Effect of temperature on embryonic and larval development of bream

Effect of temperature on embryonic and larval development of bream (Abramis brama L.)

Dariusz Kucharczyk1,*, Miroslaw Luczynski2, Roman Kujawa1

and Piotr Czerkies1

1 Department of Fisheries2 Department of Basic Fishery Sciences; Olsztyn University of Agriculture and Technology,

Oczapowskiego 5, 10-718 Olsztyn-Kortowo, Poland

Key words: Developmental rate, hatching success, incubation time, survival, growth.

ABSTRACT

Influence of water temperature on embryonic and larval development of bream (Abramis brama L.) was stdied. Eggs of bream were incubated at eight constant water temperatures between13.2 and 26.8°C. The temperature of 21.1°C gave highest hatching success, with no abnormalitiesin the eleutheroembryos and lowest mortality observed between eyed egg stage and the time ofhatching. Developmental rate increased with increasing temperature. Duration of embryonicdevelopment (y; hours) decreased with increasing incubation temperature (x; °C) according to theformula: y = 910.1 – 65.88 x + 1.318 x2. Larvae were reared at eight constant temperatures rangingfrom 13.5 to 34.0°C. The instantaneous growth rate in wet weight increased with increasing testtemperature from 13.5 to 29.9°C, and then decreased at higher temperatures. Individual growth offish and biomass production rate were highest at 27.9°C. This temperature is considered optimalwhen food availability and photoperiod are no limiting factors.

Introduction

Temperature is one of the most important environmental factors affecting incuba-tion of fish embryos (Kokurewicz, 1971) and the survival and growth of fish larvae.The effect of temperature is frequently masked by other environmental factors suchas oxygen concentration, photoperiod, or food conditons. Each fish species requiresdifferent temperature conditions for spawning, embryonic, larval, and juvelile development (Herzig and Winkler, 1986).

The functional relationship between temperature and duration of embryonicdevelopment over the full range of temperature tolerance may give recommenda-tion for temperatures optimum for egg incubation. From an ecological point of viewthis relationship is also of obvious importance. There are several descriptions of therate of bream (Abramis brama L.) embryonic development at different tempera-

Aquat.sci.59 (1997) 214–2241015-1621/97/030214-11 $ 1.50+0.20/0© Birkhäuser Verlag, Basel, 1997 Aquatic Sciences

* A bursar of Foundation for Polish Science.

tures, but in most cases the incubation was carried out only over a limited range ofwater temperatures or only over a part of the embryonic period (Dziekonska, 1956;1958; Penaz and Gajdusek, 1979). Other observations were made under naturalconditions, so that environmental factors other than temperature could influencethe results (Pliszka, 1953; Brylinska and Tadajewska, 1986). Kokurewicz (1971)reported that the range of spawning temperatures experienced by bream through-out its geographic distribution area is rather wide (10 to 27°C). This range of tem-perature is very similar to the temperatures observed in May and June on breamspawning grounds in the Kortowskie Lake, inhabited by the bream population studied. Our five year observations showed that the temperatures during spawningtime (May and June) of bream fluctuated on the spawning grounds between 13.5and 26.5°C (Kucharczyk, 1996). On the other hand, when temperature decreasedbelow 20°C bream discontinued spawning and left the spawning grounds.

Cyprinid larvae show generally higher temperature preferences than embryos(Wolnicki and Appelbaum, 1993). Besides lethal temperature effects, most studies concerned the controlling effects of temperature (Korin-Kossakowski andJezierska, 1984; Blaxter, 1992; Górny and Wolnicki, 1993). The effect of tempera-ture on the size of hatching fish embryos, on the length of the yolk-sac period, onearly development and growth rate, have been studied by numerous authors (forexample Penaz et al., 1988; Wiegand et al., 1988; 1989; Rana, 1990; Luczynski, 1991;Kamler et al., 1994). Considering the links between temperature and fish develop-ment, it has been shown that temperature affects fish populations in their naturalsurroundings (Backiel and Horoszewicz, 1970; Kokurewicz, 1971; Herzig and Winkler, 1986), being one of the most important environmental factors explainingrecruitment variations (Mills and Hurley, 1990; Leskelä and Kucharczyk, 1995).However, many fish species have a wide geographical range of occurrence, and thethermal conditons to which the particular (but often neighbouring) populations areadapted may differ considerably (Leskelä and Kucharczyk, 1995).

In this study we incubated bream eggs and reared bream larvae at eight constant temperatures (from 13.2 to 26.8°C for embryos and from 13.5 to 34.0°C for larvae), in order to observe their survival and rate of development. Such data provide a physiological basis explaining the relationship between environ-mental factors and embryonic and larval development under natural conditions(Luczynski, 1991).

Material and methods

Spawners and collection of gametes

Bream spawners were caught in the Kortowskie Lake (Olsztyn, Poland) in May1994 and transported to the hatchery where they were kept in 1000 l tanks at con-trolled temperature and light. Fish were induced to develop gametes by a series ofinjections with common carp pituitary extract and human chorionic gonadotropin(HCG) (Kucharczyk et al., 1997), at total dose of 4.0 mg kg–1 with 2200 IU kg–1 and2.0 mg kg–1 with 1100 IU kg–1, for females and males respectively. Milt was collectedfrom ten males and eggs from two females. The quality of sperm was expressed as

Effect of temperature on bream development 215

the percentage of motile spermatozoa by microscopic (500 X) observation of spermactivated with 0.5% NaCl (Babiak et al., 1995). Only samples with 80% (or more)motile spermatozoa were pooled and used in fertilization. Females were stripped ofeggs 14 hours after the last injection.

Incubation and larvae rearing system

The incubation and larvae rearing system has been described by Bardega andLuczynski (1990) and was composed of 8 units. Each unit contained two aquaria(8.11 each) working in a separate recirculated-water system with controlled tempe-rature and photoperiod.

Influence of water temperature on embryonic development

Eggs from two females were pooled, then divided into experimental batches andfertilized in a 0.5% NaCl solution. Thirty seconds after egg insemination, watertaken from the respective incubation chambers was added to the egg batches. Fertilized eggs were incubated in Petri dishes submerged in aerated aquaria at eightconstant temperatures (standard deviation in brackets) with two replicates per temperature: 13.2 (0.13), 15.0 (0.17), 17.0 (0.11), 8.5 (0.44), 21.1 (0.22), 22.9 (0.11),24.9 (0.16) and 26.8 (0.14) °C. Incubation temperature was measured with an accu-racy of 0.1 °C four to five times per day. The mean test temperatures were calculatedas the mean values of all measurements taken during experiment (until the last egghatched in each temperature). The temperatures for duplicate chambers were pooled as they were not significantly different (t-test, P < 0.001). Dissolved oxygenconcentration ranged between 10.7 and 14.2 mg O2 per litre; pH remained between7.2 and 7.7; measurements showed no ammonia in incubation water.

The time of appearance of several characteristic developmental stages wasnoted: eyed egg stage, beginning of hatching, hatching of 50% of embryos, lastembryo hatched from the egg batch. Hatching success was expressed as the percen-tage of hatched eleutheroembryos with no developmental abnormalities (e.g., sco-liosis, lordosis). Developmental advancement of hatched eleutheroembryos wasestimated using the scheme suggested by Penaz and Gajdusek (1979):

– step VI – formation of tail and its segmentation, finishing trunk segmentation,head remained markedly deflected and its base was intimate with the yolk sac.

– step VII – accomplishment of tail segmentation, separation of frontal part ofhead from yolk sac.

– step VIII – embryo straightening, separation of head from the yolk sac.

Influence of water temperature on larval development

All eggs were incubated at a constant temperature of 20°C. After hatching, samplesof 120 eleutheroembryos were transferred to eight duplicate units. Fish were ac-climated to the test temperature (standard deviation in brackets) of 13.5 (0.36), 16.4(0.36), 19.1 (0.20), 22.9 (0.31), 25.0 (0.22), 27.9 (0.22), 31.0 (0.14) and 34.0 (0.29) °Cby changing the temperature at a rate of about 1 °C h–1. Test temperatures were

216 Kucharczyk et al.

measured at least four times daily in each aquarium with the accuracy of 0.1 °C. Theaverage test temperatures were calculated as the mean values of all measurementstaken during the 21 days test. The temperatures for duplicate chambers were pooled as they did not significantly differ from each other (t-test, P < 0.001). Follow-ing the natural photoperiod observed in lakes in May – June, the experimental photoperiod was set to 18 hours light and 6 hours dark. Dissolved oxygen concen-tration ranged between 7.2 and 10.3 mg O2 per litre; pH was between 7.32 and 7.95;measurements showed no ammonia in rearing water. Fish were fed ad libitumwith Artemia sp. nauplii and with sieved zooplankton (Wolnicki and Korwin-Kossakowski, 1993; Naes et al., 1995). Rearing units were cleaned and dead fishremoved twice daily. Fish subsamples were taken before feeding in the morningafter 6, 11, 16 and 21 days of rearing and preserved in 4% formaline solution. Theamount of fish sampled was 30 minus the number of the fish that died during theperiod preceding the sampling. Fish were measured (total length) to 0.1 mm andweighed to 0.1 mg.

Statistical analysis

The differences in hatching success, weight and length were tested by Duncan’s mul-tiple range test (Platt, 1977). The instantaneous growth rate (G) and mortality rate(Z) from hatching till the end of the test were calculated according to Bagenal(1968) as:

ln (wt) – ln (w0)G = 000

t

where wt is the mean weight of the larvae at the end of the rearing period, w0 is themean weight of the larvae at the beginning of the rearing period, t is the length ofthe rearing period in days; and

ln (Nt) – ln (N0)Z = 000

t

where Nt and N0 are the numbers of the larvae at the end and at the beginning of therearing period, respectively,

Results

Influence of water temperature on embryonic development

Most of the eleutheroembryos hatched at developmental step VII. Approaching theend of the hatching period, some (about 5 – 7%) eleutheroembryos hatched atdevelopmental step VIII. Some eleutheroembryos incubated at low temperatureshatched at the earlier developmental step VI: 3.6% of embryos incubated at 13.2°Cand 0.2% at 15.0°C. Those embryos showed developmental abnormalities and diedsoon after hatching.



On the basis of the observed hatching success, the optimum incubation tempe-rature yielding hatching of at least 50% of the embryos ranged from 13.2 to 21.1 °C(Table 1). Highest hatching success (and lowest mortality rate) was observed in eggsincubated at 21.1°C. Incubation time decreased with increasing incubation tempe-rature (Fig. 1); mortality rate increased significantly at temperatures higher than21.1 °C (Fig. 2).

Table 1. Results of incubaton of bream (Abramis brama L.) eggs at different constant temperatures(± S.E.), expressed as the total number of inseminated eggs. Data marked with the same capital letters did not differ significantly (Duncan’s multiple range test, P < 0.05).

Temperture Number Results of the incubation experiment(°C) of eggs

Mortality between Mortality between Hatching Abnormalities fertilization and eyed egg stage success (%)eye pigmentation and hatching (%)(%) (%)

13.2 223± 7.5 28.5±0.5 D 1.9±0.2 A 66.0±1.0 D 3.6±0.215.0 280± 6.0 18.3±0.4 C 12.0±0.7 C 69.5±0.7 D 0.2±0.0217.0 241± 7.0 12.9±0.6 B 11.0±0.4 C 76.1±0.9 C 0.018.5 244±12.0 7.1±0.5 A 5.3±0.2 B 87.6±0.4 B 0.021.1 245± 9.5 5.5±0.4 A 1.1±0.2 A 93.4±0.2 A 0.022.9 266± 8.5 40.0±1.0 E 32.6±0.4 E 27.4±0.4 E 0.024.9 254±10.0 65.1±0.9 F 25.4±0.5 D 9.5±0.4 F 0.026.8 270± 4.5 74.9±0.6 G 23.7±0.5 D 1.4±0.2 G 0.0

Figure 1. Duration of embryonic development of bream eggs incubated at eight constant tempe-ratures. Regression equation for 50% of hatched embryos was Y = 910.1 – 65.88X + 1.318X2

(R2 = 0.994). Bars indicate S.E.


Influence of water temperature on larval development

Fastest growth of bream larvae (weight and length) was observed at a temperatureof 27.9 °C; the slowest growth was at 13.5 °C. Fish reared at the highest temperature(34.0 °C) grew much more slowly than those at 27.9 °C (Figs. 3 and 4), showing highweight and length variation.

Lowest mortality was observed at 27.9 °C; the highest was at 34 °C (Fig. 5). Theinstantaneous growth rate (in wet weight) increased with increasing temperaturefrom 13.5 to 27.9 °C, whereas at temperature from 13.5 to 27.9 °C, whereas at temperatures higher than that the growth rate decreased (Fig. 6). The highest netbiomass gain was observed at 27.9 °C.

Discussion

Water temperature influences fish embryos and larvae in a variety of ways. One ofthe responses to extreme temperatures is hatching of embryos at different develop-mental steps. In our experiment most of the eleutheroembryos hatched at develop-mental step VII, although at the end of the hatching period some embryos hatchedat developmental step VIII. A similar effect was observed by Penaz (1974) and Herzig and Winkler (1986) in bream incubated at high incubation temperatures. Atthe lowest test temperatures (13.2 and 15.0 °C) some eleutheroembryos hatched atstep VI; they showed developmental abnormalities and died soon after hatching(Table 1). Deformed and nonviable embryos generally hatch near the upper andlower incipient lethal level of incubation temperature (Herzig and Winkler, 1986).Dziekonska (1956), Backiel and Horoszewicz (1970) and Kokurewicz (1970) reportsimilar phenomena for cyprinids incubated at semilethal temperatures; Luczynski

Figure 2. Mortality rate of bream eggs incubated at eight constant temperatures. Regression equa-tion for total mortality was Y = – 832.2 + 125.14 X + 7180.0/X (R2 = 0.819).


and Kirklewska (1984) for vendace (Coregonus albula). In our study we observedanatomical abnormalities in embryos hatching at the lowest test temperatures(Table 1). Similarly, goldfish (Carassius auratus) eggs incubated at 12 °C yielded significantly higher frequencies of abnormal larvae than those incubated at highesttemperatures (Wiegand et al., 1988; 1989).

Hatching success varied with temperature. Hatching rate higher than 50%,which is a good result for bream (Herzig and Winkler, 1986) and for other cyprinids

Figure 3. Growth in wet weight of bream larvae reared at eight constant temperatures. Data fromthe same day marked with the same letter did not differ significantly (Duncan’s test. P < 0.05). Barsindicate S.E.

Figure 4. Growth in total weight of bream larvae reared at eight constant temperatures. Data fromthe same day marked with the same letter did not differ significantly (Duncan’s test. P < 0.05). Barsindicate S.E.


Figure 5. Mortality of bream larvae reared for 21 days at eight constant temperatures. Data fromthe same day marked with the same letter did not differ significantly (Duncan’s test. P < 0.05). Barsindicate S.E.

Figure 6. Effect of temperature on the mean instantaneous rate of net biomass gain of larval bream during 21 days of rearing

(Laurila et al., 1987), was observed at test temperatures ranging from 13.2 to 21.1°C(Table 1). Hatching success higher than 90% for bream from Kortowskie Lake wasobserved at the temperature of 21.1°C, whereas for bream from Lake Mondsee(Austria) it was in the temperature range of 15.1 to 16.2 (Herzig and Winkler, 1986).

Bream are known for tolerating a wide range of incubation temperatures (Koku-rewicz, 1971; Herzig and Winkler, 1986). The range of temperatures suitable for fish embryo development is usually correlated with spawning temperatures. Breamspawn at different temperatures depending on location: in the Volga River, spawn-ing occurs between 10.0 and 13.5 °C, in the Don River between 23 and 24 °C, in


Finland between 18 and 19 °C, and in Masurian Lakes, Poland, bream spawn atabout 17 °C (Kokurewicz, 1971). In Kortowskie Lake, where spawners were caught,bream spawn at 20 – 21 °C (optimal temperature for egg incubation is 21.1 °C). Inthis lake, spawning occurs a few weeks later than in some other but deeper and cooler lakes in the area. This difference might reflect the adaptation of bream populations to their particular habitats (Kokurewicz, 1970; Wiegand et al., 1989).The temperature of maximum hatching success remains in good agreement with the range of temperature in which spawning takes place (Herzig and Winkler, 1986).

Embryos, larvae and juveniles of many cyprinids prefer successively higher tem-perature habitats (Laurila et al., 1987). The relationship between temperature andthe duration of incubation time for bream is very similar to the relationship ob-served for other fish species, for example for crucian carp (Carassius carassius)(Laurila et al., 1987), ide (Leuciscus idus), tench (Tinca tinca) and roach (Rutilusrutilus) (Herzig and Winkler, 1986). Mortalities of the bream eggs were similar tothose observed for tench eggs incubated at different temperatures (Kouril et al.,1988).

The bream larvae growth (wet weight and total length, Figs. 3 and 4) and mor-tality rate (Fig. 5) showed that the optimum temperature for rearing was 27.9 °C.This result is similar to other findings concerning the influence of water temperatureon growth of cyprinid larvae, where the optimal range of temperature was usuallyfrom 25 to 28 °C (Wolnicki and Górny, 1993; 1994). In warmwater cyprinds the optimal range of temperature was even higher, exceeding 30 °C (Wolnicki andAppelbaum, 1993). The instantaneous wet weight gain of bream increased with rearing temperature and reached the maximum at 27.9 °C, then at higher tempera-tures the growth rate decreased (Fig. 6). This, again, might reflect the adaptation of the bream population studied to its natural habitat (Kokurewicz, 1971; Herzig andWinkler, 1986).

In Kortowskie Lake spawning of bream ceases when water temperature de-creases below 20 °C. However, low temperatures were not lethal to eggs or toeleutheroembryos (at 13.2 °C the survival of eggs was over 60 %) and larvae (at13.5 °C over 90 % larvae survival). The ability of a species to inhabit geographicallyvast territorias may partly depend on its ability to adopt to a variety of environ-mental conditions (Kokurewicz, 1971). For bream embryos and larvae it might beecologically more important to hatch in a given lake within that period of season inwhich larvae will find the best feeding conditions, rather than at a certain water tem-perature. Also, thermal adaptability of embryos and larvae is important for theirsurvival as the environmental temperature may vary during the developmental period (Wiegand et al., 1988). The optimum temperature range for the bream larvae in a particular habitat may differ from that found in this study, mostly be-cause of the effect of the temperature on food requirements, on the efficiency offood ingestion and assimilation. As temperature increases, food intake increasesand food conversion decreases (Goolish and Adelman, 1984; Laurila et al., 1987).On the other hand, optimum temperatures derived from the laboratory experimentmay differ from those under natural conditions, because of the possible differencesin water chemistry, fluctuations of temperature, behavioural responses to predators,etc. (Luczynski, 1991; Ziliukiene, 1995). Taking into account all the above limita-

tions, the data obtained in this study may help understanding the reproductive ecology of bream. It may also serve for developing hatchery techniques for rearingbream larve and fingerlings.

ACKNOWLEDGEMENTS

This study was supported by Project No. 05050.802 financed by Olsztyn University of Agriculture& Technology, Olszytn, Poland.

REFERENCES

Babiak, I., J. Glogowski, M. J. Luczynski, D. Kucharczyk and M. Luczynski, 1995. Cryopreserva-tion of the milt of the northern pike. J. Fish Biol. 46:819–828.

Backiel, T. and L. Horoszewicz, 1970. Temperatura a ryby. (Temperature and fish). (In Polish).Broszura Instytutu Rybactwa Sródladowego 41:1–25.

Bagenal, T., 1968. Methods for assessment of fish production in fresh waters. IBP Handbook No. 3. Blackwell Scientific Publications. Oxford. 365 pp.

Bardega, R. and M. Luczynski, 1990. Experimental hatchery and larvae rearing unit. (In Polish withEnglish summary). Acta Acad. Agricult. Tech. Olst., Protectio Aquarum et Piscatoria 18:87–93.

Blaxter, J. H. S., 1992. Temperature and larval fish. Netherlands Journal of Zoology 42:336–357.Brylinska, M. and M. Tadajewska, 1986. Leszcz (Abramis brama L.). (Bream Abramis brama L.).

pp: 267–273. (In Polish). In: M. Brylinska (ed.) Freshwater Fish in Poland, Panstwowe Wydawnictwo Naukowe, Warszawa.

Dziekonska, J., 1956. Studies on embryonic development of fish. I. Observations on the spawningand the embryonic development of bream in the Vistula Lagoon. (In Polish with English sum-mary). Pol. Arch. Hydrobiol. 3 :291 – 305.

Dziekonska, J., 1958. Studies on early development stages of fish. II. The influence of some en-vironmental conditions on the embryonic development of bream (Abramis brama L.) in theVistula Delta. (In Polish with English summary). Pol. Arch. Hydrobiol. 4 :194–206.

Goolish, E. M. and I. R. Adelman, 1984. Effects of ration size and temperature on the groth ofjuvenile common carp (Cyprinus carpio L.). Aquaculture 36:27–35.

Górny, W. and J. Wolnicki, 1993. Optimum termiczene wzrostu i przezywalnosci wylegu szczupakapodchowywanego w warunkach kontrolowanych. (Thermal optimum for the growth and suvival of pike larvae reared in controlled conditions) (In Polish) Komunikaty Rybackie (Olsztyn) 1:13–14.

Herzig, A. and H. Winkler, 1986. The influence of temperature on the embryonic development ofthree cyprinid fishes, Abramis brama, Chalcalburnus chalcoides mento and Vimba vimba. J.Fish Biol. 28:171–181.

Kamler, E., M. Szlaminska, M. Kuczynski, J. Hamackova, J. Kouril and R. Dabrowski, 1994. Tem-perature-induced changes of early development and yolk utilization in the African catfish Clarias gariepinus. J. Fish Biol. 44:311–326.

Kokurewicz, B., 1970. The effect of the temperature on embryonic development of Tinca tinca (L.)and Rutilus rutilus (L.). Zool. Pol. 20:317–337.

Kokurewicz, B., 1971. Thermal conditions for spawning and development for chosen fish species.(In Polish). Broszura Instytutu Rybactwa Sródladowego 47:1 – 18.

Korwin-Kossakowski, M. and B. Jezierska, 1984. The influence of thermal conditions on postem-bryonic development of some species of Coregonidae and Cyprinidae. Zool. Pol. 31:43–56.

Kouril, J., M. Penaz, M. Prokes and J. Hamackova, 1988. The effect of water temperature on eggincubation time in tench. Buletin VUHR Vodnany 1:3–9 (In Czech with English summary).

Kucharczyk, D., 1996. Genome engineering in bream, Abramis brama (L.). Ph. D. Thesis, OlsztynUniversity of Agriculture & Technology, Olsztyn, Poland. 93 pp. (In Polish).

Kucharczyk, D., R. Kujawa, M. Luczynski, J. Glogowski, I, Babiak and E. Wyszomirska, 1997.Induced spawning in bream (Abramis brama L.), using carp and bream pituitary extract andHCG. Aquacult. Res. 28:139–144.

Laurila, S., J. Piironen and J. Holopainen, 1987. Notes on egg development and larval and juvenilegrowth of crucian carp (Crassius carassius (L.)). Ann. Zool. Fennici 24:315–321.


Leskelä, A. and D. Kucharczyk, 1995. Effect of temperature on the growth of three forms of European whitefish (Coregonus lavaretus (L.) larvae. Arch. Hydrobiol. 46:147–152.

Luczynski, M., 1991. Temperature requirements for growth and survival of larval vendace, Coregonus albula. J. Fish Biol. 38:29–35.

Luczynski, M. and A. Kirklewska, 1984. Dependence of Coregonus albula embryogenesis rate onthe incubation temperature. Aquaculture 42:43 – 55.

Mills, C. A. and M. A. Hurley, 1990. Long term studies on the Winderme populations of perch, Perca fluviatilis, pike, Esox lucius, and arctic charr, Salvelinus alpinus. Fresh. Biol. 23:119 – 136.

Naes, T., M. Germain-Henry and K. E. Naas, 1995. First feeding of Atlantic halibut (Hippoglossushipoglossus) using different combinations of Artemia and wild zooplankton. Aquaculture130:235– 250.

Penaz, M., 1974. Influence of water temperature on incubation and hatching in Chondrostomanasus (L.). Zool. Listy 23:52–59.

Penaz, M. and J. Gajdusek, 1979. Erly development of bream, Abramis brama from the waterreservoir Mostiste, CSSR. Folia Zool. 28:347–360.

Penaz, M., E. Wohlgemuth, I. Stouracova and M. Prokes, 1988. Influence of water temperatureupon the growth and mortality rates of glass eels, Anguilla anguilla using water recirculation.Folia Zool. 37:263–272.

Platt, C., 1977. Problems with calculus of probability and statistical mathematics. 2nd ed. Pan-stwowe Wydawnictwo Naukowe, Warszawa (In Polish).

Pliszka, F., 193. Reproduction and development of Vimba vimba L. (In Polish with English sum-mary). Pol. Arch. Hydrobiol. 1 :137–163.

Rana, K. J., 1990. Influence of incubation temperature on Oreochromis niloticus eggs and fry. II.Survival, growth and feeding fry deeloping solely on their yolk reserves. Aquaculture87:183–195.

Wiegand, M. D., L. G. Buchanan, J. M. Loewen and C. M. Hewitt, 1988. Effects of rearing tempe-rature on development and survival of embryonic and larval goldfish. Aquaculture 71:209–222.

Wiegand, M. D., J. M. Hataley, C.L. Kitchen and L.G. Buchanan, 1989. Induction of developmentabnormalities in larval goldfish, Carassius auratus L., under cool incubation conditions. J. FishBiol. 35:85–95.

Wolnicki, J. and S. Appelbaum, 1993. Optimal growth temperatures for koi carp (Cyprinus carpioL.) larvae and juveniles reared under controlled conditions. Pol. Arch. Hycrobiol. 40:223–230.

Wolnicki, J. and W. Górny, 1993. Temperatura optymalna dla wzrostu mlBodocianego bolenia

Effect of temperature on embryonic and larval development of bream

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