G. EBRAHIMI, H. OURAJI

Turk J Zool 2012; 36(4) 551-558 © TÜBİTAK Research Article doi:10.3906/zoo-1008-139

Growth performance and body composition of kutum fi ngerlings, frisii kutum (Kamenskii 1901), in response to dietary protein levels

Ghaff ar EBRAHIMI, Hossein OURAJI* Department of Fisheries, Sari Agricultural Sciences and Natural Resources University, P.O. Box, 578, Sari - IRAN

Received: 31.08.2010

Abstract: A feeding trial was conducted to determine the optimal dietary crude protein requirement for Rutilus frisii kutum fi ngerlings. Five isoenergetic experimental diets were formulated to contain graded levels of protein (32%, 37%, 42%, 47%, and 52%). Triplicate groups of 80 kutum (average weight 0.5 g) were stocked in 250-L tanks and fed to apparent satiation 3 times a day for 8 weeks. Th e results indicate that the growth performance and feed utilization of kutum were signifi cantly (P < 0.05) aff ected by dietary protein level. Th e second polynomial regression of weight gain against protein level yielded an estimated optimal dietary protein requirement of 41.6%. Weight gain, specifi c growth rate, and feed effi ciency increased with increasing the dietary protein level from 32% to 42%, but decreased signifi cantly (P < 0.05) with further increases in dietary protein. Th e protein effi ciency ratio was inversely correlated with dietary protein level. Feed intake was not aff ected (P > 0.05) by dietary protein level. No signifi cant diff erence was found in the whole-body protein, lipid, moisture, or ash contents of fi sh fed the diff erent dietary protein levels. Th e results obtained from this study could be benefi cial in order to formulate artifi cial feed for aquaculture of kutum fi ngerlings.

Key words: Rutilus frisii kutum, protein requirement, growth, fi sh diet, protein effi ciency

Introduction important part of the local diet during the fi shing Kutum, Rutilus frisii kutum (Kamenskii, 1901; season, from the beginning of October to mid-April. Kutum is a migratory anadromous fi sh that spawns family ), locally known as mahi sefi d, is on aquatic weeds, gravel, and sandy substrate in rivers an important commercial fi sh in Iran. Th is species is and lagoons. Th e spawning season of the kutum in native to the and distributed from the the rivers of the southern part of Caspian Sea begins mouth of the Volga River up to the Astrabadskiy in late March and ends in mid-May (Azari Takami, Bay. Th e main population of kutum is located at the 1990). A sharp decline in the annual catch of kutum southern coast of the Caspian Sea from the Atrak observed in the 1970s and early 1980s was likely River to the Kura River (Caspian Environment; due to declining natural populations, exacerbated Razavi, 1997; Abdoli and Naderi, 2009). Kutum is a by the destruction of natural spawning areas and very popular fi sh for human consumption, especially other factors (Ghaninejad and Abdulmaleki, 2007), in northern Iran, as this fi sh species comprises an and, since then, the natural reproduction of kutum * E-mail: [email protected]

551 Growth performance and body composition of kutum fi ngerlings, Rutilus frisii kutum (Kamenskii 1901), in response to dietary protein levels has been limited. As a result, the Iranian fi sheries Materials and methods organization (Shilat) launched a restocking project Experimental diets in 1984. Th is project seems to have been successful in increasing kutum biomass in the Caspian Sea: the Five isoenergetic experimental diets were formulated annual landing of kutum increased from 563 t in to contain graded protein levels (32%, 37%, 42%, 1982 to 16,118 t in 2006 (Salehi, 2008). 47%, and 52%, wet weight basis). Ingredients were obtained from a local feed manufacturer (khorak To restock this valuable species, the Shilat dame mazandran, Sari). To determine the energy annually produces and releases more than 200 million content of the food, the amounts of protein, fat, and fi ngerlings into rivers, which carry them towards carbohydrate in each diet was determined. Th e gross the Caspian Sea (Heyrati Paykan et al., 2007). In energy content of each diet was then calculated based the restocking centers, larval rearing takes place in on 23.4, 39.2, and 17.2 MJ/kg for protein, lipid, and earthen ponds. Kutum larvae are grown in the ponds nitrogen-free extract, respectively (Kim and Lee, until a releasing weight of 1 g is attained. 2005). Th e composition and proximate analysis of Th e successful production of kutum in hatcheries the experimental diets are shown in Table 1. Th e means that a reliable supply of fi ngerlings is now experimental diets were prepared by mixing the dry available for commercially culturing this species. ingredients in a Pars electric mixer; then oil and Success of aquaculture is aff ected by several factors. suffi cient water was added to the dry mixture to form One important factor is the formulation of balanced a soft dough (approximately 40% to 50% moisture). diets for the fi sh that provide the required nutrients to Th e mixed dough was extruded through an electric support good growth and health (Salhi et al., 2004). meat grinder and dried at 60 °C for 6 h in a drying Because protein plays a key role in the growth of fi sh, oven. Diets were packed and stored at –20 °C until knowledge about the protein requirements of each utilization. species is essential for the formulation of species- and feeding trial specifi c diets. Inadequate protein in diets will result Kutum fi ngerlings were obtained from the Shahid in a reduction or cessation of growth. On the other Rajaee restocking center located on the southern hand, if excessive dietary protein were used in diets, coast of the Caspian Sea, Sari, Iran. In this center, only a part of this protein would be used to synthesize kutum were kept in earthen ponds and fed on new proteins for growth and repair, whereas the rest natural live food and commercial food. Before would be converted to meet the energy requirements starting the experiment, the fi sh were acclimated of the fi sh (Willson, 2002; Salhi et al., 2004). Th e to the experimental conditions for 2 weeks. During optimum use of protein for the promotion of growth acclimation, the fi sh were fed commercial carp feed is essential so as to make aquaculture commercially (30% protein) twice daily. Aft er acclimation, kutum viable and also to prevent organic loading in the fi ngerlings with an initial body weight of 0.5 ± 0.09 ecosystem, which ultimately leads to water pollution g were randomly distributed into 15 fi berglass tanks through a decrease in ammonia nitrogen excretion of 250 L capacity with 80 fi sh per tank. Each dietary (Kaushik and Oliva-Teles, 1985). treatment had 3 replicates. All of the tanks were Although several studies have been conducted covered with nets throughout the experiment, to to determine the nutritional requirements of kutum prevent the fi sh from jumping out. Freshwater was (Fallahi et al., 2004; Noverian et al., 2008; Noverian and supplied at a fl ow rate of 1.5 L/min to each tank. Shabanipour, 2008), there is no accurate information Water quality parameters were checked periodically; specifi cally on their protein requirements. Th erefore, pH ranged between 7.8 and 8.0; water temperature the present study was designed to estimate the ranged from 19.7 to 23.2 °C, and dissolved oxygen optimum dietary protein level and determine its was never less than 7.2 mg/L. Fish were held under eff ect on growth performance, feed utilization, and natural photoperiod conditions throughout the body composition of R. frisii kutum fi ngerlings. feeding trial.

552 G. EBRAHIMI, H. OURAJI

Table 1. Formulation and proximate composition (wet weight) of the experimental diets.

Dietary protein level (%) Ingredient (%) 32 37 42 47 52 Fish meala 38 46 54 63 71 Wheat fl our 37.8 34 30 20 15 Fish oilb 4.7 4.1 3.4 2.7 2 Soybean oil 3.8 3.8 3.85 3.9 3.9 Mineral mixturec 2 2 2 2 2 Vitamin mixtured 2 2 2 2 2 Cellulosee 11.7 8.1 4.75 6.4 4.1

Proximate composition (%) Moisture 10.24 10.48 9.68 8.9 8.16 Crude protein (Calculated) 32 37 42 47 52 Crude protein (Analyzed) 33.3 36.23 41.40 46.88 51.96 Lipid 11.66 12.33 11.93 13.16 12.69 Ash 8.07 8.78 9.48 10.56 12.85 NFEf 36.72 32.17 27.49 20.5 14.33 Gross energy (MJ/kg)g 18.68 18.84 19.09 19.65 19.60 P/E ratioh 17.82 19.22 21.68 23.85 26.50 aPars kelika Co., Mirood, Iran bHerring oil c -1 Vitamin premix contained the following vitamins (each kg diet): vitamin A, 10,000 IU; vitamin D3 2000 IU; vitamin E,

100 mg; vitamin K, 20 mg; vitamin B1, 400 mg; vitamin B2, 40 mg; vitamin B6 20 mg; vitamin B12, 0.04 mg; biotin, 0.2 mg; choline chloride, 1200 mg; folic acid, 10 mg; inositol, 200 mg; niacin, 200 mg; and pantothenic calcium, 100 mg. d -1 Contained (g kg mix): MgS04.2H2O, 127.5; KCl, 50.0; NaCl, 60.0; CaHPO4.2H2O, 727.8; FeSO4.7H2O, 25.0; ZnSO4.7H2O,

5.5; CuSO.5H2O, 0.785; MnSO4.4H2O, 2.54; CoSO4.4H2O, 0.478; Ca(IO3)2.6H2O, 0.295; and CrCl3.6H2O, 0.128. eSigma, St. Louis, MO, USA. fNitrogen-free extract (NFE ) = 1000 – (protein + lipid + moisture + ash). gBased on 23.4 kJ/g protein, 39.2 kJ/g lipid, and 17.2 kJ/g NFE. hProtein/energy ratio (g/MJ).

Fish were hand-fed the experimental diets Sample collections and chemical analysis until apparent satiation 3 times daily (7 days a At the start of the experiment, 30 fi sh from the original week) at 0700, 1200, and 1700 h, for 8 weeks. Feed population were fasted for 24 h, euthanized, and consumption was recorded for each tank, based on stored at –20 °C for initial whole-body composition the amount of feed that was taken by the fi sh. At the analysis. At the end of the experiment, 10 fi sh from end of the experimental period, the fi sh were fasted each tank were randomly sampled and euthanized for 24 h and the pooled weights of the replicates were by overdose of ethylene glycol monophenyl ether, recorded. and kept frozen (–20 °C) for determination of their

553 Growth performance and body composition of kutum fi ngerlings, Rutilus frisii kutum (Kamenskii 1901), in response to dietary protein levels fi nal whole-body composition. Th e analysis of signifi cant diff erences among treatments were diets and fi sh samples for crude protein, crude fat, found (P < 0.05), the means were compared using moisture, and ash followed the standards outlined Duncan’s multiple range test. Polynomial regression by the Association of Offi cial Analytical Chemists analysis was used to analyze the relationship between (AOAC, 1995). Crude protein content (N × 6.25) was percentage weight gain and dietary protein level determined using the Kjeldahl method, aft er acid (Kim and Lee, 2005). digestion, using an Auto Kjeldahl System (1030-Auto- analyzer, Tecator, Hoganos, Sweden). Crude lipid Results was determined by ether-extraction using a Soxtec extraction System HT (Soxtec System HT6, Tecator, Survival rate during the experimental period was Sweden). Ash was determined by muffl e furnace at 95% and above for all of the treatments. Analysis of 550 °C for 24 h. Moisture content was measured by fi sh growth performance (Table 2) indicated that fi sh drying the tissues in an oven at 105 °C for 24 h and fed a diet containing 42% protein had the highest measuring the weight loss. weight gain and specifi c growth rate, and the lowest feed conversion ratio. According to the results, Performance parameters growth of kutum increased signifi cantly (P < 0.05) Th e performance parameters including percentage with increasing dietary protein level from 32% to weight gain (WG%), specifi c growth rate (SGR), 42%, but there was a signifi cant decrease (P < 0.05) feed conversion ratio (FCR), protein effi ciency ratio in growth with increasing the dietary protein level (PER), feed effi ciency ratio (FER), feed intake (FI), from 42% to 52% (Table 2). Th e relationship between protein intake (PI), and survival percentage were weight gain and dietary protein was best expressed calculated as follows: using polynomial regression analysis (y = 0.5467 x2 + 2 WG (%) = (fi nal weight – initial weight)/initial 45.533 x – 680.08; R = 0.8088); to ensure maximum weight × 100 weight gain of fi ngerlings, the optimal dietary protein level was determined to be 41.9% (Figure). SGR (% day-1) = 100 × (ln fi nal weight – ln initial weight)/time (days)

FCR = total feed intake (g)/weight gain (g) 300 Y = -0.5467x 2 + 45.533x - 680.8 PER = weight gain (g)/total protein intake (g) R² = 0.8085 275 FER = weight gain (g)/total feed intake (g) 250 FI = total feed intake/number of fi sh Survival (%) = (fi nal number of fi sh/initial 225 number of fi sh) × 100 200 Weight gain (%) Statistical analysis 175 X = 41.9% All statistical analyses were performed using the statistical package SPSS 14.0. In this experiment, 150 27 32 37 42 47 52 each treatment (5 levels) was represented by 3 tanks Dietary protein (%) (3 replicates). From each tank, 10 fi sh, representing Figure. Relationship between percent weight gain and dietary 15% of the total number of fi sh per tank (30 fi sh per protein levels for kutum fi ngerlings as described by treatment), were randomly sampled. Descriptive second-polynomial regression. Th e vertical line in the statistics (means and standard deviations) of analysis middle of the graph represented the optimal protein level for kutum. results were calculated for each treatment. Th e homogeneity of variances of means was tested by Levene’s test. When data were normally distributed, FCR was signifi cantly aff ected (P < 0.05) by the one-way analysis of variance (ANOVA) was calculated dietary protein level. Increasing the dietary protein with percentage protein in the diet as a factor. When level from 32% to 42% decreased FCR, but, further, an

554 G. EBRAHIMI, H. OURAJI a a a a a 95.8 ± 1.9 97.5 ± 1.2 96.2 ± 1.25 95.00 ± 1.2 Survival (%) 97.08 ± 0.72 c c a b ab 6 FER 0.42 ± 0.02 0.42 ± 0.01 0.54 ± 0.02 0.49 ± 0.02 0.51 ± 0.01 c a a b a 5 PER 0.82 ± 0.02 1.33 ± 0.06 1.38 ± 0.01 1.04 ± 0.06 1.28 ± 0.07 a a a a a 4 erent protein levels. protein erent FI 2.56 ± 0.02 2.45 ± 0.12 2.55 ± 0.01 2.51 ± 0.02 2.47 ± 0.04 c c a b b 3 erent from each other (P < 0.05). each other from erent SGR 2.22 ± 0.07 2.18 ± 0.05 2.54 ± 0.07 2.40 ± 0.05 2.39 ± 0.08 cantly diff cantly c a a b bc 2 ngerlings fed diets containing diff diets containing fed ngerlings 1.85 ± 0.10 2.34 ± 0.10 2.34 ± 0.07 2.03 ± 0.11 1.97 ± 0.02 a c b b c 210.9 ± 8.3 218.5 ± 11.7 250.0 ± 10.2 247.9 ± 15.0 276.00 ± 14.4 a c c b b erent letters in the same column are signifi are column in the same letters erent Table 2. Growth and feed utilization of kutum fi kutum of utilization feed and 2. Growth Table Initial weight (g) weight Initial (g) Final weight (%) gain Weight FCR ciency ratio. ciency ciency ratio. ciency rate. c growth Dietary level protein (%) 32 0.50 ± 0.11 1.59 ± 0.05 3742 0.50 ± 0.0747 1.75 ± 0.05 0.49 ± 0.0952 1.88 ± 0.0.07 0.50 ± 0.11P value 1.74 ± 0.07 0.49 ± 0.07F value 1.55 ± 0.04 0.000 24.17 0.000 26.12 0.000 0.000 15.05 0.694 28.14 0.002 0.565 8.11 0.001 0.454 12.33 0.362 Values (expressed as mean ± SD, n = 3) with diff n = 3) with ± SD, as mean (expressed Values ratio. conversion Feed Specifi (g). intake Feed effi Protein effi Feed 1 2 3 4 5 6

555 Growth performance and body composition of kutum fi ngerlings, Rutilus frisii kutum (Kamenskii 1901), in response to dietary protein levels increase in dietary protein level to 52% signifi cantly R-squared value of the second-order polynomial increased FCR. regression analysis was higher than the R-squared FI ranged from 2.45 ± 0.02 to 2.56 ± 0.02 g/fi sh value of the broken-line model. Th e optimal dietary (Table 2) and diff erent levels of dietary protein had protein level, estimated by polynomial regression no signifi cant eff ect (P > 0.05) on feed intake. PER analysis, for maximum growth of kutum fi ngerling was signifi cantly infl uenced (P < 0.05) by the dietary was 41.9%, based on wet weight. Noverian et protein level. Th e lowest PER value was observed in al. (2005) studied the eff ects of diff erent dietary diets containing 52% protein. PER did not show any protein levels (25%, 30%, and 35%) on the growth signifi cant diff erence (P < 0.05) among fi sh fed diets performance in advanced kutum fry and found containing 32%, 37%, or 42% protein. an optimal diet of 35% protein. Th is variation in reported protein requirements may have been caused Whole-body composition of the fi ngerlings was by diff erences in fi sh size, water temperature, dietary determined at the start and end of the experiment energy level, and protein quality (Webster and Lim, (Table 3). Th e moisture content of R. frisii kutum was 2002). Th e weight gain of kutum increased with not signifi cantly diff erent among the experimental increasing the dietary protein level from 32% to 42%, diets (P > 0.05). No signifi cant diff erences were found and decreased signifi cantly (P < 0.05) thereaft er, with in the whole-body lipid, protein, and ash contents of further increases in dietary protein (Table 2). Similar fi sh fed the diff erent dietary protein levels. results have been reported in other species (Santiago Initial moisture content was signifi cantly higher and Reyes, 1991; Yang et al., 2002; Mohanta et al., (P < 0.05) than the fi nal moisture content in all of 2008). Th is is because in a high protein diet, part of the experimental groups. Although overall variation the dietary protein is metabolized and converted to in the whole-body protein content of the fi sh was low, energy rather than used for growth (Mohanta et al., fi sh fed the 47% protein diets had the highest body 2008). Dietary protein requirements of fi sh are closely protein content (15.45 ± 0.20% live weight). related to dietary energy levels. If the energy level of a diet is low, dietary protein will be used to generate energy (Salhi et al., 2004). In general, an appropriate Discussion P/E ratio in the diet is important for optimum According to Kim and Lee (2005), the broken line growth of fi sh (Tucker, 1992). Th e P/E ratios for model and second-order polynomial analysis are the optimum growth of several fi sh species ranged from methods most oft en used to estimate dietary protein 19 to 27 g/MJ (NRC, 1993). In the present study, requirements of fi sh species. Th e second-order maximum growth of kutum was obtained from the polynomial regression analysis appeared to be more diet containing 42% protein and 19.1 MJ/kg energy, appropriate in the present study because the weight corresponding to a P/E ratio of approximately 21.7 gain (%) response was curvilinear. Furthermore, the g/MJ.

Table 3. Whole-body proximate compositions (% live weight basis) of kutum fi ngerlings before and aft er feeding trial.

Final Composition Initial CP32 CP37 CP42 CP47 CP52 P value F value Moisture 76.2 ± 1.0 72.3 ± 1.3 72.2 ± 0.8 72.1 ± 0.7 72.0 ± 1.4 71.9 ± 0.7 0.991 0.066 Crude protein 12.3 ± 0.5 14.7 ± 0.6 15.2 ± 0.3 15.3 ± 0.5 15.4 ± 0.3 15.3 ± 0. 2 0.343 1.274 Crude lipid 8.4 ± 0.1 11.5 ± 0.4 11.7 ± 0.3 12.0 ± 0.4 11.7 ± 0.3 11.8 ± 0.8 0.860 0.317 Ash 2.8 ± 0.10 2.56 ± 0.06 2.45 ± 0.29 2.50 ± 0.16 2.40 ± 0.30 2.35 ± 0.21 0.804 0.401

Values are the mean ± SD of triplicate groups. Values within the same row have no signifi cant diff erences (P > 0.05).

556 G. EBRAHIMI, H. OURAJI

In the present study, the FCR of the experimental lipid content of kutum increased with up to 42% diets varied from 1.80 to 2.33. Th is result is higher protein and decreased with higher protein diets. than that reported for kutum (2-10 g) by Noverian et However, carcass lipid levels for all of the treatments al. (2005). Th e FCR means in their experiment varied were not statistically diff erent (P > 0.05). Our results between 1.45 to 1.65. Th is variation may be due to on moisture and protein contents were consistent diff erences in initial weight, water temperature, lipid with studies of juvenile bass, Centropristis type and level, dietary protein, and energy content. striata, and tiger puff er, Takifugu rubripes (Alam et Th e lowest dietary protein level (32%) produced the al., 2008; Kim and Lee, 2009). Th ere was a tendency highest FCR, probably due to the intake of insuffi cient for whole-body moisture to decrease with increasing nutrient levels to promote growth. Th e best FCR was dietary protein fed to R. frisii kutum. Diff erent results observed in fi sh fed the diet containing 42% protein. in other fi sh species like silver barb, big head carp, Th is result indicates that a diet containing 42% and Florida pompano (Trachinotus carolinus), were protein is optimal for kutum fi ngerlings. observed by Wee and Ngamsnae (1987), Santiago All experimental diets were well accepted by and Reyes (1991), and Lazo et al. (1998), respectively. kutum and the total feed intake was not aff ected by Th e chemical composition of fi sh is diff erent among dietary protein level. Since the experimental diets various species. In addition, Shearer (1994) pointed used in the present study were isoenergetic, this out that the proximate composition of fi sh is infl uenced suggests that kutum fi ngerlings controlled their feed by both endogenous factors such as fi sh size and sex, intake in order to meet their energy requirements. It as well as exogenous factors such as diet composition is generally known that fi sh eat to satisfy their energy and the culture environment. For example, when the needs (Webster and Lim, 2002). weight of a fi sh increases, the amounts of nutrients (protein, lipid, and carbohydrate) in the fi sh body In the present study, kutum fed the highest will increase (Sutton et al., 2000). protein diets (47% and 52% protein) used dietary protein less effi ciently, as refl ected by the lower PER values recorded, than fi sh fed the low protein diets. Conclusion In general, the protein effi ciency ratio in carnivorous Based on the results of this study, the maximum fi shes decreases with high protein intake, as reported, growth of Rutilus frisii kutum fi ngerlings was for example, by Yang et al. (2003) and Salhi et al. observed when fed the diet containing 42% protein (2004). Th is decrease is probably because dietary (based on wet weight) with P/E ratio of approximately protein is used as an energy source when high protein 21.7 g/MJ. From the polynomial regression diets are fed to fi sh (Jobling and Wandsvik, 1983; Yang analysis, the optimal dietary protein requirement of et al., 2003). Mohanta et al. (2008) demonstrated that kutum was estimated to be 41.6%. We suggest that in silver barb fi ngerlings Puntius gonionotus, PER diets containing 41.6% crude protein and a P/E ratio decreased signifi cantly (P < 0.05) with an increased 21.7 g/MJ can be more benefi cial for kutum fi ngerling dietary protein level, which is what this study found rearing. However, more detailed studies on the amino in kutum as well. Th e ineffi cient conversion of acid requirements of this species are required so as to protein to growth refl ects the continued catabolism formulate appropriate diets for this species. of protein for energy in the absence of any protein sparing eff ect at high protein levels. Protein sparing is the process by which the body derives energy from Acknowledgements sources other than protein. In diets with high levels Th e authors gratefully acknowledge the technical of protein, part of protein will be used to meet the assistance provided by Masoud Asghari and Majid energy requirement of the fi sh (Willson, 2002; Salhi Shaygan during this study. We wish to thank Dr. Azim et al., 2004). Mohseni, Maths Dept., Gorgan University, for his Dietary protein levels did not signifi cantly valuable assistance with the statistical modeling. We infl uence the fi nal whole-body content of the R. would like to express our thanks to Mr. M. Zarei, Mr. frisii kutum fi ngerlings (Table 3). Whole body H. Barari, and other staff at Shahid Rajaee Hatchery moisture and crude protein were not correlated to Sari, Mazandran, Iran. We thank Mr. Khalili and Mr. the dietary protein level. On the other hand, the Kamali for their help in the diet preparation.

557 Growth performance and body composition of kutum fi ngerlings, Rutilus frisii kutum (Kamenskii 1901), in response to dietary protein levels

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