Aquaculture nutrition, tập 19, số 3, 2013

Aquaculture Nutrition 2013 19; 233–249 doi: 10.1111/anu.12042 1,2 Nutrition, Metabolism and Aquaculture (NuMeA), UR 1067, Pole d’Hydrobiologie INRA, Saint-Pee-sur-Nivelle, France; Aquaculture and Fisheries Group, Wageningen Institute of Animal Sciences (WIAS), Wageningen University, Wageningen, The Netherlands A meta-analysis of available data on dose response to dietary phosphorus (P) in fish from over 70 feeding trials reported in 64 published studies covering over 40 species of fish was performed Broken-line regression was used to model the data sets The meta-analysis showed that estimated minimal dietary P level varies with the response criterion and that estimates should preferably be expressed in terms of available P than in terms of total P Estimates based on whole-body P concentration (4.7 g available P kgÀ1 dry matter, DM) or vertebral P (5.2 g available P kgÀ1 DM) were greater than that for maximizing somatic weight gain (WG) (3.5 g available P kgÀ1 DM) or plasma P concentration (2.8 g available P kgÀ1 DM) P content of fish varies linearly with body mass (3.6 g kgÀ1 live weight) Use of ingredients rich in P or of diets with high basal P content or high levels of water P concentration can affect the estimations Among the different response criteria tested, WG was found to be the most reliable and wholebody P concentration to be the most stringent criterion to estimate P requirement of a given fish species Expressing available P requirement as g P per unit DM or digestible energy (DE) in the diet was equally effective, but expressing in terms of g P intake per kg BW0.8 per day would be more precise KEY WORDS: absolute P intake, available P, broken-line regression, response criteria, weight gain, whole-body P Received August 2012; accepted 27 December 2012 Correspondence: S J Kaushik, INRA, UR 1067, Nutrition, Metabolism and Aquaculture (NuMeA), Pole d’Hydrobiologie INRA, F-64310 SaintPee-sur-Nivelle, France E-mail: kaushik@st-pee.inra.fr ª 2013 Blackwell Publishing Ltd Available data on mineral and trace element requirements of fish and crustaceans have been updated and summarized recently by the National Research Council (NRC 2011) Of all minerals considered essential for fish, requirement for phosphorus (P) is the most extensively studied Although there is a significant amount of data available in the literature on response to dietary P and P requirement based on a wide range of response variables, direct comparison of results is often difficult due to interstudy differences Meta-analysis of data from the available literature is a relevant solution for interstudy comparisons and for summarizing data (Sauvant et al 2008) Metaanalytic approach has been used to analyse data on dietary requirements for selected amino acids in animals (Simongiovanni et al 2011) as well as in fish (Kaushik & Seiliez 2010), to investigate nutrient balance in growing animals (Schulin-Zeuthen et al 2007) and to study the effects of fish meal and fish oil replacement in fish diets (Drakeford & Pascoe 2008; Sales 2009; Sales & Glencross 2011; Hua & Bureau 2012) Careful selection and standardization of data and the use of appropriate mathematical model for data analysis are essential to make the meta-analysis to be biologically relevant Till date, more than 70 studies on P requirement or P utilization have been reported for over 40 different species of fish About 90% of the studies were undertaken in the past two decades (1991–2011) and over 60% in the past decade alone (2001–2011) This reflects not only the recognition of the importance of P in growth and skeletal development but also the environmental implications of P discharge into water P requirement of fish has been estimated using a wide range of response criteria: (i) production traits such as weight gain (WG), growth rate or feed efficiency, (ii) levels of ash/P in whole body, plasma/serum, vertebrae, scale or skin, (iii) mineral balance indices such as P gain, retention and, (iv) to a limited extent, expression of genes involved in the absorption of P from the gastrointestinal tract The major and widely used response criteria are in the order of WG, whole-body P, vertebral P, plasma P and whole-body P balance Urinary P excretion has also been occasionally used, especially for large fishes The present work aims at reanalysing available data on P requirement of fish for estimating the minimal dietary P level required based on different response criteria and to identify the most stringent criterion and mode of expression through meta-analysis These were performed by delineating the interstudy differences through standardization of dependent and independent variables following selection, segregation and grouping of data Data from published literature on P requirement or P dose–response studies in fish with at least three dietary P levels were collected Data on different factors such as fish species, initial body weight, final body weight, duration of feeding trial, diet type, P concentration in basal diet, number of dietary P levels tested and corresponding dietary P concentrations, P availability, feed efficiency, major protein source, source of supplemental P, time of sampling after the last meal, type of rearing system, water temperature, salinity, P concentration of the rearing water, response variables tested, mathematical model used, if any, response criterion based on which optimal dietary P level was estimated and the corresponding estimate values were registered A database was created with the foresaid information and the corresponding data from a total of over 70 feeding trials reported in 64 published articles covering not 0.05) The FR, SGR and FCE of fish fed the protein-restricted diets were significantly lower than those in the control groups during the protein restriction period (P < 0.05) Contrarily, significant increases in above indices between the fish previously fed the protein-restricted and control diets were observed during the recovery period (P < 0.05) (Table 3) A significant increase in the PRE was observed in fish fed with the protein-restricted diets during the protein restriction period (P < 0.05), whereas a significant decrease in the PRE Table Effect of protein restriction on biometric indices and growth performance of yellow catfish (mean ± SE, n = 4)* Diets Control Condition factor (g cmÀ3) After protein 1.69 ± 0.11 restriction After recovery 2.68 ± 0.14 Hepatosomatic index (%) After protein 1.60 ± 0.14a restriction After recovery 1.74 ± 0.11 Viscerosomatic index (%) After protein 7.45 ± 0.62a restriction After recovery 9.95 ± 0.34a Survival rate (%) After protein restriction After recovery Body weight (g) Initial After protein restriction After recovery D320 D260 1.67 ± 0.10 1.77 ± 0.07 2.55 ± 0.10 2.65 ± 0.22 a 2.10 ± 0.13 1.86 ± 0.12 1.92 ± 0.17 7.13 ± 0.78a 9.26 ± 0.85b 9.40 ± 0.56a 11.21 ± 0.51b 1.58 ± 0.2 b 98.90 ± 1.92 98.90 ± 1.92 97.80 ± 1.91 100 ± 0.00 100 ± 0.00 100 ± 0.00 8.32 ± 0.08 14.36 ± 0.20a 8.35 ± 0.10 13.20 ± 0.20b 8.34 ± 0.05 12.53 ± 0.31c 22.04 ± 0.80 21.92 ± 0.24 21.70 ± 0.85 Feeding rate (% bw dayÀ1) Protein-restricted 2.53 ± 0.06a period Recovery period 2.27 ± 0.05a Specific growth rate (% dayÀ1) Protein-restricted 1.78 ± 0.03a period Recovery period 1.57 ± 0.07a Feed conversion efficiency (%) Protein-restricted 65.75 ± 4.05a period Recovery period 65.92 ± 2.16a Protein retention efficiency (%) Protein-restricted 28.40 ± 1.24a period Recovery period 28.77 ± 1.17a Protein efficiency ratio Protein-restricted 1.73 ± 0.10a period Recovery period 1.68 ± 0.04a 2.20 ± 0.09b 2.18 ± 0.11b 2.47 ± 0.10b 2.68 ± 0.06c 1.41 ± 0.08b 1.26 ± 0.05c 1.86 ± 0.12b 2.03 ± 0.08b 58.88 ± 2.66b 52.58 ± 2.78c 70.64 ± 1.54b 72.52 ± 1.32b 32.04 ± 1.04b 33.96 ± 2.05b 27.32 ± 3.76ab 25.52 ± 1.39b 1.84 ± 0.05a 2.02 ± 0.10b 1.85 ± 0.09b 1.89 ± 0.07b nificantly higher PER than that of fish fed the diets control or D320 during the protein restriction period (P < 0.05), while a significant increase in the PER was still observed in fish previously fed with the protein-restricted diets during the recovery period (P < 0.05) (Table 3) At the end of the protein restriction period, no significant differences in whole-body protein and energy contents were observed between all groups (P > 0.05) (Table 4) D260-treated fish showed significant increases in dry matter, lipid and ash contents (P < 0.05), but no significant differences in the indices mentioned above between the D320 and control groups were observed (P > 0.05) At the end of the recovery period, no significant differences in dry matter, lipid and energy contents were observed between all groups (P > 0.05) (Table 4) Meanwhile, fish previously fed the D260 diet had significantly lower protein contents than those previously fed diets control or D320 (P < 0.05), but the fish previously fed the D260 diet showed significant higher lipid contents than those previously fed diets control or D320 (P < 0.05) Whole-body amino acid compositions of fish fed with different diets are presented in Table At the end of the protein restriction period, whole-body leucine (Leu), phenylalanine (Phe), lysine (Lys) and total essential amino acid (EAA) concentrations of fish fed with D260 diet were significantly lower than those in the control groups (P < 0.05) Contrarily, whole-body glutamic acid (Glu), glycine (Gly) and total non-essential amino acid (NEAA) concentrations of fish fed with D260 diet were significantly higher than those in the control groups (P < 0.05) After weeks of recovery, no significant differences in the indices mentioned above were observed between all groups (P > 0.05), but whole-body valine (Val) content of fish previously fed with the D260 diet was significantly lower than that of the control (P < 0.05), while a significant increase in the histidine (His) content was observed in fish previously fed with the D260 diet (P < 0.05) * Means with the different superscripts letters within the same row are significantly different at P < 0.05 was observed only in fish previously fed with the D260 diet (P < 0.05), and no significant differences between the D320 and control groups were observed during the recovery period (P > 0.05) In addition, fish fed the diet D260 showed a sig- At the end of the protein restriction period, serum lysozyme and liver SOD activities of fish fed the protein-restricted diets were significantly lower than those in the control groups (P < 0.05) (Table 6) At the end of the recovery period, no significant differences in serum lysozyme activities between fish previously fed the D320 and control diets were observed Aquaculture Nutrition, 19; 430–439 ª 2012 Blackwell Publishing Ltd Table Effect of protein restriction on whole body composition of yellow catfish (on wet weight basis) (mean ± SE, n = 4)* After protein restriction Initial Dry matter (g kgÀ1) Protein (g kgÀ1) Lipid (g kgÀ1) Ash (g kgÀ1) Energy (kJ gÀ1) 240.3 140.5 33.7 53.4 4.8 Control ± ± ± ± ± 12.0 0.6 1.2 2.8 0.28 250.1 165.0 38.1 37.2 5.5 ± ± ± ± ± After recovery D320 3.1a 4.4 1.2a 2.2a 0.34 258.3 170.7 38.4 37.0 5.7 D260 ± ± ± ± ± 11.3ab 4.3 1.5a 1.8a 0.50 267.1 170.3 43.5 43.6 5.8 Control ± ± ± ± ± 8.1b 5.1 1.3b 3.4b 0.52 264.5 166.0 47.0 32.1 5.9 ± ± ± ± ± D320 2.4 1.2a 5.3 2.8a 0.21 260.8 163.1 49.4 34.4 5.9 D260 ± ± ± ± ± 3.5 2.1a 3.2 2.4a 0.11 265.4 157.6 48.4 47.6 5.8 ± ± ± ± ± 4.7 0.7b 4.4 3.0b 0.16 * Means at each sampling time with the different superscripts letters within the same row are significantly different at P < 0.05 Table Effect of protein restriction on whole body amino acid profiles of yellow catfish (mean ± SE, n = 4, expressed as g kgÀ1 of protein)* After protein restriction Amino acids Initial Thr Val Met Ile Leu Phe Lys His Arg ∑EAA Asp Serine (Ser) Glu Gly Ala Cys Tyr Pro ∑NEAA 40.9 47.6 25.2 42.1 76.2 42.3 85.5 21.1 67.6 448.5 89.9 59.6 150.5 92.0 68.1 6.1 31.4 53.9 551.5 Control ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.4 0.7 0.3 0.6 1.0 0.3 0.8 0.1 0.5 1.2 0.6 1.2 1.4 3.4 1.0 0.5 1.1 1.8 3.1 40.9 47.7 27.4 42.9 77.6 45.1 86.2 22.2 66.3 456.3 88.6 58.8 151.0 89.6 67.0 9.6 28.4 50.7 543.7 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± After recovery D320 0.4 1.0 0.4 1.0 0.7a 0.2a 0.4a 0.1 1.1 1.1a 0.8 1.0 0.3a 1.0a 0.6 0.4 1.5 1.1 1.1a 40.4 47.7 27.7 43.0 77.2 44.8 85.7 22.0 66.9 455.4 88.5 58.0 150.3 91.0 67.5 10.1 28.8 50.4 544.6 D260 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.4 0.5 0.3 1.1 1.1a 1.0ab 0.5a 0.0 0.9 1.2a 0.5 1.0 0.4a 0.8ab 0.5 0.2 0.0 0.0 1.2a 40.4 48.4 27.8 42.6 75.5 44.3 84.4 22.0 66.9 452.3 88.3 58.3 152.1 92.0 67.9 9.7 28.6 50.8 547.7 Control ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.7 1.0 0.7 0.4 0.3b 0.4b 0.5b 1.0 1.2 1.0b 0.3 1.4 0.3b 0.6b 1.6 1.3 1.2 1.0 1.0b 40.2 50.4 26.7 44.9 77.4 43.4 87.3 22.4 66.1 458.8 91.0 56.4 152.5 85.4 66.8 7.0 31.4 50.8 541.2 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± D320 0.4 0.6a 0.3 0.2 0.7 0.3 0.7 0.3a 0.3 1.5 0.5 1.0 1.3 2.6 0.1 1.7 1.9 1.0 1.5 40.4 50.3 26.5 45.1 77.2 43.4 87.1 23.0 65.6 458.6 91.1 57.0 153.5 84.3 66.6 7.7 29.8 51.0 541.4 D260 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.3 0.2a 0.6 0.4 0.2 0.7 0.7 0.4ab 0.7 1.4 0.6 0.5 1.8 1.3 0.2 0.3 1.1 1.0 1.4 40.5 46.8 26.5 44.8 77.8 42.4 88.6 23.3 66.5 457.2 91.0 57.2 152.4 84.8 66.6 7.1 32.4 51.8 542.8 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.4 1.3b 0.2 0.8 1.0 1.2 1.0 0.1b 0.5 1.2 0.5 0.8 1.2 1.6 1.1 0.3 2.1 1.3 1.2 ∑EAA, total essential amino acids; ∑NEAA, total nonessential amino acids * Means at each sampling point with the different superscripts letters within the same row are significantly different at P < 0.05 Table Lysozyme and superoxide dismutase (SOD) activities in tissues of yellow catfish at each sampling time (mean ± SE, n = 4)* After protein restriction Control À1 Serum lysozyme (lg ml ) Liver SOD (U mgÀ1 prot) After recovery D320 a 28.75 ± 1.54 194.6 ± 6.04a D260 b 24.46 ± 1.35 177.8 ± 5.25b Control b 22.23 ± 2.50 162.8 ± 6.37c D320 a 24.47 ± 1.20 176.6 ± 12.51a D260 ab 23.54 ± 2.04 222.4 ± 14.70b 22.87 ± 0.88b 252.3 ± 8.44c * Mean values at each sampling point with the different superscripts letters within the same row are significantly different at P < 0.05 (P > 0.05) (Table 6), but the fish previously fed the D260 diet still showed a significantly lower serum lysozyme activity than that of fish previously fed the control diet (P < 0.05) Fish previously fed the protein-restricted diets had significantly higher liver SOD activities than those previously fed the control diets (P < 0.05) Aquaculture Nutrition, 19; 430–439 ª 2012 Blackwell Publishing Ltd In the current study, the average SGR in terms of wet weight (SGRw) of the fish fed the control diet (390.5 g kgÀ1 crude protein) was approximately 1.78% dayÀ1, which is comparable to those (1.36–2.37% dayÀ1) reported for simi- lar-sized yellow catfish (Ye et al 2009; Luo et al 2011) It indicates that the control diet prepared for the present study was nutritionally adequate to sustain good growth of juvenile yellow catfish Fish biometrical indices such as CF represent integrative indicator of fish health condition (Mayer et al 1992) During the protein restriction period, although dietary protein levels were reduced by 7% (D320 diet) and 11% (D260 diet), respectively compared to the control diet for yellow catfish, no significant differences in CF were observed among dietary treatments in the current study It appears that protein-restricted fish were tolerant to at least 11% units lower protein level compared to the control fish for maintaining their integrative health status Metcalfe & Monaghan (2001) indicated that key tissues or organs in animals might be safeguarded, at the expense of others that have a lesser effect on fitness following a period of undernutrition In the present study, fish fed with the D260 diet showed significant higher HSI and VSI than those fed the control diets It appears that liver/viscera size of D260-treated fish has been found to be less affected than are other body parts by protein restriction, and it is to be expected that the fish shows ‘liver/viscera-sparing’ strategies at the expense of other body parts following a period of protein restriction In the present study, dietary protein restriction showed adverse effects on the final body weight and SGR of yellow catfish Similar findings were observed in hybrid tilapia (Oreochromis mossambicus O niloticus), in which the fish were deprived of food for or weeks (Wang et al 2000) In addition, similar observations were also demonstrated in barramundi (Lates calcarifer), in which the fish subjected to moderate levels of feed restriction (50% and 75% satiation) for weeks (Tian & Qin 2004), and in Chinese shrimp (Fenneropenaeus chinensis), in which the shrimp suffered weeks of protein restriction (Wu & Dong 2002) A great number of fish species have been reported to regulate their feed intake in relation to the energy content of the diet (Kaushik et al 1981; Kaushik & Luquet 1984; De la Higuera 2001) However, in the present study, although the three experimental diets were formulated to be isocaloric (gross energy: 17 kJ gÀ1), the FRs of protein-restricted fish were significantly lower than that of the control during the protein restriction period It has also been postulated that FR of the protein-restricted fish is driven mainly by dietary crude protein to gross energy ratios (21.84, 17.95 and 15.83 for Control, D320 and D260 diets, respectively) In addition, there has been one investigation on Chinese shrimp (F chinensis) showing that the FRs of protein-restricted Chinese shrimp significantly increased as the severity of protein restriction (Wu & Dong 2002) These discrepancies between results demonstrate that the effects of dietary protein restriction on FR can be attributed to differences in the duration and severity of protein restriction or different species In the current study, the improved protein utilization (in particular, PER and PRE) in yellow catfish may suggest a compensatory strategy following a period of protein restriction It appears that the protein-restricted fish consumed less protein and utilized it more efficiently for growth as dietary protein decreased In agreement with the present findings, De Silva et al (1991) and Lee et al (2002) also have noted similar improvements in protein utilization as dietary protein levels decreased in tilapia and rockfish In the present study, the protein-restricted fish showed no significant differences in the whole-body protein and energy contents, and significant increase in dry matter, lipid and ash contents were observed in fish fed with the D260 diet Nevertheless, in an experiment on Chinese shrimp (F chinensis), the whole-body crude protein, lipid and energy contents of the shrimp were positively related to the dietary protein content, whereas moisture and ash contents significantly decreased as the severity of dietary protein restriction decreased (Wu & Dong 2002) It is likely that the differences between the present observations and the findings reported by Wu & Dong (2002) in responses of whole-body composition result from variations in the severity and duration of protein restriction, quality of diet and interspecific differences In the present study, the observed lower concentrations of whole-body Leu, Phe, Lys and total EAA in fish fed with the D260 diet partially reflected the dietary AA patterns in D260 diet Leu has been shown to be a critical amino acid for increasing skeletal muscle protein synthesis in human (Nair et al 1992), and Leu flux and body protein synthesis and protein breakdown were reduced when dietary protein intake was reduced from the requirement to inadequate level (Motil et al 1981), while Lys was responsible for maintenance of Leu and other EAA economy, and they appear to be related to the nitrogen and amino acid requirements of human (Motil et al 1981) Therefore, the current findings suggest that Leu and Lys levels were regulated by whole-body and dietary protein contents, on the Aquaculture Nutrition, 19; 430–439 ª 2012 Blackwell Publishing Ltd dynamics of whole-body AA metabolism Considering the relative EAA to NEAA ratios for protein synthesis, Glu and Gly, and other NEAA, which are inadequately synthesized or not synthesized by the fish, seemed to be in excess, thus, the surplus NEAA may be retained more efficiently in whole-body in the current study However, as individual NEAA undergo extensive interconversion and metabolism within the body (Cowey & Walton 1989), the correlation in metabolic patterns of NEAA between diet and whole-body should be further investigated Like all mammals, fish have developed antioxidant enzymes to alleviate adverse effects of oxidative stress, such as lysozyme and SOD (Fevolden et al 1999; reviewed in Martı´ nezA´lvarez et al 2005) Superoxide dismutase intervenes in the first transformation by dismuting the superoxide free radicals (O2À) into H2O2 (Dorval et al 2003), while lysozyme is one of the humoral immune components of antibacterial activity and is recognized to be a stable stress indicator (Fevolden et al 1999) The present study demonstrated that serum lysozyme and liver SOD activities were negatively related to the severity of protein restriction The present findings are consistent with the results of Kiron et al (1995) who reported that rainbow trout fed a diet containing only 100 g kgÀ1 protein had reduced lysozyme activity in serum compared with fish fed diets with 350 g kgÀ1 and 500 g kgÀ1 proteins Ali et al (2003) concluded that accelerated growth (compensatory growth) occurs when favourable conditions are restored after a period of growth depression In the present study, the SGR of the previously protein-restricted fish were markedly greater than those of the controls, indicating that there was a compensatory growth response At the end of the recovery period, all previously protein-restricted fish caught up with the body weights of the control fish This suggests that all previously protein-restricted fish achieved complete growth compensation Several factors could contribute to the compensatory growth following a period of food deprivation, including higher food consumption (hyperphagia) and improvement in feed utilization (Nicieza & Metcalfe 1997; Wootton 1998; Gaylord & Gatlin 2001) In the present study, fish previously fed protein- Aquaculture Nutrition, 19; 430–439 ª 2012 Blackwell Publishing Ltd restricted diets had significantly higher FR, FCE and PER than those in the controls between all groups during the recovery period These observations suggest that compensatory growth for the previously protein-restricted fish is attributable to both the improved feed/protein utilization and increased FR However, the results of one study in Chinese shrimp (F chinensis) reported that compensatory growth for T30-treated (dietary protein content was reduced to 300 g kgÀ1) shrimp is mainly dependent on improved FCE, while that for T15-treated (dietary protein content was reduced to 150 g kgÀ1) shrimp is attributable to both the improved FCE and increasing feed intake (Wu & Dong 2002) This could be due to variations in the severity and duration of protein restriction and the duration of compensation (Nicieza & Metcalfe 1997) In previous studies, several dietary/feeding manipulations, including ration restriction (Tian & Qin 2004) and feed restriction (Wang et al 2000; Zhu et al 2001) were proposed for their application in aquaculture Compared with these dietary/feeding manipulations, using proteinrestricted feeding for inducing compensatory growth in aquaculture is of considerable interest with possible advantages including increased growth rates and feed/protein utilization, and decreased waste production Protein-restricted feeding could have beneficial effects not only on the overall efficiency of fish production but also on the environment, therefore, a period of protein restriction should be used to elicit a compensatory growth response for fishes in aquaculture practice In conclusion, dietary protein restriction showed negative effects on growth and FCE of yellow catfish during the protein restriction period, and the fish previously subjected to dietary protein restriction compensated completely in terms of final body weight, growth rate and whole-body EAA and NEAA concentrations Protein-restricted feeding has a positive impact not only on the overall efficiency of fish production, but also on the environment; much attention should be paid to the protein-restricted feeding on eliciting a compensatory growth response for fishes in aquaculture practice The authors wish to thank Jiuling Sun for his assistance in the study This research was supported by the Development Fund for Doctor in Anhui Agricultural University (grant no YJ2008-22) and Educational Commission of Hubei Province (grant no Q20101710) and International Science & Technology Cooperation Program of China (grant no 2011DFG33280) Thanks are 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