Abstract
Expansion of economically viable turbot (Scophthalmus maximus) aquaculture depends on access to brackish-cold ground water sources in various parts of the world. Since brackish water sources can adversely affect the physiology and zoo technical performance of fish due to the burden of osmoregulation, dietary salt inclusion can alleviate the negative impacts of low-saline waters in several aquaculture species. This study investigated the effects of increasing dietary salt levels on the growth, feed utilization, body composition, and tissue fatty acid composition of juvenile turbot (initial live weight 120.3 ± 0.03 g/fish). Fish were fed five experimental diets supplemented with varying levels of sodium chloride (1.8–6.4%) or a control diet without salt. Each diet was tested in triplicate tanks for 9 weeks. Results showed that increasing dietary salt intake negatively impacted turbot performance, with significant reductions in weight gain, specific growth rate, and feed conversion ratio. Dry matter and ash content in the whole body and filet increased quadratically with increasing salt levels, whereas gill moisture and protein content decreased linearly. Furthermore, the nitrogen, lipid, and energy utilization efficiencies decreased with their respective intake and gain levels. Dietary salt significantly influenced the fatty acid profiles of gill, liver, and filet tissues. In the gill, monounsaturated fatty acids (16:1n-7, ΣMUFA) and n-6 PUFA (20:2n-6) increased, whereas EPA and DHA decreased. Liver ΣSFA (16:0, 18:0) increased, and n-3 PUFA (18:3n-3, 20:5n-3) decreased with increasing dietary salt. Filet saturated fatty acids (14:0, 15:0, 17:0) and n-6 PUFA (20:2n-6, 20:4n-6) increased, while n-3 PUFA (18:3n-3, EPA) decreased with dietary salt. DHA levels in filets showed a quadratic increase. Overall, this study shows that increasing dietary salt negatively impacts turbot growth, feed utilization, and tissue fatty acid composition in brackish water, highlighting the need for further studies on salinity management strategies for turbot aquaculture.
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Introduction
Turbot is a cold-water flatfish species that is widely farmed in Europe and Asia because of its high market demand and adaptability to a wide range of salinity conditions (Person-Le Ruyet 2010; Wuertz et al. 2023). Its global production reached 77,110 tons in 2019 (FAO 2022). Turbot is an euryhaline or relatively stenohaline species that can tolerate a large range of salinities between 5 and 36‰ (Burel et al. 1996; Dietz et al. 2013; Gaumet et al. 1995). Optimum salinity conditions for turbot have been reported to be between 15 and 30‰ for growth and nutrient utilization performance (Dietz et al. 2013; Imsland et al. 2001, 2003). Fish in aquaculture conditions have little chance of sudden and dramatic changes in their environments in terms of salinity, but sometimes water with a salinity out of the optimal range of species can be used (Cech 2000; Liu et al. 2021). Recently, turbot aquaculture has been using less saline water due to the increasing use of deep-well seawater as well as the expansion of farming activities to inland areas, like in southwest Türkiye (Aksoy et al. 2012), Europe (APROMAR 2023; Person-Le Ruyet 2010), and north China (Liu et al. 2021). Therefore, turbot production in the latter areas is generally dependent on underground cold-brackish water with a salinity of 6–15‰ (Liu et al. 2021; Wang and Xu 2019; Wuertz et al. 2023). Additionally, using low-salinity waters in recirculation aquaculture systems can be advantageous because of less dependence on artificial salts (Alam et al. 2021). However, under such conditions, fish must cope with salinity stress and expend extra energy for osmoregulation, which may result in lower growth rates and feed conversion efficiency (Dietz et al. 2013; Imsland et al. 2003).
Osmoregulation is a vital physiological function for fish to maintain a stable intracellular concentration of ions in environments with variable salinity (Cech 2000). Fish osmoregulate by actively transporting ions across their gills, skin, and intestines, which require energy (Cech 2000; NRC 2011). They minimize the energy requirement of osmoregulation by seeking a medium that is isotonic with their body fluids in nature (Febry and Lutz 1987; Kidder et al. 2006). Under aquaculture conditions, euryhaline fish perform better in waters that fit their specific optimal salinity ranges (Dietz et al. 2013; Lall 2022; NRC 2011). Considering that turbot performs better when reared at intermediate salinity (ca. 20 g/L) (Imsland et al. 2001), underground waters with lower salinity could reduce growth and nutrient utilization performance. Oral administration of salt sources can be an option in hyposaline waters since the addition of salt to the diet of fish may increase the absorption of amino acids and provide ions that fish cannot extract from hypotonic environments for whole-body Na+ and Cl− homeostasis, thus saving energy expenditure (Salman 2009).
Dietary salt supplementation has increased the success of seawater adaptation by salmonids (Araujo et al. 2023; Duston 1993; Hanson et al. 2016; Pellertier and Besner 1992; Salman 2009; Salman and Eddy 1990; Staurnes and Finstad 2000; Zaugg et al. 1983). Growth and feed efficiency in several fish species, including Asian sea bass, Lates calcarifer, European seabass, Dicentrachus labrax, gilthead seabream, Sparus aurata, common carp, Cyprinus carpio, red drum, Sciaenops ocellatus, Nile tilapia, Oreochromis niloticus, and black sea bass, Centropristis striata, can be improved using moderately salt-enriched diets (%1–5) in freshwater and brackish water, potentially due to osmoregulatory advantages and the sparing of energy used in osmoregulation (Alam et al. 2015; Alam et al. 2021; Appelbaum and Arockiaraj 2009; Eroldoğan et al. 2005; Fontaínhas-Fernandes et al. 2000; Gangadhara et al. 2004; Gatlin et al. 1992; Harpaz et al. 2005). However, studies conducted in full-strength seawater indicate that the dietary inclusion of salt does not improve the growth and nutrient utilization of fish (Eroldoğan et al. 2005; Gatlin et al. 1992; Salman and Eddy 1990). This background suggests that dietary salt addition may enhance growth performance and nutrient retention in turbot maintained in brackish waters by reducing the energy expenditure for osmoregulation.
Water salinity has a significant effect on the metabolism and composition of fatty acids in fish and, in general, aquatic organisms (Gan et al. 2016; Hunt et al. 2011; Marrero et al. 2024; Tocher et al. 1995; Xie et al. 2015). In the case of Nile tilapia, Gan et al. (2016) found that only the whole body lipid content decreased with increasing salinity, indicating the potentially important role of lipids and fatty acids in the osmoregulation of fish. The decrease in salinity caused an increase in the percentages of 18:1n-9, 24:1n-9, 18:3n-3, and 18:2n-6, and a decrease in the percentages of 14:0, as observed in European sea bass (Hunt et al. 2011). Takeuchi et al. (1989) found that the total lipid of gills decreased from 897 mg of the initial value to 727 and 747 mg after adaptation to 1% or 2% salt water for 24 h. Additionally, Tocher et al. (1995) studied the effects of salinity on the fatty acid compositions of total lipid and individual glycerophospholipid classes of Atlantic salmon, Salmo salar, and turbot cells in culture and found that the most dramatic effects of salinity on total lipid fatty acids were observed in polyunsaturated fatty acids (PUFA) in turbot cells. Yet, the influence of oral salt administration on the fatty acid profiles of tissues remains unknown in turbot.
In fact, although a vast amount of information exists on the relationship between water salinity and fatty acid profiles of fish, such information, e.g., the influence of dietary salt levels on fatty acid compositions of fish tissues, is highly scarce. Chinook salmon, Oncorhynchus tshawytscha, fed diets with supplemental salt for 6 weeks showed significant changes in their fatty acid compositions, particularly 16:0, 18:2n-6, and n-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFAs), primarily eicosapentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3), compared with a control diet (Hanson et al. 2016). Exploring the influence of dietary salt on growth and tissue fatty acid profiles in turbot will be significant, considering that the expansion of turbot aquaculture will require more dilute cold waters (Aksoy et al. 2011; APROMAR 2023; Liu et al. 2021; Person-Le Ruyet 2010).
Therefore, the aim of this study was to assess the influence of different levels of dietary salt on the growth dynamics and feed utilization efficacy and the whole-body nutrient profile and tissue fatty acid compositions (gill, liver, and fillet) of turbot in brackish water.
Materials and methods
Fish and rearing conditions
The fish used in the study were selected from a large population with an initial average weight of 120.3 ± 0.03 g. Twenty fish were randomly distributed in experimental tanks with a volume of 140 L. The tanks were connected to a flow-through system running with UV-treated brackish water, and the water flow rate to each tank was 2.5 L/min. Over the study period, water temperature, dissolved oxygen, pH, and salinity were monitored daily using a hand DO meter and pH meter (YSI Model 55 and 63, YSI Inc., Yellowsprings, OH, USA). The average water temperature was 19.7 ± 1.4 °C, dissolved oxygen 7.3 ± 0.3 mg/L, pH 7.9 ± 0.1, and salinity: 8.6 ± 0.1‰, respectively. A natural photoperiod changing between 11.5–12 h light:12–12.5 h dark during a 9-week study period was used. During the study, fish in each tank were bulk weighed at 3-week intervals, and at the end of the experiment after about a 1-day starvation period under anesthesia with ethylene glycol monophenyl ether (0.3 mL/L).
At the beginning of the study, 15 fish were sampled for initial body composition, whereas at the end of the experiment, four fish from each tank were sacrificed with an overdose of ethylene glycol monophenyl ether (1.2 mL/L) to determine the final proximate composition, and the remaining four were used for organo-somatic indices. The organs, including the liver, gill, and filet of the later samples, were separated to determine their proximate and fatty acid compositions.
Experimental diets and feeding
A commercial extruded diet with a diameter of 9 mm (55% protein and 12% lipid) was coated with predetermined salt solutions (with ultra-pure water). Sodium chloride (Merck, Germany) was used as a dietary salt supplement at concentrations of 0%, (control) 1 (S1), 2 (S2), 4 (S4), and 6% (S6). The salt was first dissolved in ultrapure water and then sprayed onto the pellets and allowed to dry at room temperature for 48 h with occasional mixing. Only water was applied to the control diet. The analyzed dietary salt levels were 1.8, 3.0, 3.6, 5.3, and 6.4%, respectively (Table 1). Fish were fed their respective diets until apparent satiation by hand at 09:00 and 15:30 h.
Chemical analysis
Fish samples were stored at − 20 °C until analysis. Prior to analysis, the samples were thawed in a refrigerator overnight and then homogenized using a kitchen meat chopper (Tefal Le Hachoir 1500, France), except for liver and gill tissue, which were finely chopped using a stainless steel knife. Proximate analysis, except for crude lipid, of experimental diets and fish was performed according to the methods of AOAC (1990): dry matter at 104 °C until constant weight, ash content by incineration in a muffle furnace at 600 °C for 2 h; crude protein (N × 6.25) by the Kjeldhal method after acid digestion. Crude lipid was determined with ether extraction using an automatic extraction system (ANKOMXT15 Extractor, ANKOM Technology, Macedon, USA). For fatty acid profile determination, the lipids of all samples were extracted according to Bligh and Dyer (1959). Fatty acid methyl esters (FAME) were prepared following Ichihara et al. (1996). The fatty acids were analyzed by a gas chromatography (GC) (Focus GC, Thermo Electron, Waltham, MA) equipped with an autosampler, a flame ionization detector, and a fused silica capillary column (30 m × 0.32 mm, ID × 0.25 μm film). The oven temperature was set at 140 °C for 5 min, raised to 200 °C at a rate of 4 °C/min, and then 220 °C at a rate of 1 °C/min, while the injector and detector temperatures were set at 220 °C and 280 °C, respectively. FAMEs were identified by comparing the retention times with those of the SUPELCO standard (Sigma-Aldrich). The salt concentrations of the experimental diets were determined by the titrimetric method (James 2013).
Statistical analysis
Linear and quadratic polynomial contrasts were used to detect the linear and quadratic effects of various dietary salt levels on the variables at a level of P < 0.10 using the GLM procedure in JMP software (version 8, SAS Institute Inc., Cary, NC). A linear-quadratic nonlinear model was developed to estimate the maximum tolerable dietary salt level based on specific growth rate (SGR) values. In the model, the slope of the linear part was set to 0, while the slopes of the quadratic part were forced to get values below 0. The model was run on GraphPad Prism 7.
Results
Juvenile turbot responded to increased dietary salt levels with significant deteriorations in FW, SGR, and FCR (Table 2). The nonlinear model showed that turbot can tolerate dietary levels up to a maximum of approximately 4% (Fig. 1). However, there was no significant change in dietary feed intake (DFI) and protein efficiency ratio (PER) in response to the treatments. Body indices, including condition factor (CF) and hepato somatic index (HSI), linearly decreased with the increase of dietary salt concentrations, whereas no alteration in VSI values occurred. The nutrient utilization variables are given in Table 3. Changes in nitrogen, lipid, and energy utilization variables were mostly related to their intake and gain levels, with a significant linear decrease (P < 0.10).
The whole body, filet, viscera, liver, and gill proximate compositions are displayed in Table 4. Dietary increasing salt concentrations quadratically affected the whole body dry matter and ash and filet ash levels of turbot. There were no significant changes in the visceral and liver nutrient compositions, whereas gill dry matter and protein levels linearly reduced with the increasing salt levels.
The effects of dietary salt concentrations on gill fatty acid profiles are shown in Table 5. Although there was no significant change in saturated fatty acids, the levels of 16:1n-7 and total monounsaturated fatty acids (∑MUFA) linearly increased with dietary salt levels (P < 0.10). There was a quadratic linear increase in 20:2n-6 but a linear decrease in 20:4n-6 in response to dietary salt concentrations. The gill EPA and DHA levels linearly decreased with increasing dietary salt levels. The liver total saturated fatty acids (∑SFA) linearly increased with salt levels, mainly due to increases in 16:0 and 18:0 (Table 6). There was no significant change in monounsaturated and n-6 fatty acid groups, whereas 18:3n-3 and 20:5n-3 levels linearly decreased with increasing salt intakes (P < 0.10). The filet fatty acid compositions were significantly affected by dietary treatments (P < 0.10). (Table 7). While 14:0, 15:0, and 17:0 levels linearly increased with dietary salt levels, there was no significant change in monounsaturated fatty acids. The effect of dietary salt levels on 20:2n-6 and 20:4n-6 compositions was a significant increase. The filet 18:3n-3 and EPA levels linearly reduced with salt levels, but a quadratic linear increase occurred in the DHA levels. However, the whole body fatty acid profiles of fish did not significantly change with increasing dietary salt concentrations (Table 8).
Discussion
In diluted water, fish must meet the requirement for ions like Na+, Cl−, K+, Mg+, and Ca2+ from their diets because of the passive outward flux of ions (Gatlin et al. 1992; Salman 2009; Shaw et al. 1975; Smith et al. 1995; Tavares-Dias 2022). Therefore, euryhaline saltwater fish should be fed diets supplemented with salt when cultured in suboptimal salinity waters (Salman 2009; Wood and Bucking 2010). The results presented here showed that increasing dietary salt levels led to significant deteriorations in FW, SGR, and FCR, whereas no significant change was observed in DFI and PER, implying that high dietary salt levels may harm the growth and feed efficiency of juvenile turbot. These findings are inconsistent with some studies showing better growth performance in fish when maintained in diluted waters. For instance, red drum fed a 2% NaCI-supplemented diet showed better growth performance and feed efficiency when reared in freshwater and brackish waters but not in full-strength seawater (Gatlin et al. 1992). Dietary salt supplementation of up to 9% significantly increased growth and feed utilization performance in freshwater-adapted European seabass (Eroldoğan et al. 2005). Similarly, Asian seabass displayed an improved FCR response to dietary salt inclusion of up to 4% in freshwater, which was not the case in seawater (Harpaz et al. 2005). Parallel findings were also reported for hybrid tilapia (Oreochromis niloticus × O. aureus) by Shiau and Lu (2004), who showed that the experimental fish showed a dietary requirement of approximately 1.5 g/kg for sodium in fresh water but not in seawater due to the uptake of sodium from the water. Improvements in FW, feed conversion ratio, and PER in freshwater fish species such as rohu, Labeo rohita, mrigal, Cirrhinus mrigala, common carp, and hybrid tilapia were also observed when fish were fed diets including salt 1.0–3.0% (Cnaani et al. 2010; Gangadhara et al. 2004; Keshavanath et al. 2003). The inclusion of 5% salt in the diet of Nile tilapia significantly improved the digestibility coefficients for dry matter, protein, lipid, and ash (Hallali et al. 2018). The negative influence of increasing dietary salt content on HSI and CF values could partly explain the cause of poor growth and feed utilization due to several physiological and metabolic disruptions and increased energy demand for osmoregulation.
The influence of dietary salt on growth and feed efficiency was not always positive, as in this study (Table 2 and Fig. 1). For instance, the growth performance and feed efficiency of rainbow trout were negatively affected by increasing dietary salt concentrations (Salman and Eddy 1988a). Furthermore, the influence of dietary salt on the growth of rainbow trout appeared to be size related, with larger fish tolerating higher dietary levels, but excessive salt levels deteriorated growth performance (Park et al. 1998). A significant decrease in growth performance was observed in juvenile silver catfish (Rhamdia quelen) fed diets with increasing salt contents up to 2% when maintained in neutral pH water (Copatti et al. 2011). Welker et al. (2012) found that no change in growth and feed efficiency in channel catfish, Ictalurus punctatus, occurred after feeding diets including salt up to 4% for 10 weeks. Likewise, Santos et al. (2014) fed cobia, Rachycentron canadum, with diets including gradually increasing salt up to 10% in low salinity water (5 g/L) for 40 days and found no significant change in growth performance but a deterioration in FCR with the increase of dietary salt. Therefore, our results in turbot maintained in brackish water are consistent with the latter research findings.
Dietary salt inclusion did not significantly change DFI but linearly reduced nitrogen, lipid, and energy intakes. Salt incorporation resulted in decrease in dietary protein, lipid, and energy levels (Table 1), which could partly play a role in reduced nitrogen and energy intakes. If the experimental approach to dietary formulation was based on iso-protein, iso-lipid, and iso-energetic principles, preferably on their digestible levels (Glencross 2020), the influence of salt levels on dietary nutrient intakes could be better understood. In fact, the dilution in nutrient levels due to the increase of dietary salt incorporation should have increased DFI and nitrogen intake, considering that protein- and energy-dense diets limit those in fish (Kaushik and Schrama 2022; Saravanan et al. 2012), but this did not occur in the present study. Therefore, the reductions in nitrogen, lipid, and energy intakes appear to be a result of the increase in dietary salt rather than the nutrient dilution, considering that ad libitum feeding was made to fish to regulate their feed consumption. The nutrient utilization variables, including nitrogen, and energy utilization, also showed a significant linear decrease in response to higher salt intakes. Therefore, the negative effects of dietary salt on turbot growth and nutrient utilization could be attributed to several factors, including increased energy expenditure due to osmoregulatory stress, reduced nutrient absorption, and increased excretion of water, when the findings of former studies are considered (Park et al. 1998; Salman 2009; Salman and Eddy 1987, 1988; Santos et al. 2014; Welker et al. 2012).
The whole-body dry matter and ash were quadratically affected by increasing dietary salt levels in this study. These results are partly consistent with those in rainbow trout, tilapia (Oreochromis shiranus), and rohu, which show decreased whole-body dry matter and a U-type parabola trend when fed a diet with increasing salt levels (Gangadhara et al. 2004; Mzengereza and Kang’ombe 2015; Park et al. 1998). Alam et al. (2015) found that the whole-body proximate composition of black seabass (Centropristis striata) was affected by increasing dietary salt inclusions up to 12.5% when they were reared in two different salinities (15‰ vs 10‰) with the lowest moisture and highest lipid levels in fish fed 5% salt diets in 10‰ salinity. An 8-month study in the same species but with larger individuals in low salinity revealed that a dietary increase in salt of up to 7.5% only affected the whole body protein by a linear decrease with the dietary salt levels (Alam et al. 2021). Salt supplementation to the diet of juvenile Chinook salmon reduced the whole body dry matter and lipid levels but did not change protein and ash levels after 6 weeks (Hanson et al. 2016). It is difficult to explain the reasons for the change in the whole body composition in the present study since the influence of dietary salt levels in fish appears to change depending on species, salinity, size, and feeding duration.
As a matter of fact, previous studies have reported the effects of dietary salt incorporation on osmoregulation via the gill and intestine with salinity (Con et al. 2017; Eroldoğan et al. 2005; Hallali et al. 2018; Salman 2009). For instance, parallel regulations in response to an increase in dietary salt additions and water salinities, including elevation of chloride cell proliferation, gill Na + and K + -ATPase activity in the gill (Salman and Eddy 1987), and changes in the localization of intestinal peptide transporters toward distal regions (Con et al. 2017; Hallali et al. 2018), have been reported. Therefore, a similar influence of salt addition on tissue fatty acid metabolism and composition can be expected to be influenced by water salinity (Kolosov and Kelly 2016). However, studies on salinity changes have reported controversial findings in terms of fatty acid metabolism in fish.
The salinity challenge of Atlantic salmon at 10 and 20‰ significantly reduced gill weight to body weight percentage and total lipid level of the gill (Takeuchi et al. 1989). Similarly, we observed a linear decrease in gill dry matter and protein concentrations in the present study. Takeuchi et al. (1989) observed a significant decrease in n-3 fatty acids in the gills of Atlantic salmon exposed to 10 and 20‰ salinities compared with freshwater. This finding is consistent with those in the present study, where an increase in dietary salt levels yielded linear reductions in 20:4n-6, 20:5n-3, and 22:6n-3. Similarly, an opposite relationship between salinity and ARA, EPA, and DHA concentrations in the gills of European sea bass and black seabream (Acantahopagrus schlegelii) has been reported by Cordier et al. (2002) and Li et al. (2022). The concentrations of 20:4n-6 and 22:6n-3 within the polar lipids of Atlantic salmon gill also similarly decreased after transition to seawater (Tocher et al. 2000). However, there appear to be species-specific differences in the gill fatty acid compositions of fish in response to salinity changes because sturgeon (Acipencer naccarii) and masu salmon (O. masou) showed increased 20:4n-6, 20:5n-3, and 22:6n-3 concentrations at higher salinity compared with freshwater (Li and Yamada 1992; Martínez-Álvarez et al. 2005). The change in Lc-PUFA levels in the gill tissue in the present study can be attributed to a factor other than beta-oxidation of the fatty acids since the substrate preference for the energetic use of fatty acids in the gill is limited regardless of salinity (Crockett et al. 1999). However, a dietary increase in salt can have elevated the use of Lc-PUFAs in a higher rate of epithelial cell proliferation in the gill tissue or the important roles of these fatty acids in osmoregulation due to osmotic stress (Evans and Kültz 2020; Glencross 2009; Laurent et al. 2006).
The liver is highly sensitive in terms of bioconversion of short-chain fatty acids to Lc-PUFAs and the concomitant fatty acid compositions to changes in water salinity in fish (Marrero et al. 2021; Morais et al. 2015; Sarker et al. 2011a). As such, the response pattern of fatty acid compositions of turbot liver to increasing dietary salt inclusions was significantly influenced by the changes in dietary salt levels in the present study, with higher SFA (mainly due to 16:0 and 18:0) and lower 18:3n-3 and EPA contents when fed diets with increasing salt levels. This finding is inconsistent with that reported by Li and Yamada (1992), who found elevated n-3 PUFA fatty acid levels in the liver of masu salmon exposed to seawater compared with freshwater. Our results are partly consistent with those reported by Sarker et al. (2011b), who recorded higher EPA concentrations in the liver of red sea bream (Pagrus major) maintained at 15 and 20‰ salinity than at 33‰. Moreover, some existing studies show that low-salinity waters enhance the bioconversion capacities of linoleic and α- linolenic acids into their LC-PUFAs, particularly ARA, EPA, and DHA compared with high-salinity waters in the livers of rabbitfish (Siganus canaliculatus) (Li et al. 2008) and Senegalese sole (Solea senegalensis) (Marrero et al. 2021). The decreases in 18:3n-3 and EPA levels with increasing dietary salt could be due to the increasing use of catabolism for energetic use.
PUFAs are the group of fatty acids that were most affected by dietary salt concentrations, represented by decreases in 18:3n-3 and 20:5n-3 but increases in 20:2n-6, 20:4n-6, and DHA in the filets. These results are partly in harmony with those reported by Yu et al. (2021), who found higher levels of 20:4n-6, EPA, and DHA in the flesh of red tilapia reared in increasing salinity. These researchers attributed this increase to the higher ability of fish to bioconvert 18:3n-3 and 18:2n-6 in brackish or saline water compared with freshwater. Similarly, gray mullet (Chelon labrosus) showed an increasing bioconversion of 18:3n-3 to n-3 LC-PUFAs in muscle when reared at 20‰ compared with those reared at 35‰ (Marrero et al. 2024). The results of the present study are inconsistent with those reported by Haliloǧlu et al. (2004), who found a higher level of 20:5n-3 but lower DHA in the filets of rainbow trout reared in freshwater than those kept in saline water. Further studies are needed to fully elucidate the influence of dietary salt or salinity on the fatty acid profile of turbot filets using molecular tools.
The results of this study demonstrate that increasing dietary salt levels have a significant impact on a number of key performance indicators of juvenile turbot reared in brackish water. While turbot can tolerate dietary salt levels of up to approximately 4%, higher salt levels lead to deterioration in growth and nutrient utilization performance. Nutrient utilization, including nitrogen, lipid, and energy intakes, significantly decreased with increasing salt levels, likely due to osmoregulatory stress and reduced nutrient absorption. Additionally, increasing dietary salt content altered the proximate composition and fatty acid profiles of various tissues. As fish meal includes a significant amount of salt and is increasingly being replaced with other protein sources (plant, insect, bacterial proteins, etc.) with lower salt levels, dietary inclusions of salt sources should be considered (Rimoldi et al. 2015). However, the influence of such applications on the fatty acid biosynthesis capacities and fatty acid profiles of turbot requires further exploration.
Data availability
No datasets were generated or analysed during the current study.
References
Aksoy A, Çeliköz B, Dedebali N, Emre N, Emre Y, Ertekin H, Fedakar D,Itami T, Kocakaya S, Kurtoğlu A, Maekawa A, Mefut A, Nezaki G, Oikawa M, Öztürk E, Sakai M, Sevgili H, Sümer Ç, Süyek R Takeno N, Tekşam İ, Udagawa K, Wakita K (2011) Kalkan (Psetta maxima) Culture manual. 4th edition. In: Emre Y, Itami T, Sakai M Yiğit M(Eds). Special Publication, No:4, 124 pp. Türkiye
Alam M, Watanabe W, Myers A, Rezek T, Carroll P, Skrabal S (2015) Effects of dietary salt supplementation on growth, body composition, tissue electrolytes, and gill and intestinal Na+/K+ ATPase activities of black sea bass reared at low salinity. Aquaculture 446:250–258
Alam MS, Watanabe WO, Carroll PM (2021) Evaluation of salt-incorporated diets on growth, body composition and plasma electrolytes of black sea bass Centropristis striata reared in a semi-pilot scale low salinity recirculating aquaculture system. Aquaculture 533:736102. https://doi.org/10.1016/j.aquaculture.2020.736102
AOAC (1990) Official Methods of Analysis. Association of Official Analytical Chemists, Arlington, VA
Appelbaum S, Arockiaraj AJ (2009) Cultivation of gilthead sea bream (Sparus aurata Linnaeus, 1758) in low salinity inland brackish geothermal water. AACL Bioflux 2:197–203
APROMAR. (2023). Aquaculture in Spain. 2020. Retrieved from. https://apromar.es/informes/
Araujo BC, Symonds JE, Glencross BD, Carter CG, Walker SP, Miller MR (2023) A review of the nutritional requirements of chinook salmon (Oncorhynchus tshawytscha). NZ JL Mar Freshwat Res 57:161–190. https://doi.org/10.1080/00288330.2021.1985530
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Burel C, Person-Le Ruyet J, Gaumet F, Le Roux A, Sévère A, Boeuf G (1996) Effects of temperature on growth and metabolism in juvenile turbot. J Fish Biol 49:678–692. https://doi.org/10.1111/j.1095-8649.1996.tb00064.x
Cech J Jr (2000) Osmoregulation in bony fishes. In: Stickney RR (ed) Encyclopedia of aquaculture. John Wiley and Sons, New York, USA, pp 614–622
Cnaani A, Barki A, Slosman T, Scharcanski A, Milstein A, Harpaz S (2010) Dietary salt supplement increases the growth rate in freshwater cultured tilapia hybrids. Aquacult Res 41:1545–1548
P Con T Nitzan A Cnaani 2017 Salinity-dependent shift in the localization of three peptide transporters along the intestine of the Mozambique tilapia (Oreochromis mossambicus) Front Physiol 8 https://doi.org/10.3389/fphys.2017.00008
Copatti CE, Garcia LdO, Kochhann D, Cunha MA, Baldisserotto B (2011) Dietary salt and water pH effects on growth and Na+ fluxes of silver catfish juveniles. Acta Sci Animal Sci 33:261–266
Cordier M, Brichon G, Weber J-M, Zwingelstein G (2002) Changes in the fatty acid composition of phospholipids in tissues of farmed sea bass (Dicentrarchus labrax) during an annual cycle. Roles of environmental temperature and salinity. Comp Biochem Physiol B: Biochem Mol Biol 133:281–288. https://doi.org/10.1016/S1096-4959(02)00149-5
Crockett EL, Londraville RL, Wilkes EE, Popesco MC (1999) Enzymatic capacities for β-oxidation of fatty fuels are low in the gill of teleost fishes despite presence of fatty acid-binding protein. J Exp Zool 284:276–285. https://doi.org/10.1002/(SICI)1097-010X(19990801)284:3%3c276::AID-JEZ5%3e3.0.CO;2-N
Dietz C, Stiller KT, Griese M, Schulz C, Susenbeth A (2013) Influence of salinity on energy metabolism in juvenile turbot Psetta maxima (L.). Aquac Nutr 19:135–150. https://doi.org/10.1111/anu.12034
Duston J (1993) Effects of dietary betaine and sodium chloride on seawater adaptation in atlatic salmon parr (Salmo salar L.). Comp Biochem Physiol Com Physiol 105:673–677. https://doi.org/10.1016/0300-9629(93)90267-8
Eroldoğan OT, Kumlu M, Kır M, Kiris GA (2005) Enhancement of growth and feed utilization of the European sea bass (Dicentrarchus labrax) fed supplementary dietary salt in freshwater. Aquacult Res 36:361–369
Evans TG, Kültz D (2020) The cellular stress response in fish exposed to salinity fluctuations. J Exp Zool, Part A: Ecol Genet Physiol 333:421–435. https://doi.org/10.1002/jez.2350
FAO (2022) Fishery and Aquaculture Statistics. Global production by production source 1950–2020. FishStatJ: universal software for fishery statistical time series.
Febry R, Lutz P (1987) Energy partitioning in fish: the activityrelated cost of osmoregulation in a euryhaline cichlid. J Exp Biol 128:63–85. https://doi.org/10.1242/jeb.128.1.63%JJournalofExperimentalBiology
Fontaínhas-Fernandes A, Russell-Pinto F, Gomes E, Reis-Henriques MA, Coimbra J (2000) The effect of dietary sodium chloride on some osmoregulatory parameters of the teleost, Oreochromis niloticus, after transfer from freshwater to seawater. Fish Physiol Biochem 23:307–316
Gan L, Xu ZX, Ma JJ, Xu C, Wang XD, Chen K, Chen LQ, Li EC (2016) Effects of salinity on growth, body composition, muscle fatty acid composition, and antioxidant status of juvenile Nile tilapia Oreochromis niloticus (Linnaeus, 1758). J Appl Ichthyol 32:372–374. https://doi.org/10.1111/jai.12997
Gangadhara B, Nandeesha MC, Keshavanath P, Varghese TJ (2004) Growth response and biochemical composition of rohu, Labeo rohita, fed salt-incorporated diets. J Appl Aquac 16:169–176. https://doi.org/10.1300/J028v16n01_15
Gatlin DM III, MacKenzie DS, Craig SR, Neill WH (1992) Effects of dietary sodium chloride on red drum juveniles in waters of various salinities. Prog Fish Cult 54:220–227
Gaumet F, Boeuf G, Severe A, Le Roux A, Mayer-Gostan N (1995) Effects of salinity on the ionic balance and growth of juvenile turbot. J Fish Biol 47:865–876. https://doi.org/10.1111/j.1095-8649.1995.tb06008.x
Glencross BD (2009) Exploring the nutritional demand for essential fatty acids by aquaculture species. Rev Aquac 1:71–124. https://doi.org/10.1111/j.1753-5131.2009.01006.x
Glencross BD (2020) A feed is still only as good as its ingredients: an update on the nutritional research strategies for the optimal evaluation of ingredients for aquaculture feeds. Aquac Nutr 26(6):1871–1883. https://doi.org/10.1111/anu.13138
Haliloǧlu Hİ, Bayır A, Necdet Sirkecioǧlu A, Mevlüt Aras N, Atamanalp M (2004) Comparison of fatty acid composition in some tissues of rainbow trout (Oncorhynchus mykiss) living in seawater and freshwater. Food Chemistry 86:55–59. https://doi.org/10.1016/j.foodchem.2003.08.028
Hallali E, Kokou F, Chourasia TK, Nitzan T, Con P, Harpaz S, Mizrahi I, Cnaani A (2018) Dietary salt levels affect digestibility, intestinal gene expression, and the microbiome, in Nile tilapia (Oreochromis niloticus). PLoS ONE 13:e0202351. https://doi.org/10.1371/journal.pone.0202351
Hanson KC, Twibell RG, Glenn RA, Barron JM, Gannam AL (2016) The effects of a transition diet on the smoltification of chinook salmon. N Am J Aquac 78:307–313. https://doi.org/10.1080/15222055.2016.1185064
Harpaz S, Hakim Y, Slosman T, Eroldogan OT (2005) Effects of adding salt to the diet of Asian sea bass Lates calcarifer reared in fresh or salt water recirculating tanks, on growth and brush border enzyme activity. Aquaculture 248:315–324
Hunt AÖ, Özkan F, Engin K, Tekelioğlu N (2011) The effects of freshwater rearing on the whole body and muscle tissue fatty acid profile of the European sea bass (Dicentrarchus labrax). Aquac Int 19:51–61. https://doi.org/10.1007/s10499-010-9340-9
Ichihara K, Shibahara A, Yamamoto K, Nakayama T (1996) An improved method for rapid analysis of the fatty acids of glycerolipids. Lipids 31:535–539
Imsland AK, Foss A, Gunnarsson S, Berntssen MH, Fitzgerald R, Bonga SW, Vham E, Nævdal G, Stefansson SO (2001) The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture 198:353–367
Imsland AK, Gunnarsson S, Foss A, Stefansson SO (2003) Gill Na+, K+-ATPase activity, plasma chloride and osmolality in juvenile turbot (Scophthalmus maximus) reared at different temperatures and salinities. Aquaculture 218:671–683
James CS (2013) Analytical chemistry of foods. Springer Science & Business Media, Blackies, London
Kaushik, SJ, Schrama JW (2022). Bioenergetics. In: Hardy RW, Kaushik SJ (eds) Fish Nutrition Academic Press, 17–55
Keshavanath P, Gangadhara B, Khadri S (2003) Growth enhancement of carp and prawn through dietary sodium chloride supplementation. Aquac Asia 8:4–8
Kidder GW III, Petersen CW, Preston RL (2006) Energetics of osmoregulation: II. Water flux and osmoregulatory work in the euryhaline fish, Fundulus heteroclitus. J Exp Zool A Comp Exp Biol 305:318–327
Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160:1577–1579. https://doi.org/10.1111/j.1476-5381.2010.00872.x
Kolosov D, Kelly SP (2016) Dietary salt loading and ion-poor water exposure provide insight into the molecular physiology of the rainbow trout gill epithelium tight junction complex. J Comp Physiol B 186:739–757. https://doi.org/10.1007/s00360-016-0987-z
Lall SP (2022) The minerals. In: Kaushik SJ (ed) Hardy RW. Academic Press, Fish nutrition (fourth edition), pp 469–554
Laurent P, Chevalier C, Wood CM (2006) Appearance of cuboidal cells in relation to salinity in gills of Fundulus heteroclitus, a species exhibiting branchial Na+ but not Cl− uptake in freshwater. Cell Tissue Res 325:481–492. https://doi.org/10.1007/s00441-006-0187-3
Li H-O, Yamada J (1992) Changes of the fatty acid composition in smolts of masu salmon (Oncorhynchus masou), associated with desmoltification and sea-water transfer. Comp Biochem Physiol A: Physiol 103:221–226. https://doi.org/10.1016/0300-9629(92)90266-S
Li X, Shen Y, Bao Y, Wu Z, Yang B, Jiao L, Zhang C, Tocher DR, Zhou Q, Jin M (2022) Physiological responses and adaptive strategies to acute low-salinity environmental stress of the euryhaline marine fish black seabream (Acanthopagrus schlegelii). Aquaculture 554:738117. https://doi.org/10.1016/j.aquaculture.2022.738117
Li Y, Hu C-b, Zheng Y-J, Xia X-A, Xu W-J, Wang S, Chen W-Z, Sun Z, Huang J-H (2008) The effects of dietary fatty acids on liver fatty acid composition and δ6-desaturase expression differ with ambient salinities in Siganus canaliculatus. Comp Biochem Physiol B: Biochem Mol Biol https://doi.org/10.1016/j.cbpb.2008.06.013
Liu Z, Ma A, Yuan C, Zhao T, Chang H, Zhang J (2021) Transcriptome analysis of liver lipid metabolism disorders of the turbot Scophthalmus maximus in response to low salinity stress. Aquaculture 534:736273. https://doi.org/10.1016/j.aquaculture.2020.736273
Marrero M, Monroig Ó, Betancor M, Herrera M, Pérez JA, Garrido D, Galindo A, Giráldez I, Rodríguez C (2021) Influence of dietary lipids and environmental salinity on the n-3 long-chain polyunsaturated fatty acids biosynthesis capacity of the marine teleost Solea senegalensis. Mar Drugs 19:254
Marrero M, Monroig Ó, Pérez JA, Betancor MB, Galindo A, Bolaños A, Acosta NG, Rodríguez C (2024) Dietary LC-PUFA and environmental salinity modulate the fatty acid biosynthesis capacity of the euryhaline teleost thicklip grey mullet (Chelon labrosus). Comp Biochem Physiol C: Biochem Mol Biol 269:110865. https://doi.org/10.1016/j.cbpb.2023.110865
Martínez-Álvarez RM, Sanz A, García-Gallego M, Domezain A, Domezain J, Carmona R, del Valle Ostos-Garrido M, Morales AE (2005) Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to saltwater. Comp Biochem Physiol A: Mol Int Physiol 141:183–190. https://doi.org/10.1016/j.cbpb.2005.05.003
Morais S, Mourente G, Martínez A, Gras N, Tocher DR (2015) Docosahexaenoic acid biosynthesis via fatty acyl elongase and Δ4-desaturase and its modulation by dietary lipid level and fatty acid composition in a marine vertebrate. BBA - Mol Cell Biol Lipids 1851:588–597. https://doi.org/10.1016/j.bbalip.2015.01.014
Mzengereza K, Kang’ombe J (2015) Effect of dietary salt (sodium chloride) supplementation on growth, survival and feed utilization of Oreochromis shiranus (Trewavas, 1941). J Aquac Res Dev 7:1–5. https://doi.org/10.4172/2155-9546.1000388
NRC (2011) Nutrient requirements of fish and shrimp. National Academies Press,
Park G-S, Takeuchi T, Yokoyama M, Satoh S (1998) Effect of dietary sodium chloride levels on growth and tolerance to sea water of rainbow trout. Nippon Suisan Gakkaishi 64:469–474. https://doi.org/10.2331/suisan.64.469
Pellertier D, Besner M (1992) The effect of salty diets and gradual transfer to sea water on osmotic adaptation, gill Na+, K+-ATPase activation, and survival of brook charr, Salvelinus fontinalis, Mitchill. J Fish Biol 41:791–803. https://doi.org/10.1111/j.1095-8649.1992.tb02707.x
Person-Le Ruyet, J. (2010) Turbot culture. In: Daniels H.V. and Watanabe W.O. (Eds). Practical flatfish culture and stock enhancement. Hoboken NJ: Wiley-Blackwell. pp. 123–139. https://doi.org/10.1002/9780813810997.ch7
Rimoldi S, Bossi E, Harpaz S, Cattaneo AG, Bernardini G, Saroglia M, Terova G (2015) Intestinal B0AT1 (SLC6A19) and PEPT1 (SLC15A1) mRNA levels in European sea bass (Dicentrarchus labrax) reared in fresh water and fed fish and plant protein sources. Journal of Nutritional Science 4:e21. https://doi.org/10.1017/jns.2015.9
Salman NA, Eddy FB (1987) Response of chloride cell numbers and gill Na+K+ ATPase activity of freshwater rainbow trout (Salmo gairdneri Richardson) to salt feeding. Aquaculture 61:41–48. https://doi.org/10.1016/0044-8486(87)90336-X
Salman NA, Eddy FB (1988a) Effect of dietary sodium chloride on growth, food intake and conversion efficiency in rainbow trout (Salmo Gairdneri Richardson). Aquaculture. https://doi.org/10.1016/0044-8486(88)90012-9
Salman NA, Eddy FB (1988) Kidney function in response to salt feeding in rainbow trout (Salmo gairdneri richardson). Comp Biochem Physiol A: Physiol 89:535–539. https://doi.org/10.1016/0300-9629(88)90829-8
Salman NA, Eddy FB (1990) Increased sea-water adaptability of non-smolting rainbow trout by salt feeding. Aquaculture 86:259–270. https://doi.org/10.1016/0044-8486(90)90118-7
Salman NA (2009) Effect of dietary salt on feeding, digestion, growth and osmoregulation in teleost fish. In: Handy R, Bury N, Flik G (eds) Essential reviews in experimental biology, vol 1. Osmoregulation and ion transport: integrating physiological, molecular and environmental aspects. Society for Experimental Biology Press, London, pp 109–150
Santos RA, Bianchini A, Jorge MB, Romano LA, Sampaio LA, Tesser MB (2014) Cobia Rachycentron canadum L. reared in low-salinity water: does dietary sodium chloride affect growth and osmoregulation? Aquac Res 45:728–735. https://doi.org/10.1111/are.12017
Saravanan S, Geurden I, Figueiredo-Silva AC, Kaushik SJ, Haidar MN, Verreth JAJ, Schrama JW (2012) Control of voluntary feed intake in fish: a role for dietary oxygen demand in Nile tilapia (Oreochromis niloticus) fed diets with different macronutrient profiles. Br J Nutr 108:1519–1529. https://doi.org/10.1017/S0007114511006842
Sarker MA-A, Yamamoto Y, Haga Y, Sarker MSA, Miwa M, Yoshizaki G, Satoh S (2011a) Influences of low salinity and dietary fatty acids on fatty acid composition and fatty acid desaturase and elongase expression in red sea bream Pagrus major. Fish Sci 77:385–396. https://doi.org/10.1007/s12562-011-0342-y
Sarker MA-A, Yamamoto Y, Haga Y, Sarker MSA, Miwa M, Yoshizaki G, Satoh S (2011b) Influences of low salinity and dietary fatty acids on fatty acid composition and fatty acid desaturase and elongase expression in Red sea bream Pagrus major. Fish Sci. https://doi.org/10.1007/s12562-011-0342-y
Shaw HM, Saunders RL, Hall HC, Henderson EB (1975) Effect of dietary sodium chloride on growth of Atlantic salmon (Salmo salar). J Fish Res Board Can 32:1813–1819. https://doi.org/10.1139/f75-215
Shiau S-Y, Lu L-S (2004) Dietary sodium requirement determined for juvenile hybrid tilapia (Oreochromis niloticus × O. aureus) reared in fresh water and seawater. Br J Nutr 91:585–590. https://doi.org/10.1079/BJN20041091
Smith NF, Eddy FB, Talbot C (1995) Effect of dietary salt load on transepithelial Na+ exchange in freshwater rainbow trout (Oncorhynchus mykiss). J Exp Biol 198:2359–2364. https://doi.org/10.1242/jeb.198.11.2359
Staurnes M, Finstad B (2000) The effects of dietary NaCl supplement on hypo-osmoregulatory ability and sea water performance of Arctic charr (Salvelinus alpinus L.) smolts. Aquac Res 31:737–743. https://doi.org/10.1046/j.1365-2109.2000.00495.x
Takeuchi T, Kang S, Watanabe T (1989) Effects of environmental salinity on lipid classes and fatty scid composition in gills of atlantic salmon. B Jpn Soc Sci Fish 55:1395–1405
Tavares-Dias M (2022) Toxicity, physiological, histopathological, handling, growth and antiparasitic effects of the sodium chloride (salt) in the freshwater fish aquaculture. Aquac Res 53:715–734. https://doi.org/10.1111/are.15616
Tocher DR, Castell JD, Dick JR, Sargent JR (1995) Effects of salinity on the fatty acid compositions of total lipid and individual glycerophospholipid classes of Atlantic salmon (Salmo salar) and turbot (Scophthalmus maximus) cells in culture. Fish Physiol Biochem 14:125–137. https://doi.org/10.1007/BF00002456
Tocher DR, Bell JF, Dick JR, Henderson RCW, McGhee F, Michell D, Morris PC (2000) Polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation and the effects of dietary linseed and rapeseed oils. Fish Physiol Biochem 23:59–73. https://doi.org/10.1023/a:1007807201093
Wang H, Xu X (2019) Seawater intrusion and counter measures combining engineering controls with economic activities in Laizhou city, China. Fresenius Environ Bull 28:9661–9668
Welker TL, Lim C, Yıldırım-Aksoy M, Klesius PH (2012) Susceptibility of Nile tilapia (Oreochromis niloticus) fed with dietary sodium chloride to nitrite toxicity. Aquac Int 20:159–176. https://doi.org/10.1111/j.1365-2095.2011.00862.x
Wuertz S, Beça F, Kreuz E, Wanka KM, Azeredo R, Machado M, Costas B (2023) Two probiotic candidates of the genus Psychrobacter modulate the immune response and disease resistance after experimental infection in turbot (Scophthalmus maximus, Linnaeus 1758). Fishes 8:144. https://doi.org/10.3390/fishes8030144
Wood CM, Bucking C (2010) The role of feeding in salt and water balance. In: Farrell AP, Brauner CJ (eds) Grosell M. Fish Physiol, Academic Press, pp 165–212
Xie D, Wang S, You C, Chen F, Tocher DR, Li Y (2015) Characteristics of LC-PUFA biosynthesis in marine herbivorous teleost Siganus canaliculatus under different ambient salinities. Aquac Nutr 21:541–551. https://doi.org/10.1111/anu.12178
Yu J, Wen X, You C, Wang S, Chen C, Tocher DR, Li Y (2021) Comparison of the growth performance and long-chain polyunsaturated fatty acids (LC-PUFA) biosynthetic ability of red tilapia (Oreochromis mossambicus♀ × O. niloticus♂) fed fish oil or vegetable oil diet at different salinities. Aquaculture 542:736899. https://doi.org/10.1016/j.aquaculture.2021.736899
Zaugg WS, Roley DD, Prentice EF, Gores KX, Waknitz FW (1983) Increased seawater survival and contribution to the fishery of chinook salmon (Oncorhynchus tshawytscha) by supplemental dietary salt. Aquaculture 32:183–188. https://doi.org/10.1016/0044-8486(83)90280-6
Acknowledgements
The Japan International Cooperation Agency (JICA) and General Directorate of Fisheries and Aquaculture (GDFA), Turkey supported this study. We thank senior scientists G. Nezaki and N. Takeno and other project members for their invaluable contributions during the study.
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Open access funding provided by the Scientific and Technological Research Council of Türkiye (TÜBİTAK). This study received funds from the Japan International Cooperation Agency (JICA) and the General Directorate of Fisheries and Aquaculture (GDFA), Turkey.
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H.S. A.K. and M.O conceptualized and conducted the study, analyzed data and drafted the manuscript, F.P., Ö.A. and F.M.S analyzed samples and contributed to writing the manuscript, O.T.E. contributed to data analysis and manuscript writing. All authors read and approved the final paper.
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Sevgili, H., Kurtoğlu, A., Oikawa, M. et al. Dietary salt concentrations influence growth, nutrient utilization, and fatty acid profiles of turbot (Scophthalmus maximus) reared in brackish water. Fish Physiol Biochem (2024). https://doi.org/10.1007/s10695-024-01391-w
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DOI: https://doi.org/10.1007/s10695-024-01391-w