Physiological responses to salinity increase in blood parrotfish (Cichlasoma synspilum ♀ × Cichlasoma citrinellum ♂)
- Yanming Sui†1, 3,
- Xizhi Huang†1,
- Hui Kong1,
- Weiqun Lu1, 2Email author and
- Youji Wang1, 2Email author
© The Author(s) 2016
Received: 23 October 2015
Accepted: 27 July 2016
Published: 3 August 2016
This study aims to evaluate the effects of adding salt to water on the physiological parameters of the blood parrot cichlid (Cichlasoma synspilum ♀ × Cichlasoma citrinellum ♂). The blood parrot cichlid is a popular species in the aquarium trade because of its behaviour and beauty. Salt is usually added to water during the culture or transportation of this fish. However, the manner by which the fish adjusts its physiological responses to salinity change is unclear. The effects of salinity on serum osmolality, immune-related enzyme activities, Na+–K+-ATPase activities in the gill, skin carotenoid content and oxygen consumption were analysed. Blood parrotfish individuals were transferred from freshwater to water with four salinity levels (0.16, 2.5, 5 and 7.5 ‰) for 168 h, and physiological responses were evaluated at 0, 6, 12, 24 and 168 h. Results showed no significant differences in serum acid phosphatase and alkaline phosphatase activities, skin carotenoid content and oxygen consumption rate among the different groups. However, the serum osmolality at 6 h was significantly elevated. Moreover, salinity increase stimulated superoxide dismutase (SOD) activity from 0 to 6 h. SOD activity increased from 6 to 24 h but significantly reduced at 168 h when the fish were exposed to salt water. The SOD activity in the salinity 2.5 ‰ group recovered the initial level, whereas those in the salinity 5 and 7.5 ‰ groups decreased to levels lower than the initial level. The gill Na+–K+-ATPase activity significantly declined with time and salinity increase. Thus, adding an appropriate amount of salt can save energy consumption during osmoregulation and temporarily enhance the antioxidant activity of blood parrotfish. However, this strategy is insufficient for long-term culture. Therefore, adding salt to water only provides short-term benefit to blood parrot cichlid during transportation.
Salinity is an ecological factor with considerable importance for teleosts. A change in salinity can alter the osmotic pressure between medium and body fluid, causing osmoregulation directly in teleosts. Na+–K+-ATPase (NKA) is a membrane-spanning enzyme that actively transports Na+ out of ionocytes and K+ into ionocytes; this enzyme maintains osmotic equilibrium by providing a driving force for other ion-transporting systems (Marshall and Bryson 1998; Hirose et al. 2003; Hwang and Lee 2007). Thus, NKA is considered a good biomarker of osmoregulation in teleosts. Several recent studies have reported that NKA activity changes with environment salinity variation (Fuentes et al. 1997; Laiz-Carrion et al. 2005; Malakpour Kolbadinezhad et al. 2012; Fisher et al. 2013; Handeland et al. 2014; Imsland et al. 2014; Vargas-Chacoff et al. 2014). Previous studies indicated that transferring fish to different salinities causes changes in oxygen consumption. The oxygen consumption of the Mozambique tilapia Oreochromis mossambicus enhances when salinity is increased (Zikos et al. 2014). Cao and Wang (2015) also found that the oxygen consumption of the mudskipper Boleophthalmus pectinirostris increases significantly when the salinity is increased from 12 to 27. Similar results were obtained in the inanga Galaxias maculatus (Urbina and Glover 2015). However, previous studies obtained different results possibly because of differences in species, acclimation duration, experimental design and measurement methodology. Morgan and Iwama (1991) summarised five oxygen consumption rate patterns from previous studies: (1) no change occurs in the oxygen consumption rate; (2) the oxygen consumption rate is minimum in isotonic salinity but increases in different salinities; (3) a linear relationship exists between the oxygen consumption rate and fluctuant salinity; (4) the oxygen consumption rate increases in hypotonic water and decreases under isotonic salinity condition; and (5) the highest oxygen consumption occurs in hypertonic water. Moreover, the relationship of salinity to the immune response of teleosts has received considerable attention in recent years (Harris and Bird 2000; Zhang et al. 2011; Arnason et al. 2013; Choi et al. 2013). Superoxide dismutase (SOD) is a common antioxidant enzyme that can protect organisms against reactive oxygen species-induced damage, which may lead to many disorders (Stadtman and Levine 2003; Seifried et al. 2007). Therefore, the antioxidant status in fish can be accurately reflected by SOD activity. Ma et al. (2014) indicated that salinity regulates the antioxidant activities of the juvenile golden pompano Trachinotus ovatus. They found that the SOD activity of this species is low at 10 ‰ salinity than at higher salinity levels. Acid phosphatase (ACP) may also act as an antioxidant that inhibits membrane nicotinamide adenine dinucleotide phosphate (NADPH) oxidase activity and consequently suppresses H2O2 and O2 production by immune cells (Glew et al. 1988). In most animal cells, alkaline phosphatase (ALP) is an important non-specific phospho-monoesterase enzyme that functions in phosphate metabolism. In aquatic organisms, responses to salinity include changes in oxygen consumption (Viarengo and Nott 1993) and osmoregulation (Lovett et al. 1994). Currently, several studies have focused on the effect of salinity changes on teleost osmoregulation, oxygen consumption rate and immunity response. These studies are mostly limited to marine or estuarine fish. Hence, the effects of salinity on ornamental freshwater fish remain unknown to date.
In many ornamental fish markets in China, some aquaculturists usually add salt to water during transportation and water renewal to maintain freshwater ornamental fish in a good shape (i.e. fish are more active and bright-coloured). However, the physiological effects of increased salinity on freshwater ornamental fish are unclear. Blood parrot, commonly known as bloody parrot or blood parrotfish, is a popular ornamental freshwater fish worldwide. Blood parrot is a man-made cross-bred fish hybridised from male Cichlasoma citrinellum and female Cichlasoma synspilum in Taiwan during the late 1980s and enjoyed in many countries, such as China and Japan, in recent years because of its bright red appearance and plump body. To explain the above phenomenon and explore whether increasing salinity favours the culture or transportation in freshwater ornamental fish, we chose blood parrotfish as a model to clarify the physiological mechanism based on the following hypotheses: (1) Increased water salinity saves energy for oxygen consumption by regulating NKA activity; (2) Increased water salinity stimulates fish immune responses by increasing antioxidant enzymes; (3) Increased water salinity helps preserve the fish skin pigment. Thus, the oxygen consumption, NKA activity, serum osmolality, immune-related enzyme activities in the gill, and skin carotenoid content of blood parrotfish were investigated by transferring fish from freshwater to water with four salinity levels (0.16, 2.5, 5 and 7.5 ‰) for 168 h, and physiological parameters were evaluated at 0, 6, 12, 24 and 168 h. Our results may also provide some useful information for freshwater ornamental fish production and logistics.
Animals and sampling methods
Blood parrots C. synspilum ♀ × C. citrinellum ♂ (total length 12–14 cm, body weight 52.5–54.0 g) were originally obtained from a commercial fish farm (Jiaxing, Zhejiang, China). All fish were maintained in a freshwater (a salinity of 0.16) recirculating tank with a 12L:12D photoperiod at 28 ± 1 °C in the Aquarium of Shanghai Ocean University, Shanghai, China. The treated salt water was prepared by adding artificial sea salt to freshwater. Blood parrots were transferred directly from freshwater to treated water with different salinity levels (0.16 as control, 2.5, 5 and 7.5) at the same time by nylon-net capture. Each treatment included three tanks (50 L) as three replicates with 25 fish each tank. During the experimental period (0–168 h), fish were reared in the experimental tanks without feeding. The fish from all groups were sampled at 0, 6, 12, 24 and 168 h at each sampling time point. Five individuals were randomly selected from each tank. Fish were anaesthetised with ice and killed immediately. Blood was collected via caudal puncture using a non-heparinised 2 mL syringe and then transferred to a 1.5 mL tube on ice. Blood samples were stored at 4 °C overnight, centrifuged at 800×g for 5 min and then serum was stored at −80 °C. The gills were removed and weighed.
The tissue was homogenised in homogenisation solution (100 mM imidazole–HCl buffer, pH 7.0, 5 mM Na2 EDTA, 200 mM sucrose and 0.1 % sodium deoxycholate) with a motorised Teflon pestle at 600×g for 20 strokes on ice. After centrifugation (12,000×g for 30 min at 4 °C), the supernatant was stored at −80 °C until assay. Carotenoids were obtained from freeze dried skin in accordance with the method of Boonyaratpalin et al. (2001).
Serum osmolality (mOsm/kg) was measured using a Vapro©Model 5520 vapour pressure osmometre (Wescor Inc., Logan, Utah, USA) from 10 μL of serum. Each sample was measured in duplicate.
Serum ACP, ALP, SOD and gill NKA activity assay
The activities of ACP, ALP, SOD and NKA were determined using commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China) in accordance with the method of Ma et al. (2014). (1) ACP and ALP activities were measured by using disodium phenylphosphate as the substrate. The enzyme unit definitions of ACP (U/100 mL serum) and ALP (U/100 mL serum) were expressed as the degradation of 1 mg phenol/mg serum at 37 °C within 30 and 15 min, respectively. (2) SOD activity was assayed using the xanthine/xanthine oxidase method based on the production of O2 − anions. (3) NKA activity was measured using an endpoint phosphate ATP hydrolysis protocol following the kit. The inorganic phosphate released was determined by colorimetric assays, and NKA activity was expressed as micromole inorganic phosphate per mg protein per hour.
Oxygen consumption rate
Prior to the analysis, normality of the data was evaluated by using the Shapiro–Wilk’s test, and homogeneity of variances was checked by Levene’s test using the statistical software SPSS 17.0. One-way ANOVA was applied to evaluate the effects of salinity on all parameters at each time point, and Student–Newman–Keuls tests were performed to determine which salinity treatments were different. For the time effects, paired t test was used to compare the difference between each sampling time and 0 h at each salinity treatment, respectively. Differences were considered significant at P < 0.05. The results are expressed as mean ± SD.
Oxygen consumption rate and carotenoid content
Compared with that in the control group, the SOD activities in all trial groups increased after 6 h of exposure, suggesting that increased salinity can stimulate SOD activity within a short period. Nevertheless, high SOD activities were not maintained at all sampling times. The value changed greatly at 168 h. As shown in Fig. 3, SOD activity returned near the initial level in the salinity 2.5 ‰ group, whereas those in the salinity 5 and 7.5 ‰ groups reduced significantly by 50 and 65 %, respectively. The study on the juvenile silver pomfret Pampus argenteus by Yin et al. (2011) showed that salinity change might stimulate SOD activity to some extent, but the activity would recover more or less with the elongation of time. Similar results were also found in pompano. Liu et al. (2013) indicated that increased salinity enhances liver SOD enzyme activity. In accordance with the results of our research, adding appropriate salt to water could temporarily enhance the antioxidant ability of fish. However, this strategy is insufficient or harmful for long-term culture.
Phosphatases remove phosphate groups from their substrates by hydrolysing phosphoric acid monoesters into phosphate ions and molecules with free hydroxyl groups. ACP and ALP are important phosphatases in aquatic organisms; these enzymes participate in the degradation of foreign proteins, carbohydrates and lipids (Liu et al. 2004). ACP is a typical lysosome enzyme that plays a role in killing and digesting pathogens in immune responses (Yin et al. 2014). ALP is a multi-functional enzyme involved in immune responses (Xing et al. 2002). Both enzymes are sensitive to environment change. In the present study, ACP activity did not change significantly, indicating that increased salinity levels only slightly affected the physiological functions of blood parrotfish. The result is supported by Fang et al. (2014), who found that the ACP activities in the gill and kidney of the juvenile tongue sole Cynoglossus semilaevis show no significant difference between low salinity and high salinity treatments. Similar to ACP activities, ALP activities were also not affected by increased salinity. However, the ALP activity in the serum of the cobia Rachycentron canadum increases when the salinity is within the range of 5 to 37 (Feng et al. 2007). In general, ACP and ALP activities were not significantly altered. This result indicates that blood parrotfish can easily adapt to salinity increase.
Salinity and osmolality (mean ± SD, n = 5) of trial water during the experiment period
0.16 ± 0.01
2.5 ± 0.05
5 ± 0.06
7.5 ± 0.05
21 ± 1
82.5 ± 1.1
251 ± 1.2
210 ± 1.5
The carotenoid content of the skin in some ornamental fish is crucial because it would affect acceptability by consumers. In a recent study, Eslamloo et al. (2015) have stated that background colour could affect goldfish skin pigmentation. The carotenoid concentration in the skin significantly decreases in white background in comparison with the other groups. Doolan et al. (2008) recommended that holding snapper in white cages at high densities greatly improves skin lightness in comparison with black cages. In the present study, the carotenoid contents in the blood parrotfish skin did not change in the various salinity groups. This result implies that salinity change could not affect the skin pigmentation of blood parrotfish.
On the basis of the estimated parameters, adding appropriate salt into water provides benefits to the transportation or short-term culture of blood parrotfish by temporarily elevating the antioxidant ability of this ornamental fish. However, this strategy is insufficient for long-term culture.
YJ, YM and WQ conceived and designed the study, YM and Hui carried out the experiments, YM, XZ and YJ drafted manuscript and participated in data analysis. WQ and YJ supervised and approved the designed the study, statistical analysis and manuscript writing. All authors read and approved the final manuscript.
This work was supported in part by National Natural Science Foundation of China (Project Nos. 31572599, 31072228, 41376134, 31302207), Shanghai Municipal Natural Science Foundation (Project Nos. 13ZR1455700). The authors are grateful to the two anonymous reviewers for their constructive comments.
The authors declare that they have no competing interests.
Compliance with ethical guidelines
All experimental procedures with live fish were performed in accordance with the guidelines on the care and use of animals for scientific purposes set by the Institutional Animal Care and Use Committee (IACUC) of Shanghai Ocean University, Shanghai, China.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
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