Survival, growth and digestive enzyme activity of juveniles of ... - Uesc

Aquaculture 271 (2007) 319 – 325 www.elsevier.com/locate/aqua-online

Survival, growth and digestive enzyme activity of juveniles of the fat snook (Centropomus parallelus) reared at different salinities Mônica Y. Tsuzuki a,⁎, Juliet K. Sugai b , Julio Cesar Maciel a , Claire J. Francisco a , Vinícius R. Cerqueira a a

b

Laboratório de Piscicultura Marinha, Departamento de Aqüicultura, Centro de Ciências Agrárias, Universidade Federal de Santa Catarina (Federal University of Santa Catarina), C.P. 476, Florianópolis, SC, 88040-970, Brazil Departamento de Bioquímica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina (Federal University of Santa Catarina), C.P. 476, Florianópolis, SC, 88040-900, Brazil Received 2 September 2006; received in revised form 6 May 2007; accepted 7 May 2007

Abstract The effect of salinity on survival, growth and activity of digestive enzymes was evaluated in the fat snook (Centropomus parallelus). Juveniles of 76 days after hatching (0.35 g) were reared at 5, 15 and 35 ppt, in triplicate, for 50 days, at 0.6 fish/l. Snook presented excellent survival (N 93.3%) at 5, 15 and 35 ppt, demonstrating the euryhalinity of the species. At the end of the experiment, no differences in weight and specific-growth rates (mean 1.8%/day) were observed, however, total and standard length values were higher at 15 ppt when compared to those at 5 ppt (P N 0.05). The best results in food conversion ratio (1.3) and digestive enzymes activity were obtained at 15 ppt. The activity of total alkaline proteinase was significantly affected at this salinity (0.124 ± 0.006 Δ absorbance366 nm/min/ml/mg protein), being two-fold and six-fold higher, compared to 35 and 5 ppt, respectively. The activity of total amylase was higher at 15 and 35 ppt (mean 0.016 ± 0.001 μmol reducing sugar/min/ml/mg protein), compared to 5 ppt (P b 0.05). Results indicate that fat snook reared at 15 ppt presented a higher potential for a more efficient digestibility and nutrient absorption, especially proteins. Additionally, at this salinity, the energetic demand for osmoregulation is probably reduced by the isosmotic medium, leading to growth enhancement. In terms of production costs, feeding expenses can be lowered at this salinity due to a better food conversion ratio. © 2007 Elsevier B.V. All rights reserved. Keywords: Fat snook; Centropomus parallelus; Salinity; Survival; Growth; Digestive enzymes

1. Introduction The fat snook (Centropomus parallelus), Centropomidae family, is distributed from southeast Florida, EUA to Florianópolis, southern Brazil. It can be found in coastal areas, bays, estuaries and brackish lagoons, freshwater

⁎ Corresponding author. Tel.: +55 48 3232 7532. E-mail address: [email protected] (M.Y. Tsuzuki). 0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2007.05.002

environments and occasionally in hypersaline lagoons (Cervigón et al., 1992). Fat snook is considered as a valuable fish species due to the quality of its flesh, being appreciated for sportive and artisanal fisheries. In general, species of the Centropomidae family present a good potential for cultivation, as they adapt well to captive conditions and accept artificial diets. They are also resistant to husbandry and variations of physicochemical parameters of the water (Chapman et al., 1982; Tucker, 1987).

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In Brazil, the technology for mass production of fat snook juveniles is already available (Alvarez-Lajonchère et al., 2002). However, further studies are needed at the grow-out phase to determine the feasibility of its production at a commercial level. Currently, fat snook culture is done at a discontinuous and non-quantified approach by small producers in marine, brackish and freshwater environments, in different regions of the country (Cerqueira and Tsuzuki, 2003). Fat snook is considered as an euryhaline fish (Rivas, 1986; Tsuzuki et al., 2007), nevertheless, the viability and potential of cultivation of this species in environments of different salinities has never been evaluated. According to Iwama (1996), salinity can change the amount of energy available for fish growth by altering the energetic cost for ionic and osmotic regulation. Several authors have studied the influence of water salinity on fish growth, and very often salinity affects growth. For instance, growth enhancement was observed in lower salinity levels (0–9 ppt), in the striped bass (Morone saxatilis) larvae (Peterson et al., 1996), milkfish (Chanos chanos) fry (Alava, 1998), and wild juveniles of fat snook (Rocha et al., 2004). In these cases, better growth rates in such conditions were attributed to a preference by younger fish to environments of lower salinity levels found in estuaries or freshwater environments during their natural development (Alava, 1998), or a lower energetic requirement for maintenance of the osmotic and ionic equilibrium in lower salinities (from low to intermediate levels) compared to salt water. Better growth rates have also been obtained at intermediate salinities (10–19 ppt) in juvenile turbot (Scophthalmus maximus=Psetta maxima) (Gaumet et al., 1995), golden-line seabream (Sparus sarba =Rhabdosargus sarba) (150–250 g) (Woo and Kelly, 1995), young grey mullet (Mugil sp.) (De Silva and Perera, 1976; Peterson et al., 1996). These studies support the hypothesis that the energetic cost for osmoregulation is lower at an isosmotic medium, in which gradients between the blood and water are minimal, and the energy saved is directed for increasing growth. However, higher salinity levels (20–55 ppt) have also shown to improve growth in other species such as the black bream (Acanthopagrus butcheri) juvenile (Partridge and Jenkins, 2002), southern flounder (Paralichthys lethostigma) larvae (Moustakas et al., 2004), european seabass (Dicentrarchus labrax) fingerlings (Eroldogan et al. 2004), and milkfish juvenile (Swanson, 1998). In most of these cases, higher growth in saltwater, compared to freshwater, is attributed to a lower energetic cost for osmoregulation in waters of higher salinities. Therefore, the effect of salinity affecting the growth and survival of euryhaline fish is species-specific, and may also change during the ontogenetic development.

Salinity can also influence the activity of digestive enzymes, and in this regard affect growth performance (Moutou et al., 2004). Exposure of fish to various salinities results in changes in drinking rates (Usher et al., 1988), and it is possible that the activity of digestive enzymes could be affected by the salinity of gut content. The objective of the present study was to evaluate the effect of salinity on survival and growth, and the activity of digestive enzymes in juveniles of the fat snook (C. parallelus). 2. Material and methods 2.1. Animals and general rearing conditions The experiment was developed at the Marine Fish Culture Laboratory (LAPMAR), Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil. Fat snook (C. parallelus) broodstock were held and spawned at 35 ppt, 26 °C. Juveniles obtained by hormonally induced fish (Ferraz et al., 2002) were reared following methods previously described (Alvarez-Lajonchère et al., 2002), and weaned to an artificial diet approximately 45 days after hatching. Until the start of the experiment, they were kept at 25 °C, 35 ppt salinity, under natural photoperiod, and fed a commercial dry pellet (50% Crude Protein; 7% Fat). 2.2. Experimental design Juveniles of 76 days after hatching (DAH), 0.35 ± 0.1 g weight, 33.6 ± 0.2 mm total length and 26.4± 0.3 mm standard length (mean ± SE), were stocked in circular tanks (60 l), at a stocking density of 35 fish/tank (0.6 fish/l). The experiment consisted of rearing fish at three salinities (5, 15 and 35 ppt), in triplicate, for 50 days. Prior to the trial, acclimation to salinity was done by gradually decreasing water salinity at an approximate rate of 6 ppt per day until reaching 15 ppt, and at a rate of 3 ppt per day until final salinity of 5 ppt. Salinity levels were obtained by mixing dechlorinated tap water with natural seawater, and measured with a Bernauer Model F3000 optical refractometer (Bernauer Aquacultura, Blumenau, Brazil, 1 ppt precision). Temperature was controlled at 25 °C by thermostat-heaters, and dissolved oxygen levels were kept at near saturation levels. Fish were fed with the same diet as previously described. Feeding was done to apparent satiation twice a day, by offering few pellets each time for approximately 1 min at each tank until all tanks have finished, and repeating this process until all fish stopped feeding.

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The amount of feed offered was daily recorded for apparent food conversion ratio calculation: FCR = weight of feed (g) × biomass gain (g). Metabolic and food wastes were daily siphoned, and 100% of the water was renewed. Fish measurements (n = 35 for each replicate) were done at the beginning (76 DAH), after 30 days (106 DAH) and 50 days (126 DAH) of experiment, by rapidly anesthetizing fish with benzocaine (84 g of benzocaine/ l alcohol 98%), weighing to the nearest 0.01 g using a digital scale and measuring them (total and standard length) to the nearest 1 mm using a caliper. Feeding was discontinued 24 h prior to measurements. Daily specificgrowth rate was calculated as SGR = 100 (ln Wt − ln W0) / T (%/day), where ln Wt and ln W0 are the natural logarithms of final and initial weight, respectively, and T is the period of growth (days). Twice daily, temperature and dissolved oxygen (DO) were measured with oxymeter YSI Model 51 (Yellow Springs Instrument Company, Yellow Springs, Ohio, USA). Total ammonia-nitrogen (TAN) was monitored weekly with Tetratest® Kit (Tetra Werke, Melle, Germany), and un-ionized ammonia (NH3-N) was calculated from TAN, pH level and temperature.

and 5 mg of starch. Optical absorbance of reducing sugars was corrected using substrate/enzyme blank values. The total amylase activity was expressed as specific activity (μmol reducing sugars/min/ml/mg protein in the extract, U/mg protein) at 37 °C. Total alkaline proteinase activity of the extract was measured using the azocasein (Sigma Chemical Co, St Louis, Missouri, USA) hydrolysis method described by Garcia-Carreño et al. (1997). The enzymatic system was incubated for 10 min at 22– 25 °C, and the absorbance at 366 nm for the released dye was estimated. The control (blank) was assayed by adding 20% trichloroacetic acid to the reaction system before substrate addition. The total alkaline proteinase was expressed as specific activity, the difference in the absorption at 366 nm between sample and blank per minute, per ml, and per mg protein in the extract (Δ absorbance366 nm/min/ml/mg protein). Soluble protein of crude enzyme extracts was quantified (Lowry et al., 1951) using bovine serum albumin (Sigma Chemical Co., St. Louis, USA) as standard. The enzymatic assays were performed in duplicate for each homogenate per replicate (six determinations per salinity).

2.3. Enzymatic analysis

2.4. Statistical analysis

In order to evaluate the effect of salinity on the digestive enzymes activity of fat snook, at the end of the experiment above described, two juveniles were sampled from each replicate and salinity, and immediately frozen at −20 °C until the preparation of the homogenate for enzyme activity analysis. The juveniles sampled were individually dissected under-ice and the whole gut was extracted, washed in distilled water, and sliced into small pieces. Tissues were homogenized in ice-cold distilled water (1:16, w/v) using a van Potter homogenizer for 2.5 min and centrifuged at 27,167 ×g for 15 min at 4 °C. The supernatant was used for enzyme and soluble protein assays. Total amylase activity was estimated using soluble starch as substrate as described by Aguillar-Quaresma and Sugai (2005). The released reducing sugar was assayed using maltose (E. Merck, Darmstadt, Germany) as the standard. In order to quantify endogenous reducing sugars in the homogenates, as well as in the starch solution (substrate) as a result of the possible non-enzymatic hydrolysis of this starch, assay mixtures of enzyme and substrate blanks were also used. These were obtained by incubating the buffer, sodium chloride, and enzyme extract without substrate (starch) for 15 min at 37 °C, and subsequently boiling in a water bath for 3 min, before finally adding 2 ml of cold distilled water

Differences in survival, growth, food conversion rates and digestive enzyme activity were evaluated by one-way analysis of variance (ANOVA), with subsequent Tukey test. Statistical significance was assumed as P b 0.05. 3. Results The water quality parameters monitored during the experiment were maintained at desirable levels and did not vary among the treatments and replicates (P N 0.05). Temperature was kept at 24.7 ± 0.3 °C (mean ± SE), pH at 7.4 ± 0.6, and dissolved oxygen at 5.8 ± 0.8 mg/l. Total ammonia-nitrogen (TAN) varied from 0.33 to 0.75 ± 0.01 mg/l, and un-ionized ammonia (NH3-N) from 0.01 to 0.03 ± 0.01 mg/l. Survival rates were higher than 93.3% at the different salinities (Table 1). Table 1 shows that growth as weight and specificgrowth rate was similar at 5, 15 and 35 ppt after 30 and 50 days of experiment (P N 0.05). Total and standard length also did not differ significantly among treatments after 30 days of cultivation (106 DAH). However, after 50 days, higher growth related to these parameters was observed at 15 ppt, but only compared to 5 ppt (P b 0.05). No significantly differences were found at 5 and 35 ppt, and at 15 and 35 ppt. The apparent food

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Table 1 Survival, growth and apparent food conversion ratio in fat snook, Centropomus parallelus juveniles at different salinities, after 30 and 50 days of cultivation Days of cultivation

Salinity (ppt)

Survival rate (%)

Weight (g)

Total length (mm)

Standard length (mm)

Specific-growth rate (%/day)

Apparent food conversion ratio

30

5 15 35 5 15 35

98.1 ± 0.91 100.0 ± 0.00 96.2 ± 0.94 94.3 ± 2.83 100.0 ± 0.00 93.3 ± 0.02

0.53 ± 0.01 0.59 ± 0.13 0.53 ± 0.01 0.84 ± 0.02 0.91 ± 0.02 0.86 ± 0.02

38.3 ± 0.81 40.5 ± 0.43 39.3 ± 0.40 45.9 ± 0.53a 47.8 ± 0.02b 46.9 ± 0.42ab

30.2 ± 0.72 32.1 ± 0.22 31.1 ± 0.32 36.7 ± 0.32a 38.2 ± 0.13b 37.3 ± 0.35ab

1.4 ± 0.81 1.8 ± 0.51 1.4 ± 0.84 1.7 ± 0.52 1.9 ± 0.34 1.7 ± 0.63

1.3 ± 0.04 1.1 ± 0.05 1.2 ± 0.05 1.6 ± 0.03a 1.3 ± 0.06b 1.6 ± 0.14a

50

Data presented as mean ± standard error (n = 32–35). Means with different letters in the same column, at the same day of cultivation, are significantly different (P b 0.05). Initial values for 76 DAH juveniles: weight: 0.35 ± 0.08 g; total length: 33.6 ± 0.29 mm; standard length: 26.4 ± 0.26 mm.

conversion ratio was similar for the different treatments after 30 days, but at the end of the experiment it was lower (1.3) at 15 ppt, compared to the other salinities (1.6) (P b 0.05) (Table 1). The specific activity of total amylase was 0.007 ± 0.001; 0.016 ± 0.001 and 0.017 ± 0.002 μmol reducing sugar/min/ml/mg protein (mean ± SE) at 5, 15 and 35 ppt, respectively (Fig. 1). The total amylase activity of fish reared at 15 and 35 ppt was significantly higher than the activity of those found in fish reared at 5 ppt (P b 0.05). The total alkaline proteinase activity was 0.021 ± 0.002; 0.124 ± 0.006 and 0.052 ± 0.004 Δ absorbance366 nm/min/ ml/mg protein for 5, 15 and 35 ppt, respectively. As a result, after 50 days, the total alkaline proteinase activity in the digestive tract of fish reared at 15 ppt was two-fold and six-fold higher, compared to those reared at 35 and 5 ppt, respectively (P b 0.05) (Fig. 1).

Fig. 1. Activity of total amylase and total alkaline proteinase in the digestive tract of fat snook juveniles reared at 5, 15 and 35 ppt. Specific activity of total amylase = μmol reducing sugars/min/ml/mg protein at pH 6.8 and 37 °C). Specific activity of total alkaline proteinase = Δ absorbance366 nm/min/ml/mg protein. Data presented as mean ± SE. Means with different letters in the same digestive enzyme, and at different salinities are significantly different (P b 0.05).

4. Discussion In the present study, it was verified that after 50 days of cultivation, fat snook juveniles presented excellent survival at 5, 15 and 35 ppt, demonstrating the euryhalinity of this species. It is known that Centropomus sp. usually spawn nearshore, and after hatching, larvae are carried by currents to protected estuarine areas (Gilmore et al., 1983; McMichael et al., 1989). Depending on the life stage, snooks can explore different estuarine habitats, with salinities ranging from 0 to 30 ppt (Aliume et al., 1997), implying certain metabolic constraints (Peterson and Gilmore, 1991; Aliume et al., 1997; Peters et al., 1998). Although several marine fish species can stand a strong gradient of variation in salinity, part of the metabolic energy is spent in the osmoregulatory process (Marais, 1978; Moser and Miller, 1994). Even in species with lower metabolic rates, osmoregulation appears to use a high proportion of the available energy, ranging from 20 to 50% of the total energetic expenditure (Boeuf and Payan, 2001). In relation to growth, although no significant differences in weight and specific-growth rates were detected in the present study, total and standard lengths were higher at 15 ppt, but only when compared to 5 ppt. Several authors reported better performance in fish cultivated at intermediate salinities. For instance, Lambert et al. (1994) feeding Atlantic cod (Gadus morhua) larvae at 7, 14 and 28 ppt, did not find differences in food capture. However, higher growth rates were obtained at the intermediate salinity (14 ppt), possibly due to a more efficient conversion ratio. In the case of whitefish larvae (Chirostoma estor estor), Martinez-Palácios et al. (2004) obtained greater specific-growth rates at 10 and 15 ppt, compared to those at 0 and 5 ppt, but net production, based on survival and growth, was clearly superior at 10 ppt, with a very low response at 0 ppt. Woo and Kelly (1995) found that the

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growth and protein efficiency (weight gain/protein consumed) ratios in 150–250 g golden-line seabream (Sparus sarba = Rhabdosargus sarba) cultivated at 15 ppt were consistently higher than other salinities. Wada et al. (2004), in experiments with spotted halibut (Verasper variegatus) juveniles, found that fish kept at 8 and 16 ppt, showed higher growth rates in terms of weight and length, than fish kept at 32 ppt (control) and at 4 ppt. Marine fish usually regulate their plasmatic ions in a way that the osmotic pressure of their fluids is kept at 10 and 15 ppt (Brett, 1979; Jobling, 1994). Therefore, the hypothesis that the energetic cost for osmoregulation is lower at an isosmotic medium, where the gradients between blood and water are minimum, and the energy saved is sufficient enough to increase growth, is supported by a number of studies (Morgan and Iwana, 1991; Soengas et al., 1995; Altinok and Grizzle, 2001; Boeuf and Payan, 2001). In studies related to the effect of salinity on the digestive enzymes, it was observed that transference of fish to different salinities can result in alteration of the digestive enzymes activity (Moutou et al., 2004). The activities of total alkaline proteinase and chymotrypsin intestinal were lower in gilthead sea bream (Sparus aurata) held at 20 ppt compared to 33 ppt, but at the lowest salinity, the activity of trypsin was higher (Moutou et al., 2004). Similarly, Woo and Kelly (1995) observed that golden-line sea bream exposed to 7 ppt exhibited significantly higher trypsin activity compared to 15 ppt and 35 ppt. These studies indicate that the activity of different proteinase subclasses may be influenced by water salinity. Changes in their activity may influence digestion and absorption of dietary protein, once trypsin and chymotrypsin are the major intestinal (alkaline) proteinases. These enzymes are synthetized as inactive zymogens in the pancreatic cells and activated by specific proteolysis and release into the gut lumen. In this regard, Moutou et al. (2004) suggested that changes in water salinity most likely influence either the activation of each zymogen separately, since it takes place outside the cell boundaries, in the intestinal lume, or the activity of each proteinase itself. Few studies have examined the growth rate and activity of digestive enzymes ratios of fish reared at different salinities (Woo and Kelly, 1995; Lemieux et al., 1999; Moutou et al., 2004), sometimes leading to different conclusions. For instance, when analyzing the correlation coefficient between the final body weight and total alkaline proteinase and chymotrypsin activities, Moutou et al. (2004) observed negative relations,

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showing that the gilthead sea bream that grew best had the lowest alkaline proteinase and chymotrypsin activities at 20 ppt compared to 33 ppt. In golden-line seabream, the optimal growth rate was observed at 15 ppt than at 7 and 35 ppt. In this case, fish exposed to 7 ppt exhibited significantly higher trypsin activity compared to 15 ppt and 35 ppt. Therefore, at an isosmotic environment golden-line seabream did not exhibit significantly higher intestinal trypsin activity (Woo and Kelly, 1995). In the present study, juvenile fat snook showed higher activity of total alkaline proteinases at 15 ppt than fish reared in both 35 and 5 ppt, and also had higher growth (total and standard length) when compared to 5 ppt. Therefore, further investigation is required in order to clarify this subject. Through a comparative study of the digestive proteolytic and amylase activity, it is possible to predict the digestive ability of different species in relation to protein and carbohydrate contents of the diet (Hidalgo et al., 1999). Several works reported that the ratio of total proteinase: total amylase activity in omnivorous and herbivorous fish was lower than in carnivorous fish (Hofer and Schiemer, 1981; Ugolev et al., 1983). In fat snook, considering this ratio (7.7; 3.0; and 3.0 at 15, 35, and 5 ppt, respectively), it can be seen that this fish shows characteristics of a carnivorous species, as already expected. However, more important is the fact that fat snook presented higher potential (2.5 times) to digest proteins than carbohydrates at an isosmotic salinity (15 ppt) compared to 35 and 5 ppt. These results are in accordance with the lower food conversion ratio (1.3) obtained at 15 ppt. Therefore, results of the present study show that fat snook reared at 15 ppt have a more efficient digestibility and nutrient absorption. Complementary, at this salinity, the energetic demand is probably reduced by the isosmotic medium, leading to growth enhancement. In terms of production costs, feed expenses can be reduced due to a better food conversion and digestive efficiency at 15 ppt. This is a very relevant fact, since feeding costs in carnivorous fish can represent up to 60% of the total costs in a fish farming activity (Stickney, 1994). Acknowledgements This work was supported by the CAPES Brazilian Coordination for the Improvement of Higher Education Personel through scholarships. We would like to thank Israel Diniz and Antônio Carlos Sayão as well as the rest of the group at LAPMAR for their technical assistance, and Robert Vassalo-Agius for helping improve the clarity of the manuscript.

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