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Effect of temperature and feeding frequency on growth performances, feed efficiency and body composition of pikeperch juveniles (Sander lucioperca)
Aquaculture 289 (2009) 70–73
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Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e
Effect of temperature and feeding frequency on growth performances, feed efficiency and body composition of pikeperch juveniles (Sander lucioperca) Neil Wang ⁎, Xuliang Xu, Patrick Kestemont Research Unit in Organismal Biology, University of Namur (FUNDP), 61 rue de Bruxelles, B-5000 Namur, Belgium
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Article history: Received 29 July 2008 Received in revised form 7 January 2009 Accepted 8 January 2009 Keywords: Pikeperch Growth Temperature Feeding
a b s t r a c t Pikeperch, Sander lucioperca, is a promising candidate for inland aquaculture diversification. Few studies have investigated the effects of temperature on growth despite it is the main determining factor in fish. Temperature namely acts on metabolism and thus influences feed intake. The aim of this study was to investigate the interactive effects of temperature and feeding on pikeperch growth. Eighteen groups of 21 fish (6.4 g mean weight) were reared in 18 tanks during 56 days according to a complete design testing 3 temperatures (20, 24 or 28 °C) and 3 feeding frequencies (1, 3 or 6 times a day to apparent satiation) in duplicate. Feed intake (FI) was recorded throughout the experiment. At the end of the study, fish were weighted for calculation of weight gain (WG), specific growth rate (SGR) and feed efficiency (FE). Total carcass protein and lipid content were determined. Protein and lipid retention efficiencies (PRE and LRE) were calculated. Based on the results, an optimal feeding rate was estimated for each rearing temperature. Temperature and feeding frequency had an interactive effect on WG and independently influenced SGR, FI and FE (P b 0.05). WG, SGR and FE were the highest at 28 °C and/or when fish were fed 3 times a day (14.4 ± 0.4 g, 1.7–2.0 ± 0.04% and 0.95–0.97 ± 0.03% respectively). FI was the highest at 28 °C (13.1 ± 0.16 g) or when fish were fed 6 times a day (13.5 ± 0.16 g). PRE and LRE were significantly affected by feeding frequency only (P b 0.05). They were lower when fish were fed 6 times a day than in the two other treatments (25.7 ± 1.4% against 33.6–35.0 ± 0.4% and 42.7 ± 5.5% against 62.0–63.3 ± 5.5% respectively). Fish protein content was significantly affected by temperature only (P b 0.05) and was lower at 28 °C than at 20 or 24 °C (13.6 ± 0.3% against 15.9–16.3 ± 0.3% respectively). No significant effect was observed on the fish lipid content. The best growth performances (WG and FE) were observed when fish were reared at 28 °C and fed 3 times a day. At this feeding frequency, the optimal feeding rates were estimated as 1.5, 1.8 and 2.0% of fish body weight at 20, 24 and 28 °C respectively. Further studies investigating the effect of these factors on larger fish (100–2000 g) are required. In addition, the effects of other main factors influencing growth like photoperiod should be investigated. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Pikeperch, Sander lucioperca, is one of the most promising Percid species for diversification in inland aquaculture in Europe. Indeed, it is a species of high economic interest that grows relatively fast (Hilge and Steffens, 1996; Kestemont and Mélard, 2000). In all fish species, growth optimization is of paramount importance for profitability of fish farming activity. Within a given species, numerous factors can influence fish growth, among which the most important are probably temperature and feeding (Gardeur et al., 2007). Temperature regulates metabolic activity and all fish species are characterised by a range of temperature within which growth is maximal (Jobling, 1996; Person-Le Ruyet et al., 2006; Bjornsson et al., ⁎ Corresponding author. Tel.: +33 81 72 43 71; fax: +32 81 72 43 62. E-mail address: [email protected] (N. Wang). 0044-8486/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2009.01.002
2007). In general, Percid fishes are quite thermophilic and display the fastest growth at relatively warm temperature for temperate fish species. Thus, optimal temperature requirements have been found to be around 23–24 °C for Yellow perch (Perca flavescens) and Eurasian perch (Perca fluviatilis) and 24–26 °C for walleye (Sander vitreus), (Brown et al., 1996; Mélard et al., 1996; Summerfelt and Summerfelt, 1996). Regarding pikeperch, most studies on growth have been performed at 20–24 °C (Jankowska et al., 2003; Zakes et al., 2003, 2004; Nyina-Wamwiza et al., 2005; Molnar et al., 2006; Schulz et al., 2005, 2008). Recently, Ronyai and Csengeri (2008) showed that pikeperch reared at 25 °C grows faster than at 20 °C. However, according to Hokanson (1977) and Hilge and Steffens (1996), optimal temperature might rather be within the range of 24–30 °C. Thus, optimal temperature has not been clearly determined yet. This area should be further investigated, since temperature especially governs the effects of other environmental or nutritional factors on fish growth
N. Wang et al. / Aquaculture 289 (2009) 70–73
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Table 1 Results of WG, CV, SGR, FI and FE according to temperature and feeding rate
Table 3 Effect of rearing temperature on SGR, FI, FE and carcass protein content
Temperature
Frequency
WG (g)
CV (%)
SGR (%)
FI (g)
FE
Temperature
SGR (%)
FI (g fish− 1)
FE
Protein (% of w.w.)
20 20 20 24 24 24 28 28 28
1 3 6 1 3 6 1 3 6
5.6 ± 0.4 a 6.6 ± 0.4 ab 6.9 ± 0.4 ab 7.9 ± 0.4 b 10.5 ± 0.4 cd 9.9 ± 0.4 c 11.2 ± 0.4 cd 14.4 ± 0.4 e 11.7 ± 0.4 d
43.6 ± 4.7 40.4 ± 4.7 48.0 ± 4.7 46.5 ± 4.7 44.0 ± 4.7 39.0 ± 4.7 37.4 ± 4.7 31.4 ± 4.7 34.4 ± 4.7
1.1 ± 0.07 1.3 ± 0.07 1.3 ± 0.07 1.5 ± 0.07 1.8 ± 0.07 1.6 ± 0.07 2.0 ± 0.07 2.1 ± 0.07 1.8 ± 0.07
7.0 ± 0.3 8.8 ± 0.3 11.0 ± 0.3 8.6 ± 0.3 10.8 ± 0.3 13.7 ± 0.3 11.1 ± 0.3 12.6 ± 0.3 15.8 ± 0.3
0.81 ± 0.05 0.75 ± 0.05 0.63 ± 0.05 0.92 ± 0.05 0.97 ± 0.05 0.72 ± 0.05 1.02 ± 0.05 1.14 ± 0.05 0.74 ± 0.05
20 (n = 6) 24 (n = 6) 28 (n = 6)
1.2 ± 0.04 a 1.6 ± 0.04 b 2.0 ± 0.04 c
8.9 ± 0.16 a 11.0 ± 0.16 b 13.1 ± 0.16 c
0.73 ± 0.03 a 0.87 ± 0.03 b 0.97 ± 0.03 c
16.3 ± 0.3 a 15.9 ± 0.3 a 13.6 ± 0.3 b
Data are expressed as mean ± S.E.M. A significant interaction effect was detected for WG only (P b 0.05). Different letters indicate significant difference between means (P b 0.05).
(Jobling, 1996; Gardeur et al., 2007). Namely, the optimal feeding rate is highly dependent on water temperature (Kestemont and Barras, 2001). Little information is available about the adequate feeding regime to be given to growing pikeperch. In most studies on pikeperch growth, feed has been delivered to satiation or in excess (Nyina-Wamwiza et al., 2005; Molnar et al., 2006; Schulz et al., 2008). Zakes et al. (2003) have suggested that feeding rate of at least 2% of biomass at 22 °C could be optimal for pikeperch growth from 25 to 70 g. In larger fish (84–300 g), Ronyai and Csengeri (2008) reported optimal feeding rates of 1.2–2% (decreasing with fish weight) at 25 °C. However, the optimal feeding rate is size and temperature dependent and nothing is known about optimal temperature and feeding rate for other ranges of fish size. Consequently, the aim of this study was to identify optimal temperature and feeding rate maximizing growth in juvenile pikeperch. To this respect, fish were fed to satiation one to several times a day. For each rearing temperature, optimal feeding rates were estimated according to the eaten quantity of food that maximized growth and feed efficiency. 2. Materials and methods 2.1. Experimental design A batch of 420 pikeperch fingerlings (6.4 ± 0.4 g) was provided by a commercial fish farm (Excellence Fish, Horst, The Netherlands). After one week of acclimation in laboratory facilities, fish were divided into 18 groups of 21 fish each and transferred into 120-L rectangular tanks after individual weighting. Three temperatures (20, 24 and 28 °C) and three feeding frequencies were tested in duplicate. Photoperiod was set at 12L:12D. Fish were fed by hand to satiation, either once, 3 or 6 times a day with a commercial grower diet (CATCO Grower-12 EX, 1.2 mm, Coppens, The Netherlands). This feed was chosen for its high protein and low lipid contents (45% protein, 12% lipid), as recommended for growth of pikeperch fingerling (Nyina-Wamwiza et al., 2005). Total amount of given food was evaluated daily. Experiment lasted 56 days. Water quality was monitored twice a week. pH and Table 2 Results of protein and lipid content and retention efficiencies according to temperature and feeding rate Temperature
Frequency
Protein
Lipid
PRE
LRE
20 20 20 24 24 24 28 28 28
1 3 6 1 3 6 1 3 6
15.9 ± 0.5 16.5 ± 0.5 16.6 ± 0.5 16.2 ± 0.5 16.0 ± 0.5 15.6 ± 0.5 13.5 ± 0.5 13.7 ± 0.5 13.7 ± 0.5
7.5 ± 0.8 7.8 ± 0.8 6.9 ± 0.8 6.2 ± 0.8 7.1 ± 0.8 5.6 ± 0.8 6.3 ± 0.8 5.7 ± 0.8 5.1 ± 0.8
33.6 ± 2.4 32.2 ± 2.4 27.3 ± 2.4 36.9 ± 2.4 38.0 ± 2.4 27.1 ± 2.4 30.3 ± 2.4 34.9 ± 2.4 22.7 ± 2.4
70.7 ± 9.5 67.1 ± 9.5 58.5 ± 9.5 55.8 ± 9.5 64.4 ± 9.5 36.8 ± 9.5 59.6 ± 9.5 58.4 ± 9.5 32.9 ± 9.5
Data are expressed as mean ± S.E.M. No significant interaction was detected for any parameter (P N 0.05).
Data are expressed as mean ± S.E.M. Different letters indicate significant difference (P b 0.05).
dissolved oxygen were maintained above 7.5 and 7 mg L − 1 respectively. N–NH+4 and N–NO−2 concentrations remained below 1 mg L− 1. At the end of the trial, all fish were killed by a blow on the head and individually weighted. Three fish per tank were randomly chosen and pooled to determine carcass protein and lipid contents. 2.2. Chemical analysis Total protein content was determined by the Kjeldahl method (N ⁎ 6.25). Total lipids were extracted with chloroform/methanol/ water (2:2:1.8, V:V:V) with the method of Bligh and Dyer (1959). BHA (0.02%) was added to chloroform/methanol as an antioxidant. Results were expressed in percentage of wet weight. 2.3. Variables and statistics The following parameters were calculated: Weight Gain (WG, g) = Final weight (Wf) − Initial weight (Wi) Specific Growth Rate (SGR, % d− 1) = 100 ⁎ Ln (Wf/Wi) / Experiment duration Feed Efficiency (FE) = (Wf − Wi) / Total Feed Intake (TFI) Protein retention efficiency (PRE, %) = 100 ⁎ (Final protein content − Initial protein content of fish) / TFI protein content Lipid retention efficiency (LRE, %) = 100 ⁎ (Final lipid content − Initial lipid content of fish) / TFI lipid content. Experimental design was analysed with a GLM procedure of the SAS Software, taking the tank as the experimental unit. Variables were analysed following a design of two-way ANOVA. Following ANOVA, significant differences between means were detected with the LSD test. The minimum levels of significance were set at P b 0.05 for both ANOVA and mean comparisons. All data are expressed as means ± standard error of the mean (S.E.M.). After analysis of the results, an optimal feeding rate was estimated for each temperature tested, according to the feeding regime giving both the highest growth and feed efficiency. It was calculated as the solution FR of an estimated growth model following the geometric sequence: Wn + 1 = Wn + FR ⁎ FE ⁎ Wn; where Wn is the weight of fish at day n, FE is feed efficiency over the whole experimental period, W0 is the initial weight of fish, W56 is the final weight of fish at the end of the experiment and FR is the feeding rate. Since the study was conducted over a short period of time, it is here assumed that FR was estimable as a constant throughout the experiment. The term (FR ⁎ FE ⁎ Wn) corresponds to the weight gain of fish at day n. At day 56, FR = [(W56 / W0)1/56 − 1] / FE. Table 4 Effect of feeding frequency on SGR, FI, FE, protein retention efficiency (PRE) and lipid retention efficiency (LRE) Feeding frequency SGR (%) 1 (n = 6) 3 (n = 6) 6 (n = 6)
FI (g fish− 1) FE (%)
PRE (%)
LRE (%)
1.5 ± 0.04 a 8.9 ± 0.16 a 0.91 ± 0.03 a 33.6 ± 1.4 a 62.0 ± 5.5 a 1.7 ± 0.04 b 10.7 ± 0.16 b 0.95 ± 0.03 a 35.0 ± 1.4 a 63.3 ± 5.5 a 1.6 ± 0.04 ab 13.5 ± 0.16 c 0.70 ± 0.03 b 25.7 ± 1.4 b 42.7 ± 5.5 b
Data are expressed as mean ± S.E.M. Different letters indicate significant difference (P b 0.05).
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3. Results No fish died during the experiment. All data recorded and calculated at the end of the experiment according to temperature and feeding frequency are presented in Tables 1 and 2. First of all, temperature and feeding regime interacted on fish weight gain (Table 1). Weight gain was the lowest at 20 °C whatever the feeding regime tested, ranging from 5.6 to 6.9 g and the highest at 28 °C when fish were fed 3 times a day (WG = 14.4 g). For each feeding regime, weight gain significantly increased with temperature. At 24 °C, growth was reduced when fish were fed once a day compared to the growth of fish fed 3 or 6 times a day. At 28 °C, the weight gains of fish groups fed once or 6 times a day were not significantly different. SGR increased significantly with water temperature, from 1.2% d− 1 at 20 °C to 2.0% d− 1 at 28 °C (Table 3). It was also influenced by feeding frequency and was lower in groups fed once than in groups fed 3 times a day (Table 4). SGR of fish fed 6 times a day did not differ significantly from the two other treatments. Temperature and feeding regime independently influenced fish feed intake and feed efficiency. Total feed intake significantly increased with water temperature and feeding frequency. Feed efficiency also significantly increased with water temperature, while it was higher in fish fed once or 3 times a day than in fish fed 6 times a day. Carcass lipid content did not differ between treatments. It ranged from 5.7 to 7.4% according to the water temperature and from 5.9 to 6.7% according to the feeding regime applied. Carcass protein content was significantly higher at 20 °C and 24 °C than at 28 °C (Table 3). PRE and LRE were higher when fish were fed once or 3 times a day than when they were fed 6 times a day. Regardless of temperature, SGR and feed efficiency were maximal when fish were fed 3 times a day. Consequently, for each rearing temperature, the optimal feeding rate was estimated according to the experimental data (weight and feed efficiency) obtained on fish fed 3 times a day. As a result, optimal feeding rates (expressed in percent of fish biomass per day) that maximized growth under our laboratory conditions were found to be 1.5% at 20 °C, 1.8% at 24 °C and 2% at 28 °C, taking 13.0, 16.9 and 20.8 g for W56 and 0.825, 0.965 and 1.06 for FE respectively. 4. Discussion To our knowledge, this study was the first to investigate the concurrent effects of temperature and feeding on pikeperch growth. Our results are globally in accordance with the data available in the literature. The SGR value of fish reared at 24 °C (1.6% d− 1) was close to that of pikeperch reared under similar temperature conditions in other studies (SGR of 1.35–1.5% d− 1), (Schulz et al., 2005; Molnar et al., 2006). First of all, weight gain, SGR and feed efficiency were higher in fish held at 28 °C than in fish held at 20 or 24 °C. Therefore, our study demonstrates for the first time that optimal temperature for pikeperch early ongrowing is clearly higher than temperatures that have been applied in previous experiments and is probably around 28 °C, as suggested by Hokanson (1977) and Hilge and Steffens (1996). It makes it one of the most thermophilic Percid species studied so far and is similar to what is found in some Cyprinids such as tench (Tinca tinca), roach (Rutilus rutilus), goldfish (Carassius auratus) and in European catfish (Silurus glanis), (Hilge, 1985; Wolnicki and Korwin-Kossakowski, 1993; Kestemont, 1995; Van Dijk et al., 2002). Nevertheless, some authors have reported that optimal temperature may decrease with fish weight in some species like African catfish (Clarias gariepinus), carp (Cyprinus carpio), Atlantic cod (Gadus morhua) or Atlantic halibut (Hippoglossus hippoglossus), (Hogendoorn et al., 1983; Cuenco et al., 1985; Bjornsson and Tryggvadottir, 1996; Bjornsson et al., 2007). Consequently, as recommended by Ronyai and Csengeri
(2008), the effect of temperature on growth should be further investigated for larger pikeperch from 100 g to 1–2 kg, which is the commercial size range. Feed efficiencies were the highest when fish were fed once or 3 times a day and a more frequent hand-feeding did not lead to an increase of growth despite a higher feed intake. This suggests that the amount of feed ingested by pikeperch fed 3 times a day is probably close to the optimal amount for which growth is maximal. This is in accordance with the conclusions of Alanara et al. (2001) and Booth et al. (2008) who claimed that one to four meals per day may be sufficient for Salmonids and Australian snapper (Pagrus auratus) to achieve maximum feed intake and growth. Reasons for which growth significantly decreased when fish were fed 6 times a day at 28 °C are unclear. According to Johansen and Jobling (1998), repeated feeding throughout long periods of the day would increase swimming activity of fish, resulting in energy expenditure and lower growth rate. Besides, fish carcass protein content decreased with increasing water temperature, as observed by Peres and Oliva-Teles (1999) in juvenile seabass (Dicentrarchus labrax), suggesting a modulation of protein metabolism by temperature. Protein and lipid retentions decreased with increasing feeding frequency as observed in turbot fed increasing amount of food (Van Ham et al., 2003). According to these authors, lower protein and lipid retentions could be explained by a higher energy requirement for feed assimilation at higher feed consumption, which is usually accompanied by reduced nutrient absorption. Thus, it appears that in juvenile pikeperch, a feeding frequency of 3 times a day would be close to the upper limit at which growth and feed efficiency are maximized. Therefore, for each temperature, we chose to estimate the optimal feeding rates at this feeding frequency. The rate found for pikeperch held at 24 °C (1.8% of fish biomass per day) was identical to the one given by the model of Mélard et al. (1996) for Eurasian perch of same weight reared at 23 °C. From our results, we conclude that optimal feeding rate at 28 °C may be about 2% of fish body weight when distributed 3 times a day. However, we are aware that other factors that were not taken into account in this study might interact with temperature, especially feed composition or photoperiod. For example, Zakes et al. (2003) also found an optimal feeding rate of 2% for pikeperch of 25–70 g despite their fish were reared at only 22 °C. In their study, feed protein and lipid contents were higher than in our experiment (54:18 vs 46:12 P:L respectively). In addition, feed delivery was continuous over 19 h per day and fish were held under continuous lighting, while we applied a 12L:12D photoperiod. Nyina-Wamwiza et al. (2005) have shown that the protein/lipid ratio of the diet has an impact on pikeperch growth. However, Gardeur et al. (2007) have pointed out the fact that temperature and photoperiod play a more important role than feeding frequency or feed lipid content in the determinism of Eurasian perch growth. Therefore, taken together, the results suggest that rearing pikeperch at 28 °C under a daylength period longer than 12 h might be an effective method to enhance fish growth. At this photoperiodic regime, optimal feeding rate would probably be more than 2%.
5. Conclusion This study was the first to investigate the optimal rearing temperature and feeding rate in small juvenile pikeperch. It was shown that rearing pikeperch juvenile at 28 °C, giving 3 meals per day clearly enhances growth. Following this procedure, a feeding rate of 2% might be an optimal one to maximize growth. Further experiments should address these questions for bigger fish classes (i.e. 100–2000 g) as optimal rearing temperature may decrease with fish weight. In addition, pikeperch ongrowing requires more information about the effects of other major factors like photoperiod.
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Effect of temperature and feeding frequency on growth performances, feed efficiency and body composition of pikeperch juveniles (Sander lucioperca) Neil Wang ⁎, Xuliang Xu, Patrick Kestemont Research Unit in Organismal Biology, University of Namur (FUNDP), 61 rue de Bruxelles, B-5000 Namur, Belgium
a r t i c l e
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Article history: Received 29 July 2008 Received in revised form 7 January 2009 Accepted 8 January 2009 Keywords: Pikeperch Growth Temperature Feeding
a b s t r a c t Pikeperch, Sander lucioperca, is a promising candidate for inland aquaculture diversification. Few studies have investigated the effects of temperature on growth despite it is the main determining factor in fish. Temperature namely acts on metabolism and thus influences feed intake. The aim of this study was to investigate the interactive effects of temperature and feeding on pikeperch growth. Eighteen groups of 21 fish (6.4 g mean weight) were reared in 18 tanks during 56 days according to a complete design testing 3 temperatures (20, 24 or 28 °C) and 3 feeding frequencies (1, 3 or 6 times a day to apparent satiation) in duplicate. Feed intake (FI) was recorded throughout the experiment. At the end of the study, fish were weighted for calculation of weight gain (WG), specific growth rate (SGR) and feed efficiency (FE). Total carcass protein and lipid content were determined. Protein and lipid retention efficiencies (PRE and LRE) were calculated. Based on the results, an optimal feeding rate was estimated for each rearing temperature. Temperature and feeding frequency had an interactive effect on WG and independently influenced SGR, FI and FE (P b 0.05). WG, SGR and FE were the highest at 28 °C and/or when fish were fed 3 times a day (14.4 ± 0.4 g, 1.7–2.0 ± 0.04% and 0.95–0.97 ± 0.03% respectively). FI was the highest at 28 °C (13.1 ± 0.16 g) or when fish were fed 6 times a day (13.5 ± 0.16 g). PRE and LRE were significantly affected by feeding frequency only (P b 0.05). They were lower when fish were fed 6 times a day than in the two other treatments (25.7 ± 1.4% against 33.6–35.0 ± 0.4% and 42.7 ± 5.5% against 62.0–63.3 ± 5.5% respectively). Fish protein content was significantly affected by temperature only (P b 0.05) and was lower at 28 °C than at 20 or 24 °C (13.6 ± 0.3% against 15.9–16.3 ± 0.3% respectively). No significant effect was observed on the fish lipid content. The best growth performances (WG and FE) were observed when fish were reared at 28 °C and fed 3 times a day. At this feeding frequency, the optimal feeding rates were estimated as 1.5, 1.8 and 2.0% of fish body weight at 20, 24 and 28 °C respectively. Further studies investigating the effect of these factors on larger fish (100–2000 g) are required. In addition, the effects of other main factors influencing growth like photoperiod should be investigated. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Pikeperch, Sander lucioperca, is one of the most promising Percid species for diversification in inland aquaculture in Europe. Indeed, it is a species of high economic interest that grows relatively fast (Hilge and Steffens, 1996; Kestemont and Mélard, 2000). In all fish species, growth optimization is of paramount importance for profitability of fish farming activity. Within a given species, numerous factors can influence fish growth, among which the most important are probably temperature and feeding (Gardeur et al., 2007). Temperature regulates metabolic activity and all fish species are characterised by a range of temperature within which growth is maximal (Jobling, 1996; Person-Le Ruyet et al., 2006; Bjornsson et al., ⁎ Corresponding author. Tel.: +33 81 72 43 71; fax: +32 81 72 43 62. E-mail address: [email protected] (N. Wang). 0044-8486/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2009.01.002
2007). In general, Percid fishes are quite thermophilic and display the fastest growth at relatively warm temperature for temperate fish species. Thus, optimal temperature requirements have been found to be around 23–24 °C for Yellow perch (Perca flavescens) and Eurasian perch (Perca fluviatilis) and 24–26 °C for walleye (Sander vitreus), (Brown et al., 1996; Mélard et al., 1996; Summerfelt and Summerfelt, 1996). Regarding pikeperch, most studies on growth have been performed at 20–24 °C (Jankowska et al., 2003; Zakes et al., 2003, 2004; Nyina-Wamwiza et al., 2005; Molnar et al., 2006; Schulz et al., 2005, 2008). Recently, Ronyai and Csengeri (2008) showed that pikeperch reared at 25 °C grows faster than at 20 °C. However, according to Hokanson (1977) and Hilge and Steffens (1996), optimal temperature might rather be within the range of 24–30 °C. Thus, optimal temperature has not been clearly determined yet. This area should be further investigated, since temperature especially governs the effects of other environmental or nutritional factors on fish growth
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Table 1 Results of WG, CV, SGR, FI and FE according to temperature and feeding rate
Table 3 Effect of rearing temperature on SGR, FI, FE and carcass protein content
Temperature
Frequency
WG (g)
CV (%)
SGR (%)
FI (g)
FE
Temperature
SGR (%)
FI (g fish− 1)
FE
Protein (% of w.w.)
20 20 20 24 24 24 28 28 28
1 3 6 1 3 6 1 3 6
5.6 ± 0.4 a 6.6 ± 0.4 ab 6.9 ± 0.4 ab 7.9 ± 0.4 b 10.5 ± 0.4 cd 9.9 ± 0.4 c 11.2 ± 0.4 cd 14.4 ± 0.4 e 11.7 ± 0.4 d
43.6 ± 4.7 40.4 ± 4.7 48.0 ± 4.7 46.5 ± 4.7 44.0 ± 4.7 39.0 ± 4.7 37.4 ± 4.7 31.4 ± 4.7 34.4 ± 4.7
1.1 ± 0.07 1.3 ± 0.07 1.3 ± 0.07 1.5 ± 0.07 1.8 ± 0.07 1.6 ± 0.07 2.0 ± 0.07 2.1 ± 0.07 1.8 ± 0.07
7.0 ± 0.3 8.8 ± 0.3 11.0 ± 0.3 8.6 ± 0.3 10.8 ± 0.3 13.7 ± 0.3 11.1 ± 0.3 12.6 ± 0.3 15.8 ± 0.3
0.81 ± 0.05 0.75 ± 0.05 0.63 ± 0.05 0.92 ± 0.05 0.97 ± 0.05 0.72 ± 0.05 1.02 ± 0.05 1.14 ± 0.05 0.74 ± 0.05
20 (n = 6) 24 (n = 6) 28 (n = 6)
1.2 ± 0.04 a 1.6 ± 0.04 b 2.0 ± 0.04 c
8.9 ± 0.16 a 11.0 ± 0.16 b 13.1 ± 0.16 c
0.73 ± 0.03 a 0.87 ± 0.03 b 0.97 ± 0.03 c
16.3 ± 0.3 a 15.9 ± 0.3 a 13.6 ± 0.3 b
Data are expressed as mean ± S.E.M. A significant interaction effect was detected for WG only (P b 0.05). Different letters indicate significant difference between means (P b 0.05).
(Jobling, 1996; Gardeur et al., 2007). Namely, the optimal feeding rate is highly dependent on water temperature (Kestemont and Barras, 2001). Little information is available about the adequate feeding regime to be given to growing pikeperch. In most studies on pikeperch growth, feed has been delivered to satiation or in excess (Nyina-Wamwiza et al., 2005; Molnar et al., 2006; Schulz et al., 2008). Zakes et al. (2003) have suggested that feeding rate of at least 2% of biomass at 22 °C could be optimal for pikeperch growth from 25 to 70 g. In larger fish (84–300 g), Ronyai and Csengeri (2008) reported optimal feeding rates of 1.2–2% (decreasing with fish weight) at 25 °C. However, the optimal feeding rate is size and temperature dependent and nothing is known about optimal temperature and feeding rate for other ranges of fish size. Consequently, the aim of this study was to identify optimal temperature and feeding rate maximizing growth in juvenile pikeperch. To this respect, fish were fed to satiation one to several times a day. For each rearing temperature, optimal feeding rates were estimated according to the eaten quantity of food that maximized growth and feed efficiency. 2. Materials and methods 2.1. Experimental design A batch of 420 pikeperch fingerlings (6.4 ± 0.4 g) was provided by a commercial fish farm (Excellence Fish, Horst, The Netherlands). After one week of acclimation in laboratory facilities, fish were divided into 18 groups of 21 fish each and transferred into 120-L rectangular tanks after individual weighting. Three temperatures (20, 24 and 28 °C) and three feeding frequencies were tested in duplicate. Photoperiod was set at 12L:12D. Fish were fed by hand to satiation, either once, 3 or 6 times a day with a commercial grower diet (CATCO Grower-12 EX, 1.2 mm, Coppens, The Netherlands). This feed was chosen for its high protein and low lipid contents (45% protein, 12% lipid), as recommended for growth of pikeperch fingerling (Nyina-Wamwiza et al., 2005). Total amount of given food was evaluated daily. Experiment lasted 56 days. Water quality was monitored twice a week. pH and Table 2 Results of protein and lipid content and retention efficiencies according to temperature and feeding rate Temperature
Frequency
Protein
Lipid
PRE
LRE
20 20 20 24 24 24 28 28 28
1 3 6 1 3 6 1 3 6
15.9 ± 0.5 16.5 ± 0.5 16.6 ± 0.5 16.2 ± 0.5 16.0 ± 0.5 15.6 ± 0.5 13.5 ± 0.5 13.7 ± 0.5 13.7 ± 0.5
7.5 ± 0.8 7.8 ± 0.8 6.9 ± 0.8 6.2 ± 0.8 7.1 ± 0.8 5.6 ± 0.8 6.3 ± 0.8 5.7 ± 0.8 5.1 ± 0.8
33.6 ± 2.4 32.2 ± 2.4 27.3 ± 2.4 36.9 ± 2.4 38.0 ± 2.4 27.1 ± 2.4 30.3 ± 2.4 34.9 ± 2.4 22.7 ± 2.4
70.7 ± 9.5 67.1 ± 9.5 58.5 ± 9.5 55.8 ± 9.5 64.4 ± 9.5 36.8 ± 9.5 59.6 ± 9.5 58.4 ± 9.5 32.9 ± 9.5
Data are expressed as mean ± S.E.M. No significant interaction was detected for any parameter (P N 0.05).
Data are expressed as mean ± S.E.M. Different letters indicate significant difference (P b 0.05).
dissolved oxygen were maintained above 7.5 and 7 mg L − 1 respectively. N–NH+4 and N–NO−2 concentrations remained below 1 mg L− 1. At the end of the trial, all fish were killed by a blow on the head and individually weighted. Three fish per tank were randomly chosen and pooled to determine carcass protein and lipid contents. 2.2. Chemical analysis Total protein content was determined by the Kjeldahl method (N ⁎ 6.25). Total lipids were extracted with chloroform/methanol/ water (2:2:1.8, V:V:V) with the method of Bligh and Dyer (1959). BHA (0.02%) was added to chloroform/methanol as an antioxidant. Results were expressed in percentage of wet weight. 2.3. Variables and statistics The following parameters were calculated: Weight Gain (WG, g) = Final weight (Wf) − Initial weight (Wi) Specific Growth Rate (SGR, % d− 1) = 100 ⁎ Ln (Wf/Wi) / Experiment duration Feed Efficiency (FE) = (Wf − Wi) / Total Feed Intake (TFI) Protein retention efficiency (PRE, %) = 100 ⁎ (Final protein content − Initial protein content of fish) / TFI protein content Lipid retention efficiency (LRE, %) = 100 ⁎ (Final lipid content − Initial lipid content of fish) / TFI lipid content. Experimental design was analysed with a GLM procedure of the SAS Software, taking the tank as the experimental unit. Variables were analysed following a design of two-way ANOVA. Following ANOVA, significant differences between means were detected with the LSD test. The minimum levels of significance were set at P b 0.05 for both ANOVA and mean comparisons. All data are expressed as means ± standard error of the mean (S.E.M.). After analysis of the results, an optimal feeding rate was estimated for each temperature tested, according to the feeding regime giving both the highest growth and feed efficiency. It was calculated as the solution FR of an estimated growth model following the geometric sequence: Wn + 1 = Wn + FR ⁎ FE ⁎ Wn; where Wn is the weight of fish at day n, FE is feed efficiency over the whole experimental period, W0 is the initial weight of fish, W56 is the final weight of fish at the end of the experiment and FR is the feeding rate. Since the study was conducted over a short period of time, it is here assumed that FR was estimable as a constant throughout the experiment. The term (FR ⁎ FE ⁎ Wn) corresponds to the weight gain of fish at day n. At day 56, FR = [(W56 / W0)1/56 − 1] / FE. Table 4 Effect of feeding frequency on SGR, FI, FE, protein retention efficiency (PRE) and lipid retention efficiency (LRE) Feeding frequency SGR (%) 1 (n = 6) 3 (n = 6) 6 (n = 6)
FI (g fish− 1) FE (%)
PRE (%)
LRE (%)
1.5 ± 0.04 a 8.9 ± 0.16 a 0.91 ± 0.03 a 33.6 ± 1.4 a 62.0 ± 5.5 a 1.7 ± 0.04 b 10.7 ± 0.16 b 0.95 ± 0.03 a 35.0 ± 1.4 a 63.3 ± 5.5 a 1.6 ± 0.04 ab 13.5 ± 0.16 c 0.70 ± 0.03 b 25.7 ± 1.4 b 42.7 ± 5.5 b
Data are expressed as mean ± S.E.M. Different letters indicate significant difference (P b 0.05).
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3. Results No fish died during the experiment. All data recorded and calculated at the end of the experiment according to temperature and feeding frequency are presented in Tables 1 and 2. First of all, temperature and feeding regime interacted on fish weight gain (Table 1). Weight gain was the lowest at 20 °C whatever the feeding regime tested, ranging from 5.6 to 6.9 g and the highest at 28 °C when fish were fed 3 times a day (WG = 14.4 g). For each feeding regime, weight gain significantly increased with temperature. At 24 °C, growth was reduced when fish were fed once a day compared to the growth of fish fed 3 or 6 times a day. At 28 °C, the weight gains of fish groups fed once or 6 times a day were not significantly different. SGR increased significantly with water temperature, from 1.2% d− 1 at 20 °C to 2.0% d− 1 at 28 °C (Table 3). It was also influenced by feeding frequency and was lower in groups fed once than in groups fed 3 times a day (Table 4). SGR of fish fed 6 times a day did not differ significantly from the two other treatments. Temperature and feeding regime independently influenced fish feed intake and feed efficiency. Total feed intake significantly increased with water temperature and feeding frequency. Feed efficiency also significantly increased with water temperature, while it was higher in fish fed once or 3 times a day than in fish fed 6 times a day. Carcass lipid content did not differ between treatments. It ranged from 5.7 to 7.4% according to the water temperature and from 5.9 to 6.7% according to the feeding regime applied. Carcass protein content was significantly higher at 20 °C and 24 °C than at 28 °C (Table 3). PRE and LRE were higher when fish were fed once or 3 times a day than when they were fed 6 times a day. Regardless of temperature, SGR and feed efficiency were maximal when fish were fed 3 times a day. Consequently, for each rearing temperature, the optimal feeding rate was estimated according to the experimental data (weight and feed efficiency) obtained on fish fed 3 times a day. As a result, optimal feeding rates (expressed in percent of fish biomass per day) that maximized growth under our laboratory conditions were found to be 1.5% at 20 °C, 1.8% at 24 °C and 2% at 28 °C, taking 13.0, 16.9 and 20.8 g for W56 and 0.825, 0.965 and 1.06 for FE respectively. 4. Discussion To our knowledge, this study was the first to investigate the concurrent effects of temperature and feeding on pikeperch growth. Our results are globally in accordance with the data available in the literature. The SGR value of fish reared at 24 °C (1.6% d− 1) was close to that of pikeperch reared under similar temperature conditions in other studies (SGR of 1.35–1.5% d− 1), (Schulz et al., 2005; Molnar et al., 2006). First of all, weight gain, SGR and feed efficiency were higher in fish held at 28 °C than in fish held at 20 or 24 °C. Therefore, our study demonstrates for the first time that optimal temperature for pikeperch early ongrowing is clearly higher than temperatures that have been applied in previous experiments and is probably around 28 °C, as suggested by Hokanson (1977) and Hilge and Steffens (1996). It makes it one of the most thermophilic Percid species studied so far and is similar to what is found in some Cyprinids such as tench (Tinca tinca), roach (Rutilus rutilus), goldfish (Carassius auratus) and in European catfish (Silurus glanis), (Hilge, 1985; Wolnicki and Korwin-Kossakowski, 1993; Kestemont, 1995; Van Dijk et al., 2002). Nevertheless, some authors have reported that optimal temperature may decrease with fish weight in some species like African catfish (Clarias gariepinus), carp (Cyprinus carpio), Atlantic cod (Gadus morhua) or Atlantic halibut (Hippoglossus hippoglossus), (Hogendoorn et al., 1983; Cuenco et al., 1985; Bjornsson and Tryggvadottir, 1996; Bjornsson et al., 2007). Consequently, as recommended by Ronyai and Csengeri
(2008), the effect of temperature on growth should be further investigated for larger pikeperch from 100 g to 1–2 kg, which is the commercial size range. Feed efficiencies were the highest when fish were fed once or 3 times a day and a more frequent hand-feeding did not lead to an increase of growth despite a higher feed intake. This suggests that the amount of feed ingested by pikeperch fed 3 times a day is probably close to the optimal amount for which growth is maximal. This is in accordance with the conclusions of Alanara et al. (2001) and Booth et al. (2008) who claimed that one to four meals per day may be sufficient for Salmonids and Australian snapper (Pagrus auratus) to achieve maximum feed intake and growth. Reasons for which growth significantly decreased when fish were fed 6 times a day at 28 °C are unclear. According to Johansen and Jobling (1998), repeated feeding throughout long periods of the day would increase swimming activity of fish, resulting in energy expenditure and lower growth rate. Besides, fish carcass protein content decreased with increasing water temperature, as observed by Peres and Oliva-Teles (1999) in juvenile seabass (Dicentrarchus labrax), suggesting a modulation of protein metabolism by temperature. Protein and lipid retentions decreased with increasing feeding frequency as observed in turbot fed increasing amount of food (Van Ham et al., 2003). According to these authors, lower protein and lipid retentions could be explained by a higher energy requirement for feed assimilation at higher feed consumption, which is usually accompanied by reduced nutrient absorption. Thus, it appears that in juvenile pikeperch, a feeding frequency of 3 times a day would be close to the upper limit at which growth and feed efficiency are maximized. Therefore, for each temperature, we chose to estimate the optimal feeding rates at this feeding frequency. The rate found for pikeperch held at 24 °C (1.8% of fish biomass per day) was identical to the one given by the model of Mélard et al. (1996) for Eurasian perch of same weight reared at 23 °C. From our results, we conclude that optimal feeding rate at 28 °C may be about 2% of fish body weight when distributed 3 times a day. However, we are aware that other factors that were not taken into account in this study might interact with temperature, especially feed composition or photoperiod. For example, Zakes et al. (2003) also found an optimal feeding rate of 2% for pikeperch of 25–70 g despite their fish were reared at only 22 °C. In their study, feed protein and lipid contents were higher than in our experiment (54:18 vs 46:12 P:L respectively). In addition, feed delivery was continuous over 19 h per day and fish were held under continuous lighting, while we applied a 12L:12D photoperiod. Nyina-Wamwiza et al. (2005) have shown that the protein/lipid ratio of the diet has an impact on pikeperch growth. However, Gardeur et al. (2007) have pointed out the fact that temperature and photoperiod play a more important role than feeding frequency or feed lipid content in the determinism of Eurasian perch growth. Therefore, taken together, the results suggest that rearing pikeperch at 28 °C under a daylength period longer than 12 h might be an effective method to enhance fish growth. At this photoperiodic regime, optimal feeding rate would probably be more than 2%.
5. Conclusion This study was the first to investigate the optimal rearing temperature and feeding rate in small juvenile pikeperch. It was shown that rearing pikeperch juvenile at 28 °C, giving 3 meals per day clearly enhances growth. Following this procedure, a feeding rate of 2% might be an optimal one to maximize growth. Further experiments should address these questions for bigger fish classes (i.e. 100–2000 g) as optimal rearing temperature may decrease with fish weight. In addition, pikeperch ongrowing requires more information about the effects of other major factors like photoperiod.
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