohar, Y., Stefansson,
S.O., Taranger, G.L., 2008. The combined effects of temperature and GnRHa
treatment on the nal stages of sexual maturation in Atlantic salmon (Salmo
salar L.). Fish Physiol. Biochem. 34, 289298.
arski, D., Kucharczyk, D., Targoska, K., Jamrz, M., Krejszeff, S., Targoska, K.,
2009. Application of ovopel and ovaprim and their combinations in controlled
reproduction of two reophilic cyprinid sh species. Pol. J. Nat. Sci. 24, 235244.
arski, D., Kucharczyk, D., Sasinowski, W., Targoska, K., Targoska, K., 2010. The
inuence of temperature on successful reproductions of burbot, Lota Lota (L.)
under hatchery conditions. Pol. J. Nat. Sci. 25, 93105.