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Effects of feed palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream (Megalobrama amblycephala)
Applied Clay Science 114 (2015) 197–201
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Research paper
Effects of feed palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream (Megalobrama amblycephala) Ruiqiang Zhang, Xue Yang, Yueping Chen, Rui Yan, Chao Wen, Wenbin Liu, Yanmin Zhou ⁎ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu, China
a r t i c l e
i n f o
Article history: Received 27 January 2015 Received in revised form 26 May 2015 Accepted 29 May 2015 Available online 18 June 2015 Keywords: Palygorskite Pellet quality Performance Trace elements Blunt snout bream
a b s t r a c t The study aimed to investigate the effect of feed palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream, Megalobrama amblycephala. Diets without (control group) or with 2% palygorskite were pelleted and were measured for pelleting technological characteristics. Then the diets were fed to two groups of fish in four replicates (30 fish per replicate) for six weeks. Compared with the control group, dietary 2% palygorskite inclusion enhanced pellet production rate, pellet durability and the degree of starch gelatinization of pellet, and reduced percentage of fines. There was no difference in the weight gain, feed conversion rate, condition factor, hepatosomatic index and viscera/body ratio of fish between groups. Palygorskite supplementation significantly enhanced the Fe content in the blood and muscle and Zn content in the muscle, but reduced muscular Cd concentration. However, the accumulations of Cu and Pb in the body were not affected by palygorskite. The results indicated that dietary palygorskite supplementation could enhance pellet production efficiency, pellet quality, and alter trace elements accumulation in the tissues without impairing growth performance of blunt snout bream. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Palygorskite as a magnesium aluminum phyllosilicate is usually present in nature as a fibrillar silicate clay mineral with reactive –OH groups on the surface (Huang et al., 2007; Pappas et al., 2010) and its cation exchange capacity usually ranges between 0.3 and 0.4 meq/g (Murray, 2000). Additionally, palygorskite usually exhibits prominent adhesive and high absorption capacity due to its chemical and physical characteristics (Carretero, 2002; Carretero and Lagaly, 2007; Viseras et al., 2007; Pappas et al., 2010; Zhang et al., 2013). Previous finding has demonstrated that dietary palygorskite inclusion could enhance growth performance of weaned piglets (Zhang et al., 2013), and it can be used as a binding agent to improve feed characteristics of pelleted diets (Pappas et al., 2010). Heavy metals accumulated in the animal would pose a serious threat to human health throughout the food chain (Zhuang et al., 2009). Clay minerals are widely used for the removal of heavy metal ions (Bradl, 2004; Liu et al., 2014). Potgieter et al. (2006) found that the metal ions (Pb and Cr) from aqueous solution can be adsorbed successfully in significant amounts by palygorskite. Meanwhile, montmorillonite ⁎ Corresponding author at: College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Tel.: + 86 25 84396067; fax: + 86 25 84395314. E-mail address: [email protected] (Y. Zhou).
http://dx.doi.org/10.1016/j.clay.2015.05.025 0169-1317/© 2015 Elsevier B.V. All rights reserved.
inclusion has been demonstrated to reduce Cd and Pb accumulation in the tissues of aquatic animals (Kim et al., 2009; Dai et al., 2010). Blunt snout bream (Megalobrama amblycephala) is originally produced in Liangzi Lake in Ezhou (Hubei, China) and its main distribution is in the middle reaches of the Yangtze River (Tsao, 1960). This fish is now widely given feed in pellet form. Pellet characteristics as fines percentage and durability play vital roles in affecting the cost, performance and water environment in fishing industry (Hansen and Storebakken, 2007; Solà-Oriol et al., 2009), and it has received increasing attention in aquaculture industry (Den Hartog and Sijtsma, 2009; Abdollahi et al., 2013). Thus, it is meaningful and necessary to develop an economical artificial pellet feed with optimum quality for blunt snout bream. Currently, little is known about the application effect of palygorskite on the aquatic animals. The present study was therefore conducted to study the effect of palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream.
2. Materials and methods 2.1. Palygorskite Palygorskite was provided by Jiangsu Sinitic Biotech Co., Ltd. (Xuyi, Jiangsu, China). The purity of palygorskite as determined by X-ray
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diffraction was 85% w/w. The contents of all the heavy metals were under the limits of hygienic standard for feeds in China (AQSIQ, 2001). 2.2. Diets The two diets were prepared in the South Jiangsu Feed Co., Ltd. (Wuxi, Jiangsu, China). Formulation and proximate composition of the diets are presented in Table 1. Feed ingredients were milled in a hammer mill (DFZC-1265, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) equipped with a 1.0 mm screen prior to conditioning in a double-shaft conditioner (BCTC10, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) for 65 s. The mash was then pelleted in a pellet mill (DPBS-520.178, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) and was subsequently stabilized in a particle stabilizer (SWDBP5, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China). The electrical energy consumption and pellet production rate during the pellet process were recorded and calculated as described by Cabrera et al. (1994) and Moritz et al. (2002). Cooled pellets were collected in portions of 25 kg in paper bags to determine feed characteristics (6 bags per diet). Durability, the percentage of fines in the pellet and pellet stability in water were determined according to the method described by Zhang (2003). In detail, to measure fines percentage, pellet samples (around 1.5 kg) were placed on a vibratory shaker (XSB-88, Shangyu Laboratory Machinery Plant, Zhejiang, China) equipped with a 2-mm sieve. Pellets were then shaken for 1 min and the amount of pellets that forced through the apertures was collected in a pan located on the base. The percentage of fines was expressed as the percentage of pellets that lost compared with the initial pellets placed. As for durability determination, around 500 g pellet exempted from fines was placed in the pellet durability tester (THB30, Wuxi Taihu Grain Machinery Co., Ltd., Jiangsu, China) for 10 min at the speed of 500 r/min. After that, pellet samples were placed on the vibratory shaker for 1 min. Durability was calculated as the percentage of pellets that forced through the apertures compared to the initial pellets placed. Pellet water stability expressed as dissolved weight loss was calculated as the percentage of pellets which dissolved in the deionized water with temperature of 25 °C and depth of 5.5 cm within 5 min to the initial pellets (on dry matter basis). Degree of starch gelatinization was determined according to the method as described by Zoebel and Stephen (2006). Gelatinized
Table 1 The formulation and proximate composition of the diets (%).
starch was quantitatively converted into reducing sugar by β-amylase in 1 h at 40 °C. Then, ferricyanide method was used to determine the degree of starch gelatinization by measuring the amount of reducing sugars. 2.3. Experimental fish and feeding trial The experimental design and procedures were approved by the Institutional Animal Care and Use Committee of Nanjing Agricultural University (Nanjing, China). Blunt snout bream (M. amblycephala) was obtained from the Fish Hatchery of Yangzhou (Jiangsu, China). Fish were reared in an indoor circulatory system for 1 week to accustom to the experimental conditions by feeding a commercial diet prior to the experiment. After the acclimation, fish of similar sizes (initial average weight, 11.61 ± 0.05 g) were randomly distributed into 8 flowthrough rectangular aquariums (155 L each) with 30 fish per tank. Fish in each aquarium were randomly assigned to one of two experimental diets. Each diet was tested in four replicates. Fish were handfed to apparent satiation three times daily (07:00, 12:00 and 17:00 h) for six weeks. A 12:12 h light:dark regime (07:00–19:00 h, light period) was maintained by timed fluorescent lighting. Water temperature varied from 25 to 28 °C, and pH fluctuated between 7.0 and 7.5. Dissolved oxygen was maintained above 5.00 mg/L during the feeding trial. Total ammonia nitrogen and nitrite nitrogen were maintained below 0.4 mg/L and 0.064 mg/L, respectively.
2.4. Sample collection At the end of the feeding trial, fish were starved for 24 h prior to harvest. Fish were then anesthetized in diluted MS-222 (tricainemethanesulfonate, Sigma, USA) at the concentration of 100 mg/L. The total number and weight of fish in each cage were then determined. Whole blood samples from four fish in each tank were rapidly taken from caudal vessel into heparinized Eppendorf tubes and were stored at − 20 °C until analysis after individual body weight measurement. These fish were later sampled for analysis of viscera/body ratio and hepatosomatic index. Also, individual liver and back muscle were quickly removed and stored at − 20 °C for subsequent analysis. 2.5. Trace element determination
Ingredients
Basal diet
Palygorskite dietc
Fish meal Soybean meal Rapeseed meal Cottonseed meal Wheat Rice bran Wheat middlings Soybean oil Calcium biphosphate Sodium chloride Palygorskite Premixa Proximate composition Moistureb Crude proteinb Crude lipidb Crude fiberb Nitrogen-free extractb
8.00 23.00 14.00 14.00 16.00 13.00 5.00 3.00 2.50 0.50 0.00 1.00
8.00 23.00 14.00 14.00 16.00 13.00 5.00 3.00 2.50 0.50 2.00 1.00
10.50 32.34 6.74 5.08 35.14
10.39 31.70 6.61 4.98 34.45
a Supplied per kg diet the following elements and vitamins: Cu, 5 mg; Fe, 120 mg; Zn, 120 mg; Mg, 100 mg; Mn, 20 mg; Se, 0.25 mg; I, 0.6 mg; Co, 0.07 mg; Vitamin A, 9,000 IU; Vitamin D3, 2,000 IU; Vitamin E, 100 mg; Vitamin K3, 2.2 mg; Vitamin B1, 3.2 mg; Vitamin B2, 10.9 mg; Vitamin B6, 5.0 mg; Vitamin B12, 0.016 mg; Vitamin C, 100 mg; Niacinamide, 10 mg; Pantothenic, 20 mg; Folic acid, 3 mg; Choline, 600 mg; Biotin, 0.15 mg; Inositol, 200 mg. b Calculated level. c Basal diet supplemented with 2% palygorskite.
The contents of Fe, Zn, Cu, Pb and Cd in the diets, blood, fresh liver and muscle samples were measured according to the method described by Wu et al. (2013). Briefly, approximately 2.0 g of the samples (2 mL for blood) was firstly dissolved in an appropriate amount of 65% nitric acid and perchloric acid (3:1, V/V) and then digested on a heating block, after which they were diluted with ultra-pure water to a final volume of 25 mL. Blanks and standard solutions were prepared. After that, samples were analyzed by inductively coupled plasma mass spectrometry using an Optimal 2100DV instrument (Perkin-Elmer-Sciex, Norwalk, NY, USA) equipped with a standard spray chamber and a cross-flow nebulizer. The measured contents of trace elements in the diets are presented in Table 2. Table 2 Chemical analysis of some elements in the diets (mg/kg). Items
Basal diet
Palygorskite dieta
Fe Cu Zn Pb Cd
1236.64 ± 156.62 13.36 ± 0.16 173.55 ± 11.23 0.16 ± 0.04 0.26 ± 0.04
1332.17 ± 141.60 15.10 ± 0.70 180.84 ± 13.79 0.29 ± 0.04 0.30 ± 0.01
a
Basal diet supplemented with 2% palygorskite.
R. Zhang et al. / Applied Clay Science 114 (2015) 197–201
2.6. Statistical analysis
199
Table 4 Effects of palygorskite inclusion on the pellet technological characteristics.
The data regarding pellet production efficiency was expressed by average value. Other data were analyzed as a completely randomized design using one-way ANOVA by the statistical package for the social sciences (SPSS, 2008). For all tests, the differences were considered to be significant at P b 0.05. The means and standard errors were presented.
Items
Basal diet
Palygorskite dieta
P value
Fines percentage (%) Durability (%) Dissolved weight loss (%) Degree of starch gelatinization (%)
1.50 ± 0.02 97.30 ± 0.10 13.86 ± 1.14 44.24 ± 0.28
1.10 ± 0.04 97.52 ± 0.15 11.52 ± 1.56 49.88 ± 1.63
0.001 0.287 0.294 0.021
a
Basal diet supplemented with 2% palygorskite.
3. Results 3.1. Pellet characteristics Compared with the control group, supplementation of palygorskite enhanced the feed pellet production rate by 5.26% (Table 3). As indicated in Table 4, palygorskite inclusion enhanced the degree of starch gelatinization (P = 0.021) and decreased the percentage of fines (P = 0.001). The durability and water stability of pellets were improved by palygorskite inclusion as evidenced by the numerically higher pellet durability and lower dissolved weight loss though not significantly (P N 0.05). 3.2. Growth performance There were no significant differences (Table 5) in the final body weight, weight gain or feed conversion ratio (P N 0.05) of blunt snout bream between the two groups. Similarly, dietary palygorskite supplementation did not affect the condition factor, hepatosomatic index or viscera/body ratio (P N 0.05). 3.3. Trace element content As indicated in Table 6, compared with the control group, palygorskite supplementation significantly enhanced the Fe content in the blood (P = 0.023) and muscle (P = 0.005) as well as Zn content in the muscle (P = 0.013). In contrast, palygorskite reduced muscular Cd accumulation (P = 0.026). Pb was not detected in the blood and muscle. The content of other trace elements were unaffected by palygorskite inclusion even though the Cu content in the liver was numerically lower than that of the control (P N 0.05). 4. Discussion The pellet production rate was enhanced in the present study, indicating that palygorskite supplementation can improve the production efficiency during the feed manufacture. The pellet process of animal feed is largely affected by the following factors including feed composition, particle size, inclusion of binders and other factors related to the process of pelleting per se such as conditioning, distance between roller and die and hole compression (Angulo et al., 1995, 1996; Pappas et al., 2010). Physical pellet durability usually expressed as pellet durability index (ASAE, 1997) is defined as the ability of pellet to withstand fragmentation and abrasion during mechanical and pneumatic handling as bagging, storage and transport without breaking up and generating a high proportion of fines (Cramer et al., 2003). Pellet water stability is another important parameter to evaluate the quality of aquaculture feed (Obaldo et al., 2002; Sørensen et al., 2010). High pellet water stability is defined as the retention of pellet physical integrity with minimal Table 3 Effects of palygorskite inclusion on pellet production efficiency.
Items
Basal diet
Palygorskite dietf
P value
Initial body weight (g) Final body weight (g) Weight gain (%)a Feed conversion ratiob Condition factor (%)c Hepatosomatic index (%)d Viscera/body ratio (%)e
11.58 ± 0.05 17.68 ± 0.13 52.77 ± 1.68 2.34 ± 0.14 2.22 ± 0.08 2.07 ± 0.16 14.38 ± 0.74
11.66 ± 0.09 17.64 ± 0.78 51.23 ± 5.75 2.35 ± 0.25 2.17 ± 0.06 2.21 ± 0.17 14.42 ± 0.49
0.478 0.954 0.810 0.949 0.610 0.570 0.901
Weight gain (WG, %) = (Wt − W0) × 100 / W0. Feed conversion ratio (FCR) = feed consumption (g) / fish weight gain (g). Condition factor (CF, %) = (W/L3) × 100 (W = body wet weight in grams, L = length in centimeters). d Hepatosomatic index (HSI, %) = liver weight (g) × 100 / body weight (g). e Viscera/body ratio (VBR, %) = viscera weight (g) × 100 / wet body weight (g). f Basal diet supplemented with 2% palygorskite. b
Basal diet
Palygorskite diet
Pellet production rate (ton/h) Electrical energy consumption (kWh/ton)
5.70 10.16
6.00 10.12
Basal diet supplemented with 2% palygorskite.
Table 5 Effects of palygorskite inclusion on the growth performance of blunt snout bream.
a
Items
a
disintegration and nutrient leaching while in the water until consumed by the animal. Clays can be incorporated as agglomerant in animal diets in order to improve feed manufacture (Angulo et al., 1995; Xia et al., 2004; Pappas et al., 2010). In the present study, we found that dietary 2% palygorskite inclusion significantly reduced the fines percentage in pellet. Meanwhile, the durability and water stability of pellets were also improved by palygorskite supplementation. Similar result was observed by Pappas et al. (2010) in which pellets manufactured with 1% added palygorskite showed better pellet quality than these manufactured without palygorskite. The decreased fines percentage could result from special sorptive and colloidal–rheological properties of palygorskite, which are the basis for its most technological applications (Galan, 1996; Liu, 2007; Pappas et al., 2010). Palygorskite could absorb polar liquids and forms gels due to its characteristics, which may in turn improve durability and therefore result in reduced fines percentage and dissolved weight loss possibly by increasing solid– solid bonding interactions (Pappas et al., 2010). Starch gelatinization is the process where starch and water are subjected to heat and it can cause starch granules to swell (Lund and Lorenz, 1984). Gelatinization opens the granule's structure and thus enzymes can enter the starch granules, markedly increasing susceptibility for amylolytic degradation (Rooney and Pflugfelder, 1986). Previous studies have shown that the digestibility of starch can be enhanced by gelatinization (Wilson, 1994; Stone et al., 2003; Krogdahl et al., 2005). Aside from heat, water play vital role in the starch gelatinization (Lund and Lorenz, 1984) and is a prerequisite to initiate starch gelatinization. In this study, palygorskite inclusion improved the degree of starch gelatinization, and this may be due to its high absorption and adsorption capacity for moisture that could hold more moisture, which can facilitate starch gelatinization (Thomas et al., 1998). The enhanced starch gelatinization induced by palygorskite inclusion may also contribute to the simultaneous improvements in the fines percentage, durability and dissolved weight loss since gelatinized starch has a potential to act as a binder. The higher pellet production rate may also result from the more moisture which would aid in lubricating the pellet die (Moritz et al., 2003). In the current study, we noticed that fish fed diet supplemented with palygorskite showed similar growth performance to those given basal diet, which indicated that 2% palygorskite supplementation would not impair the growth performance of fish. Zhang et al. (2013) reported
a
c
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Table 6 Effects of palygorskite inclusion on some trace elements content of blood, liver and muscle in blunt snout bream. Items
Basal diet
Palygorskite dieta
P value
Blood (mg/L) Fe Cu Zn Pb Cd
218.62 ± 10.73 0.77 ± 0.01 2.53 ± 0.11 – 0.016 ± 0.007
258.38 ± 2.50 0.76 ± 0.01 2.38 ± 0.01 – 0.018 ± 0.005
0.023 0.323 0.292 – 0.876
Liver (mg/kg) Fe Cu Zn Pb Cd
79.23 ± 10.85 11.99 ± 0.81 30.82 ± 5.56 0.250 ± 0.004 0.105 ± 0.015
75.43 ± 1.19 9.54 ± 0.41 33.62 ± 3.20 0.376 ± 0.046 0.098 ± 0.007
0.760 0.054 0.685 0.113 0.699
Muscle (mg/kg) Fe Cu Zn Pb Cd
2.66 ± 0.64 0.49 ± 0.04 5.47 ± 0.05 – 0.018 ± 0.002
7.02 ± 0.43 0.42 ± 0.06 7.55 ± 0.48 – 0.009 ± 0.002
0.005 0.382 0.013 – 0.026
a
Basal diet supplemented with 2% palygorskite.
that palygorskite supplementation at level of 2000 mg/kg improved feed conversion ratio in weaned piglets, but a higher inclusion of palygorskite at level of 3000 mg/kg exerted no beneficial effects on the growth performance. However, Pappas et al. (2010) found that 1% palygorskite supplementation to a corn–soybean based diet did not have detected effects on the body mass, feed conversion ratio as well as mortality of broilers, which was similar to the results in the present study. These discrepancies regarding the application effect of palygorskite in animal nutrition aforementioned may be due to the animal species, properties of palygorskite and dosage. It is worthy to note that fish fed diet supplemented with palygorskite achieved similar growth performance to those fed basal diet even though the nutrient content as crude protein and energy were numerically lower in the palygorskite diet. Palygorskite inclusion could enhance growth performance due to the absorption capacity of adverse factors occurred in the feed and a reduction in intestinal impairment in weaned piglets (Zhang et al., 2013). Also, it has been reported that palygorskite can improve the activities of intestinal digestive enzymes and improve intestinal morphology (Qiao et al., 2015). These factors may together contribute to the similar performance found in our study. Palygorskite supplementation significantly enhanced Fe content in the blood and muscle, and Zn content in the muscle. However, Tang et al. (2014) found that dietary palygorskite inclusion from 1800 to 3000 mg/kg did not affect serum and fecal Zn content in the weaned piglets. The discrepancy may be due to the animal species, measured organs, inclusion rate and especially the source of the palygorskite. For the clay application in aquatic animals, Kim et al. (2009) have found that inclusion of montmorillonite decreased Cd accumulation in tissues as muscles and kidney of carp, Carassius auratus. Cd is one of the most deleterious xenobiotics in aquatic ecosystems. Freshwater fish are particularly vulnerable to Cd exposure that can induce renal damage, hypertension, proteinuria and testicular atrophy (ATSDR, 1999), and would finally result in economic loss in fish industry (Zirong and Shijun, 2007). In the present study, palygorskite supplementation reduced the Cd content in the muscle, indicating that the palygorskite could also help to improve the safety of bream products, and this was likely to result from palygorskite's high absorption and adsorption capacity (Viseras et al., 2007). Similarly, in an in vitro study, ÁlvarezAyuso and García-Sánchez (2007) found that palygorskite could successfully remove Cd from aqueous solution and the sorption process appeared to be relatively fast. Heavy metal as Cd and Pb would compete with Fe and Zn in absorption in intestine (Hamilton et al., 1978; Cerklewski, 1984; Flora et al., 1989). Thus, the decreased Cd
accumulation and the enhanced Fe, Zn content may result from their antagonist effect. The purity of palygorskite would affect its adsorption behavior (Zhou and Murray, 2003). In an in vitro study by Shirvani et al. (2006), the common associated mineral of palygorskite, calcite, exhibited an inferior adsorption capacity for Cd, indicating the content of associated minerals can affect the physical and chemical properties of palygorskite and a higher purity can facilitate its application. However, the most widely used palygorskite in animal feed is the natural palygorskite and its application effect on animals including growth performance, nutrient utilization and immunity is the key point that animal nutritionists care. In conclusion, dietary 2% palygorskite inclusion could enhance pellet production efficiency, pellet quality, and trace element content, and reduce Cd accumulation in the tissues without impairing the growth performance of blunt snout bream. Also, palygorskite as an ingredient could be applied to other aquatic animals feeds according to its beneficial effect in the current study. Acknowledgments The study is funded by the Jiangsu Provincial Cooperative Innovation Fund–Prospective Joint Research Project (BY2012206) and the National Technology System for Conventional Freshwater Fish Industries of China (CARS-46-20). References Abdollahi, M.R., Ravindran, V., Svihus, B., 2013. Pelleting of broiler diets: an overview with emphasis on pellet quality and nutritional value. Anim. Feed Sci. Technol. 179, 1–23. Álvarez-Ayuso, E., García-Sánchez, A., 2007. Removal of cadmium from aqueous solutions by palygorskite. J. Hazard. Mater. 147, 594–600. Angulo, E., Brufau, J., Esteve-Garcia, E., 1995. Effect of sepiolite on pellet durability in feeds differing in fat and fibre content. Anim. Feed Sci. Technol. 53, 233–241. Angulo, E., Brufau, J., Esteve-Garcia, E., 1996. Effect of a sepiolite product on pellet durability in pig diets differing in particle size and in broiler starter and finisher diets. Anim. Feed Sci. Technol. 63, 25–34. AQSIQ, 2001. GB/T 13078-2001, Hygienical Standard for Feeds. General Administration of Quality Supervision. Inspection and Quarantine of the People's Republic of China, China. ASAE, 1997. Cubes, pellets and crumbles-definitions and methods for determining density, durability and moisture. ASAE Standard 269.4. Agricultural Engineers Yearbook of Standards. American Society of Agricultural Biological Engineers. St. Joseph, MI, USA. ATSDR, 1999. Agency for Toxic Substances and Disease Registry, Department of Health and Human, Services, USA. Bradl, H.B., 2004. Adsorption of heavy metal ions on soils and soils constituents. J. Colloid Interface Sci. 277, 1–18. Cabrera, M.R., Hancock, J.D., Bramel-Cox, P.J., Hines, R.H., Behnke, K.C., 1994. Effects of corn, sorghum genotype, and particle size on milling characteristics and growth performance in broiler chicks. Poult. Sci. 73, 11. Carretero, M.I., 2002. Clay minerals and their beneficial effects upon human health. A review. Appl. Clay Sci. 21, 155–163. Carretero, M.I., Lagaly, G., 2007. Clays and health: an introduction. Appl. Clay Sci. 36, 1–3. Cerklewski, F.L., 1984. Postabsorptive effect of increased dietary zinc on toxicity and removal of tissue lead in rats. J. Nutr. 114, 550–554. Cramer, K.R., Wilson, K.J., Moritz, J.S., Beyer, R.S., 2003. Effect of sorghum-based diets subjected to various manufacturing procedures on broiler performance. J. Appl. Poult. Res. 12, 404–410. Dai, W., Du, H., Fu, L., Liu, H., Xu, Z., 2010. Effect of montmorillonite on dietary lead (Pb) accumulation in tissues of tilapia (Oreochromis niloticus). Appl. Clay Sci. 47, 193–195. Den Hartog, L.A., Sijtsma, S.R., 2009. Influence of Feed Processing Technology on Pig Performance. Recent Advances In Animal Nutrition. p. 227. Flora, S.J.S., Singh, S., Tandon, S.K., 1989. Thiamine and zinc in prevention or therapy of lead intoxication. J. Int. Med. Res. 17, 68–75. Galan, E., 1996. Properties and applications of palygorskite–sepiolite clays. Clay Miner. 31, 443–454. Hamilton, D.L., Bellamy, J.E.C., Valberg, J.D., Valberg, L.S., 1978. Zinc, cadmium, and iron interactions during intestinal absorption in iron-deficient mice. Can. J. Physiol. Pharmacol. 56, 384–389. Hansen, J.Ø., Storebakken, T., 2007. Effects of dietary cellulose level on pellet quality and nutrient digestibilities in rainbow trout (Oncorhynchus mykiss). Aquaculture 272, 458–465. Huang, J., Liu, Y., Jin, Q., Wang, X., Yang, J., 2007. Adsorption studies of a water soluble dye, Reactive Red MF-3B, using sonication-surfactant-modified attapulgite clay. J. Hazard. Mater. 143, 541–548. Kim, S.G., Du, H.H., Dai, W., Zhang, X.F., Xu, Z.R., 2009. Influence of montmorillonite on cadmium accumulation in carp, Carassius auratus. Appl. Clay Sci. 43, 473–476. Krogdahl, Å., Hemre, G.I., Mommsen, T.P., 2005. Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac. Nutr. 11, 103–122.
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Research paper
Effects of feed palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream (Megalobrama amblycephala) Ruiqiang Zhang, Xue Yang, Yueping Chen, Rui Yan, Chao Wen, Wenbin Liu, Yanmin Zhou ⁎ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu, China
a r t i c l e
i n f o
Article history: Received 27 January 2015 Received in revised form 26 May 2015 Accepted 29 May 2015 Available online 18 June 2015 Keywords: Palygorskite Pellet quality Performance Trace elements Blunt snout bream
a b s t r a c t The study aimed to investigate the effect of feed palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream, Megalobrama amblycephala. Diets without (control group) or with 2% palygorskite were pelleted and were measured for pelleting technological characteristics. Then the diets were fed to two groups of fish in four replicates (30 fish per replicate) for six weeks. Compared with the control group, dietary 2% palygorskite inclusion enhanced pellet production rate, pellet durability and the degree of starch gelatinization of pellet, and reduced percentage of fines. There was no difference in the weight gain, feed conversion rate, condition factor, hepatosomatic index and viscera/body ratio of fish between groups. Palygorskite supplementation significantly enhanced the Fe content in the blood and muscle and Zn content in the muscle, but reduced muscular Cd concentration. However, the accumulations of Cu and Pb in the body were not affected by palygorskite. The results indicated that dietary palygorskite supplementation could enhance pellet production efficiency, pellet quality, and alter trace elements accumulation in the tissues without impairing growth performance of blunt snout bream. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Palygorskite as a magnesium aluminum phyllosilicate is usually present in nature as a fibrillar silicate clay mineral with reactive –OH groups on the surface (Huang et al., 2007; Pappas et al., 2010) and its cation exchange capacity usually ranges between 0.3 and 0.4 meq/g (Murray, 2000). Additionally, palygorskite usually exhibits prominent adhesive and high absorption capacity due to its chemical and physical characteristics (Carretero, 2002; Carretero and Lagaly, 2007; Viseras et al., 2007; Pappas et al., 2010; Zhang et al., 2013). Previous finding has demonstrated that dietary palygorskite inclusion could enhance growth performance of weaned piglets (Zhang et al., 2013), and it can be used as a binding agent to improve feed characteristics of pelleted diets (Pappas et al., 2010). Heavy metals accumulated in the animal would pose a serious threat to human health throughout the food chain (Zhuang et al., 2009). Clay minerals are widely used for the removal of heavy metal ions (Bradl, 2004; Liu et al., 2014). Potgieter et al. (2006) found that the metal ions (Pb and Cr) from aqueous solution can be adsorbed successfully in significant amounts by palygorskite. Meanwhile, montmorillonite ⁎ Corresponding author at: College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Tel.: + 86 25 84396067; fax: + 86 25 84395314. E-mail address: [email protected] (Y. Zhou).
http://dx.doi.org/10.1016/j.clay.2015.05.025 0169-1317/© 2015 Elsevier B.V. All rights reserved.
inclusion has been demonstrated to reduce Cd and Pb accumulation in the tissues of aquatic animals (Kim et al., 2009; Dai et al., 2010). Blunt snout bream (Megalobrama amblycephala) is originally produced in Liangzi Lake in Ezhou (Hubei, China) and its main distribution is in the middle reaches of the Yangtze River (Tsao, 1960). This fish is now widely given feed in pellet form. Pellet characteristics as fines percentage and durability play vital roles in affecting the cost, performance and water environment in fishing industry (Hansen and Storebakken, 2007; Solà-Oriol et al., 2009), and it has received increasing attention in aquaculture industry (Den Hartog and Sijtsma, 2009; Abdollahi et al., 2013). Thus, it is meaningful and necessary to develop an economical artificial pellet feed with optimum quality for blunt snout bream. Currently, little is known about the application effect of palygorskite on the aquatic animals. The present study was therefore conducted to study the effect of palygorskite inclusion on pelleting technological characteristics, growth performance and tissue trace elements content of blunt snout bream.
2. Materials and methods 2.1. Palygorskite Palygorskite was provided by Jiangsu Sinitic Biotech Co., Ltd. (Xuyi, Jiangsu, China). The purity of palygorskite as determined by X-ray
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diffraction was 85% w/w. The contents of all the heavy metals were under the limits of hygienic standard for feeds in China (AQSIQ, 2001). 2.2. Diets The two diets were prepared in the South Jiangsu Feed Co., Ltd. (Wuxi, Jiangsu, China). Formulation and proximate composition of the diets are presented in Table 1. Feed ingredients were milled in a hammer mill (DFZC-1265, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) equipped with a 1.0 mm screen prior to conditioning in a double-shaft conditioner (BCTC10, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) for 65 s. The mash was then pelleted in a pellet mill (DPBS-520.178, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China) and was subsequently stabilized in a particle stabilizer (SWDBP5, Bühler Changzhou Machinery Co., Ltd., Jiangsu, China). The electrical energy consumption and pellet production rate during the pellet process were recorded and calculated as described by Cabrera et al. (1994) and Moritz et al. (2002). Cooled pellets were collected in portions of 25 kg in paper bags to determine feed characteristics (6 bags per diet). Durability, the percentage of fines in the pellet and pellet stability in water were determined according to the method described by Zhang (2003). In detail, to measure fines percentage, pellet samples (around 1.5 kg) were placed on a vibratory shaker (XSB-88, Shangyu Laboratory Machinery Plant, Zhejiang, China) equipped with a 2-mm sieve. Pellets were then shaken for 1 min and the amount of pellets that forced through the apertures was collected in a pan located on the base. The percentage of fines was expressed as the percentage of pellets that lost compared with the initial pellets placed. As for durability determination, around 500 g pellet exempted from fines was placed in the pellet durability tester (THB30, Wuxi Taihu Grain Machinery Co., Ltd., Jiangsu, China) for 10 min at the speed of 500 r/min. After that, pellet samples were placed on the vibratory shaker for 1 min. Durability was calculated as the percentage of pellets that forced through the apertures compared to the initial pellets placed. Pellet water stability expressed as dissolved weight loss was calculated as the percentage of pellets which dissolved in the deionized water with temperature of 25 °C and depth of 5.5 cm within 5 min to the initial pellets (on dry matter basis). Degree of starch gelatinization was determined according to the method as described by Zoebel and Stephen (2006). Gelatinized
Table 1 The formulation and proximate composition of the diets (%).
starch was quantitatively converted into reducing sugar by β-amylase in 1 h at 40 °C. Then, ferricyanide method was used to determine the degree of starch gelatinization by measuring the amount of reducing sugars. 2.3. Experimental fish and feeding trial The experimental design and procedures were approved by the Institutional Animal Care and Use Committee of Nanjing Agricultural University (Nanjing, China). Blunt snout bream (M. amblycephala) was obtained from the Fish Hatchery of Yangzhou (Jiangsu, China). Fish were reared in an indoor circulatory system for 1 week to accustom to the experimental conditions by feeding a commercial diet prior to the experiment. After the acclimation, fish of similar sizes (initial average weight, 11.61 ± 0.05 g) were randomly distributed into 8 flowthrough rectangular aquariums (155 L each) with 30 fish per tank. Fish in each aquarium were randomly assigned to one of two experimental diets. Each diet was tested in four replicates. Fish were handfed to apparent satiation three times daily (07:00, 12:00 and 17:00 h) for six weeks. A 12:12 h light:dark regime (07:00–19:00 h, light period) was maintained by timed fluorescent lighting. Water temperature varied from 25 to 28 °C, and pH fluctuated between 7.0 and 7.5. Dissolved oxygen was maintained above 5.00 mg/L during the feeding trial. Total ammonia nitrogen and nitrite nitrogen were maintained below 0.4 mg/L and 0.064 mg/L, respectively.
2.4. Sample collection At the end of the feeding trial, fish were starved for 24 h prior to harvest. Fish were then anesthetized in diluted MS-222 (tricainemethanesulfonate, Sigma, USA) at the concentration of 100 mg/L. The total number and weight of fish in each cage were then determined. Whole blood samples from four fish in each tank were rapidly taken from caudal vessel into heparinized Eppendorf tubes and were stored at − 20 °C until analysis after individual body weight measurement. These fish were later sampled for analysis of viscera/body ratio and hepatosomatic index. Also, individual liver and back muscle were quickly removed and stored at − 20 °C for subsequent analysis. 2.5. Trace element determination
Ingredients
Basal diet
Palygorskite dietc
Fish meal Soybean meal Rapeseed meal Cottonseed meal Wheat Rice bran Wheat middlings Soybean oil Calcium biphosphate Sodium chloride Palygorskite Premixa Proximate composition Moistureb Crude proteinb Crude lipidb Crude fiberb Nitrogen-free extractb
8.00 23.00 14.00 14.00 16.00 13.00 5.00 3.00 2.50 0.50 0.00 1.00
8.00 23.00 14.00 14.00 16.00 13.00 5.00 3.00 2.50 0.50 2.00 1.00
10.50 32.34 6.74 5.08 35.14
10.39 31.70 6.61 4.98 34.45
a Supplied per kg diet the following elements and vitamins: Cu, 5 mg; Fe, 120 mg; Zn, 120 mg; Mg, 100 mg; Mn, 20 mg; Se, 0.25 mg; I, 0.6 mg; Co, 0.07 mg; Vitamin A, 9,000 IU; Vitamin D3, 2,000 IU; Vitamin E, 100 mg; Vitamin K3, 2.2 mg; Vitamin B1, 3.2 mg; Vitamin B2, 10.9 mg; Vitamin B6, 5.0 mg; Vitamin B12, 0.016 mg; Vitamin C, 100 mg; Niacinamide, 10 mg; Pantothenic, 20 mg; Folic acid, 3 mg; Choline, 600 mg; Biotin, 0.15 mg; Inositol, 200 mg. b Calculated level. c Basal diet supplemented with 2% palygorskite.
The contents of Fe, Zn, Cu, Pb and Cd in the diets, blood, fresh liver and muscle samples were measured according to the method described by Wu et al. (2013). Briefly, approximately 2.0 g of the samples (2 mL for blood) was firstly dissolved in an appropriate amount of 65% nitric acid and perchloric acid (3:1, V/V) and then digested on a heating block, after which they were diluted with ultra-pure water to a final volume of 25 mL. Blanks and standard solutions were prepared. After that, samples were analyzed by inductively coupled plasma mass spectrometry using an Optimal 2100DV instrument (Perkin-Elmer-Sciex, Norwalk, NY, USA) equipped with a standard spray chamber and a cross-flow nebulizer. The measured contents of trace elements in the diets are presented in Table 2. Table 2 Chemical analysis of some elements in the diets (mg/kg). Items
Basal diet
Palygorskite dieta
Fe Cu Zn Pb Cd
1236.64 ± 156.62 13.36 ± 0.16 173.55 ± 11.23 0.16 ± 0.04 0.26 ± 0.04
1332.17 ± 141.60 15.10 ± 0.70 180.84 ± 13.79 0.29 ± 0.04 0.30 ± 0.01
a
Basal diet supplemented with 2% palygorskite.
R. Zhang et al. / Applied Clay Science 114 (2015) 197–201
2.6. Statistical analysis
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Table 4 Effects of palygorskite inclusion on the pellet technological characteristics.
The data regarding pellet production efficiency was expressed by average value. Other data were analyzed as a completely randomized design using one-way ANOVA by the statistical package for the social sciences (SPSS, 2008). For all tests, the differences were considered to be significant at P b 0.05. The means and standard errors were presented.
Items
Basal diet
Palygorskite dieta
P value
Fines percentage (%) Durability (%) Dissolved weight loss (%) Degree of starch gelatinization (%)
1.50 ± 0.02 97.30 ± 0.10 13.86 ± 1.14 44.24 ± 0.28
1.10 ± 0.04 97.52 ± 0.15 11.52 ± 1.56 49.88 ± 1.63
0.001 0.287 0.294 0.021
a
Basal diet supplemented with 2% palygorskite.
3. Results 3.1. Pellet characteristics Compared with the control group, supplementation of palygorskite enhanced the feed pellet production rate by 5.26% (Table 3). As indicated in Table 4, palygorskite inclusion enhanced the degree of starch gelatinization (P = 0.021) and decreased the percentage of fines (P = 0.001). The durability and water stability of pellets were improved by palygorskite inclusion as evidenced by the numerically higher pellet durability and lower dissolved weight loss though not significantly (P N 0.05). 3.2. Growth performance There were no significant differences (Table 5) in the final body weight, weight gain or feed conversion ratio (P N 0.05) of blunt snout bream between the two groups. Similarly, dietary palygorskite supplementation did not affect the condition factor, hepatosomatic index or viscera/body ratio (P N 0.05). 3.3. Trace element content As indicated in Table 6, compared with the control group, palygorskite supplementation significantly enhanced the Fe content in the blood (P = 0.023) and muscle (P = 0.005) as well as Zn content in the muscle (P = 0.013). In contrast, palygorskite reduced muscular Cd accumulation (P = 0.026). Pb was not detected in the blood and muscle. The content of other trace elements were unaffected by palygorskite inclusion even though the Cu content in the liver was numerically lower than that of the control (P N 0.05). 4. Discussion The pellet production rate was enhanced in the present study, indicating that palygorskite supplementation can improve the production efficiency during the feed manufacture. The pellet process of animal feed is largely affected by the following factors including feed composition, particle size, inclusion of binders and other factors related to the process of pelleting per se such as conditioning, distance between roller and die and hole compression (Angulo et al., 1995, 1996; Pappas et al., 2010). Physical pellet durability usually expressed as pellet durability index (ASAE, 1997) is defined as the ability of pellet to withstand fragmentation and abrasion during mechanical and pneumatic handling as bagging, storage and transport without breaking up and generating a high proportion of fines (Cramer et al., 2003). Pellet water stability is another important parameter to evaluate the quality of aquaculture feed (Obaldo et al., 2002; Sørensen et al., 2010). High pellet water stability is defined as the retention of pellet physical integrity with minimal Table 3 Effects of palygorskite inclusion on pellet production efficiency.
Items
Basal diet
Palygorskite dietf
P value
Initial body weight (g) Final body weight (g) Weight gain (%)a Feed conversion ratiob Condition factor (%)c Hepatosomatic index (%)d Viscera/body ratio (%)e
11.58 ± 0.05 17.68 ± 0.13 52.77 ± 1.68 2.34 ± 0.14 2.22 ± 0.08 2.07 ± 0.16 14.38 ± 0.74
11.66 ± 0.09 17.64 ± 0.78 51.23 ± 5.75 2.35 ± 0.25 2.17 ± 0.06 2.21 ± 0.17 14.42 ± 0.49
0.478 0.954 0.810 0.949 0.610 0.570 0.901
Weight gain (WG, %) = (Wt − W0) × 100 / W0. Feed conversion ratio (FCR) = feed consumption (g) / fish weight gain (g). Condition factor (CF, %) = (W/L3) × 100 (W = body wet weight in grams, L = length in centimeters). d Hepatosomatic index (HSI, %) = liver weight (g) × 100 / body weight (g). e Viscera/body ratio (VBR, %) = viscera weight (g) × 100 / wet body weight (g). f Basal diet supplemented with 2% palygorskite. b
Basal diet
Palygorskite diet
Pellet production rate (ton/h) Electrical energy consumption (kWh/ton)
5.70 10.16
6.00 10.12
Basal diet supplemented with 2% palygorskite.
Table 5 Effects of palygorskite inclusion on the growth performance of blunt snout bream.
a
Items
a
disintegration and nutrient leaching while in the water until consumed by the animal. Clays can be incorporated as agglomerant in animal diets in order to improve feed manufacture (Angulo et al., 1995; Xia et al., 2004; Pappas et al., 2010). In the present study, we found that dietary 2% palygorskite inclusion significantly reduced the fines percentage in pellet. Meanwhile, the durability and water stability of pellets were also improved by palygorskite supplementation. Similar result was observed by Pappas et al. (2010) in which pellets manufactured with 1% added palygorskite showed better pellet quality than these manufactured without palygorskite. The decreased fines percentage could result from special sorptive and colloidal–rheological properties of palygorskite, which are the basis for its most technological applications (Galan, 1996; Liu, 2007; Pappas et al., 2010). Palygorskite could absorb polar liquids and forms gels due to its characteristics, which may in turn improve durability and therefore result in reduced fines percentage and dissolved weight loss possibly by increasing solid– solid bonding interactions (Pappas et al., 2010). Starch gelatinization is the process where starch and water are subjected to heat and it can cause starch granules to swell (Lund and Lorenz, 1984). Gelatinization opens the granule's structure and thus enzymes can enter the starch granules, markedly increasing susceptibility for amylolytic degradation (Rooney and Pflugfelder, 1986). Previous studies have shown that the digestibility of starch can be enhanced by gelatinization (Wilson, 1994; Stone et al., 2003; Krogdahl et al., 2005). Aside from heat, water play vital role in the starch gelatinization (Lund and Lorenz, 1984) and is a prerequisite to initiate starch gelatinization. In this study, palygorskite inclusion improved the degree of starch gelatinization, and this may be due to its high absorption and adsorption capacity for moisture that could hold more moisture, which can facilitate starch gelatinization (Thomas et al., 1998). The enhanced starch gelatinization induced by palygorskite inclusion may also contribute to the simultaneous improvements in the fines percentage, durability and dissolved weight loss since gelatinized starch has a potential to act as a binder. The higher pellet production rate may also result from the more moisture which would aid in lubricating the pellet die (Moritz et al., 2003). In the current study, we noticed that fish fed diet supplemented with palygorskite showed similar growth performance to those given basal diet, which indicated that 2% palygorskite supplementation would not impair the growth performance of fish. Zhang et al. (2013) reported
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Table 6 Effects of palygorskite inclusion on some trace elements content of blood, liver and muscle in blunt snout bream. Items
Basal diet
Palygorskite dieta
P value
Blood (mg/L) Fe Cu Zn Pb Cd
218.62 ± 10.73 0.77 ± 0.01 2.53 ± 0.11 – 0.016 ± 0.007
258.38 ± 2.50 0.76 ± 0.01 2.38 ± 0.01 – 0.018 ± 0.005
0.023 0.323 0.292 – 0.876
Liver (mg/kg) Fe Cu Zn Pb Cd
79.23 ± 10.85 11.99 ± 0.81 30.82 ± 5.56 0.250 ± 0.004 0.105 ± 0.015
75.43 ± 1.19 9.54 ± 0.41 33.62 ± 3.20 0.376 ± 0.046 0.098 ± 0.007
0.760 0.054 0.685 0.113 0.699
Muscle (mg/kg) Fe Cu Zn Pb Cd
2.66 ± 0.64 0.49 ± 0.04 5.47 ± 0.05 – 0.018 ± 0.002
7.02 ± 0.43 0.42 ± 0.06 7.55 ± 0.48 – 0.009 ± 0.002
0.005 0.382 0.013 – 0.026
a
Basal diet supplemented with 2% palygorskite.
that palygorskite supplementation at level of 2000 mg/kg improved feed conversion ratio in weaned piglets, but a higher inclusion of palygorskite at level of 3000 mg/kg exerted no beneficial effects on the growth performance. However, Pappas et al. (2010) found that 1% palygorskite supplementation to a corn–soybean based diet did not have detected effects on the body mass, feed conversion ratio as well as mortality of broilers, which was similar to the results in the present study. These discrepancies regarding the application effect of palygorskite in animal nutrition aforementioned may be due to the animal species, properties of palygorskite and dosage. It is worthy to note that fish fed diet supplemented with palygorskite achieved similar growth performance to those fed basal diet even though the nutrient content as crude protein and energy were numerically lower in the palygorskite diet. Palygorskite inclusion could enhance growth performance due to the absorption capacity of adverse factors occurred in the feed and a reduction in intestinal impairment in weaned piglets (Zhang et al., 2013). Also, it has been reported that palygorskite can improve the activities of intestinal digestive enzymes and improve intestinal morphology (Qiao et al., 2015). These factors may together contribute to the similar performance found in our study. Palygorskite supplementation significantly enhanced Fe content in the blood and muscle, and Zn content in the muscle. However, Tang et al. (2014) found that dietary palygorskite inclusion from 1800 to 3000 mg/kg did not affect serum and fecal Zn content in the weaned piglets. The discrepancy may be due to the animal species, measured organs, inclusion rate and especially the source of the palygorskite. For the clay application in aquatic animals, Kim et al. (2009) have found that inclusion of montmorillonite decreased Cd accumulation in tissues as muscles and kidney of carp, Carassius auratus. Cd is one of the most deleterious xenobiotics in aquatic ecosystems. Freshwater fish are particularly vulnerable to Cd exposure that can induce renal damage, hypertension, proteinuria and testicular atrophy (ATSDR, 1999), and would finally result in economic loss in fish industry (Zirong and Shijun, 2007). In the present study, palygorskite supplementation reduced the Cd content in the muscle, indicating that the palygorskite could also help to improve the safety of bream products, and this was likely to result from palygorskite's high absorption and adsorption capacity (Viseras et al., 2007). Similarly, in an in vitro study, ÁlvarezAyuso and García-Sánchez (2007) found that palygorskite could successfully remove Cd from aqueous solution and the sorption process appeared to be relatively fast. Heavy metal as Cd and Pb would compete with Fe and Zn in absorption in intestine (Hamilton et al., 1978; Cerklewski, 1984; Flora et al., 1989). Thus, the decreased Cd
accumulation and the enhanced Fe, Zn content may result from their antagonist effect. The purity of palygorskite would affect its adsorption behavior (Zhou and Murray, 2003). In an in vitro study by Shirvani et al. (2006), the common associated mineral of palygorskite, calcite, exhibited an inferior adsorption capacity for Cd, indicating the content of associated minerals can affect the physical and chemical properties of palygorskite and a higher purity can facilitate its application. However, the most widely used palygorskite in animal feed is the natural palygorskite and its application effect on animals including growth performance, nutrient utilization and immunity is the key point that animal nutritionists care. In conclusion, dietary 2% palygorskite inclusion could enhance pellet production efficiency, pellet quality, and trace element content, and reduce Cd accumulation in the tissues without impairing the growth performance of blunt snout bream. Also, palygorskite as an ingredient could be applied to other aquatic animals feeds according to its beneficial effect in the current study. Acknowledgments The study is funded by the Jiangsu Provincial Cooperative Innovation Fund–Prospective Joint Research Project (BY2012206) and the National Technology System for Conventional Freshwater Fish Industries of China (CARS-46-20). References Abdollahi, M.R., Ravindran, V., Svihus, B., 2013. Pelleting of broiler diets: an overview with emphasis on pellet quality and nutritional value. Anim. Feed Sci. Technol. 179, 1–23. Álvarez-Ayuso, E., García-Sánchez, A., 2007. Removal of cadmium from aqueous solutions by palygorskite. J. Hazard. Mater. 147, 594–600. Angulo, E., Brufau, J., Esteve-Garcia, E., 1995. Effect of sepiolite on pellet durability in feeds differing in fat and fibre content. Anim. Feed Sci. Technol. 53, 233–241. Angulo, E., Brufau, J., Esteve-Garcia, E., 1996. Effect of a sepiolite product on pellet durability in pig diets differing in particle size and in broiler starter and finisher diets. Anim. Feed Sci. Technol. 63, 25–34. AQSIQ, 2001. GB/T 13078-2001, Hygienical Standard for Feeds. General Administration of Quality Supervision. Inspection and Quarantine of the People's Republic of China, China. ASAE, 1997. Cubes, pellets and crumbles-definitions and methods for determining density, durability and moisture. ASAE Standard 269.4. Agricultural Engineers Yearbook of Standards. American Society of Agricultural Biological Engineers. St. Joseph, MI, USA. ATSDR, 1999. Agency for Toxic Substances and Disease Registry, Department of Health and Human, Services, USA. Bradl, H.B., 2004. Adsorption of heavy metal ions on soils and soils constituents. J. Colloid Interface Sci. 277, 1–18. Cabrera, M.R., Hancock, J.D., Bramel-Cox, P.J., Hines, R.H., Behnke, K.C., 1994. Effects of corn, sorghum genotype, and particle size on milling characteristics and growth performance in broiler chicks. Poult. Sci. 73, 11. Carretero, M.I., 2002. Clay minerals and their beneficial effects upon human health. A review. Appl. Clay Sci. 21, 155–163. Carretero, M.I., Lagaly, G., 2007. Clays and health: an introduction. Appl. Clay Sci. 36, 1–3. Cerklewski, F.L., 1984. Postabsorptive effect of increased dietary zinc on toxicity and removal of tissue lead in rats. J. Nutr. 114, 550–554. Cramer, K.R., Wilson, K.J., Moritz, J.S., Beyer, R.S., 2003. Effect of sorghum-based diets subjected to various manufacturing procedures on broiler performance. J. Appl. Poult. Res. 12, 404–410. Dai, W., Du, H., Fu, L., Liu, H., Xu, Z., 2010. Effect of montmorillonite on dietary lead (Pb) accumulation in tissues of tilapia (Oreochromis niloticus). Appl. Clay Sci. 47, 193–195. Den Hartog, L.A., Sijtsma, S.R., 2009. Influence of Feed Processing Technology on Pig Performance. Recent Advances In Animal Nutrition. p. 227. Flora, S.J.S., Singh, S., Tandon, S.K., 1989. Thiamine and zinc in prevention or therapy of lead intoxication. J. Int. Med. Res. 17, 68–75. Galan, E., 1996. Properties and applications of palygorskite–sepiolite clays. Clay Miner. 31, 443–454. Hamilton, D.L., Bellamy, J.E.C., Valberg, J.D., Valberg, L.S., 1978. Zinc, cadmium, and iron interactions during intestinal absorption in iron-deficient mice. Can. J. Physiol. Pharmacol. 56, 384–389. Hansen, J.Ø., Storebakken, T., 2007. Effects of dietary cellulose level on pellet quality and nutrient digestibilities in rainbow trout (Oncorhynchus mykiss). Aquaculture 272, 458–465. Huang, J., Liu, Y., Jin, Q., Wang, X., Yang, J., 2007. Adsorption studies of a water soluble dye, Reactive Red MF-3B, using sonication-surfactant-modified attapulgite clay. J. Hazard. Mater. 143, 541–548. Kim, S.G., Du, H.H., Dai, W., Zhang, X.F., Xu, Z.R., 2009. Influence of montmorillonite on cadmium accumulation in carp, Carassius auratus. Appl. Clay Sci. 43, 473–476. Krogdahl, Å., Hemre, G.I., Mommsen, T.P., 2005. Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac. Nutr. 11, 103–122.
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