Dynamics of indices of metabolism in muscle tissue, liver and gonads of Abramis brama in different periods of the annual cycle

Keywords: bream; sex; gonad maturity; condition factor; spawning.


The aim of this research was to study the dynamics of metabolism in the body of bream Abramis brama (L.) at different periods of the annual cycle: pre-spawning, spawning, post-spawning and feeding. The object of the study was 55 male and 53 female bream aged 9–13 years, to reduce the effect of age on the studied parameters. Individuals were measured, weighed, gender was determined, gonad maturity stage, age; the condition factor and organ indices were calculated. The content of moisture, dry matter, lipids, proteins, ash and nitrogen-free extracts (NFE) in the muscles, liver and gonads of male and female bream have been analyzed. The lowest coefficients of condition factor were found in bream during the autumn feeding season, the highest in males during spawning, in females before and after spawning. In the muscle tissue of male and female bream the content of metabolic products in the feeding period and before spawning differed slightly. In the spawning period, the muscles of males exceeded the muscle tissue of females in lipid content by more than two times. In the annual cycle of the bream, the ovaries contain more protein than the testes. The bream of different sex revealed differences in the intensity of metabolic processes during the maturation of gonads: in males, energy costs are more pronounced after wintering before spawning, while in females, during spawning. The main energy reserve in the form of lipids in the annual cycle changes more significantly in the body of male bream than in females. Ovarian maturation requires more metabolite reserves than maturation of the testes, however, males have increased expenditure associated with reproductive behaviour during spawning. Therefore, the total energy contribution to reproduction may be the same for female and for male bream. Bream’s liver and muscle tissue can serve as a source of energy during food shortages and during spawning. In the annual cycle, the condition factor of bream increases due to an increase in the moisture content in the muscles.


Adams, S. M., McLean, R. B., & Parrotta, J. A. (1982). Energy partitioning in largemouth bass under conditions of seasonally fluctuating prey availability. Transactions of the American Fisheries Society, 111(5), 549–558.

Aidos, I., van der Padt, A., Luten, J. B., & Boom, R. M. (2002). Seasonal changes in crude and lipid composition of herring fillets, byproducts, and respective produced oils. Journal of Agricultural and Food Chemistry, 50(16), 4589–4599.

Ali, M., Iqbal, F., Salam, A., Iram, S., & Athar, M. (2005). Comparative study of body composition of different fish species from brackish water pond. International Journal of Environmental Science and Technology, 2(3), 229–232.

Bilokon, G. S., Marenkov, O. M., & Dvoretskiy, A. I. (2013). Contents of radionuclides and heavy metals in fish roe of commercial fish of the Zaporizhya Reservoir. Nuclear Physics and Atomic Energy, 14(1), 81–85.

Brodersen, J., Hansen, J. H., & Skov, C. (2019). Partial nomadism in large-bodied bream (Abramis brama). Ecology of Freshwater Fish, 28(4), 650–660.

Carter, C. G., & Houlihan, D. F. (2001). Protein synthesis. Fish Physiology, 20, 31–75.

Craig, J. F. (1977). The body composition of adult perch, Perca fluviatilis in Windermere, with reference to seasonal changes and reproduction. Journal of Animal Ecology, 46(2), 617–632.

Craig, S. R., MacKenzie, D. S., Jones, G., & Gatlin III, D. M. (2000). Seasonal changes in the reproductive condition and body composition of free-ranging red drum, Sciaenops ocellatus. Aquaculture, 190, 89–102.

Dabhade, V. F., Pathan, T. S., Shinde, S. E., Bhandare, R. Y., & Sonawane, D. L. (2009). Seasonal variations of protein in the ovary of fish Channa gachua. Recent Research in Science and Technology, 1(2), 78–80.

Dawson, A. S., & Grimm, A. S. (1980). Quantitative seasonal changes in the protein, lipid and energy content of the carcass, ovaries and liver of adult female plaice, Pleuronectes platessa L. Journal of Fish Biology, 16(5), 493–504.

Diamond, M. (1985). Some observations of spawning by roach, Rutilus rutilus L., and bream, Abramis brama L., and their implications for management. Aquaculture Research, 16(4), 359–367.

Diana, J. S., & Mackay, W. C. (1979). Timing and magnitude of energy deposition and loss in the body, liver, and gonads of northern pike (Esox lucius). Journal of the Fisheries Board of Canada, 36(5), 481–487.

Ding, H., Zhang, Z., Xie, C., Liu, C., Chen, F., Huang, D., Li, Z., & Chen, Y. (2019). An assessment of European bream Abramis brama (Linnaeus, 1758) fishery in the downstream of the Irtysh River in China. Journal of Freshwater Ecology, 34(1), 107–122.

do Carmo Silva, J. P., da Costa, M. R., & Araújo, F. G. (2019). Energy acquisition and allocation to the gonadal development of Cynoscion leiachus (Perciformes, Sciaenidae) in a tropical Brazilian bay. Marine Biology Research, 15(2), 170–180.

Flath, L. E., & Diana, J. S. (1985). Seasonal energy dynamics of the alewife in southeastern Lake Michigan. Transactions of the American Fisheries Society, 114(3), 328–337.

Flerova, E. A. (2014). Fiziologo-biohimicheskie metody issledovaniya ryb [Physiological and biochemical methods for the study of fish]. Izdatel’stvo Yaroslavl State Agricultural Academy, Yaroslavl (in Russian).

German, A. V. (2019). Disturbance of synchronous oocyte development in bream Abramis brama L. from the Rybinsk Reservoir. Inland Water Biology, 12(1), 128–131.

Gorbatenko, K. M., & Lazhentsev, A. E. (2016). The biochemical composition and calorie density of the walleye pollock Theragra chalcogramma in the Sea of Okhotsk. Russian Journal of Marine Biology, 42(7), 591–601.

Grande, M., Murua, H., Zudaire, I., Arsenault-Pernet, E. J., Pernet, F., & Bodin, N. (2016). Energy allocation strategy of skipjack tuna Katsuwonus pelamis during their reproductive cycle. Journal of Fish Biology, 89(5), 2434–2448.

Grigorakis, K., Alexis, M. N., Taylor, K. A., & Hole, M. (2002). Comparison of wild and cultured gilthead sea bream (Sparus aurata); composition, appearance and seasonal variations. International Journal of Food Science and Technology, 37(5), 477–484.

Grigorjev, V. N. (2007). Izmenenie pokazatelej rosta i koefficienta upitannosti gustery Blicca bjoerkna (Cyprinidae) v verhnej chasti Kujbyshevskogo vodohranilishcha v usloviyah transformacii ego ekosistemy [The growth parameters variability and weight-length relation indexes of white bream Blicca bjoerkna (Cyprinidae) in the upper Kuybyshev Reservoir in changing condition of its ecosystem]. Uchenye Zapiski Kazanskogo Universiteta, Seriya Estestvennye Nauki, 149(2), 69–74 (in Russian).

Guijarro, A. I., Lopez-Patiño, M. A., Pinillos, M. L., Isorna, E., De Pedro, N., Alonso-Gómez, A. L., Alonso-Bedate, M., & Delgado, M. J. (2003). Seasonal changes in haematology and metabolic resources in the tench. Journal of Fish Biology, 62(4), 803–815.

Hiraoka, Y., Okochi, Y., Ohshimo, S., Shimose, T., Ashida, H., Sato, T., & Ando, Y. (2019). Lipid and fatty acid dynamics by maternal Pacific bluefin tuna. PloS One, 14(9), 1–18.

Hossain, M. A., Al-Abdul-Elah, K., & Yaseen, S. B. (2019). Seasonal variations in proximate and fatty acid composition of sobaity sea bream (Sparidentex hasta) in Kuwait waters. Journal of the Marine Biological Association of the United Kingdom, 99(4), 991–998.

Htun-Han, M. (1978). The reproductive biology of the dab Limanda limanda (L.) in the North Sea: Gonosomatic index, hepatosomatic index and condition factor. Journal of Fish Biology, 13(3), 369–378.

Ilmast, N. V. (2005). Vvedenie v ihtiologiyu [Introduction to Ichthyology]. Karelian Research Center of the Russian Academy of Sciences, Petrozavodsk (in Russian).

Islam, M. N., & Joadder, M. A. R. (2005). Seasonal variation of the proximate composition of freshwater Gobi, Glossogobius giuris (Hamilton) from the River Padma. Pakistan Journal of Biological Sciences, 8(4), 532–536.

Jan, U., Shah, M., Manzoor, T., & Ganie, S. A. (2012). Seasonal and monthly variations of protein content in the muscle of fish Schizothorax esocinus. Recent Research in Science and Technology, 4(7), 5–7.

John Kiran, P., Annapurna, Y., Krishna, P., & Sreeramulu, K. (2017). Seasonal variation of proximate composition of Istiophorus platypterus from Visakhapatnam fishing harbor, East Coast of India. International Journal of Bioassays, 6, 5530–5534.

Jøsrgensen, E. H., Johansen, S. J. S., & Jobling, M. (1997). Seasonal patterns of growth, lipid deposition and lipid depletion in anadromous Arctic charr. Journal of Fish Biology, 51(2), 312–326.

Karabanov, D. P., Pavlov, D. D., Bazarov, M. I., Borovikova, E. A., Smirnov, A. K., & Stolbunov, I. A. (2018). Alien species of fish in the littoral of Volga and Kama reservoirs (results of complex expeditions of IBIW RAS in 2005–2017). Transactions of Papanin Institute for Biology of Inland Waters RAS, 82(85), 67–80.

Khalko, V. V. (2018). Sexual dimorphism of physiological and biochemical state of trunk muscle in bleak (Alburnus alburnus L.) (Cypriniformes, Cyprinidae) spawners of the Rybinsk Reservoir in the Prespawning Period. Inland Water Biology, 11(2), 214–218.

Komova, N. I., Chuiko, G. M., Morozov, A. A., & Yurchenko, V. V. (2017). Reproductive parameters of roach Rutilus rutilus (L.) from the Rybinsk Reservoir reaches differing in anthropogenic loads. Inland Water Biology, 10(3), 296–300.

Kornienko, G. G., Dudkin, S. I., Sergeeva, S. G., Ruzhinskaya, L. P., Tsema, N. I., Bugaev, L. A., & Voykina, A. V. (2017). Fiziologo-biohimicheskaya harakteristika ryb Azovo-Chernomorskogo bassejna v usloviyah sovremennoj antropogennoj nagruzki [Physiological and biochemical characteristics of the Azov and Black sea fishes undergoing anthropogenic pressure]. Bulletin оf Kamchatka State Technical University, 40, 58–66 (in Russian).

Kosker, A. R., Ozogul, F., Durmus, M., Ucar, Y., Ozogul, Y., Boga, E., & Ayas, D. (2018). Seasonal changes in proximate composition and mineral-heavy metal content of pufferfish (Lagocephalus sceleratus) from northeastern Mediterranean sea. Turkish Journal of Fisheries and Aquatic Sciences, 18(11), 1269–1278.

Kostić, J., Kolarević, S., Kračun-Kolarević, M., Aborgiba, M., Gačić, Z., Lenhardt, M., & Vuković-Gačić, B. (2016). Genotoxicity assessment of the Danube River using tissues of freshwater bream (Abramis brama). Environmental Science and Pollution Research, 23(20), 20783–20795.

Kozlova, T. A. (1997). Seasonal cycles in total chemical composition of two Lake Baikal benthic-pelagic sculpins (Cottocomephorus, Cottoidei). Journal of Fish Biology, 50(4), 734–743.

Krivobok, M. N., & Tarkovskaya, O. I. (1960). Opredelenie srokov nerestovyh migracij salaki na osnovanii izucheniya ee zhirovogo obmena [Determining the timing of spawning migrations of herring based on the study of its fat metabolism]. VNIRO Proceedings, 42, 171–188 (in Russian).

Kumar, M., Varghese, T., Sahu, N. P., Gupta, G., & Dasgupta, S. (2019). Changes in the biochemical and mineral composition of hilsa shad, Tenualosa ilisha (Hamilton, 1822) during upstream spawning migration. International Journal of Current Microbiology and Applied Sciences, 8(6), 338–346.

Lloret, J., Shulman, G. E., & Love, R. M. (2014). Condition and health indicators of exploited marine fishes. Wiley-Blackwell.

Marenkov, O. N. (2018). Ecological and biological aspects of zander and Volga zander reproduction under conditions of the Zaporizhzhia reservoir (Ukraine). Ukrainian Journal of Ecology, 8(1), 441–450.

Matondo, B. N., Ovidio, M., Philippart, J. C., & Poncin, P. (2009). Hybridization behaviour between two common European cyprinid fish species – silver bream, Blicca bjoerkna and common bream, Abramis brama – in a controlled environment. Animal Biology, 59(1), 97–108.

Medford, B. A., & Mackay, W. C. (1978). Protein and lipid content of gonads, liver, and muscle of northern pike (Esox lucius) in relation to gonad growth. Journal of the Fisheries Research Board of Canada, 35(2), 213–219.

Mello, L. G. S., & Rose, G. A. (2005). Seasonal cycles in weight and condition in Atlantic cod (Gadus morhua L.) in relation to fisheries. ICES Journal of Marine Science, 62(5), 1006–1015.

Mikryakov, V. R., Gudkov, D. I., Mikryakov, D. V., Pomortseva, N. L., & Balabanova, L. V. (2013). Comparative characteristics of leucocytes compositions in the crucian carp Carassius carassius (Cyprinidae) from the waterbodies of the Chernobyl exclusion zone and from the Rybinsk reservoir. Journal of Ichthyology, 53(9), 753–757.

Munakata, A., & Kobayashi, M. (2010). Endocrine control of sexual behavior in teleost fish. General and Comparative Endocrinology, 165(3), 456–468.

Parrish, C. C. (1999). Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts, M. T., & Wainman, B. C. (Eds.). Lipids in freshwater ecosystems. Springer. Pp. 4–20.

Payuta, A. A., & Flerova, E. A. (2019). Some indicators of metabolism in the muscles, liver, and gonads of pike-perch Sander lucioperca and sichel Pelecus cultratus from the Gorky Reservoir. Journal of Ichthyology, 59(2), 255–262.

Petenuci, M. E., Rocha, I. D. N. A., de Sousa, S. C., Schneider, V. V. A., da Costa, L. A. M. A., & Visentainer, J. V. (2016). Seasonal variations in lipid content, fatty acid composition and nutritional profiles of five freshwater fish from the Amazon basin. Journal of the American Oil Chemists’ Society, 93(10), 1373–1381.

Plack, P. A., Pritchard, D. J., & Fraser, N. W. (1971). Egg proteins in cod serum. Natural occurrence and induction by injections of oestradiol 3-benzoate. Biochemical Journal, 121(5), 847–856.

Poncin, P., Matondo, B. N., Termol, C., Kestemont, P., & Philippart, J. C. (2011). Relationships between circulating androgens, aggressive behaviour and breeding tubercles in males of the common bream Abramis brama L. in an aquarium environment. Fish Physiology and Biochemistry, 37(3), 533–542.

Pradhan, S. C., Patra, A. K., & Pal, A. (2015). Seasonal analysis of the biochemical composition of muscle and liver of Catla catla in a tropical climate of India. Comparative Clinical Pathology, 24(3), 593–603.

Pravdin, I. F. (1966). Rukovodstvo po izucheniyu ryb [Fish study guide]. Pishchevaya Promyshlennost’, Moscow (in Russian).

Rajasilta, M. (1992). Relationship between food, fat, sexual maturation, and spawning time of Baltic herring (Clupea harengus membras) in the Archipelago Sea. Canadian Journal of Fisheries and Aquatic Sciences, 49(4), 644–654.

Rao, A. C., & Krishnan, L. (2011). Biochemical composition and changes in biological indices associated with maturation of the ovary in the spiny cheek grouper Epinephelus diacanthus (Valenciennes, 1828). Indian Journal of Fisheries, 58(2), 45–52.

Romotowska, P. E., Karlsdóttir, M. G., Gudjónsdóttir, M., Kristinsson, H. G., & Arason, S. (2016). Seasonal and geographical variation in chemical composition and lipid stability of Atlantic mackerel (Scomber scombrus) caught in Icelandic waters. Journal of Food Composition and Analysis, 49, 9–18.

Shankar, D. S., & Kulkarni, R. S. (2006). Effect of cortisol on female freshwater fish Notopterus notopterus. Journal of Environmental Biology, 27(4), 727–731.

Shatunovskii, M. I. (1980). Ekologicheskie zakonomernosti obmena veshchestv morskih ryb [Ecological patterns of metabolism of marine fish]. Nauka, Moscow (in Russian).

Shreni, K. D. (1980). Seasonal variations in the chemical composition of the catfish, Heteropneustes fossilis (Bloch). Proceedings – Animal Sciences, 89(2), 191–196.

Shulman, G. E., & Love, R. M. (1999). The biochemical ecology of marine fishes. Volume 36. Academic Press.

Shulman, G. E., Revina, N. I., & Safyanova, T. E. (1970). Svyaz’ fiziologicheskogo sostoyaniya s osobennostyami ovogeneza pelagicheskih ryb [The relationship of the physiological state with the peculiarities of ovogenesis of pelagic fish]. VNIRO Proceedings, 69, 96–108 (in Russian).

Smith, C., & Wootton, R. J. (2016). The remarkable reproductive diversity of teleost fishes. Fish and Fisheries, 17(4), 1208–1215.

Soyano, K., & Mushirobira, Y. (2018). The mechanism of low-temperature tolerance in fish. In: Iwaya-Inoue, M., Sakurai, M., & Uemura, M. (Eds.). Survival strategies in extreme cold and desiccation. Springer. Pp. 149–164.

Sutharshiny, S., Sivashanthini, K., & Thulasitha, W. S. (2013). Lipid changes in relation to maturation and spawning of tropical double spotted queenfish, Scomberoides lysan (Forsskål, 1775). Asian Journal of Animal and Veterinary Advances, 8(4), 555–570.

Turdakov, A. F. (1972). Vosproizvoditel’naya sistema samcov ryb [Reproductive system of male fish]. Ilim, Frunze (in Russian).

Tyheev, A. A., & Tomitova, E. A. (2016). Morfologicheskaya kartina gonad samok plotvy v osennij period v Istominskom soru Kabanskogo rajona Respubliki Buryatiya [Morphological image of gonads of roach females during the autumn period inthe Istominsky sorof the Kabansky district of the Rebublic of Buryatia]. Vestnik IrGSHA, 74, 62–70 (in Russian).

Tzikas, Z., Amvrosiadis, I., Soultos, N., & Georgakis, S. (2007). Seasonal variation in the chemical composition and microbiological condition of Mediterranean horse mackerel (Trachurus mediterraneus) muscle from the North Aegean Sea (Greece). Food Control, 18(3), 251–257.

Varkentin, A. I. (2015). Sezonnaya dinamika zrelosti gonad i pokazatelej upitannosti mintaya (Theragra chalcogramma) v severnoj chasti Ohotskogo morya [Seasonal dynamics of gonads maturity and indices of body condition for walleye pollock Theragra chalcogramma in the northern part of the Okhotsk Sea]. Izvestia TINRO, 180, 77–92 (in Russian).

Venkatesan, V., Gandhi, V., & Zacharia, P. U. (2013). Observations on the utilization of the biochemical constituents during maturation of the butterfish Scatophagus argus (L. 1766) from Palk Bay, south east coast of India. Indian Journal of Geo-Marine Sciences, 42(1), 75–81.

Viegas, I., de Albuquerque Carvalho, R., Pardal, M. Â., & Jones, J. G. (2012). Advances and applications of tracer measurements of carbohydrate metabolism in fish. In: Türker, H. (Ed.). New advances and contributions to fish biology. Intech Open.

Wallace, R. A., & Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist, 21(2), 325–343.

Wootton, R. J. (1974). The inter-spawning interval of the female three-spined stickleback, Gasterosteus aculeatus. Journal of Zoology, 172(3), 331–342.

Wootton, R. J. (1985). Energetics of reproduction. In: Tytler, P., & Calow, P. (Eds.). Fish energetics. Springer. Pp. 231–254.

Wootton, R. J., & Smith, C. (2015). Reproductive biology of teleost fishes. John Wiley & Sons.

Yeannes, M. I., & Almandos, M. E. (2003). Estimation of fish proximate composition starting from water content. Journal of Food Composition and Analysis, 16(1), 81–92.

Yeganeh, S., Shabanpour, B., Hosseini, H., Imanpour, M. R., & Shabani, A. (2012). Comparison of farmed and wild common carp (Cyprinus carpio): Seasonal variations in chemical composition and fatty acid profile. Czech Journal of Food Sciences, 30(6), 503–511.

Zaboukas, N., Miliou, H., Megalofonou, P., & Moraitou-Apostolopoulou, M. (2006). Biochemical composition of the Atlantic bonito Sarda sarda from the Aegean Sea (Eastern Mediterranean Sea) in different stages of sexual maturity. Journal of Fish Biology, 69(2), 347–362.

Žák, J., Prchalová, M., Šmejkal, M., Blabolil, P., Vašek, M., Matěna, J., Říha, M., Peterka, J., Seďa, J., & Kubečka, J. (2020). Sexual segregation in European cyprinids: Consequence of response to predation risk influenced by sexual size dimorphism. Hydrobiologia, 847(6), 1439–1451.

Zarubin, O. L., Zarubina, N. E., Kostyuk, V. A., Malyuk, I. A., Gudkov, D. I., Volkova, E. N., Belyaev, V. V., Kaglyan, A. E., Nazarov, A. B., Belokon, A. S., & Marenkov, O. N. (2013). Specific activity 137Cs at fishes of Ukraine. Current state. Nuclear Physics and Atomic Energy, 14(2), 177–182.

Zorica, B., Anđelić, I., & Keč, V. Č. (2019). Sardine (Sardina pilchardus) spawning in the light of fat content analysis. Scientia Marina, 83(3), 207–213.