Journal of Thermal Biology 45 (2014) 6268Contents lists available at ScienceDirectJournal of Thermal Biologyjournal homepage: www.elsevier.com/locate/jtherbioEffect of temperature on the effectiveness of articial reproduction of dace [Cyprinidae (Leuciscus leuciscus (L.))] under laboratory and eld conditionsJoanna Nowosada, Katarzyna Targoskaa, Rafa Chwaluczykb, Rafa Kaszubowskic, Dariusz Kucharczyka,na Department of Lake and River Fisheries, University of Warmia and Mazury in Olsztyn, Poland b Czarci Jar Fish Farm, Polandc Janowo Fish Farm, Polanda r t i c l e i n f oArticle history:Received 13 March 2014 Received in revised form 19 July 2014Accepted 31 July 2014 Available online 7 August 2014Keywords:Temperature uctuations DaceReproduction Spawning effectiveness1. Introduction a b s t r a c tThis 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 11.070.3 C (Czarci Jar Fish Farm) and 13.271.4 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.are in danger of extinction due to global warming (McGrath, 2012).Water warming and seasonal temperature uctuations signi-Temperature is one of the most important environmental factors 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 speciesn 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.2014.07.0110306-4565/& 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 con-ditions 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 matura-tion 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 adminis-tration of the appropriate hormonal agents that can guaranteeJ. Nowosad et al. / Journal of Thermal Biology 45 (2014) 626863biotechnological 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 im-portant 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 environ-ment 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 popu-lations 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 tempera-tures). 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 daceunder laboratory and eld conditions. 2. Materials and methods2.1. Brood-stock handling and managementDace 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 (north-east 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 at a concentration of 0.4 cm3 dm3. 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 (germ-inal 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 tem-perature was raised from 5 C to 9.5 C during 6 days.2.2. Hormonal stimulation and temperatureTwo 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 differentdoses were used: 0.2 and 1.0 pellet kg1. One Ovopel pellet (average weight about 25 mg) contains 1820 g mammalian GnRH analogue (D-Ala6, Pro9NetPro9NEt-mGnRHa) and 810 mgof 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 resolvinginjection 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).64J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 62682.2.1. Experiment I: the reproduction of dace at three constant temperaturesFish were divided into three temperature groups: 9.5 C,12.0 C and 14.5 C (70.1 C) (called group T9.5, group T12.0 and group T14.5). The temperature in each experimental group was estab-lished (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 temperaturesFor 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 in 1000 dm3 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-egg-stagen100%/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 incubationThe 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 sepa-rately into plastic bowls and then 100150 eggs, in triplicate, from each female were placed on separate Petri dishes for the fertilisa-tion test. Only sperm samples with a milt motility higher than 60% were used to fertilise the eggs. Samples of fertilised eggs were incubated to the eyed-egg-stage in 100 dm3 basins placed in a recirculating system up to 12 C (70.1) which was found to be the optimal temperature for dace embryo development (Kupren et al.,2010, 2011). 3. Results3.1. Experiment IPresent 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 signi-cant differences were found in the pseudo-gonado-somatic index (Po0.05) (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 IISpawning 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 (mean7SD) on the farms was 11.070.3 and 13.271.4 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 (mean7SD) and the embryo survival rate were signicantly higher (Po0.05) 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.Table 1The outcome of dace reproduction under laboratory conditions at three tempera-tures: 9.5 C, 12.0 C and 14.5 oC. The data are presented as a mean7SD. The datadenoted with different letters were statistically different (Po0.05).2.4. Statistical analysisT9.5T12.0T14.5The data expressed as percentages were log-transformed before calculations. ANOVA was used to test the effect temperatureon milt quantity and quality as well as on embryo survival to the Initial BW [g] BWI [%]Ovulating females [%]Latency time [h] 120.7748.4 121.7743.3 119.8743.6 102.171.7102.471.6 102.172.7 9489100487242603648eyed-egg-stage. The signicance of differences between groupswas estimated using a post-hoc Duncan's multiple range test with a signicance level of o0.05. PGSI [%]Embryo survival rate to eyed-egg-stage [%] 17.672.8 92.172.6a 16.773.8 92.773.8a 18.074.3 87.576.0bJ. Nowosad et al. / Journal of Thermal Biology 45 (2014) 626865Fig. 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 mean7SD.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 mean7SD. The data in rows denoted with different letters were statistically different (Po0.05).66J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268Table 2both in breeding and in the natural environment (Okuzawa et al.,The outcome of dace reproduction under eld conditions in the Czarci Jar Fish Farm and Janowo Fish Farm. The data are presented as a mean7SD. The data denoted with different letters were statistically different (Po0.05).Czarci Jar Fish Farm Janowo Fish Farm 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, ineffect, results in precipitation of spawning and extends theTemperature [C] Initial BW [g] BWI [%]Ovulating females [%] Latency time [h]PGSI [%]Embryo survival rate to eyed-egg-stage [%]4. Discussion 11.070.3 122.8721.1 102.171.7 1004260 28.075.5a 86.274.2a 13.271.4 116.0721.9 101.671.4 753660 22.374.0b 63.9716.0b 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 cypri-nids: 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 toprotect endangered species depends on how well the speciesTo 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 hightemperature or is it merely an adaptation to changes in the biology has been elucidated. Therefore, it is important to deter-mine 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 ovulatingfemales and a decrease in the embryo survival rate. On the other hand,environment? Since dace live in a huge area in Eurasiaa temperature increase resulted in a decrease in the spermiation 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 13.271.4 C (mean7SD) 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 tem-perature 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 variousdisturbances in the reproductive cycle, or even inhibit spawning, (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 reproductionprocess and inhibition of ovulation caused by a sudden increase inFig. 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) 626867Fig. 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 mean7SD. The data in rows denoted with different letters were statistically different (Po0.05).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).5. ConclusionsIn conclusion, it appears that dace is not as strongly stenother-mic (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 mightstrongly inuence the natural population. AcknowledgementsThis study was nanced by Innovations in nsh aquaculture with special reference to reproduction, Operational Programme Sustainable Development of the Fisheries Sector and Coastal Fish-ing Areas 20072013 (OR14-61724-OR1400003/09/10/11).ReferencesAugustyn, 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 experi-mental 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,68J. Nowosad et al. / Journal of Thermal Biology 45 (2014) 6268Ovaprim, 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 polya-canthus. 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 eggquality 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 thegenus 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 daceLeuciscus leuciscus in a southern chalk stream. Ann. Rep. F. B. 54, 123136. Mann, R.H.K., 1996. Environmental requirements of European non-salmonid sh inrivers. 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. Compar-ison of temperature shock timing to induced articial mitotic gynogenesis and androgenesis in common tench. Aquac. Int., http://dx.doi.org/10.1007/s10499-014-9796-0, 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 human-modied 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. Hydrobiologia675, 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.