Chinese Journal of Oceanology and Limnology   2016, 34 (4): 740-748     PDF       
http://dx.doi.org/10.1007/s00343-016-5350-4
Institute of Oceanology, Chinese Academy of Sciences
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Article Information

Benli WU(吴本丽), Xiaoqin XIONG(熊小琴), Shouqi XIE(解绶启), Jianwei WANG(王剑伟)
Dietary lipid and gross energy affect protein utilization in the rare minnow Gobiocypris rarus
Journal of Oceanology and Limnology, 34(4): 740-748
http://dx.doi.org/10.1007/s00343-016-5350-4

Article History

Received: Dec. 11, 2014
Accepted: May. 8, 2015
Dietary lipid and gross energy affect protein utilization in the rare minnow Gobiocypris rarus
Benli WU(吴本丽)1,2, Xiaoqin XIONG(熊小琴)1,2, Shouqi XIE(解绶启)3, Jianwei WANG(王剑伟)1        
1. Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institution of Hydrobiology, Chinese Academy of Science s, Wuhan 430072, China;
2. University of Chinese Academy of Sciences, Beijing 100049, China;
3. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
ABSTRACT: An 8-week feeding trial was conducted to detect the optimal dietary protein and energy, as well as the effects of protein to energy ratio on growth, for the rare minnow (Gobiocypris rarus), which are critical to nutrition standardization for model fish. Twenty-four diets were formulated to contain three gross energy (10, 12.5, 15 kJ/g), four protein (20%, 25%, 30%, 35%), and two lipid levels (3%, 6%). The results showed that optimal dietary E/P was 41.7-50 kJ/g for maximum growth in juvenile rare minnows at 6% dietary crude lipid. At 3% dietary lipid, specific growth rate (SGR) increased markedly when E/P decreased from 62.5 kJ/g to 35.7 kJ/g and gross energy was 12.5 kJ/g, and from 75 kJ/g to 42.9 kJ/g when gross energy was 15.0 kJ/g. The optimal gross energy was estimated at 12.5 kJ/g and excess energy decreased food intake and growth. Dietary lipid exhibited an apparent protein-sparing effect. Optimal protein decreased from 35% to 25%-30% with an increase in dietary lipid from 3% to 6% without adversely effecting growth. Dietary lipid level affects the optimal dietary E/P ratio. In conclusion, recommended dietary protein and energy for rare minnow are 20%-35% and 10-12.5 kJ/g, respectively.
Key words: rare minnow     Gobiocypris rarus     protein to energy ratio (E/P)     crude lipid     growth    
1 INTRODUCTION

Dietary protein contentis a key nutritional factor affectingthe growth performance of fish (Jauncey, 1982; Al Hafedh et al., 1999) . However, any consideration of nutritional requirements in fish must take into account the balanceof a range of nutrients, which can interact with significant outcomes (Smith, 1989; De Silva et al., 1991) .Therefore, in additionto protein, it is also importantto determine the dietary content of carbohydrates and lipids, which are used as non-protein energy sources. Imbalance in dietary nutrients may decrease growth, nutrientutilization, and body lipiddeposition ( Garling Jr and Wilson, 1976) . Both under- and over-nutrition could have adverse effects on fish growth and physiology (Kaushik, 1995) . The optimum dietary proteincontent for good performance depends on the energy content of food (Cowey, 1979; Salhi et al., 2004) . An optimal dietary protein to energy ratio (E/P) is important because any excess or deficiencyof non-protein energy results in lower proteinand energy utilization and may also depress fish growth performance (Shiau and Peng, 1993; Lupatsch et al., 1998; Ali and Jauncey, 2005; Tibbetts et al., 2005) . The E/P ratio has been studiedfor several speciessuch as channel catfish (Garling and Wilson, 1976) , Nile tilapia (El-Sayed and Teshima, 1992) , Asian seabass (Catacutan and Coloso, 1995) , and grouper (Shiau and Lan, 1996) . Dietary lipidis a good energy source for fish and exhibits a protein-sparing effect (Reinitz et al., 1978; Kim and Lee, 2005) .

The rare minnow (Gobiocypris rarus) is a small cyprinid fish endemic to Sichuan Province, China. It has been cultured for use as a potentialmodel fish under laboratory conditions since 1990 (Cao and Wang, 2003) . However, little research relating to its nutrition has been conducted to date. Previous experiments have shown that at the specific energy level of 17.0 kJ/g, the optimal protein and lipid requirements are 32.6% and 7.07%, respectively (Wu et al., unpublished data) . An energy level of 17.0 kJ/g in that trial was probably and overestimation because of relatively low feed consumption. Lower consumption of high-energy food may lead to a reduction in growth resultingfrom a deficiency of necessary nutrients (Lovell, 1979;Daniels and Robinson, 1986) . The present study was conducted to detectthe optimal proteinand energy levels, as well as the effects of E/P on growth for rare minnows, to provide a nutritionstandard for the small model fish.

2 MATERIAL AND METHOD 2.1 Fish rearing

All rare minnows were from a closed colony (IHB, Institute of Hydrobiology, CAS) and kept in a 1 000-L quadrate resinous tank before grouping.The larvae were fed with Artemia nauplii, which were gradually replaced by red worms (Chironomus larva) for 45 days. Healthy individuals of similar size were allocated to several polycarbonate tanks (40 cm×20 cm×25 cm) . Water was recycled at 0.6-1.0 L/min for each tank, and 1/3 of the tank’s volume was replaced with freshwater daily. Thirty-five individuals were stocked per tank, which were coveredby nets to prevent the fish from jumping out. The fish were acclimated with mixed experimental diets at least 7 days before being moved to small test tanks. The fish were fed with designed feeds for 15 min to apparentsatiation at 10:00 and 16:00 d aily. Three tanks were used for each diet and the amount fed was recordeddaily. Uneaten food was siphonedand dried to calculate food consumption. During the 8-week feeding trial, light period was artificially controlled at 14 h from 08:00 to 22:00 (80-100 lx) . The water temperature, pH, and dissolved oxygen were monitoreddaily. The temperature was 25.0−26.0℃, pH was 7.8−8.5, and dissolved oxygen was 7.5−8.5mg/L (HQ30d, Hach, Loveland, Co., USA) . The NH4-N, NO2-N, and hardness were determined weekly (APHA, 1992) .

2.2 Diet preparation

For nutrient sources, casein and gelatinwere used for protein (4:1) , fish and soybeanoils for lipids (1:1) , and dextrin for carbohydrates. All raw materialswere crushed, passed througha sieve (60 mesh, 250 μm) and manuallymixed. Water (30%) was added to the homogeneous compoundsand the mix was placed into a household noodle maker (LM-20, Limai, China) with a perforated metal plate (0.5 mm) to produce pellets that could be consumedby small fish. All diets were stored at -4℃ beforeuse. Twenty-four diets were designedbased on preliminary experiments, which determined the suitable rangesof protein and energy. Crude lipid (CL) was fixed at 3% and 6%, crudeprotein (CP) was 20%-35%, and the gross energy (GE) levels were regulated by carbohydrates at 10.0 kJ/g, 12.5 kJ/g, and 15.0 kJ/g (Table 1) .

Table 1 Formulation and proximate chemical composition of experimental diets
2.3 Sampling and chemicalanalysis

The fish were anesthetized by MS-222 (100×10-6) and measuredafter 24 h of fasting for each tank. The initial and final fish body weight and length were measured individually. Six individuals from each tank were dissectedto obtain the hepatosomatic index (HSI) , visceral-somatic index (VSI) , and length of intestinal tract to body length index (DSI) . Twenty individuals were collected after measuring for final body composition analysis (AOAC, 2005) .Dry matter and ash in diets and fish carcasseswere determinedgravimetrically after drying for 10 h at 105℃ in an oven and after combustion for 24 h at 550℃ in a muffle furnace.Crude protein (N×6.25) was determined according to the Kjeldahlmethod (Kjeltec Auto Analyzer2300, Foss, Eden Prairie, MN, USA) .Crude lipid was determined gravimetrically in the samplesfollowing ether extraction (Soxtec system HT 1043, Tecator, Extraction Unit, Hoganas, Sweden) .The energy value was acquiredby a Phillipson microbomb calorimeter (Gentry Instruments Inc., Aiken, SC, USA) .

2.4 Statisticalanalysis

All statistical analysis was carried out in SPSS Version 19.0 (SPSS, Chicago, IL, USA) . The measured data were subjectedto one, two, and three-way analysis of variance (ANOVA) . Significant differences among treatments were tested using Tukey’s multiplerange tests and results of P<0.05 were deemed statistically significant. Duncan’s multiple comparison was carried out to determinethe differencesamong groups.

3 RESULT 3.1 Growth performance

There was no mortality during the trial in all treatments. Final body weightswere significantly different in fish fed with diets varyingin crude protein (CP) , crude lipid (CL) , and gross energy (GE; P<0.01; Tables 2 and 3) . When fed diets with 6% lipid, fish showed relatively better growth at D (20, 6, 10) , D (25, 6, 12.5) , and D (30, 6, 12.5) and the corresponding E/P was 50 kJ/g, 50 kJ/g, and 41.7 kJ/g. Minimumbody weight gain occurredat D (35, 6, and 10) , at which the E/P was 28.6 kJ/g. When lipid was reduced to 3%, fish fed on D (35, 3, 12.5) achieved a final body weight of 0.348 g and an SGR of 2.95%/d, with an E/P of 35.7 kJ/g; whereas fish fed on D (20, 3, 15) exhibited minimum growth with an E/P of 75 kJ/g. Generally, feed with a gross energy of 12.5 kJ/g wassuffcient for rearing rare minnowsand surplus dietary energy could improve growth and decreasefood intake. Crude proteinlevels of 20%-35% in diets could meet the requirement for juvenilegrowth in rare minnows when the energy or lipid levelsare appropriate. CF, VSI, HSI, and DSI were higher in higher body weight groups. FCR fluctuated among groups and was higher in 3% lipid diets comparedwith 6% lipid diets at identical protein and energy levels.Additionally, some individuals, especiallythose fed with D (30, 6, 12.5) , reached sexual maturity during the experimental period and both male and femalegonads were well-developed.

Table 2 Growth performance of fish fed with varying crude protein (CP) , gross energy (GE) , and crude lipid (mean±S.E.)
Table 3 Three-way analysisof variance results for growth performanceof rare minnows fed with varyingcrude protein (CP) , gross energy (GE) , and crude lipid (CL) (mean±S.E.)

Growth rates were divergent in diff erent periods of the trial. Out of the groups fed 6% lipid diets, the maximum body weight was obtained in fish fed D (20,6, 10) and SGR decreased rapidlywith increasing protein at a low gross energy of 10 kJ/g in the first 4 weeks. There was no significant difference in SGRs when the energy was 15.0 kJ/g (P<0.05; Fig. 1a) . However, in the latter 4 weeks of the trial, groups fed D (25, 6, 12.5) and D (30, 6, 12.5) diets grew faster than others (Fig. 1b) . There were some differences when crude lipid was 3%. In the first 4 weeks, SGR increased with increasing proteinwhen gross energy was either 12.5 kJ/g or 15.0 kJ/g, but decreased moderately with increasing proteinat the low energy levelof 10 kJ/g (Fig. 2a) . For the latter 4 weeks, the D (35, 3, 12.5) diet was obviously good for growth (Fig. 2b) .

Figure 1 Specific growth rates (SGR 1-28 d=100 (ln28 d BW-lnIBW) /28; SGR 29-56 d=100 (lnFBW-ln28 d BW) /28) of fish during the first (a) and second (b) 4 weeks of the trial when fed diets with 6% crude lipid and varying protein and gross energy
Figure 2 Specific growth rates (SGRs) of fish during the first (a) and second (b) 4 weeksof the trial when fed diets with 3% crude lipid and varyingprotein and gross energy
3.2 Suitable E/P

Figure 3 showsthat, at 6% dietary lipid, SGR reached its maximumand then decreasedwith increased dietary proteinat 12.5 kJ/g and 15 kJ/g gross energy, but decreased with increased dietary protein at 10 kJ/g gross energy. The groupsfed diets with 12.5 kJ/g gross energy grew relativelywell compared with those on lower (10.0 kJ/g) or higher (15.0 kJ/g) gross energy. The optimal content of crude protein was 27.0% based on the regression relationship. When gross energy was 10 kJ/g, SGR decreased with a decreasein E/P from 50.0 kJ/g to 28.6 kJ/g, and relativeoptimal crude proteinwas 20%. There was no significant difference in SGR for different protein contents (20%−35%) or E/P (75−42.9 kJ/g) when gross energy increased to 15 kJ/g, but the relative optimal concentration of crude proteinwas 30%, especially in the latter period of the trial. According to the SGR in variousgroups, we speculated that the optimalE/P for juvenile rare minnows was 41.7−50 kJ/g when energy was 10−15 kJ/g and crude lipid 6%. The levelof protein should increasewhen gross energy increases, but by no more than 30% for this particular species.

Figure 3 Specific growth rates (SGR 1-56 d=100 (lnFBW-lnIBW) /56) during the entire feeding trial in fish fed diets with 6% crude lipid and varying protein and gross energy

There were some differences when crude lipid was 3%. As Fig. 4 shows, SGR increased with increased dietary proteinat 12.5 kJ/g and 15 kJ/g gross energy, but the SGR did not increase with increased dietary protein at 10 kJ/g gross energy. There was no significant difference in SGR at a low gross energy of 10 kJ/g. Maximum SGR also occurred at 12.5 kJ/g, but the proteinrequirement increased even more to 35%. SGR increased markedlywith the decrease in E/P from 62.5 kJ/g to 35.7 kJ/g at a gross energy of 12.5 kJ/g; and from 75 kJ/g to 42.9 kJ/g at a gross energy of 15.0 kJ/g.

Figure 4 Specific growth rates (SGRs) during the entire feeding trial in fish fed diets with 3% crude lipid and varying protein and gross energy
4 DISCUSSION 4.1 Suitable E/P for growth

The effect of E/P on rare minnowgrowth was obvious, as the growthrate decreased with increased dietary proteinat low gross energy of 10 kJ/g. Fish tend to consume more food at low grossenergy. This response brings about an increased proteinintake, which would lead to intensivespecific dynamic action (SDA) becauseof complex catabolicand synthesis activities. That increased dietary protein leads to increases in SDA has been reportedin many fish species (Medland and Beamish, 1985; Peres and Oliva-Teles, 1999; Fu et al., 2005) .Other studies have shown that dietary proteinaffects SDA more than lipids and carbohydrates (Jobling and Davies, 1980; Tandler and Beamish, 1981; Zanotto et al., 1997) . Some researchhas indicated a positive relationship between SD A and growth, showing that intensive SDA stimulates fast growth (Jobling, 1983; Brown and Cameron, 1991; Chakraborty et al., 1995; Carter and Hauler, 2000) . In the present study, growth decreased with increased dietaryprotein. This result supports the idea that there is a competitive relationship between SDA and growth, which has been reportedin metabolic studiesfor species like catfish and rainbow trout (Legrow and Beamish, 1986; Cui and Liu, 1990; Ai and Xie, 2006) .However, increased dietaryprotein did not seem to affect SGR at the high gross energy of 15.0 kJ/g. E/P plays an important role in improving the utilization of both protein and energy as well as enhancingfeed effciency (Winfree and Stickney, 1981; Lee et al., 2002; Mathis et al., 2003; Wang et al., 2006) . Excess protein may be used for energy ratherthan for growth, whereas the dietary lipid or carbohydrate did not provide energy. Excessive energy could restrict food intake, which would subsequently reduce protein consumption if dietary proteinwas low (NRC, 1993) . Long-term dietaryconsumption of foods high in calories, protein, and fat could lead to decreases in growth hormones (Yang et al., 1987) . In this study, excessive energy also brought about lipid deposition, especially in viscera. Fish usually respondto being fed low-energy dietsby increasing feed consumption, apparently to maintain nutrientand energy intake (Boujard and Médale, 1994) .For rare minnows, suitable E/Ps are 41.7−50 kJ/g at 6% lipid and 35.7 kJ/g at 3% lipid. In the presentstudy a diet of 20%−35% proteinand 10−12.5 kJ/g achieved a reasonable E/P for juvenilerare minnows.

4.2 Effect of lipid on E/P

Growth increased when dietary protein increased from 20% to 35% at 3% lipid and a highergross energy of 12.5 kJ/g and 15 kJ/g, but was restricted at a low grossenergy of 10 kJ/g (Fig. 2) . Optimaldietary protein was 27% at 6% lipid, and a low-lipiddiet of 3% couldpotentially be used in daily feeding if paired with high protein levelsof 35% or more. Both protein and grossenergy levels were lowerthan other carnivorous fishes such as groupers, which suggested that when the energy and protein requirements were 14.3−15.8 kJ/g and 44%−50%, respectively, the optimal E/P was 32.5−35.8kJ/g (Shiau and Lan, 1996) . For black carp, the optimal proteinlevel is 35%−40%, energy is 13.4−15.3 kJ/g, and E/P is 38.0 kJ/g (Dai et al., 1988) . Optimal E/P fluctuated with variations in nutritionlevels. In the present study, increasing lipidalso increased optimalE/P, which suggests that increasing lipids from 3% to 6% could significantly decreasethe requirement of dietary protein without adverse effects on growth for rare minnows. Dietarylipids can provideenergy while decreasing dietary proteinrequirements (Reinitz et al., 1978;Shiau and Huang, 1990) . A protein-sparing effect has been reported in several fish species, and so an appropriate increase of either lipids or carbohydrates would improve the effciencyof protein utilization (Wilson, 1989; Cho and Kaushik, 1990; Lee et al., 2002; Kim and Lee, 2005) . Certainly, nutrition content shouldmeet the requirement for amino and fattyacids. The excessiveincrease of lipids did not enhance growth, and even causedadverse effects, especially in the latterhalf of the trial period. Overabundance of lipids food perishability and adversely affects fish (Company, 1999) . The fish were fed to apparent satiationin this study, which implies that fish had eaten to satisfy their energy requirements (Lee and Putnam, 1973; Lee et al., 2002) . Rare minnows could also adjust food intake to satisfy nutritional requirements. The fish grew well on D (20, 6.10) , and tended to eat more when diets were low in protein and energy. Lower protein in diets leads to higher proteinutilization effciency (Samantaray and Mohanty, 1997) . Optimalenergy was estimated to be 12.5 kJ/g in the present study and high energy had negative effects on growth for G. rarus, not only because of nutrient imbalance but also becauseof the reduction in appetite and lower nutrientintake (Page and Andrews, 1973; Bromley, 1980; Raven et al., 2006) .

In conclusion, this study reveals the effect of E/P on growth.Diets with 10−12.5kJ/g gross energy and 20%−35% protein could representoptimal E/P for maximum growth; however, optimal E/P is affected by dietarylipid. There is an apparentprotein-sparing effect by increasing lipid in diets with suitableenergy levels, and the utilization of protein is more effcient in diets with 6% lipidthan those with 3% lipid. Dietary gross energy and lipid content could affect the use of protein in rare minnows. The requirements for dietary protein, lipid, and gross energy were also affected by environmental factors such as temperature, dissolved oxygen, and feeding regime.The nutrition standardization for this model fish demands artificial diets with balanced nutrients and suitable feeding strategies.

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