Trop Anim Health Prod (2015) 47:1397–1403 DOI 10.1007/s11250-015-0877-5
REGULAR ARTICLES
Effect of passion fruit seed meal on growth performance, carcass, and blood characteristics in starter pigs Marcelise Regina Fachinello 1 & Paulo Cesar Pozza 1 & Ivan Moreira 2 & Paulo Levi Oliveira Carvalho 3 & Leandro Dalcin Castilha 1 & Tiago Junior Pasquetti 1 & Lucas Antonio Costa Esteves 1 & Laura Marcela Diaz Huepa 1
Received: 3 January 2015 / Accepted: 15 June 2015 / Published online: 1 July 2015 # Springer Science+Business Media Dordrecht 2015
Abstract Two experiments were carried out in Paraná State, Brazil, to evaluate the nutritional value of passion fruit seed meal (PFM) and to study the effect of PFM on growth performance, carcass, and blood characteristics in starter pigs (Topigs 20 × Tybor). In experiment 1, 25 castrated males, averaging 19.1-kg body weight, were individually fed in a completely randomized block design, consisting of five treatments and five replicates and an experimental period that lasted 14 days. In experiment 2, a total of 60 pigs (30 females and 30 castrated males) were distributed in a randomized block design with five treatments, six replications, and two animals per experimental unit and 90 days of experimentation. For both experiments, the same PFM inclusion rates were used in the experimental diets, namely, 0, 4, 8, 12, and 16 %. The metabolizable energy of PFM was estimated to be 15.0 MJ/kg. Inclusion of PFM at any level did not affect average daily gain, daily feed intake, feed/gain ratio, backfat thickness, loin depth, and plasma or blood components. It is concluded that passion fruit seed meal for swine in the starting phase can be added at a rate of up to 16 % in the diet without
* Marcelise Regina Fachinello [email protected] 1
Departamento de Zootecnia, Universidade Estadual de Maringá, Av. Colombo, 5790 Bloco J45, Maringá, Paraná 87020-900, Brazil
2
Departamento de Zootecnia, Universidade Tecnológica Federal do Paraná — Campos Dois Vizinhos, Estrada para Boa Esperança, Km 04 Zona Rural, Dois Vizinhos, Paraná 85660-000, Brazil
3
Departamento de Zootecnia, Universidade Estadual do Oeste do Paraná — Campos Marechal Cândido Rondon, Rua Pernambuco, 1777, Marechal Cândido Rondon, Paraná 85960-000, Brazil
any negative effects on growth performance, carcass, and blood characteristics in starter commercial line pigs. Keywords Blood component . Carcass characteristic . Growth performance . Nutritional value . Passion fruit seed meal . Plasma component
Introduction Pig meat production costs depend heavily on the price of feedstuffs used in the diet, and so, there is a continuous search for alternative feedstuffs that do not negatively affect animal performance. Agro-industrial residues of fruit processing are potential substitutes for conventional feedstuffs. We have focused on the passion fruit because Brazil is the largest producer and consumer of passion fruit, with an annual production of 776,000 t (IBGE 2013). According to Ferrari et al. (2004), only 23 % of passion fruit is removed during juice extraction, and of the 77 % residue, the seed represents 6–12 % of the total weight of the fruit. The seeds of passion fruit contain about 50 % acid detergent fiber and 55 % neutral detergent fiber (Valadares et al. 2006), 26 % fat, and 15.6 % crude protein (Ferrari et al. 2004). Passion fruit by-products have been evaluated in livestock diets (Romo and Nava 2007; Azevedo et al. 2011) because they can generate extra income for the industry and reduce the disposal of residues. Except the study of Perondi et al. (2014) who included passion fruit seed meal (PFM) up to 16 % in the diet of growing and finishing castrated male pigs and did not find any reduction in animal performance, reports on the use of PFM in pig diets are very limited. Therefore, our work was designed to determine the nutritional value of PFM at different levels of replacement and to find out the effect of
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PFM on the growth, carcass, and blood characteristics in starter pigs.
Sniffen et al. (1992). Pectin content was determined according to Carvalho et al. (2006) and total polyphenol content according to Pierpoint (2004).
Materials and methods
Experiment 2
Two separated experiments were carried out in the Iguatemi Experimental Farm, belonging to the Universidade Estadual de Maringá, located in Paraná State, Brazil (23° 21′ S, 52° 04′ W, altitude 564 m). Average maximum and minimum temperatures were 23.3 and 18.5 °C, respectively, and relative humidity ranged from 18 to 47 %.
Daily feed intake (DFI), average daily gain (ADG), and feed/gain ratio (F/G) were determined. Backfat thickness (BT) and loin depth (LD) were evaluated at the end of the experiment, by using an eco-camera (Aloka® SSD-500 Vet) coupled to an 11.5 cm and 3.5 MHz probe. To determine plasma urea nitrogen (PUN), the blood samples were collected at the beginning (baseline) and end of the experiment without fasting period, and for the other blood parameters, a 6-h fasting period was used. Total cholesterol (TC), total protein (TP), albumin (AL), globulin (GB), and triglyceride (TG) levels were analyzed by using commercial kits. Additionally, tubes containing EDTA were utilized for blood collection in order to determine the hematocrit percentage (Htc), after which the blood was centrifuged (10,000 rpm) for 5 min.
Animals, experimental design, and diets All animal procedures were approved by the Committee for Ethics in Animal Experimentation (CEAE) of the university (protocol 096/2012). In experiment 1, 25 castrated males (Topigs 20 × Tybor) were used, averaging 19.1±2.8 kg initial body weight, individually allotted in metabolism cages, and distributed in a completely randomized block design, consisting of five treatments and five replicates. The experimental period lasted 14 days, with 9 days for animal adaptation to metabolism cages and diets and 5 days were used for feces and urine collection. Iron oxide was used in the experimental diets to set the beginning and end of the collection period. In experiment 2, 60 pigs (30 females and 30 castrated males) with an average initial body weight of 15.5±0.9 kg were used, distributed in a randomized block design with five treatments, six replicates, and two animals per experimental unit. Animals were housed in suspended pens with frontal feeders and nipple-type drinkers in the back. Diets and water were freely offered during all experimental periods with duration 90 days (Table 1). In both experiments, the treatments consisted of diets with different levels of PFM inclusion (0, 4, 8, 12, and 16 %), and were formulated to meet the nutritional recommendations proposed by Rostagno et al. (2011).
Statistical analysis Digestible dry matter (DDM), digestible organic matter (DOM), digestible energy (DE), metabolizable energy (ME), digestible protein (DP), digestible ether extract (DEE), digestible neutral detergent fiber (DNDF), digestible acid detergent fiber (DADF) of PFM were determined by the technique of linear equations adjustments, in which the slope of the linear regression equations represents the mentioned parameters (Adeola and Ileleji 2009). The other studied parameters were submitted to analysis of variance and the degrees of freedom relative to the levels of PFM inclusion were deployed in orthogonal polynomials to obtain the regression equation. The statistical analyses were performed using the SAEG program (UFV 2007). Initial PUN was used as covariate for this parameter. Initial and final body weights were also used as covariate for performance and carcass quantitative characteristics, respectively.
Studied parameters Experiment 1
Results
PFM, experimental diets and feces were submitted to the analyses of dry matter (DM), organic matter (OM), mineral matter (MM), crude protein (CP), ether extract (EE), gross energy (GE), crude fiber (CF), acid detergent fiber (ADF), neutral detergent fiber (NDF), hemicellulose, cellulose, lignin and pH, according to the methodology described by Silva and Queiroz (2009). Fatty acids profile was determined at the chemistry department of the university. Total carbohydrates and non-fiber carbohydrates were determined according to
Experiment 1 PFM had a high content of GE and EE (Table 2), and lipid profile predominantly consisted of unsaturated fatty acids, mainly linoleic acid (64.0 %). High levels of NDF and ADF were also recorded, along with a low lignin and high pectin content. PFM also contains high amounts of total carbohydrates; however, non fibrous carbohydrates content is relatively low.
Trop Anim Health Prod (2015) 47:1397–1403 Table 1
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Composition of diets containing levels of passion fruit seed meal (PFM) for pigs
Ingredients (%)
Corn
Females
Castrated males
Levels of inclusion (%)
Levels of inclusion (%)
0
4
8
12
16
0
4
8
12
16
67.5
64.1
60.7
57.2
53.8
68.5
65.1
61.7
58.3
54.8
Soybean meal
28.0
27.6
27.2
26.7
26.3
27.0
26.6
26.1
25.7
25.3
Dicalcium phosphate Limestone
1.5 0.84
1.5 0.85
1.5 0.86
1.5 0.87
1.4 0.88
1.4 0.98
1.4 0.98
1.4 0.99
1.4 0.99
1.4 1.0
Soybean oil Salt
0.72 0.46 0.5
0.54 0.46 0.5
0.36 0.46 0.5
0.19 0.46 0.5
0.0 0.46 0.5
0.70 0.46 0.5
0.52 0.46 0.5
0.35 0.46 0.5
0.17 0.46 0.5
0.0 0.46 0.5
0.31 0.08 0.07 0.01
0.33 0.08 0.08 0.01
0.34 0.09 0.09 0.01
0.35 0.09 0.10 0.01
0.36 0.11 0.10 0.01
0.3 0.07 0.06 0.01
0.31 0.07 0.07 0.01
0.32 0.08 0.07 0.01
0.33 0.08 0.08 0.01
0.35 0.09 0.09 0.01
0.02 0.005 0.0
0.02 0.005 4.0
0.02 0.005 8.0
0.02 0.005 12.0
0.02 0.005 16.0
0.02 0.005 0.0
0.02 0.005 4.0
0.02 0.005 8.0
0.02 0.005 12.0
0.02 0.005 16.0
ME (MJ/kg) Crude protein (%) Ether extract (%) Neutral detergent fiber (%)
13.7 18.5 3.73 8.2
13.7 18.5 4.15 13.4
13.7 18.5 4.58 15.0
13.7 18.5 5.00 16.5
13.7 18.5 5.42 18.1
13.7 18.1 3.65 8.47
13.7 18.1 4.10 13.4
13.7 18.1 4.55 15.0
13.7 18.1 5.00 16.5
13.7 18.1 5.44 18.1
Acid detergent fiber (%) Available phosphorus (%)
4.54 0.38
6.14 0.38
7.74 0.38
9.34 0.38
10.94 0.38
4.49 0.36
6.09 0.36
7.69 0.36
9.29 0.36
10.9 0.36
Calcium (%) SID lysine (%) SID methionine + cystine (%)
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
SID threonine (%) SID tryptophan (%)
0.68 0.19
0.68 0.19
0.68 0.19
0.68 0.19
0.68 0.19
0.65 0.19
0.65 0.19
0.65 0.19
0.65 0.19
0.65 0.19
Vitamin and minerala L-Lysine HCl DL-methionine L-Threonine L-Tryptophan Antioxidantb Growth promoterc PFM Calculated composition
a
Vitamin and mineral mix for pigs in the initial phase (content/kg: vitamin A—1,800,000 UI; vitamin D3—360,000 UI; vitamin E—4000 mg; vitamin K3—600 mg; vitamin B1—280 mg; vitamin B2—800 mg; vitamin B6—300 mg; vitamin B12—3600 mg; pantotenic acid—3200 mg; niacin— 6000.0 mg; folic acid—80 mg; biotin—20.0 mg; choline—31.2 g; copper—50.0 g; iron—20.0 g; manganese—11.0 g; cobalt—120 mg; iodine— 200 mg; zinc—18.0 g; selenium—60.0 mg; lysine—140.4 g)
b
BHT
c
Leucomag (30 %)
The fitted equations for DE and ME were Ŷ=16.6x+0.066 (r2 = 0.97) and Ŷ = 15.0x + 0.0065 (r2 = 0.95), respectively (Fig. 1), providing values of 16.6 MJ DE/kg and 15.0 MJ ME/kg, represented by the slope coefficients, and ME/DE ratio close to 0.90. Coefficients of digestibility and metabolism of GE were 71.4 and 64.3 % (Table 3), respectively. The digestible EE (DEE=17.3x−0.604; r2 =0.99), CP (DCP=8.0x+0.115, r2 =0.90), NDF (DNDF=25.0x−0.235; r2 =0.91), and ADF (DADF=19.6x+0.036; r2 =0.80) were estimated at 17.3, 8.0, 25.0, and 19.6 %, respectively; representing the slope coefficients of the adjusted equations (Table 3). The digestibility coefficients of ADF and NDF were
relatively high, but the PFM showed high content of pectin, what may have contributed for this high digestibility. Experiment 2 There was no effect of PFM inclusion (P>0.05) on DFI, ADG, or F/G (Table 4), and the same response was also observed (P>0.05) for the final weight (29.7 to 31.5 kg) when the initial weight was used as covariate in the model. Similarly, the results obtained for parameters BT and LD, were not affected (P > 0.05) by PFM inclusion. No differences (P > 0.05) were observed for PUN, TG, TP, and Htc
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Table 2 Chemical, energy, and physical composition of passion fruit seed meal
Table 3
Apparent digestibility of nutrients of passion fruit seed meal
Digestibility coefficient
Percent (%)
Dry matter
67.6
Organic matter
67.2
Gross energy Metabolization coefficient gross energy
71.4 64.3
0.08
Crude protein Ether extract
70.5 92.9
Total phosphorus (%) Available phosphorus (%)
0.43 0.14
Neutral detergent fiber
49.9
3.52 26.4
Acid detergent fiber Digestible nutrients
44.8
Mineral matter (%) Crude fiber (%) Ether extract (%)
18.8
Dry matter (%) Organic matter (%)
62.4 59.6
Neutral detergent fiber (%)
50.2
Digestible energy (MJ/kg)
15.0
Acid detergent fiber (%) Cellulose (%) Hemicellulose (%)
43.7 37.0 6.51
Metabolizable energy (MJ/kg) Protein (%)
16.6 8.0
Lignin (%)
5.77
Ether extract (%) Neutral detergent fiber (%)
17.3 25.0
Pectin (%) Total carbohydrates (%) Non fibrous carbohydrates (%)
18.3 58.5 8.31
Acid detergent fiber (%)
19.6
Polyphenols mgeq/g pH Fatty acids Palmitic (%)
4.01 4.7
Nutrients
Passion fruit seed meal
Dry matter (%)
92.2
Organic matter (%)
88.7
Crude protein (%) Gross energy MJ/kg
11.3 23.3
Calcium (%)
11.3
due to the high standard error obtained (Table 5). The AB and GB in blood plasma was not affected (P>0.05) by PFM levels, and A:G ratio even showed the same response, as a consequence of the results obtained for its isolated parameters.
Stearic (%) Oleic (%) Linoleic (%)
3.54 19.5 64.0
Discussion
Linolenic (%) Saturated (%) Unsaturated (%)
0.40 15.4 84.6
Experiment 1
25,0 20,0
Ŷ = 16.6x + 0.066 r² = 0.97
15,0 10,0 5,0 0,0 0,00
0,50 1,00 1,50 Intake of passion fruit seed meal (kg)
DE intake according to the consumption of the PFM
a)
Metabolizable energy intake (MJ)
Fig. 1 Graphical representation of a digestible energy (DE) and b metabolizable energy (ME) of passion fruit seed meal (PFM)
Digestible energy intake (MJ)
(Table 5) so PFM inclusion up to 16 % did not affect any of the evaluated parameters. A decrease in TC was expected according to increasing levels of PFM in the experimental diets, but this parameter was not influenced by PFM inclusion, probably
The obtained CP (11.3 %) and EE (18.8 %) are within the range reported by Romo and Nava (2007), but seeds of passion fruit is a source of fiber, mainly consisting of cellulose, hemicellulose, and pectic substances (Chau and Huang 2004), which is in agreement with NDF and ADF obtained (Table 2). It is well known that increased fiber in diets for 25,0 20,0
Ŷ = 15.0x + 0.0065 r² = 0.95
15,0 10,0 5,0 0,0 0,00
0,50 1,00 1,50 Intake of passion fruit seed meal (kg)
ME intake according to the consumption of the PFM
b)
Trop Anim Health Prod (2015) 47:1397–1403 Table 4
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Growth performance and carcass characteristics of starter pigs fed passion fruit seed meal (PFM)
Parameters
Mean±SEa
PFM inclusion (%)
P value Linb
Quac
30.3±0.34 0.69±0.01
NS NS
NS NS
1.40±0.02 2.03±0.04
NS NS
NS NS
0
4
8
12
16
Initial body weight kg
15.4
15.3
15.5
15.7
15.2
15.4±0.09
Final body weight kg Average daily gain kg
31.5 0.75
29.9 0.68
29.7 0.66
30.7 0.69
29.8 0.68
Feed daily intake kg Feed/Gain
1.44 1.93
1.43 2.10
1.33 2.02
1.35 1.97
1.43 2.13
Loin depth cm
2.45
2.62
2.33
2.49
2.31
2.44±0.05
NS
NS
Backfat thickness cm
0.52
0.49
0.49
0.48
0.52
0.50±0.01
NS
NS
a
Standard error
b
Linear effect
c
Quadratic effect
growing pigs is an undesirable factor, because it decreases the digestibility of nutrients. However, DE (16.6 MJ/kg) and ME (15.0 MJ/kg) were high and superior than those obtained by Perondi et al. (2014) when evaluating PFM for growing pigs, but these authors used a PFM with a higher NDF content (52.0 %). The digestibility and metabolizability coefficients of GE of corn and sorghum (Rostagno et al. 2011) are higher than that obtained for PFM. The high NDF of the PFM may be associated with these results, due to the negative effects of fiber on the energy digestibility. The ME/DE may be associated with the protein quality, since low quality protein, or in excess, leads to a decrease in the ME, because amino acids not used for protein synthesis are catabolized leading to urea excretion (NRC 2012). In this way, the ME/ED obtained (0:90) shows a relationship with the CP utilization, once low DC of CP can be attributed to increases in MM and ADF in the diet, since protein digestibility
Table 5 Blood characteristics of starter pigs fed passion fruit seed meal (PFM)
Parameters
is reduced by around 0.4 and 0.2 g/kg DM for each additional gram of ash and ADF in the diet (Noblet and Perez 1993), partially explaining the CP digestibility obtained (70.5 %) compared with that of conventional feedstuffs. Furthermore, the CP digestibility can also be influenced by high pectin levels (Drochner et al. 2004). Experiment 2 Previous studies with by-products from fruit processing (Pascoal et al. 2010; Noh et al. 2014) demonstrated a high potential to be used in pig diets. In this sense, Perondi et al. (2014) evaluating PFM in pig diets did not observe differences in the performance of growing and finishing pigs, until 16 % of inclusion in the diets. These results corroborates our findings, in which the inclusion levels of PFM did not affect the performance; what may be due to the inclusion of soybean oil and industrial amino acids in the diets, in order to become
Mean±SEa
PFM inclusion (%) 0
4
8
12
16
Plasma urea nitrogen (mg/dL) Total cholesterol (mg/dL) Triglycerides (mg/dL)
16.8 73.1 35.6
17.9 68.6 39.3
17.6 72.4 44.2
16.8 66.1 33.2
18.0 64.3 32.7
Total protein (g/d) Albumin (g/d) Globulin (g/d) Albumin/Globulin Hematocrits (%)
5.42 3.24 2.18 1.49 30.8
5.38 3.18 2.20 1.59 30.7
5.74 3.20 2.54 1.52 30.8
5.48 3.19 2.29 1.42 34.2
5.35 3.10 2.25 1.42 34.7
a
Standard error
b
Linear effect
c
Quadratic effect
P value Linb
Quac
17.4±0.26 68.9±1.71 37.0±2.15
NS NS NS
NS NS NS
5.47±0.07 3.18±0.02 2.29±0.07 1.42±0.03 32.2±0.90
NS NS NS NS NS
NS NS NS NS NS
1402
isoenergetic and with the same amount of amino acids, thereby maintaining the nutritional quality of the diet according to the inclusion of the PFM in the diets. Diets or ingredients with high fiber contents can negatively influence the voluntary intake and nutrient digestibility in young pigs (Wilfart et al. 2007). In this study, besides the fact that PFM inclusion increased the fiber content in the diet, we did not observe negative effects on animal performance, possibly due to the high pectin content of the PFM, unlike celluloses, it is highly degraded in the extensions of the colon (Drochner et al. 2004). In the same way, PFM inclusion did not affect LD and BT, which may have occurred because the diets had the same amount of energy and amino acids, which is important because protein deposition depends on the supply of energy and available amino acids in the diet (Milgen and Noblet 2003). Also, animal performance was similar until 16 % of PFM inclusion in the diet. However, including PFM, it was not economically viable for levels evaluated according to the prices paid by PFM and the others ingredients used in the experimental diets. Pectin is often considered as a potential carbohydrate that decreases plasma cholesterol (Kreuzer et al. 2002), but plasma cholesterol was not affected (Table 5), despite high pectin amounts in the PFM. There is evidence that plasma triglyceride are influenced by energy in the diet. Thus, as the diets were isoenergetic (Table 1), there might not have been differences among the studied treatments. PUN indicates an adequate protein supply (Pedersen and Boisen 2001), indicating that PFM inclusion in the diets were effective when supplemented with amino acids, once this parameter was not affected (Table 5). A moderate protein deficiency may cause a decrease in serum protein, mainly albumin, without altering the globulin content (Miyada et al. 1997). In this study these parameters were not affected and corroborate the results obtained for PUN. There is also an evidence that hematocrit may be related to the lysine content of the diet (Miyada et al. 1997); but in our study, the diets had the same lysine amounts, explaining the similar results obtained (Table 5) for this parameter.
Conclusion From the above experiment, it was evident that the metabolizable energy of the passion fruit seed meal for swine in the starting phase was 15.0 MJ/kg and PFM could be added up to 16 % in the diet without any negative effects on growth performance, carcass, and blood characteristics in starter commercial line pigs.
Conflict of interest The authors declare that they have no conflict of interest.
Trop Anim Health Prod (2015) 47:1397–1403
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1403 diets: II. Carbohydrate and protein availability, Journal of Animal Science, 70, 3562–3577 UFV, Universidade Federal De Viçosa, 2007. Central de processamento de dados - UFV/CPD: SAEG - Sistema para análises estatísticas 9.1. Viçosa Valadares, S.C.F., Magalhães, K.A., Rocha Junior, V.R. and Capelle, E.R., 2006. Tabela brasileira de composição de alimentos para bovinos, (Universidade Federal de Viçosa, Viçosa) Wilfart, A., Montagne, L., Simmins, H., Noblet, J. and Van Milgen, J., 2007. Effect of fibre content in the diet on the mean retention time in different segments of the digestive tract in growing pigs. Livestock Science, 109, 27–29
REGULAR ARTICLES
Effect of passion fruit seed meal on growth performance, carcass, and blood characteristics in starter pigs Marcelise Regina Fachinello 1 & Paulo Cesar Pozza 1 & Ivan Moreira 2 & Paulo Levi Oliveira Carvalho 3 & Leandro Dalcin Castilha 1 & Tiago Junior Pasquetti 1 & Lucas Antonio Costa Esteves 1 & Laura Marcela Diaz Huepa 1
Received: 3 January 2015 / Accepted: 15 June 2015 / Published online: 1 July 2015 # Springer Science+Business Media Dordrecht 2015
Abstract Two experiments were carried out in Paraná State, Brazil, to evaluate the nutritional value of passion fruit seed meal (PFM) and to study the effect of PFM on growth performance, carcass, and blood characteristics in starter pigs (Topigs 20 × Tybor). In experiment 1, 25 castrated males, averaging 19.1-kg body weight, were individually fed in a completely randomized block design, consisting of five treatments and five replicates and an experimental period that lasted 14 days. In experiment 2, a total of 60 pigs (30 females and 30 castrated males) were distributed in a randomized block design with five treatments, six replications, and two animals per experimental unit and 90 days of experimentation. For both experiments, the same PFM inclusion rates were used in the experimental diets, namely, 0, 4, 8, 12, and 16 %. The metabolizable energy of PFM was estimated to be 15.0 MJ/kg. Inclusion of PFM at any level did not affect average daily gain, daily feed intake, feed/gain ratio, backfat thickness, loin depth, and plasma or blood components. It is concluded that passion fruit seed meal for swine in the starting phase can be added at a rate of up to 16 % in the diet without
* Marcelise Regina Fachinello [email protected] 1
Departamento de Zootecnia, Universidade Estadual de Maringá, Av. Colombo, 5790 Bloco J45, Maringá, Paraná 87020-900, Brazil
2
Departamento de Zootecnia, Universidade Tecnológica Federal do Paraná — Campos Dois Vizinhos, Estrada para Boa Esperança, Km 04 Zona Rural, Dois Vizinhos, Paraná 85660-000, Brazil
3
Departamento de Zootecnia, Universidade Estadual do Oeste do Paraná — Campos Marechal Cândido Rondon, Rua Pernambuco, 1777, Marechal Cândido Rondon, Paraná 85960-000, Brazil
any negative effects on growth performance, carcass, and blood characteristics in starter commercial line pigs. Keywords Blood component . Carcass characteristic . Growth performance . Nutritional value . Passion fruit seed meal . Plasma component
Introduction Pig meat production costs depend heavily on the price of feedstuffs used in the diet, and so, there is a continuous search for alternative feedstuffs that do not negatively affect animal performance. Agro-industrial residues of fruit processing are potential substitutes for conventional feedstuffs. We have focused on the passion fruit because Brazil is the largest producer and consumer of passion fruit, with an annual production of 776,000 t (IBGE 2013). According to Ferrari et al. (2004), only 23 % of passion fruit is removed during juice extraction, and of the 77 % residue, the seed represents 6–12 % of the total weight of the fruit. The seeds of passion fruit contain about 50 % acid detergent fiber and 55 % neutral detergent fiber (Valadares et al. 2006), 26 % fat, and 15.6 % crude protein (Ferrari et al. 2004). Passion fruit by-products have been evaluated in livestock diets (Romo and Nava 2007; Azevedo et al. 2011) because they can generate extra income for the industry and reduce the disposal of residues. Except the study of Perondi et al. (2014) who included passion fruit seed meal (PFM) up to 16 % in the diet of growing and finishing castrated male pigs and did not find any reduction in animal performance, reports on the use of PFM in pig diets are very limited. Therefore, our work was designed to determine the nutritional value of PFM at different levels of replacement and to find out the effect of
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PFM on the growth, carcass, and blood characteristics in starter pigs.
Sniffen et al. (1992). Pectin content was determined according to Carvalho et al. (2006) and total polyphenol content according to Pierpoint (2004).
Materials and methods
Experiment 2
Two separated experiments were carried out in the Iguatemi Experimental Farm, belonging to the Universidade Estadual de Maringá, located in Paraná State, Brazil (23° 21′ S, 52° 04′ W, altitude 564 m). Average maximum and minimum temperatures were 23.3 and 18.5 °C, respectively, and relative humidity ranged from 18 to 47 %.
Daily feed intake (DFI), average daily gain (ADG), and feed/gain ratio (F/G) were determined. Backfat thickness (BT) and loin depth (LD) were evaluated at the end of the experiment, by using an eco-camera (Aloka® SSD-500 Vet) coupled to an 11.5 cm and 3.5 MHz probe. To determine plasma urea nitrogen (PUN), the blood samples were collected at the beginning (baseline) and end of the experiment without fasting period, and for the other blood parameters, a 6-h fasting period was used. Total cholesterol (TC), total protein (TP), albumin (AL), globulin (GB), and triglyceride (TG) levels were analyzed by using commercial kits. Additionally, tubes containing EDTA were utilized for blood collection in order to determine the hematocrit percentage (Htc), after which the blood was centrifuged (10,000 rpm) for 5 min.
Animals, experimental design, and diets All animal procedures were approved by the Committee for Ethics in Animal Experimentation (CEAE) of the university (protocol 096/2012). In experiment 1, 25 castrated males (Topigs 20 × Tybor) were used, averaging 19.1±2.8 kg initial body weight, individually allotted in metabolism cages, and distributed in a completely randomized block design, consisting of five treatments and five replicates. The experimental period lasted 14 days, with 9 days for animal adaptation to metabolism cages and diets and 5 days were used for feces and urine collection. Iron oxide was used in the experimental diets to set the beginning and end of the collection period. In experiment 2, 60 pigs (30 females and 30 castrated males) with an average initial body weight of 15.5±0.9 kg were used, distributed in a randomized block design with five treatments, six replicates, and two animals per experimental unit. Animals were housed in suspended pens with frontal feeders and nipple-type drinkers in the back. Diets and water were freely offered during all experimental periods with duration 90 days (Table 1). In both experiments, the treatments consisted of diets with different levels of PFM inclusion (0, 4, 8, 12, and 16 %), and were formulated to meet the nutritional recommendations proposed by Rostagno et al. (2011).
Statistical analysis Digestible dry matter (DDM), digestible organic matter (DOM), digestible energy (DE), metabolizable energy (ME), digestible protein (DP), digestible ether extract (DEE), digestible neutral detergent fiber (DNDF), digestible acid detergent fiber (DADF) of PFM were determined by the technique of linear equations adjustments, in which the slope of the linear regression equations represents the mentioned parameters (Adeola and Ileleji 2009). The other studied parameters were submitted to analysis of variance and the degrees of freedom relative to the levels of PFM inclusion were deployed in orthogonal polynomials to obtain the regression equation. The statistical analyses were performed using the SAEG program (UFV 2007). Initial PUN was used as covariate for this parameter. Initial and final body weights were also used as covariate for performance and carcass quantitative characteristics, respectively.
Studied parameters Experiment 1
Results
PFM, experimental diets and feces were submitted to the analyses of dry matter (DM), organic matter (OM), mineral matter (MM), crude protein (CP), ether extract (EE), gross energy (GE), crude fiber (CF), acid detergent fiber (ADF), neutral detergent fiber (NDF), hemicellulose, cellulose, lignin and pH, according to the methodology described by Silva and Queiroz (2009). Fatty acids profile was determined at the chemistry department of the university. Total carbohydrates and non-fiber carbohydrates were determined according to
Experiment 1 PFM had a high content of GE and EE (Table 2), and lipid profile predominantly consisted of unsaturated fatty acids, mainly linoleic acid (64.0 %). High levels of NDF and ADF were also recorded, along with a low lignin and high pectin content. PFM also contains high amounts of total carbohydrates; however, non fibrous carbohydrates content is relatively low.
Trop Anim Health Prod (2015) 47:1397–1403 Table 1
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Composition of diets containing levels of passion fruit seed meal (PFM) for pigs
Ingredients (%)
Corn
Females
Castrated males
Levels of inclusion (%)
Levels of inclusion (%)
0
4
8
12
16
0
4
8
12
16
67.5
64.1
60.7
57.2
53.8
68.5
65.1
61.7
58.3
54.8
Soybean meal
28.0
27.6
27.2
26.7
26.3
27.0
26.6
26.1
25.7
25.3
Dicalcium phosphate Limestone
1.5 0.84
1.5 0.85
1.5 0.86
1.5 0.87
1.4 0.88
1.4 0.98
1.4 0.98
1.4 0.99
1.4 0.99
1.4 1.0
Soybean oil Salt
0.72 0.46 0.5
0.54 0.46 0.5
0.36 0.46 0.5
0.19 0.46 0.5
0.0 0.46 0.5
0.70 0.46 0.5
0.52 0.46 0.5
0.35 0.46 0.5
0.17 0.46 0.5
0.0 0.46 0.5
0.31 0.08 0.07 0.01
0.33 0.08 0.08 0.01
0.34 0.09 0.09 0.01
0.35 0.09 0.10 0.01
0.36 0.11 0.10 0.01
0.3 0.07 0.06 0.01
0.31 0.07 0.07 0.01
0.32 0.08 0.07 0.01
0.33 0.08 0.08 0.01
0.35 0.09 0.09 0.01
0.02 0.005 0.0
0.02 0.005 4.0
0.02 0.005 8.0
0.02 0.005 12.0
0.02 0.005 16.0
0.02 0.005 0.0
0.02 0.005 4.0
0.02 0.005 8.0
0.02 0.005 12.0
0.02 0.005 16.0
ME (MJ/kg) Crude protein (%) Ether extract (%) Neutral detergent fiber (%)
13.7 18.5 3.73 8.2
13.7 18.5 4.15 13.4
13.7 18.5 4.58 15.0
13.7 18.5 5.00 16.5
13.7 18.5 5.42 18.1
13.7 18.1 3.65 8.47
13.7 18.1 4.10 13.4
13.7 18.1 4.55 15.0
13.7 18.1 5.00 16.5
13.7 18.1 5.44 18.1
Acid detergent fiber (%) Available phosphorus (%)
4.54 0.38
6.14 0.38
7.74 0.38
9.34 0.38
10.94 0.38
4.49 0.36
6.09 0.36
7.69 0.36
9.29 0.36
10.9 0.36
Calcium (%) SID lysine (%) SID methionine + cystine (%)
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.77 1.07 0.60
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
0.73 1.04 0.58
SID threonine (%) SID tryptophan (%)
0.68 0.19
0.68 0.19
0.68 0.19
0.68 0.19
0.68 0.19
0.65 0.19
0.65 0.19
0.65 0.19
0.65 0.19
0.65 0.19
Vitamin and minerala L-Lysine HCl DL-methionine L-Threonine L-Tryptophan Antioxidantb Growth promoterc PFM Calculated composition
a
Vitamin and mineral mix for pigs in the initial phase (content/kg: vitamin A—1,800,000 UI; vitamin D3—360,000 UI; vitamin E—4000 mg; vitamin K3—600 mg; vitamin B1—280 mg; vitamin B2—800 mg; vitamin B6—300 mg; vitamin B12—3600 mg; pantotenic acid—3200 mg; niacin— 6000.0 mg; folic acid—80 mg; biotin—20.0 mg; choline—31.2 g; copper—50.0 g; iron—20.0 g; manganese—11.0 g; cobalt—120 mg; iodine— 200 mg; zinc—18.0 g; selenium—60.0 mg; lysine—140.4 g)
b
BHT
c
Leucomag (30 %)
The fitted equations for DE and ME were Ŷ=16.6x+0.066 (r2 = 0.97) and Ŷ = 15.0x + 0.0065 (r2 = 0.95), respectively (Fig. 1), providing values of 16.6 MJ DE/kg and 15.0 MJ ME/kg, represented by the slope coefficients, and ME/DE ratio close to 0.90. Coefficients of digestibility and metabolism of GE were 71.4 and 64.3 % (Table 3), respectively. The digestible EE (DEE=17.3x−0.604; r2 =0.99), CP (DCP=8.0x+0.115, r2 =0.90), NDF (DNDF=25.0x−0.235; r2 =0.91), and ADF (DADF=19.6x+0.036; r2 =0.80) were estimated at 17.3, 8.0, 25.0, and 19.6 %, respectively; representing the slope coefficients of the adjusted equations (Table 3). The digestibility coefficients of ADF and NDF were
relatively high, but the PFM showed high content of pectin, what may have contributed for this high digestibility. Experiment 2 There was no effect of PFM inclusion (P>0.05) on DFI, ADG, or F/G (Table 4), and the same response was also observed (P>0.05) for the final weight (29.7 to 31.5 kg) when the initial weight was used as covariate in the model. Similarly, the results obtained for parameters BT and LD, were not affected (P > 0.05) by PFM inclusion. No differences (P > 0.05) were observed for PUN, TG, TP, and Htc
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Table 2 Chemical, energy, and physical composition of passion fruit seed meal
Table 3
Apparent digestibility of nutrients of passion fruit seed meal
Digestibility coefficient
Percent (%)
Dry matter
67.6
Organic matter
67.2
Gross energy Metabolization coefficient gross energy
71.4 64.3
0.08
Crude protein Ether extract
70.5 92.9
Total phosphorus (%) Available phosphorus (%)
0.43 0.14
Neutral detergent fiber
49.9
3.52 26.4
Acid detergent fiber Digestible nutrients
44.8
Mineral matter (%) Crude fiber (%) Ether extract (%)
18.8
Dry matter (%) Organic matter (%)
62.4 59.6
Neutral detergent fiber (%)
50.2
Digestible energy (MJ/kg)
15.0
Acid detergent fiber (%) Cellulose (%) Hemicellulose (%)
43.7 37.0 6.51
Metabolizable energy (MJ/kg) Protein (%)
16.6 8.0
Lignin (%)
5.77
Ether extract (%) Neutral detergent fiber (%)
17.3 25.0
Pectin (%) Total carbohydrates (%) Non fibrous carbohydrates (%)
18.3 58.5 8.31
Acid detergent fiber (%)
19.6
Polyphenols mgeq/g pH Fatty acids Palmitic (%)
4.01 4.7
Nutrients
Passion fruit seed meal
Dry matter (%)
92.2
Organic matter (%)
88.7
Crude protein (%) Gross energy MJ/kg
11.3 23.3
Calcium (%)
11.3
due to the high standard error obtained (Table 5). The AB and GB in blood plasma was not affected (P>0.05) by PFM levels, and A:G ratio even showed the same response, as a consequence of the results obtained for its isolated parameters.
Stearic (%) Oleic (%) Linoleic (%)
3.54 19.5 64.0
Discussion
Linolenic (%) Saturated (%) Unsaturated (%)
0.40 15.4 84.6
Experiment 1
25,0 20,0
Ŷ = 16.6x + 0.066 r² = 0.97
15,0 10,0 5,0 0,0 0,00
0,50 1,00 1,50 Intake of passion fruit seed meal (kg)
DE intake according to the consumption of the PFM
a)
Metabolizable energy intake (MJ)
Fig. 1 Graphical representation of a digestible energy (DE) and b metabolizable energy (ME) of passion fruit seed meal (PFM)
Digestible energy intake (MJ)
(Table 5) so PFM inclusion up to 16 % did not affect any of the evaluated parameters. A decrease in TC was expected according to increasing levels of PFM in the experimental diets, but this parameter was not influenced by PFM inclusion, probably
The obtained CP (11.3 %) and EE (18.8 %) are within the range reported by Romo and Nava (2007), but seeds of passion fruit is a source of fiber, mainly consisting of cellulose, hemicellulose, and pectic substances (Chau and Huang 2004), which is in agreement with NDF and ADF obtained (Table 2). It is well known that increased fiber in diets for 25,0 20,0
Ŷ = 15.0x + 0.0065 r² = 0.95
15,0 10,0 5,0 0,0 0,00
0,50 1,00 1,50 Intake of passion fruit seed meal (kg)
ME intake according to the consumption of the PFM
b)
Trop Anim Health Prod (2015) 47:1397–1403 Table 4
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Growth performance and carcass characteristics of starter pigs fed passion fruit seed meal (PFM)
Parameters
Mean±SEa
PFM inclusion (%)
P value Linb
Quac
30.3±0.34 0.69±0.01
NS NS
NS NS
1.40±0.02 2.03±0.04
NS NS
NS NS
0
4
8
12
16
Initial body weight kg
15.4
15.3
15.5
15.7
15.2
15.4±0.09
Final body weight kg Average daily gain kg
31.5 0.75
29.9 0.68
29.7 0.66
30.7 0.69
29.8 0.68
Feed daily intake kg Feed/Gain
1.44 1.93
1.43 2.10
1.33 2.02
1.35 1.97
1.43 2.13
Loin depth cm
2.45
2.62
2.33
2.49
2.31
2.44±0.05
NS
NS
Backfat thickness cm
0.52
0.49
0.49
0.48
0.52
0.50±0.01
NS
NS
a
Standard error
b
Linear effect
c
Quadratic effect
growing pigs is an undesirable factor, because it decreases the digestibility of nutrients. However, DE (16.6 MJ/kg) and ME (15.0 MJ/kg) were high and superior than those obtained by Perondi et al. (2014) when evaluating PFM for growing pigs, but these authors used a PFM with a higher NDF content (52.0 %). The digestibility and metabolizability coefficients of GE of corn and sorghum (Rostagno et al. 2011) are higher than that obtained for PFM. The high NDF of the PFM may be associated with these results, due to the negative effects of fiber on the energy digestibility. The ME/DE may be associated with the protein quality, since low quality protein, or in excess, leads to a decrease in the ME, because amino acids not used for protein synthesis are catabolized leading to urea excretion (NRC 2012). In this way, the ME/ED obtained (0:90) shows a relationship with the CP utilization, once low DC of CP can be attributed to increases in MM and ADF in the diet, since protein digestibility
Table 5 Blood characteristics of starter pigs fed passion fruit seed meal (PFM)
Parameters
is reduced by around 0.4 and 0.2 g/kg DM for each additional gram of ash and ADF in the diet (Noblet and Perez 1993), partially explaining the CP digestibility obtained (70.5 %) compared with that of conventional feedstuffs. Furthermore, the CP digestibility can also be influenced by high pectin levels (Drochner et al. 2004). Experiment 2 Previous studies with by-products from fruit processing (Pascoal et al. 2010; Noh et al. 2014) demonstrated a high potential to be used in pig diets. In this sense, Perondi et al. (2014) evaluating PFM in pig diets did not observe differences in the performance of growing and finishing pigs, until 16 % of inclusion in the diets. These results corroborates our findings, in which the inclusion levels of PFM did not affect the performance; what may be due to the inclusion of soybean oil and industrial amino acids in the diets, in order to become
Mean±SEa
PFM inclusion (%) 0
4
8
12
16
Plasma urea nitrogen (mg/dL) Total cholesterol (mg/dL) Triglycerides (mg/dL)
16.8 73.1 35.6
17.9 68.6 39.3
17.6 72.4 44.2
16.8 66.1 33.2
18.0 64.3 32.7
Total protein (g/d) Albumin (g/d) Globulin (g/d) Albumin/Globulin Hematocrits (%)
5.42 3.24 2.18 1.49 30.8
5.38 3.18 2.20 1.59 30.7
5.74 3.20 2.54 1.52 30.8
5.48 3.19 2.29 1.42 34.2
5.35 3.10 2.25 1.42 34.7
a
Standard error
b
Linear effect
c
Quadratic effect
P value Linb
Quac
17.4±0.26 68.9±1.71 37.0±2.15
NS NS NS
NS NS NS
5.47±0.07 3.18±0.02 2.29±0.07 1.42±0.03 32.2±0.90
NS NS NS NS NS
NS NS NS NS NS
1402
isoenergetic and with the same amount of amino acids, thereby maintaining the nutritional quality of the diet according to the inclusion of the PFM in the diets. Diets or ingredients with high fiber contents can negatively influence the voluntary intake and nutrient digestibility in young pigs (Wilfart et al. 2007). In this study, besides the fact that PFM inclusion increased the fiber content in the diet, we did not observe negative effects on animal performance, possibly due to the high pectin content of the PFM, unlike celluloses, it is highly degraded in the extensions of the colon (Drochner et al. 2004). In the same way, PFM inclusion did not affect LD and BT, which may have occurred because the diets had the same amount of energy and amino acids, which is important because protein deposition depends on the supply of energy and available amino acids in the diet (Milgen and Noblet 2003). Also, animal performance was similar until 16 % of PFM inclusion in the diet. However, including PFM, it was not economically viable for levels evaluated according to the prices paid by PFM and the others ingredients used in the experimental diets. Pectin is often considered as a potential carbohydrate that decreases plasma cholesterol (Kreuzer et al. 2002), but plasma cholesterol was not affected (Table 5), despite high pectin amounts in the PFM. There is evidence that plasma triglyceride are influenced by energy in the diet. Thus, as the diets were isoenergetic (Table 1), there might not have been differences among the studied treatments. PUN indicates an adequate protein supply (Pedersen and Boisen 2001), indicating that PFM inclusion in the diets were effective when supplemented with amino acids, once this parameter was not affected (Table 5). A moderate protein deficiency may cause a decrease in serum protein, mainly albumin, without altering the globulin content (Miyada et al. 1997). In this study these parameters were not affected and corroborate the results obtained for PUN. There is also an evidence that hematocrit may be related to the lysine content of the diet (Miyada et al. 1997); but in our study, the diets had the same lysine amounts, explaining the similar results obtained (Table 5) for this parameter.
Conclusion From the above experiment, it was evident that the metabolizable energy of the passion fruit seed meal for swine in the starting phase was 15.0 MJ/kg and PFM could be added up to 16 % in the diet without any negative effects on growth performance, carcass, and blood characteristics in starter commercial line pigs.
Conflict of interest The authors declare that they have no conflict of interest.
Trop Anim Health Prod (2015) 47:1397–1403
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