Feasibility of Partial Replacement of Fishmeal with Proteins from Different Sources in Diets of Korean Rockfish (Sebastes schlegeli)

YAN Quangen, ZHU Xiaoming YANG Yunxia HAN Dong and XIE Shouqi

1) Institute of Hydrobiology, The Chinese Academy of Sciences; State Key Laboratory of Freshwater Ecology and Biotechnology, Wuhan 430072, P. R. China

2) University of Chinese Academy of Sciences, Beijing 100049, P. R. China

Feasibility of Partial Replacement of Fishmeal with Proteins from Different Sources in Diets of Korean Rockfish (Sebastes schlegeli)

YAN Quangen1),2), ZHU Xiaoming1), YANG Yunxia1), HAN Dong1), and XIE Shouqi1),*

1) Institute of Hydrobiology, The Chinese Academy of Sciences; State Key Laboratory of Freshwater Ecology and Biotechnology, Wuhan 430072, P. R. China

2) University of Chinese Academy of Sciences, Beijing 100049, P. R. China

An 8-week feeding experiment was conducted in an indoor recirculation seawater system to investigate the effects of partial replacement of dietary fishmeal with proteins from five sources on the growth performance and feed utilization of Sebastes schlegeli. Six isonitrogenous and isoenergetic diets were formulated using fishmeal (FM, the control) as sole protein source, or proteins from five sources including poultry by-product meal (PBM), meat and bone meal (MBM), soybean meal (SBM), cottonseed meal (CSM) and canola meal (CNM). Fifteen percent of the crude protein provided by fish meal was replaced, respectively. The results showed that the differences in specific growth rate (SGR) and survival rate (SR) among fish fed PBM, MBM, SBM, CSM and whole FM diets were not significant. However, SGR and SR of fish fed CNM diet was significantly lower than that of other treatments. Feeding rate, feed conversion, nutrient retention showed similar patterns to that of growth. Fish fed CSM and CNM showed significantly lower apparent digestibility coefficient (ADC) of dry matter and gross energy than those fed others while fish fed CNM showed lower ADC of crude protein than those fed others (P<0.05). These results suggested that it was feasible to substitute 15% dietary protein provided by fishmeal with PBM, MBM, SBM and CSM, respectively, but not with CNM as the replacement with CNM reduced fish growth and feed utilization.

replacement; fishmeal; protein source; growth performance; feed utilization; Sebastes schlegeli

1 Introduction

Due to the shortage of natural resources, fishmeal price is continuously increasing, and subsequently feed cost is maintaining high. Thus, reducing fishmeal supple- mentation in aqua-feed becomes an urgent issue, especially in the feed of carnivorous fish, in which fishmeal is basic dietary protein. A number of studies on fishmeal replacement have been conducted all over the world and a rapid progress has been made (Gatlin et al., 2007; Cheng et al., 2010; Lin et al., 2011; Burr et al., 2012).

Rendered animal protein ingredients, mainly poultry by-product meal (PBM) and meat and bone meal (MBM), are economical sources of rich proteins. However, the use of most of these products has been greatly limited for various reasons, such as poor digestibility and quality instability. The composition and freshness of the raw materials can have significant effects on the nutritional quality (Kureshy et al., 2000). The heat treatment required for cooking and drying the raw material may result in either change in protein or damage to amino acids and other nutrients through oxidation of sulfhydryl (-SH) bonds into disulphide bonds (S-S), non-peptide crosslinking, Maillard reactions, oxidative degradation, and even pyrolysis (Otterburn, 1989; Phillips, 1989). In addition, PBM and MBM tend to be methionine deficient and ash content high.

Plant sources of proteins such as soybean meal (SBM), cottonseed meal (CSM), and canola meal (CNM) are also widely used in fish feeds. Soybean meal is believed to be one of the most promising, which has been widely used as a source of proteins in fish feeds due to its relatively acceptable amino acid profile, consistent composition, and steady supply at a reasonable price (Dersjant-Li, 2002; Gatlin et al., 2007). However, soybean meal has potential problems associated with insufficient levels of lysine and methionine, presence of anti-nutritional factors, and poor palatability (Dersjant-Li, 2002; Gatlin et al., 2007). Additionally, soybean meal contains low levels of available minerals such as phosphorus. Rapeseed meal has been the object of numerous studies in rainbow trout as potential substitute of fish meal (McCurdy and March, 1992; Go-mes et al., 1993). While the advantage of rapeseed meal is the quality of its proteins, it contains a high quantity of fibre and other anti-nutrition factors, such as tannins, sinapin and phytic acid. Rapeseeds are also known to contain glucosinolates, whose metabolites have a goitrogenic activity in all animals including fish (Higgs et al., 1982; Teskeredžić et al., 1995). However, the quality of rapeseed meal has been considerably improved with the breeding of new varieties (Brassica napus and Brassica campestris), namely Canola, which are low in both glucosinolates (antithyroid factors) and erucic acid (Higgs et al., 1983). Cottonseed meal (CSM) has been used in animal feeds since early 20th century. Gossypol is the main anti-nutrition factor restricting the use of CSM in animal feeds (Gatlin et al., 2007; Cai et al., 2011).

Korean rockfish (Sebastes schlegeli), a carnivorous demersal species, is an important cultured species in China and other Asian countries. The protein requirement of S. schlegeli is relatively high (Kim et al., 2001). Thus, the replacement of dietary fishmeal by proteins from other sources is especially important for S. schlegeli. The present study was conducted, aiming to investigate the effects of partially replacing fishmeal (15% of the crude protein provided by fish meal) by proteins from different sources on the growth performance, feed utilization and body composition of S. schlegeli. The protein sources tested included poultry byproduct meal, meat and bone meal, soybean meal, cottonseed meal and canola meal.

2 Materials and Methods

2.1 Culture System

The feeding trial was conducted in 18 conical aquariums (Φ, 47–57 cm; V, 84 L) in an indoor recirculating seawater system (3 L min-1). Through filtering cotton, water from the aquariums flows to a filtering pool with activated carbon and coral, and then was pumped to a sedimentation tank (1.8 m3). After sand-filtered in the sedimentation tank, the water flows back to the aquariums. During the experiment, the tank water temperature ranged from 17 to 22℃, salinity from 30 to 34 and acidity from pH7.6 to pH8.5, and dissolved oxygen was maintained > 5 mg L-1and ammonia nitrogen < 0.4 mg L-1. The photoperiod was 12 L (7:00–19:00): 12 D (19:00– 7:00).

2.2 Experimental Diets

Six isonitrogenous (44%–45% crude protein of dry matter) and isoenergetic (17–18 kJ g-1gross energy of dry matter) diets were formulated. The control (FM diet) was formulated using fishmeal (FM) as a sole protein source. The other 5, PBM, MBM, SBM, CSM and CNM diets, were formulated by replacing 15% of the crude protein provided by fish meal used in control with poultry by-product meal (PBM), meat and bone meal (MBM), soybean meal (SBM), cottonseed meal (CSM) and canola meal (CNM), respectively. An inert digestion indicator (1% Cr2O3) was supplemented in each diet to determine the apparent digestibility of nutrients. The chemical composition and supplier of the alternative protein sources used in this experiment were presented in Table 1.

The formulation and chemical composition of the experimental diets were presented in Table 2. All ingredients were thoroughly mixed. The dough was cold-press pelleted (Φ 2–3 mm) with a laboratory feed pelleter. The diets were dried at 50℃ and stored at -17℃ until used.

Table 1 Chemical composition of protein sources used in the present experiment†

2.3 Experimental Procedure

The fish used in this experiment were captured from offshore area of Qingdao. The fish was first immersed with salt and then transferred to cement pool (5 m×3 m× 1.2 m; 14 m3). After 3 weeks acclimation to the pellet diets, the fish was transferred to the recirculating seawater system. Then the fish was fed experimental diets (the mixture of 6 experimental diets) twice a day (9:00 and 15:00) for 2 weeks to acclimate to the experimental diet and condition.

At the initiation of the experiment, the fish (average body weight 7.75 g ± 0.03 g) were fasted for 24 h. Apparently healthy fish of similar sizes were selected for the experiment and weighed. A total of 270 fish individuals were randomly distributed into 18 aquariums, 15 each. Triplicate groups of 10 fish were sampled randomly as initial samples for the assay of chemical composition and energy. During the experimental period, the fish was fed to satiation twice a day (9:00 and 15:00). The feed remnant was collected 1 h after feeding, dried at 70℃ and weighed. From day 10 after the initiation of the experiment, fresh and intact feces were collected daily. After slightly washed with fresh water to remove the impurities and salt, the feces was dried at 70℃ and stored at -20℃. The feeding trial lasted for 8 weeks. At the termination ofthe experiment, all of the experimental fish were fasted for 24 h before harvest. Five fish each aquarium were weighed, dried at 70℃ and stored for the assay of chemical composition and energy. The leaching rate of experimental diets in the experimental condition was determined to correct the feeding rate.

Table 2 Formulation and chemical composition of the experimental diets (g kg-1in dry matter)

2.4 Analysis and Measurement

The dry matter, crude protein, crude lipid, ash, and energy contents in diets and fish body, the crude protein and energy content in feces were assayed. The protocol followed the AOAC (1984) guidelines. Briefly, samples of diets and fish were dried to constant weight at 105℃ to determine dry matter. Crude protein was determined by measuring nitrogen (N×6.25) using the Kjeldahl method. Lipid was determined using chloroform-ether extraction (Wang et al., 1993); and ash by combustion at 550℃ and energy by Phillipson microbomb calorimeter (Gentry Instrument Inc., Aiken, USA). The Cr2O3contents in diets and feces were determined using the method described by Bolin et al. (1952). Three replicates were used when the Cr2O3content was determined.

2.5 Calculation of Variables

The following variables were calculated:

Protein retention efficiency (PRE, %)=

Energy retention efficiency (ERE, %)=

where Wtand W0were final and initial fish weight, respectively; t was the experimental duration in day; I was total feed intake during the experimental period; Ptand P0were final and initial protein content of fish body, respectively; Etand E0were gross energy content of final and initial fish body, respectively; P and E were crude protein and gross energy content of diet, respectively; Ntand N0were final and initial number of fish, respectively. All weight in the equations refers to wet weight.

Apparent digestibility coefficients (%) were calculated as follows:

Apparent digestibility coefficient of protein (energy) (%)

where C1and C2were Cr2O3content in diet and feces, respectively; X1and X2were protein (energy) content in diet and feces, respectively. The equation calculates apparent digestibility coefficient of dry matter when X2= X1=1.

2.6 Statistical Analysis

All data were subjected to one-way analysis of variance (one-way ANOVA) in Statistical 6.0 for Windows. Differences among the means were tested by Duncan’s multiple range tests. The level of significance was chosen at P < 0.05.

3 Results

3.1 Feeding Rate

No significant differences in feeding rate (FR) were observed among fish fed PBM, MBM, SBM and the control diet (P > 0.05) (Table 3). However, fish fed CSM and CNM diet showed significantly lower FR compared to the control diet (P < 0.05).

3.2 Apparent Digestibility Coefficient

The apparent digestibility coefficient (ADC) of dry matter in fish fed CSM and CNM diets was significantly lower than that in fish fed PBM, MBM, SBM and control diets (P < 0.05), and the lowest ADC of dry matter wasfound in fish fed CNM diet (Table 3). There were no significant differences in ADC of dry matter among PBM, MBM, SBM and control diets (P > 0.05). The ADC of protein in fish fed CNM diet was significantly low compared to that in fish fed PBM, MBM, SBM and control diets (P < 0.05), and no significant difference in ADC of protein was observed among PBM, MBM, SBM, CSM and control diets (P > 0.05). The ADC of energy in fish fed control diet was significantly higher than that in fish fed SBM, CSM and CNM diets (P < 0.05), and no significant difference in ADC of energy was observed among PBM, MBM and control diets (P > 0.05).

Table 3 Apparent digestibility coefficient of juvenile Korean rockfish fed diets containing proteins from different sources

3.3 Growth and Feed Utilization

Fish fed CNM diet showed significantly lower final body weight and specific growth rate (SGR) compared to the control and other groups (P < 0.05), and no significant differences were observed between the fish fed PBM, MBM, SBM, CSM and the control diet (P > 0.05) (Table 4). The feed conversion ratio (FCR) in fish fed CNM diet was significantly higher than that in other groups (P < 0.05). The protein retention efficiency (PRE) in fish fed PBM diet was significantly higher compared to other groups (P < 0.05) except the CSM group (P > 0.05). Fish fed CNM diet showed significantly lower PRE compared to other groups (P < 0.05). No significant differences in PRE were observed among MBM, SBM, CSM and the control group (P > 0.05). The energy retention efficiency (ERE) and survival rate (SR) had the same pattern as that of SGR.

Table 4 Growth performance and feed utilization of juvenile Korean rockfish fed diets containing proteins from different sources

3.4 Chemical Composition of Whole Fish Body

The dry matter and gross energy contents in fish fed CSM diet were significantly lower than that of the control group (P < 0.05) (Table 5). The dry matter, crude protein, crude lipid and gross energy contents in fish fed CNM diet were significantly lower than that of other groups (P < 0.05). No significant difference in protein and lipid contents was observed among PBM, MBM, SBM, CSM and control diets (P > 0.05). There was no signifycant difference in ash content of whole fish body among diets tested (P > 0.05).

Table 5 Body composition of juvenile Korean rockfish fed diets containing proteins from different sources†

4 Discussion

PBM is cheaper than fishmeal, while it contains protein similar to fishmeal (56.4%–84.2%). Some essential amino acids of PBM is lower than that of fishmeal. (Shiau, 2008; Yu, 2008). Early studies on the apparent digestibility of PBM revealed that PMB is digestible for rainbow trout and Atlantic cod (Bureau et al., 1999; Tibbetts et al., 2006). In Korean rockfish, the dry matter digestibility, protein digestibility, and protein retention efficiency of PMB were higher than those in fish fed fishmeal-based control diet, thus making fish grow faster than those fed other diets. This indicated that PBM is highly potent for being formulated into Korean rockfish diet. This finding is in accordance with the documented in juvenile African catfish diet (40% of total protein is replaced with PBM) (Abdel-Warith et al., 2001) and hybrid striped bass (nearly half is replaced with PMB) (Rawles et al., 2006). In gibel carp and humpback grouper diets, good quality PBM could replace more than half of the protein from marine fish meal (Yang et al., 2006; Shapawi et al., 2007).In tilapia and gilthead bream diets, 100% fishmeal could be replaced by PBM without a significant influence on growth performance (El-Sayed 1998; Nengas et al., 1999). PBM seems to be a good source of dietary protein for Korean rockfish culture.

MBM is less efficiently utilized than PMB by fish due to its low crude protein digestibility and poor amino acids profile (Yang et al., 2004; Ye et al., 2010). The reported replacement of fishmeal by MBM varied between 25% and 45% (El-Sayed, 1998; Bharadwaj et al., 2002; Ai et al., 2006). Such a replacement was even less than 20% in yellowtail diet (Shimeo et al., 1993). A replacement of fishmeal with 5% MBM in juvenile red drum diet significantly depressed its weight gain (Kureshy et al., 2000). In the present study, we found that a replacement of 15% fishmeal crude protein with MBM did not significantly influence the nutrient digestibility and growth performance of Korean rockfish. However, the feeding rate in fish fed MBM-supplemented diets was decreased in comparison with those fed control diet. The poor palatability had been proven to be an important factor inhibiting the utilization of MBM by fish. As was confirmed by studies carried out in gilthead seabream, red drum and hybrid striped bass, replacements of fishmeal with MBM to high percentages reduced the feed intake and subsequently depressed the growth performance of fish (Kureshy et al., 2000; Bharadwaj et al., 2002). The poor palatability is the major adverse factor of dietary MBM for utilization in Korean rockfish diet.

As the sources of animal feed proteins, plant proteins take an portion of replacing fishmeal. Among plant sources of proteins, soybean meal is believed to be one of the most promising, which has been widely used in fish feed (Lin and Luo, 2011). For some omnivorous species, the percentage of replacement may reach as high as 70% (Lin and Luo, 2011). For marine carnivorous species, SBM may replace as high as 10%–40% of fishmeal without reducing the growth and protein utilization of fish (Tantikitti et al., 2005; Wang et al., 2006; Yun et al., 2013). In the present study, fish fed SBM-supplemented diet (15% of fishmeal crude protein) did not significantly reduce the feeding rate, digestibility, growth, survival rate, and feed efficiency, indicating Korean rockfish is able to utilize SBM at a low level to replace fishmeal as Atlantic cod does (Tibbetts et al., 2006).

In comparison with SBM, CSM is a less commonly used plant source in aqua-feed because of its low digestibility, poor amino acid profile, limited availability, variable quality and among others. Free gossypol in CSM is an important toxin to some animals. Previous studies suggested that CSM may replace fishmeal to low percentages (Cheng and Hardy, 2002; Lim et al., 2009). High gossypol content causes not only direct toxic effect on fish tissues, but also the decrease of the availability of lysine as it chelates lysine (Gatlin et al., 2007). In the present study, the feeding rate and nutrient digestibility in Korean rockfish fed CSM were significantly lower than those fed control diet, indicating that the supplementation of CSM reduced the palatability and digestion of diet. Such a scenario was also documented in tilapia (Guimaraes et al., 2008). However, the growth and survival rate of fish fed CSM-supplemented diets were not significantly lower than those fed control diet. This was show that the low substitution percentage of dietary CSM was available for Korean rockfish.

Of all sources of proteins used in the present study, CNM was the only one which significantly reduced the growth and survival rates of Korean rockfish, indicating that Korean rockfish is less able to digest CNM. This finding is in accordance with the documented in Japanese seabass and Chinook salmon. For these fish species, 20%–25% of replacement of fishmeal crude proteins with CNM significantly decreases the growth and feed utilization of fish (Higgs et al., 1982; Cheng et al., 2010). However, some previous studies found that up to 36% of CNM in channel catfish diet did not significantly decrease the growth of fish (Webster et al., 1997). CNM had limiting factors such as low digestible proteins and digestible energy contents, unbalanced amino acid profile, and anti-nutritional factors (mainly fiber, sinapine, tannins and phytic acid), which may subsequently reduce palatability and nutrient digestibility (Bell, 1993; Tibbetts et al., 2006). In the present study, the feeding rate, nutrient digestibility and feed efficiency of Korean rockfish were significantly reduced by supplementary CNM. The poor palatability and deficient utilization of CNM-supplemented diet of Korean rockfish may explain the reduced growth and survival rate of fish observed early (Higgs et al., 1982; Webster et al., 1997; Cheng et al., 2010).

In conclusion, we found that PBM, MBM, SBM and CSM may replace fishmeal in Korean rockfish diet at a low percentage, for example 15% as was tried in this study. We also found that the growth and feed utilization of Korean rockfish were reduced when 15% of dietary fishmeal proteins was replaced with CNM.

Acknowledgements

The authors would like to thank Mr. Guanghan Nie for his technical support and Prof. Qinghui Ai for his kind suggestions to the manuscript. The project was funded by National Key Basic Research Program (2009CB118702), and partly by the Knowledge Innovation Program of the Chinese Academy of Sciences.

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(Edited by Qiu Yantao)

(Received March 15, 2013; revised April 28, 2013; accepted September 18, 2014)

© Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2014

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E-mail: sqxie@ihb.ac.cn