Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0103
Animal Reproduction (AR)
ORIGINAL ARTICLE

Carotenoids and retinoids in the gonad of brood-stock pikeperch: accumulation during vitellogenesis and influence on egg quality in farmed pikeperch Sander lucioperca

Sven Wuertz; Axel Orban; Fabian Johannes Schaefer; Julia Lynne Overton; Angela Krüger

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Abstract

Carotenoids are determinants of reproductive fitness and egg quality. Here we studied the accumulation of astaxanthin (AX), canthaxanthin (CA) zeaxanthin (ZX), lutein (LU), retinol (RX) and dehydroretinol (DR) during vitellogenesis comparing previtellogenic and vitellogenic pikeperch (Sander lucioperca) eggs (n = 5 each), as well as selected tissues (liver, fat and muscles) in first süawning females (1176-1450 g). Futhermore, we compared egg batches with high (88-99% hatching rate, n = 5) or low (40-67% hatching rate, n= 5) egg quality. Vitellogenic follicles revealed higher concentrations of DR, RX, ZX and LU compared to previtellogenic follicles. Neither CA nor AX was detectable. In parallel, DR and RX were mobilized in the liver. In adipose and muscle tissue, comparing previtellogenic and vitellogenic females, no significant differences in carotenoid/retinoid content were observed. In high quality egg batches, both DR and RX were increased. LU was lower in high quality than in low quality eggs. In a conclusion, the amount of retinoids seems suboptimal in low quality egg batches and increased DR and RX are desirable in pikeperch. Since hypervitaminosis of retinoids can be problematic though, supplementation of the food with carotenoids, which can serve as precursors for retinoids, has to be carried out carefully.

Keywords

Sander, egg quality, vitellogenesis, retinol, hatching rate

References

Aas GH, Bjerkeng B, Storebakken T, Ruyter B. Blood appearance, metabolic transformation and plasma transport proteins of (14)C-astaxanthin in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem. 1999;21(4):325-34. http://dx.doi.org/10.1023/A:1007890224389.

Alijanpour N, Bani A, Tizkar B, Amiri K, Nazari RM. Carotenoid content and colour of eggs in migratory broodstock kutum (Rutilus frisii kutum Kamensky, 1901) (Osteichthyes: Cyprinidae) in the Shirud and Tajan Rivers, south Caspian Sea. Ital J Zool. 2015;82(1):25-32. http://dx.doi.org/10.1080/11250003.2014.982217.

Amar EC, Kiron V, Satoh S, Watanabe T. Enhancement of innate immunity in rainbow trout (Oncorhynchus mykiss Walbaum) associated with dietary intake of carotenoids from natural products. Fish Shellfish Immunol. 2004;16(4):527-37. http://dx.doi.org/10.1016/j.fsi.2003.09.004. PMid:15123294.

Anbazahan SM, Mari LSS, Yogeshwari G, Jagruthi C, Thirumurugan R, Arockiaraj J, Velanganni AAJ, Krishnamoorthy P, Balasundaram C, Harikrishnan R. Immune response and disease resistance of carotenoids supplementation diet in Cyprinus carpio against Aeromonas hydrophila. Fish Shellfish Immunol. 2014;40(1):9-13. http://dx.doi.org/10.1016/j.fsi.2014.06.011. PMid:24954837.

Ando S, Hatano M. Bilirubin-binding protein in the serum of spawning-migrating Chum salmon, Oncorhynchus keta - its identity with carotenoid carrying lipoprotein. Fish Physiol Biochem. 1988;5(2):69-78. http://dx.doi.org/10.1007/BF01875644. PMid:24226620.

Ando S, Hatano M. Distribution of carotenoids in the eggs from four species of salmonids. Comp Biochem Physiol B. 1991;99(2):341-4. http://dx.doi.org/10.1016/0305-0491(91)90052-F. PMid:1764913.

Ando S, Takeyama T, Hatano M. Deterioration of Chum salmon muscle during spawning migration. Part VIII. Transport associated with serum vitellogenin of carotenoid in Chum salmon (Oncorhynchus keta). Agr Biol Chem. 1986;50(3):557-63. http://dx.doi.org/10.1271/bbb1961.50.557.

Bell JG, McEvoy J, Tocher DR, Sargent JR. Depletion of alpha-tocopherol and astaxanthin in Atlantic salmon (Salmo salar) affects autoxidative defense and fatty acid metabolism. J Nutr. 2000;130(7):1800-8. http://dx.doi.org/10.1093/jn/130.7.1800. PMid:10867054.

Bjerkeng B, Johnsen G. Frozen storage quality of rainbow trout (Oncorhynchus mykiss) as affected by oxygen, illumination, and fillet pigment. J Food Sci. 1995;60(2):284-8. http://dx.doi.org/10.1111/j.1365-2621.1995.tb05656.x.

Bjerkeng B. Carotenoid pigmentation of salmonid fishes - recent progress. In: Avances en Nutrición Acuícola V. Memorias del V Simposium Internacional de Nutrición Acuícola; 2000 Nov 19-22; Mérida, Mexico. Monterrey: Universidad Autónoma de Nuevo León; 2000. p. 71-89.

Castenmiller JJM, West CE. Bioavailability and bioconversion of carotenoids. Annu Rev Nutr. 1998;18(1):19-38. http://dx.doi.org/10.1146/annurev.nutr.18.1.19. PMid:9706217.

Choe E, Min DB. Mechanisms of antioxidants in the oxidation of foods. Compr Rev Food Sci Food Saf. 2009;8(4):345-58. http://dx.doi.org/10.1111/j.1541-4337.2009.00085.x.

Christiansen R, Lie O, Torrissen OJ. Growth and survival of Atlantic salmon, Salmo salar L., fed different dietary levels of astaxanthin in first-feeding fry. Aquacult Nutr. 1995;1(3):189-98. http://dx.doi.org/10.1111/j.1365-2095.1995.tb00043.x.

Christiansen R, Torrissen OJ. Growth and survival of Atlantic salmon, Salmo salar L. fed different dietary levels of astaxanthin in juveniles. Aquacult Nutr. 1996;2(1):55-62. http://dx.doi.org/10.1111/j.1365-2095.1996.tb00008.x.

Costa DP, Miranda KC. The use of carotenoid pigments as food additives for aquatic organisms and their functional roles. Rev Aquacult. 2020;12(3):1567-78.

Fontagné S, Bazin D, Brèque J, Vachot C, Bernarde C, Rouault T, Bergot P. Effects of dietary oxidized lipid and vitamin A on the early development and antioxidant status of Siberian sturgeon (Acipenser baeri) larvae. Aquaculture. 2006;257(1-4):400-11. http://dx.doi.org/10.1016/j.aquaculture.2006.01.025.

García-Chavarría M, Lara-Flores M. The use of carotenoid in aquaculture. Res J Fish Hydrobiol. 2013;8(2):38-49.

Gesto M, Castro LFC, Reis-Henriques MA, Santos MM. Tissue-specific distribution patterns of retinoids and didehydroretinoids in rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol B. 2012;161(1):69-78. http://dx.doi.org/10.1016/j.cbpb.2011.09.006. PMid:21946003.

Gupta AK, Seth K, Maheshwari K, Baroliya PK, Meena M, Kumar A, Vinayak V, Harish. Biosynthesis and extraction of high-value carotenoid from algae. Front Biosci. 2021;26(6):171-90. http://dx.doi.org/10.52586/4932. PMid:34162044.

Güroy B, Şahin İ, Mantoğlu S, Kayalı S. Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellow tail cichlid Pseudotropheus acei. Aquacult Int. 2012;20(5):869-78. http://dx.doi.org/10.1007/s10499-012-9512-x.

Hardy RW, Torrissen OJ, Scott TM. Absorption and distribution of C-14-labeled canthaxanthin in rainbow trout (Oncorhynchus mykiss). Aquaculture. 1990;87(3-4):331-40. http://dx.doi.org/10.1016/0044-8486(90)90070-4.

Hermelink B, Kleiner W, Schulz C, Kloas W, Wuertz S. Photo-thermal manipulation for the reproductive management of pikeperch Sander lucioperca. Aquacult Int. 2017;25(1):1-20. http://dx.doi.org/10.1007/s10499-016-0009-x.

Hermelink B, Wuertz S, Rennert B, Kloas W, Schulz C. Temperature control of pikeperch (Sander lucioperca) maturation in recirculating aquaculture systems-induction of puberty and course of gametogenesis. Aquaculture. 2013;400-401:36-45. http://dx.doi.org/10.1016/j.aquaculture.2013.02.026.

Hermelink B, Wuertz S, Trubiroha A, Rennert B, Kloas W, Schulz C. Influence of temperature on puberty and maturation of pikeperch, Sander lucioperca. Gen Comp Endocrinol. 2011;172(2):282-92. http://dx.doi.org/10.1016/j.ygcen.2011.03.013. PMid:21439285.

Honeyfield DC, Daniels ME, Brown LR, Arts MT, Walsh MG, Brown SB. Survey of four essential nutrients and thiaminase activity in five Lake Ontario prey fish species. J Great Lakes Res. 2012;38(1):11-7. http://dx.doi.org/10.1016/j.jglr.2011.11.008.

Johnson EA, An GH. Astaxanthin from microbial sources. Crit Rev Biotechnol. 1991;11(4):297-326. http://dx.doi.org/10.3109/07388559109040622.

Khanzadeh M, Fereidouni AE, Berenjestanaki SS. Effects of partial replacement of fish meal with Spirulina platensis meal in practical diets on growth, survival, body composition, and reproductive performance of three-spot gourami (Trichopodus trichopterus) (Pallas, 1770). Aquacult Int. 2016;24(1):69-84. http://dx.doi.org/10.1007/s10499-015-9909-4.

Lampert JM, Holzschuh J, Hessel S, Driever W, Vogt K, von Lintig J. Provitamin A conversion to retinal via the beta,beta-carotene-15,15 '-oxygenase (bcox) is essential for pattern formation and differentiation during zebrafish embryogenesis. Development. 2003;130(10):2173-86. http://dx.doi.org/10.1242/dev.00437. PMid:12668631.

Lappalainen J, Dorner H, Wysujack K. Reproduction biology of pikeperch (Sander lucioperca (L.)) - a review. Ecol Freshwat Fish. 2003;12(2):95-106. http://dx.doi.org/10.1034/j.1600-0633.2003.00005.x.

Levi L, Levavi-Sivan B, Lubzens E. Expression of genes associated with retinoid metabolism in the trout ovarian follicle. Biol Reprod. 2008;79(3):570-7. http://dx.doi.org/10.1095/biolreprod.107.066548. PMid:18463359.

Li H, Tyndale ST, Heath DD, Letcher RJ. Determination of carotenoids and all-trans-retinol in fish eggs by liquid chromatography-electrospray ionization-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;816(1-2):49-56. http://dx.doi.org/10.1016/j.jchromb.2004.11.005. PMid:15664333.

Lubzens E, Lissauer L, Levavi-Sivan B, Avarre JC, Sammar M. Carotenoid and retinoid transport to fish oocytes and eggs: what is the role of retinol binding protein? Mol Aspects Med. 2003;24(6):441-57. http://dx.doi.org/10.1016/S0098-2997(03)00040-2. PMid:14585315.

Maden M. Vitamin A and the developing embryo. Postgrad Med J. 2001;77(910):489-91. http://dx.doi.org/10.1136/pmj.77.910.489. PMid:11470926.

Matsuno T, Katsuyama M, Maoka T, Hirono T, Komori T. Reductive metabolic pathways of carotenoids in fish (3s,3's)-astaxanthin to tunaxanthin A, B and C. Comp Biochem Physiol B. 1985;80(4):779-89. http://dx.doi.org/10.1016/0305-0491(85)90461-4.

Mejri S, Tremblay R, Vandenberg G, Moren M, Khemis IB, Audet C. Differences in nutrient content of eggs and larvae as indicators for improvement of broodstock nutrition in walleye (Sander vitreus) production. Can J Zool. 2017;95(5):299-310. http://dx.doi.org/10.1139/cjz-2016-0176.

Metusalach, Synowiecki J, Brown J, Shahidi F. Deposition and metabolism of dietary canthaxanthin in different organs of Arctic charr (Salvelinus alpinus L). Aquaculture. 1996;142(1-2):99-106. http://dx.doi.org/10.1016/0044-8486(95)01239-7.

Miki W. Biological functions and activities of animal carotenoids. Pure Appl Chem. 1991;63(1):141-6. http://dx.doi.org/10.1351/pac199163010141.

Müller-Belecke A, Zienert S. Out-of-season spawning of pike perch (Sander lucicoperca L.) without the need for hormonal treatments. Aquacult Res. 2008;39(12):1279-85. http://dx.doi.org/10.1111/j.1365-2109.2008.01991.x.

O’Byrne SM, Blaner WS. Retinol and retinyl esters: biochemistry and physiology. J Lipid Res. 2013;54(7):1731-43. http://dx.doi.org/10.1194/jlr.R037648. PMid:23625372.

Olson JA. Provitamin-a function of carotenoids - the conversion of beta-carotene into vitamin A. J Nutr. 1989;119(1):105-8. http://dx.doi.org/10.1093/jn/119.1.105. PMid:2643691.

Ørnsrud R, Graff LE, Høie S, Totland GK, Hemre GI. Hypervitaminosis A in first-feeding fry of the Atlantic salmon (Salmo salar L.). Aquacult Nutr. 2002;8(1):7-13. http://dx.doi.org/10.1046/j.1365-2095.2002.00185.x.

Ørnsrud R, Lock EJ, Waagbø R, Krossøy C, Fjelldal PG. Establishing an upper level of intake for vitamin A in Atlantic salmon (Salmo salar L.) postsmolts. Aquacult Nutr. 2013;19(5):651-64. http://dx.doi.org/10.1111/anu.12013.

Palace VP, Evans RE, Wautier K, Baron CL, Werner J, Klaverkamp JF, Kidd KA, Dick TA. Altered distribution of lipid-soluble antioxidant vitamins in juvenile sturgeon exposed to waterborne ethynylestradiol. Environ Toxicol Chem. 2001a;20(10):2370-6. http://dx.doi.org/10.1002/etc.5620201032. PMid:11596772.

Palace VP, Wautier K, Evans RE, Baron CL, Werner J, Ranson C, Klaverkamp JF, Kidd K. Effects of 17-beta estradiol exposure on metallothionein and fat soluble antioxidant vitamins in juvenile lake trout (Salvelinus namaycush). Bull Environ Contam Toxicol. 2001b;66(5):591-6. PMid:11443328.

Policar T, Schaefer FJ, Panana E, Meyer S, Teerlinck S, Toner D, Żarski D. Recent progress in European percid fish culture production technology-tackling bottlenecks. Aquacult Int. 2019;27(4):1175. http://dx.doi.org/10.1007/s10499-019-00457-4.

Rajasingh H, Oyehaug L, Vage DI, Omholt SW. Carotenoid dynamics in Atlantic salmon. BMC Biol. 2006;4(1):10. http://dx.doi.org/10.1186/1741-7007-4-10. PMid:16620373.

Ram S, Mitra M, Shah F, Tirkey SR, Mishra S. Bacteria as an alternate biofactory for carotenoid production: a review of its applications, opportunities and challenges. J Funct Foods. 2020;67:103867. http://dx.doi.org/10.1016/j.jff.2020.103867.

Sathyaruban S, Uluwaduge DI, Yohi S, Kuganathan S. Potential natural carotenoid sources for the colouration of ornamental fish: a review. Aquacult Int. 2021;29(4):1507-28. http://dx.doi.org/10.1007/s10499-021-00689-3.

Schaefer FJ, Overton JL, Bossuyt J, Zarski D, Kloas W, Wuertz S. Management of pikeperch Sander lucioperca (Linnaeus, 1758) sperm quality after stripping. J Appl Ichthyology. 2016a;32(6):1099-106. http://dx.doi.org/10.1111/jai.13144.

Schaefer FJ, Overton JL, Kloas W, Wuertz S. Length rather than year-round spawning, affects reproductive performance of RAS-reared F-generation pikeperch, Sander lucioperca (Linnaeus, 1758) - Insights from practice. J Appl Ichthyology. 2018;34(3):617-21. http://dx.doi.org/10.1111/jai.13628.

Schaefer FJ, Overton JL, Wuertz S. Pikeperch Sander lucioperca egg quality cannot be predicted by total antioxidant capacity and mtDNA fragmentation. Anim Reprod Sci. 2016b;167:117-24. http://dx.doi.org/10.1016/j.anireprosci.2016.02.016. PMid:26922635.

Schiedt K. Absorption and metabolism of carotenoids in birds, fish and crustaceans. In: Britton G, Liaaen-Jensen S, Pfander H, editors. Carotenoids biosynthesis and metabolism. Basel: Birkhäuser; 1998. p. 285-358.

Segner H, Arend P, Vonpoeppinghausen K, Schmidt H. The effect of feeding astaxanthin to Oreochromis niloticus and Colisa labiosa on the histology of the liver. Aquaculture. 1989;79(1-4):381-90. http://dx.doi.org/10.1016/0044-8486(89)90480-8.

Torrissen OJ, Christiansen R. Requirements for carotenoids in fish diets. J Appl Ichthyology. 1995;11(3-4):225-30. http://dx.doi.org/10.1111/j.1439-0426.1995.tb00022.x.

Torrissen OJ, Hardy RW, Shearer KD. Pigmentation in salmonids - carotenoid deposition and metabolism. CRC Crit Rev Aquat Sci. 1989;1(27):209-25.

Tzanova M, Argirova M, Atanasov V. HPLC quantification of astaxanthin and canthaxanthin in Salmonidae eggs. Biomed Chromatogr. 2017;31(4):e3852. http://dx.doi.org/10.1002/bmc.3852. PMid:27615726.

Wold HL, Wake K, Higashi N, Wang D, Kojima N, Imai K, Blomhoff R, Senoo H. Vitamin A distribution and content in tissues of the lamprey, Lampetra japonica. Anat Rec A Discov Mol Cell Evol Biol. 2004;276A(2):134-42. http://dx.doi.org/10.1002/ar.a.10345. PMid:14752852.

Wuertz S, Hermelink B, Schulz C. Pike perch in recirculation aquaculture. Global Aquacul All. 2012;15(3):2.

Żarski D, Horváth JA, Held JA, Kucharczyk D. Artificial reproduction of percid fishes. In: Kestamont P, Dabrowski K, Sommerfeldt RC, editors. Biology and culture of percid fishes: pinciples and practices. Dordrecht: Springer; 2015. p. 123-61. http://dx.doi.org/10.1007/978-94-017-7227-3_4.
 


Submitted date:
12/09/2022

Accepted date:
02/27/2023

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