Abstract
The study investigated the effects of seawater acclimation at constant and diel temperatures on the growth, osmoregulation, and branchial phospholipid fatty acid (PLFA) composition in rainbow trout (Oncorhynchus mykiss). The fish (initial weight, 62.28 ± 0.41 g) were reared at a constant 13.0 °C (CT) or with a diel cycle of either 13.0 ± 1.0 °C (VT2) or 13.0 ± 2.0 °C (VT4) for 6 weeks, and subsequently subjected to seawater acclimation. Diel temperature variations (of up to 4 °C) did not affect the growth rate of rainbow trout maintained in freshwater, but alleviated the impairment on the growth after seawater challenge. Under all temperature conditions, rainbow trout were well prepared to seawater acclimation. The diel cyclic temperature resulted in fish with reduced fluctuations in plasma electrolyte levels, branchial Na+–K+ ATPase activity, and plasma osmolality. In freshwater, the sum of the monounsaturated fatty acids was significantly higher in the VT4 relative to CT and VT2 treatment. Conversely, the sum of polyunsaturated fatty acids was significantly lower in the VT4 fish. After seawater transfer, the branchial PLFA profiles of the fish significantly changed, but those in CT and VT2 did not recover afterwards (the degree of unsaturation was downregulated). The PLFA composition of fish in the VT4 treatment appeared to be steadier under seawater acclimation. This study suggests that a diel cyclic temperature (13.0 ± 2.0 °C) can alleviate the impairment of growth, enhance osmoregulation capability, and improve the stability of the branchial PLFA composition in rainbow trout after seawater acclimation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Andersen OS, Koeppe RE II (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36(1):107–130. https://doi.org/10.1146/annurev.biophys.36.040306.132643
Austreng E, Storebakken T, Åsgård T (1987) Growth rate estimates for cultured Atlantic salmon and rainbow trout. Aquaculture 60(2):157–160. https://doi.org/10.1016/0044-8486(87)90307-3
Berg OK, Finstad B, Grande G, Wathne E (1990) Growth of Atlantic salmon (Salmo salar L.) in a variable diel temperature regime. Aquaculture 90(3–4):261–266. https://doi.org/10.1016/0044-8486(90)90250-Q
Blicher A, Wodzinska K, Fidorra M, Winterhalter M, Heimburg T (2009) The temperature dependence of lipid membrane permeability, its quantized nature, and the influence of anesthetics. Biophys J 96(11):4581–4591. https://doi.org/10.1016/j.bpj.2009.01.062
Bonga SEW (1997) The stress response in fish. Physiol Rev 77(3):591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Boyd CE, Tucker CS (1998) Water quality and aquaculture: preliminary considerations. In: Pond aquaculture water quality management. Springer US, Boston, pp 1–7. https://doi.org/10.1007/978-1-4615-5407-3_1
Bradford MM (1976) A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254
Brijs J, Hennig GW, Gräns A, Dekens E, Axelsson M, Olsson C (2017) Exposure to seawater increases intestinal motility in euryhaline rainbow trout (Oncorhynchus mykiss). J Exp Biol 220(13):2397–2408. https://doi.org/10.1242/jeb.156000
Brown MS, Jones PL, Tromp JJ, Van Rijn CA, Collins RA, Afonso LOB (2018) The physiology of saltwater acclimation in large juvenile Atlantic salmon Salmo salar. J Fish Biol 93(3):540–549. https://doi.org/10.1111/jfb.13649
Carveth CJ, Widmer AM, Bonar SA, Simms JR (2007) An examination of the effects of chronic static and fluctuating temperature on the growth and survival of spikedace, Meda fulgida, with implications for management. J Therm Biol 32(2):102–108. https://doi.org/10.1016/j.jtherbio.2006.11.002
Chong PL, Fortes PA, Jameson DM (1985) Mechanisms of inhibition of (Na,K)-ATPase by hydrostatic pressure studied with fluorescent probes. J Biol Chem 260(27):14484–14490. http://www.jbc.org/content/260/27/14484.abstract
Cornelius F (2001) Modulation of Na, K-ATPase and Na-ATPase activity by phospholipids and cholesterol. I. Steady-state kinetics. Biochemistry 40(30):8842–8851. https://doi.org/10.1021/bi010541g
Cornell BA, Separovic F (1983) Membrane thickness and acyl chain length. BBA-Biomembranes 733(1):189–193. https://doi.org/10.1016/0005-2736(83)90106-2
Crawshaw LI (2015) Responses to rapid temperature change in vertebrate ectotherms. Am Zool 19(1):225–237. https://doi.org/10.1093/icb/19.1.225
Deamer DW, Bramhall J (1986) Permeability of lipid bilayers to water and ionic solutes. Chem Phys Lipids 40(2):167–188. https://doi.org/10.1016/0009-3084(86)90069-1
Dong S (2019) Researching progresses and prospects in large salmonidae farming in Cold Water Mass of Yellow Sea. J Ocean Univ China 49(03):1–6. https://doi.org/10.16441/j.cnki.hdxb.20180303
Eldridge WH, Sweeney BW, Law JM (2015) Fish growth, physiological stress, and tissue condition in response to rate of temperature change during cool or warm diel thermal cycles. Can J Fish Aquat Sci 72(10):1527–1537. https://doi.org/10.1139/cjfas-2014-0350
Eliason EJ, Farrell AP (2016) Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet. J Fish Biol 88(1):359–388. https://doi.org/10.1111/jfb.12790
Elliott JM, Elliott JA (2010) Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change. J Fish Biol 77(8):1793–1817. https://doi.org/10.1111/j.1095-8649.2010.02762.x
Ernst R, Ejsing CS, Antonny B (2016) Homeoviscous adaptation and the regulation of membrane lipids. J Mol Biol 428(24 (Part A)):4776–4791. https://doi.org/10.1016/j.jmb.2016.08.013
Evans DH (2002) Cell signaling and ion transport across the fish gill epithelium. J Exp Zool 293(3):336–347. https://doi.org/10.1002/jez.10128
Fjelldal PG, Hansen T, Huang T-s (2011) Continuous light and elevated temperature can trigger maturation both during and immediately after smoltification in male Atlantic salmon (Salmo salar). Aquaculture 321(1–2):93–100. https://doi.org/10.1016/j.aquaculture.2011.08.017
Folch J, Lees M, Stanley GS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509
Gennis RB (1989) Biomembranes: molecular structure and function. Springer, New York. https://doi.org/10.1007/978-1-4757-2065-5
Gunther SJ, Moccia RD, Bureau DP (2007) Patterns of growth and nutrient deposition in lake trout (Salvelinus namaycush), brook trout (Salvelinus fontinalis) and their hybrid, F1 splake (Salvelinus namaycush × Salvelinus fontinalis) as a function of water temperature. Aquacult Nutr 13(3):230–239. https://doi.org/10.1111/j.1365-2095.2007.00472.x
Handeland S, Berge Å, Björnsson BT, Lie Ø, Stefansson S (2000) Seawater adaptation by out-of-season Atlantic salmon (Salmo salar L.) smolts at different temperatures. Aquaculture 181(3–4):377–396. https://doi.org/10.1016/S0044-8486(99)00241-0
Handeland SO, Imsland AK, Bjornsson BT, Stefansson SO (2013) Long-term effects of photoperiod, temperature and their interaction on growth, gill Na+, K+-ATPase activity, seawater tolerance and plasma growth-hormone levels in Atlantic salmon Salmo salar. J Fish Biol 83(5):1197–1209. https://doi.org/10.1111/jfb.12215
Hazel JR (1979) Influence of thermal acclimation on membrane lipid composition of rainbow trout liver. Am J Physiol-Reg I 236(1):R91–R101. https://doi.org/10.1152/ajpregu.1979.236.1.R91
Hazel JR (1990) Adaptation to temperature: phospholipid synthesis in hepatocytes of rainbow trout. Am J Physiol-Reg I 258(6):R1495–R1501. https://doi.org/10.1152/ajpregu.1990.258.6.R1495
Hazel JR, Williams EE, Livermore R, Mozingo N (1991) Thermal adaptation in biological membranes: Functional significance of changes in phospholipid molecular species composition. Lipids 26(4):277–282. https://doi.org/10.1007/bf02537137
Hennessey TM, Nelson DL (1983) Biochemical studies of the excitable membrane of Paramecium tetraurelia. VIII. Temperature-induced changes in lipid composition and in thermal avoidance behavior. BBA-Biomembranes 728(2):145–158. https://doi.org/10.1016/0005-2736(83)90466-2
Houston AH, Reaves RS, Madden JA, DeWilde MA (1968) Environmental temperature and the body fluid system of the fresh-water teleost-I. Ionic regulation in thermally acclimated rainbow trout, Salmo gairdneri. Comp Biochem Physiol 25(2):563–581. https://doi.org/10.1016/0010-406X(68)90369-1
Huang M, Zhou Y, Liu C, Davis DA, Li L, Gao Q, Dong S (2020) Fatty acid composition, osmolality, Na+, K+-ATPase activity, cortisol content and antioxidant status of rainbow trout (Oncorhynchus mykiss) in response to various dietary levels of eicosapentaenoic acid and docosahexaenoic acid. Aquac Res 00:1–13. https://doi.org/10.1111/are.14617
Kaneko T, Suzuki R, Watanabe S, Miyanishi H, Matsuzawa S, Furihata M, Ishida N (2019) Past seawater experience enhances subsequent growth and seawater acclimability in a later life stage in rainbow trout Oncorhynchus mykiss. Fish Sci 85(6):925–930. https://doi.org/10.1007/s12562-019-01351-x
Liu C, Zhou Y, Dong K, Sun D, Gao Q, Dong S (2018) Differences in fatty acid composition of gill and liver phospholipids between Steelhead trout Oncorhynchus mykiss and Atlantic salmon Salmo salar under declining temperatures. Aquaculture 495:815–822. https://doi.org/10.1016/j.aquaculture.2018.06.045
Liu C, Ge J, Zhou Y, Thirumurugan R, Gao Q, Dong S (2020) Effects of decreasing temperature on phospholipid fatty acid composition of different tissues and hematology in Atlantic salmon (Salmo salar). Aquaculture 515:734587. https://doi.org/10.1016/j.aquaculture.2019.734587
McCormick SD (2012) Smolt physiology and endocrinology. In: McCormick SD, Farrell AP, Brauner CJ (eds) Euryhaline fishes, vol 32. Elsevier, Oxford, pp 199–251. https://doi.org/10.1016/B978-0-12-396951-4.00005-0
Mehner T, Schiller S, Staaks G, Ohlberger J (2011) Cyclic temperatures influence growth efficiency and biochemical body composition of vertically migrating fish. Freshw Biol 56(8):1554–1566. https://doi.org/10.1111/j.1365-2427.2011.02594.x
Miranda EJ, Hazel JR (2002) The effect of acclimation temperature on the fusion kinetics of lipid vesicles derived from endoplasmic reticulum membranes of rainbow trout (Oncorhynchus mykiss) liver. Comp Biochem Phys A 131(2):275–286. https://doi.org/10.1016/s1095-6433(01)00451-2
Pisano OM, Kuparinen A, Hutchings JA (2019) Cyclical and stochastic thermal variability affects survival and growth in brook trout. J Therm Biol 84:221–227. https://doi.org/10.1016/j.jtherbio.2019.07.012
Sala-Rabanal M, Sánchez J, Ibarz A, Fernández-Borràs J, Blasco J, Gallardo MA (2003) Effects of low temperatures and fasting on hematology and plasma composition of gilthead sea bream (Sparus aurata). Fish Physiol Biochem 29(2):105–115. https://doi.org/10.1023/b:fish.0000035904.16686.b6
Sardella BA, Matey V, Cooper J, Gonzalez RJ, Brauner CJ (2004) Physiological, biochemical and morphological indicators of osmoregulatory stress in `California’ Mozambique tilapia (Oreochromis mossambicus × O. urolepis hornorum) exposed to hypersaline water. J Exp Biol 207(8):1399–1413. https://doi.org/10.1242/jeb.00895
Scheuerell MD, Schindler DE (2003) Deil vertical migration by juvenile sockeye salmon: empirical evidence for the antipredation window. Ecology 84(7):1713–1720. https://doi.org/10.1890/0012-9658(2003)084[1713:Dvmbjs]2.0.Co;2
Shivkamat P, Roy R (2005) Regulation of membrane lipid bilayer structure during salinity adaptation: a study with the gill epithelial cell membranes of Oreochromis niloticus. Comp Biochem Phys B 142(1):28–36. https://doi.org/10.1016/j.cbpc.2005.05.014
Sims DW, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, Hutchinson N, Budd GC, Righton D, Metcalfe JD, Nash JP, Morritt D (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. J Anim Ecol 75(1):176–190. https://doi.org/10.1111/j.1365-2656.2005.01033.x
Spector AA (1999) Essentiality of fatty acids. Lipids 34(1):S1–S3. https://doi.org/10.1007/BF02562220
Thomas RE, Gharrett JA, Carls MG, Rice SD, Moles A, Korn S (1986) Effects of fluctuating temperature on mortality, stress, and energy reserves of juvenile coho salmon. Trans Am Fish Soc 115(1):52–59. https://doi.org/10.1577/1548-8659(1986)115%3c52:Eoftom%3e2.0.Co;2
Thomas K, Hansen T, Brophy D, Maoiléidigh N, Fjelldal P (2019) Experimental investigation of the effects of temperature and feeding regime on scale growth in Atlantic salmon Salmo salar post-smolts. J Fish Biol. https://doi.org/10.1111/jfb.13971
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11(2):107–184. https://doi.org/10.1080/713610925
Todd AS, Coleman MA, Konowal AM, May MK, Johnson S, Vieira NKM, Saunders JF (2008) Development of new water temperature criteria to protect Colorado’s fisheries. Fisheries 33(9):433–443. https://doi.org/10.1577/1548-8446-33.9.433
Tunnah L, Currie S, Maccormack TJ (2017) Do prior diel thermal cycles influence the physiological response of Atlantic salmon (Salmo salar) to subsequent heat stress? Can J Fish Aquat Sci 74(1):127–139. https://doi.org/10.1139/cjfas-2016-0157
Vorobyov I, Olson Timothy E, Kim Jung H, Koeppe Roger E, Andersen Olaf S, Allen Toby W (2014) Ion-Induced defect permeation of lipid membranes. Biophys J 106(3):586–597. https://doi.org/10.1016/j.bpj.2013.12.027
Wallaert C, Babin PJ (1994) Thermal adaptation affects the fatty acid composition of plasma phospholipids in trout. Lipids 29(5):373–376. https://doi.org/10.1007/bf02537193
Wang M, Lu D (2005) Diurnal and seasonal variation of clear-sky land surface temperature of several representative land surface types in China retrieved by GMS 5. Acta Meteorol Sin 63(6):957–968. https://doi.org/10.3321/j.issn:0577-6619.2005.06.012
Wendelaar Bonga SE, Greven JAA (1978) The relationship between prolactin cell activity, environmental calcium, and plasma calcium in the teleost Gasterosteus aculeatus. Observations on stanniectomized fish. Gen Comp Endocr 36(1):90–101. https://doi.org/10.1016/0016-6480(78)90054-0
Wigham T, Ball JN (1977) Effect of environmental salinity changes on the secretory activity of prolactin cells in ocular pituitary transplants in Poecilia latipinna (teleostei). Gen Comp Endocr 31(1):148–153. https://doi.org/10.1016/0016-6480(77)90201-5
Zwingelstein G, Bodennec J, Brichon G, Abdul-Malak N, Chapelle S, El Babili M (1998) Formation of phospholipid nitrogenous bases in euryhaline fish and crustaceans. I. Effects of salinity and temperature on synthesis of phosphatidylserine and its decarboxylation. Comp Biochem Phys B 120(3):467–473. https://doi.org/10.1016/S0305-0491(98)10031-7
Acknowledgements
The authors would like to express our gratitude to those who have critically reviewed this manuscript and helped collect samples. This study was funded by the National Key Research and Development Program of China (Project No. 2019YFD0901000), the National Natural Science Foundation of China (No. 31702364), and the Primary Research and Development Program of Shandong Province (Nos. 2018CXGC0101 and SD2019YY006).
Funding
This study was funded by the National Key Research and Development Program of China (Project No. 2019YFD0901000), the National Natural Science Foundation of China (NSFC) (No. 31702364), and the Primary Research and Development Program of Shandong Province (Nos. 2018CXGC0101 and SD2019YY006).
Author information
Authors and Affiliations
Contributions
JG carried out the entire experiment, analysed the data and drafted the manuscript with the guidance of YZ and SD. MH, QD and RL helped analyse samples. QG, and YD helped edit this manuscript. YZ was responsible for the integrity of the work as a whole.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
All experiments were performed under license of the Animal Experimentation Committee of the Ocean University of China.
Additional information
Communicated by B. Pelster.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ge, J., Huang, M., Zhou, Y. et al. Effects of seawater acclimation at constant and diel cyclic temperatures on growth, osmoregulation and branchial phospholipid fatty acid composition in rainbow trout Oncorhynchus mykiss. J Comp Physiol B 191, 313–325 (2021). https://doi.org/10.1007/s00360-020-01330-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-020-01330-0