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Cuban Journal of Agricultural Science

Print version ISSN 0864-0408On-line version ISSN 2079-3480

Cuban J. Agric. Sci. vol.53 no.4 Mayabeque Oct.-Dec. 2019  Epub Dec 05, 2019

 

ANIMAL SCIENCE

Effect of the inclusion of beet pulps of different origin on the digestibility and nutritional value of diets for fattening rabbits

O. Arce1  * 

G. Alagón2 

L. Ródenas3 

E. Martínez-Paredes3 

V.J. Moya3 

J.J. Pascual3 

C. Cervera3 

1Facultad de Ciencias Agrarias y Naturales, Universidad Técnica de Oruro, Avda. 6 de octubre 5715, Cas Postal 49, Oruro, Bolivia,

2Facultad de Agronomía y Zootecnia, Universidad Nacional de San Antonio Abad del Cusco, Avda. de la Cultura 733, Ap. Postal 921, Cusco, Perú

3Instituto de Ciencia y Tecnología Animal, Universitat Politècnica de València, Camino de Vera, 14, Valencia 46071, España

ABSTRACT

To determine the digestibility variability of beet pulps (BP) in the nutritional value of diets for fattening rabbits, the substitution of 20 % of a control feed with BP from five different origins was evaluated. Rabbits of 42 days of age and 1.49 ± 0.208 kg of weight were used, housed in individual cages and with ad libitum feeding. The digestibility of feed components was determined by the conventional in vivo method of total fecal collection. The digestibility of each of beet pulps was determined by the substitution method. There was no effect of the substitution of components of the control feed with 20 % of BP from different sources in the voluntary intake of rabbits (P> 0.05). The inclusion of BP in diets increases the digestibility of dry matter, organic matter, gross energy and all fibrous fractions, and decreases the digestibility of crude protein. However, the effect was more or less important depending on the origin of BP (P <0.05), especially on the digestibility of all fibrous fractions, being the BP collected in summer the one with the highest digestibility. The origin of the BP also affected its nutritional value, giving values of digestible energy between 11.8 and 14.5 MJ kg DM-1 and digestible protein between 3.8 and 6.6 %.

Key words: digestibility; energy; beet pulp; Oryctolagus cuniculus

INTRODUCTION

The rabbit (Oryctolagus cuniculus) has many competitive advantages, from the point of view of feeding for its own digestive characteristics, such as cecotrophy or the use of fibrous components of the diet. However, digestive pathologies such as epizootic rabbit enteropathy (ERE), frequent digestive disease in rabbits after weaning (Bäuerl et al.2014 and Badiola et al. 2016), are responsible for 60 % of the total mortality in the fattening period (de Rozas et al. 2005) and for significant reductions in the effectiveness of food use and in the growth of the affected animals that survive.

Although the causative agents have not yet been described, it is known that the disease can be controlled with antibiotics. However, processes such as the emergence of antibiotic-resistant bacteria cause the need to develop nutritional strategies to reduce the use of antibiotics in animal feed, which has stimulated the development of researches aimed at enhancing the use of functional nutrients to maximize the development and functionality of the organism and prevent pathologies (Abad-Guamán et al. 2018).

Due to the digestive physiology of the rabbit, fiber is very important as the main component of the diet responsible for proper digestion, its positive impact on digestion and intestinal health (Cobos, 1993). It is known that moderate levels of soluble fiber in the diet can reduce the mortality of rabbits affected by ERE (Trocino et al. 2013 and Ocasio Vega et al. 2018b). It has been observed that the higher fiber content, both soluble, insoluble or digestible and indigestible, improves the health status of animals under these conditions (Martínez-Vallestín et al. 2013), so that currently the recommendations of feed fiber levels for fattening rabbits usually include all types of fibers (De Blas and Mateos, 2010).

An abundant by-product of sugar industry is beet pulp (BP), which is rich in high digestibility fiber (de Blas et al. 2002). In this regard, Santoma (1989) recommended including BP in feed diets for rabbits and thus avoiding digestive disorders. However, its use has as disadvantages the high variability of some components of its chemical composition according to its origin (Arce et al. 2019), and that the data on its nutritional value are limited and vary according to the evaluation method used in its determination (Carabaño and Fraga, 1992).

This greater inclusion of pulps in rabbit feeds and the variability of the product itself, both in relation to the vegetable variety of beet and that due to the inclusion of molasses or vinasse during the industrial process that generates the by-product, highlights the need to know its nutritional characteristics and digestibility in rabbits. Therefore, the objective of this study was to evaluate the variability of the digestive value of BP included in the feed of fattening rabbits, using BP items from different sugar factories.

MATERIALS AND METHODS

Animals and feeding. The study was carried out in a farm from the Instituto de Ciencia and Tecnología de Producción Animal from the Universidad Politécnica de Valencia. For the experiment, 90 crossed rabbits of Lines R and V, of 42 days old and 1.49 ± 0.208 kg live weight, distributed in 6 groups were used. The animals were placed in independent metabolic cages (44 x 52 x 32 cm), with galvanized sheet metal side walls and metal rods on the roof, floor and front, arranged in two linear batteries placed on a single floor. Each cage was provided with a 1.8 kg capacity galvanized sheet hopper feeder, located in the front part of the cage, automatic bowl-type drinker on the rear wall of the cage and a galvanized sheet metal funnel that covered the entire bottom of the cage, in an inverted cone with a bevel terminal and a plastic bottle with its millimeter mesh screen and protection chamber as a faeces collector, to avoid contamination of feces due to contact with urine.

Six diets were formulated using the Solver application from the Excel program, a basal diet without BP (Control) and five experimental diets (R1 to R5, table 1) in which 20 % of the basal diet was substituted by BP from different factories in Spain (BP1 to 5), which varied in the varieties of beet used and, mainly, in the content of the different fibrous fractions, as shown in table 2.

Table 1 Ingredients (% DM) of the control feed and the different experimental feeds that included beet pulps from different factories. 

Raw matters Control feed Feeds with BP
Barley 2 rows 29 23.1
Wheat bran 17 13.5
BP 1 to 5 0 20
Beet molasses 1 0.8
Sunflower meal 30 8.5 6.8
Henified alfafa 27 21.5
Grape pip 6.5 5.2
Soybean husk 3.3 2.6
Oat husk 3.3 2.6
Soybean olein 2 1.6
DL-Methionine 0.06 0.05
L-Lisyne 0.3 0.26
L-Threonine 0.18 0.15
L-Tryptophan 0.1 0.08
Calcium carbonate 0.46 0.46
Sodium chloride 0.5 0.5
1Vitamin corrector 0.5 0.5
2Antibiotics 0.3 0.3

1Vitamin corrector and trace elements (L511R; Trouw Nutrition España, S.A.): Vitamin A:

8.375 IU; vitamin D3: 750 IU; vitamin E: 20 mg; Vitamin K3: 1 mg; vitamin B1: 1 mg; vitamin B2: 2 mg; vitamin B6: 1 mg; nicotinic acid: 20 mg; choline chloride: 250 mg; magnesium: 290 mg; manganese: 20 mg; zinc: 60 mg; iodine: 1.25 mg; iron: 26 mg; copper: 10 mg; cobalt: 0.7 mg; mixture of butyl hydroxylanysole and ethoxiquin: 4 mg.

2Dinco-spectim (29ppm dincomycin + 29 ppm espectinomycin), 120 ppm neomycin, Apsamix Tiamulin (50 ppm tiamulin) normally used in rabbit farms with a high incidence of epizootic enteropathy).

Table 2 Chemical composition (% DM) of beet pulps (BP 1 to 5) used in the formulation of experimental feed. 

Indicator BP1 BP2 BP3 BP4 BP5
Ashes 8.4 5.6 6.8 7.4 7.2
Crude protein 9.5 8.4 8.0 8.9 8.6
CP linked to NDF 4.0 6.2 6.1 8.3 5.2
Starch 1.1 1.5 1.2 0.9 0.5
Crude fat 1.1 1.3 1.4 1.2 1.0
N DF 35.2 36.7 37.1 43.2 41.3
ADF 19.2 20.9 23.3 22.3 23.6
ADL 3.3 3.4 2.53 3.8 2.91
FSND 44.8 49.1 53.4 46.3 35.9

DM: dry matter, CP linked to NDF: crude protein linked to neutral detergent fiber, NDF: neutral detergent fiber, ADF: acid detergent fiber, ADL: acid detergent lignin, FSND: fiber soluble in neutral detergent.

For the formulation of diets, the nutritional requirements of fattening rabbits (de Blas and Mateos 2010) were taken into account and the nutritional value of each diet is shown in table 3.

Table 3 Chemical composition (% DM) of control and experimental feed with the addition of 20 % beet pulp from different factories (R1 to R5). 

Nutrients Feed
Control R1 R2 R3 R4 R5
Control diet 100 80 80 80 80 80
BP 20 20 20 20 20
Nutritional value
Dry matter (%) 90.84 90.98 90.99 90.85 90.89 90.52
Ashes 7.40 7.13 7.11 7.41 7.56 7.44
Crude protein 14.36 13.13 12.79 13.14 13.10 13.49
CP linked to NDF 2.22 2.98 3.81 4.16 3.57 3.50
Starch 18.07 13.91 13.70 14.04 13.50 14.50
Crude fat 4.37 3.69 3.87 3.95 4.07 3.53
GE (MJ kg-1) 18.85 18.79 18.75 18.50 18.70 18.39
NDF 37.81 38.40 36.77 36.90 38.87 38.76
ADF 20.35 20.97 20.48 20.88 21.25 21.38
ADL 5.76 4.86 4.98 5.08 5.09 5.18
Hemicelluloses 17.46 17.43 16.29 16.02 17.62 17.38
Celluloses 14.59 16.11 15.5 15.80 16.16 16.20
FSND 13.25 17.42 15.40 16.95 15.19 16.65

CP linked to NDF: crude protein linked to neutral detergent, GE: gross energy, NDF: neutral detergent fiber, ADF: acid detergent fiber, ADL: acid detergent lignin, FSND: fiber soluble in neutral detergent.

The rabbit feeding was ad libitum during all the research.

Determination of feed digestibility. The digestibility of feeds was determined directly by the conventional method in vivo by total fecal collection, with an adaptation period of 7 days and another of 4- day collection (Pérez et al. 1995). Daily checks were performed at 8:00 a.m. The feces were stored in well-identified polyethylene bags and stored at -20°C until complete collection. Then they were dried in an oven at 60°C until constant weight. Subsequently, the dried material was milled to a particle size of 1 mm and kept in tightly sealed bottles until used for the corresponding chemical analyzes.

The apparent digestibility (CD) of dry matter (DM), organic matter (OM), gross energy (GE), crude protein (CP), crude fat (CF), neutral detergent fiber (NDF), acid detergent fiber (ADF), hemicelluloses (HE), celluloses (CE) and fiber soluble in neutral detergent (FSND) was determined of each of feeds, using the following formula:

CD, % =Ingested amount gExcreted amount gIngested amount gx100

Chemical analysis. The chemical analyzes of BP, feed and feces were carried out by the official methods of the AOAC (2016) for DM, total ashes (TA), CP, crude protein linked to neutral detergent fiber (CPNDF), GF, NDF, ADF and acid detergent lignin (ADL). The starch (S) and FSND content was also determined by the method based on mass changes between crude fiber wastes from Ankom extraction, ethanol insoluble wastes and fat extraction (Martínez-Vallespín et al. 2011). The hemicellulose content was estimated by difference between NDF and DFA and cellulose content by difference between ADF and ADL.

The GE was determined by combustion in an adiabatic calorimetric pump (Gallenkamp) following the EGRAN (2001) recommendations.

Determination of digestible energy and digestible protein of beet pulps: The digestible protein (DP, % DM) and digestible energy (DE, kJ g-1 DM) content of each of the five beet pulps used in experimental feed were calculated according to the substitution method (Villamide et al. 2001), which is based on the principle of addition of the different raw materials that are included in the feed weighted according to their inclusion percentage, and responds to the following mathematical formula:

DPRx= DRx DC x 0.8/0.2

Where:

DPRx

- DE (kJ g-1 DM) or DP (% DM) of beet pulp x (1 to 5),

DRx

- DE (kJ g-1 DM) or DP (% DM) of feed Rx (1 to 5) which contained the BPx,

DC

- DE (kJ g-1 DM) or DP (% DM) of control feed

Statistical analysis. The data were analyzed by analysis of variance in a completely randomized design, with 6 treatments and between 11 to 27 repetitions (rabbits) per treatment, using the GLM procedure of SAS (SAS, 2010), according to the following fixed linear additive model, at a level of significance of α= 0.05:

yij=μ+τi+ij

Where:

i

- Feed (control, R1, R2, R3, R4 and R5)

j

- Rabbits (1, 2, 3… n)

yij

- Observed value of a response variable of the experimental unit that receives the i-th feed in the j-th rabbit.

µ

- General mean

τi

- Variation between treatments (feed)

ij

- Variation between repetitions (rabbits)

RESULTS AND DISCUSSION

Feed digestibility. Following the Pérez et al. (1995) recommendations, during the experimental development two rabbits were removed for showing symptoms of digestive dysfunction, the rest of the animals without any symptoms showed a weight gain of 50 g day-1, which is an adequate value for these animals.

Table 4 shows the obtained results regarding intake and apparent digestibility of feed. There was no effect of the substitution of components of the control diet for 20% of BP from different sources in the voluntary intake of rabbits (P> 0.05).

The inclusion of BP increased the apparent digestibility of the DM, OM and GE of the diet (P <0.001), which seems to be a consequence of the increased digestibility of all fibrous fractions (NDF, ADF, CE and HE, and FSND, P <0.001), regarding the control diet.

However, these increases were variable according to the BP that would have been included in the diet. The DMD and OMD increased between 2 to 5 % and the GED between 2 and 7 %, except the R4 diet, which increase was not significant regarding the control diet and which contained the BP with the highest values of insoluble fibers (NDF, ADF and ADL).

Table 4 Effect of the replacement of 20 % of the control feed by beet pulp from different factories (R1 to R5) on the ingestion and apparent digestibility in rabbits (mean ± standard error). 

Control R1 R2 R3 R4 R5 P value
DMI (g d-1) 139.0±3.7 120.0±5.6 126.0±5.9 136.0±5.6 131.0±5.6 131.0±5.4 0.1089
DMD (%) 59.3±0.5a 61.6±0.7bc 62.9±0.7c 61.4±0.7bc 60.0±0.7ab 62.8±0.7c <0.001
OMD (%) 59.3±0.5a 62.1±0.7bc 63.2±0.7c 61.6±0.7bc 60.2±0.7ab 62.6±0.7c <0.001
GED (%) 58.0±0.4a 61.6±0.7c 62.1±0.7c 60.6±0.7bc 59.4±0.7ab 61.3±0.7bc <0.001
CPD (%) 72.1±0.7c 68.9±1.0ab 69.6±1.1abc 68.9±1.0ab 68.6±1.0a 71.7±1.0bc 0.0143
DNDF (%) 22.4±0.7a 30.9±1.1cd 30.2±1.2bcd 26.9±1.1b 28.4±1.1bc 31.9±1.1d <0.001
DADF (%) 11.5±0.9a 18.5±1.4b 19.2±1.4b 14.9±1.4ab 16.0±1.4b 18.3±1.3b <0.001
HED (%) 35.3±0.8a 45.9±1.3bc 44.1±1.3bc 42.4±1.3b 43.2±1.3b 46.9±1.2c <0.001
CED (%) 16.6±1.1a 24.5±1.7bc 24.4±1.8bc 18.5±1.7a 19.8±1.7ab 26.7±1.6c <0.001
DFSND (%) 64.5±0.4a 72.8±0.6c 72.8±0.6c 74.6±0.6c 69.1±0.6b 74.1±0.5c <0.001

abcdMeans with different letters on the same row are significantly different (P <0.05).

DMI=dry matter intake; DMD = dry matter digestibility; OMD = organic matter digestibility; GED = gross energy digestibility; CPD = crude protein digestibility; DNDF = digestibility of neutral detergent fiber; DADF = digestibility of acid detergent fiber; CED = cellulose digestibility; HED = hemicellulose digestibility; DFSND = digestibility of fiber soluble in neutral detergent

The digestibility of the soluble fiber fraction was significantly higher (P <0.001) in all R feeds versus control feed. The feed that included BP with higher FSND content recorded higher increases in the digestibility coefficient (13 % for R1 and R2, and 16% for R3), with the exceptions of feed R4, which registered the lowest increase (7 %) despite that the value of FSND was high, and of the R5 feed, with an increase of 16 %, despite having the lowest content in FSND. The obtained results on the digestibility of the FSND fraction can be affected by interactions with the secretion of intestinal mucin (Abad-Guamán et al. 2015), but they may also be very affected by the analytical method of determining this fraction, since the increases of the fraction in experimental feed have been lower than expected (between -6 % for R5 and -25 % for R2) according to the concentration of FSND obtained in the analysis of raw matter, therefore, it would be desirable to review the real value of this determination.

Increases in feed digestibility coefficients when including variable proportions of BP have been recorded by other authors (de Blas and Villamide, 1990, García et al. 1993, Carabaño et al. 1997, Gidenne and Jehl 1996, Falcao- e-Cunha et al. 2004, Gómez-Conde et al. 2007 and 2009, Xiccato et al. 2011 and Trocino et al. 2013), showing great variability in the values obtained by each other in the digestibility of the different fractions.

The chemical composition of the fibrous fractions is very complex because it includes very different groups of molecules (Gidenne 2003), and the fiber of the BP has particular characteristics, such as the high value of FSND, but also of soluble and insoluble non-starchy polysaccharides and other non-water soluble cell wall carbohydrates, such as some pectins (Gidenne et al. 2010), whose digestibility can be highly variable, both in ileum and caecum.

Therefore, it seems that the analytical separation of the fibrous fractions in soluble and non-soluble in neutral detergent is not sufficient to interpret the variability in the digestion of the fibrous components, main fractions of the BP, and a more precise analysis that assesses concrete chemical groups would be necessary.

Coinciding with that recorded by other authors, the incorporation of BP into the diet decreased the CPD component compared to the control feed (P <0.05), despite the low CP content of the BP, which could be linked to the fact that most part of CP is linked to the NDF fraction (Arce et al. 2019), which makes digestion difficult. The DP content of the different BP was low (table 5), mainly due to their low value in CP, but also because the digestibility coefficients between the different BP significantly varied (P <0.05), with higher values in the BP5, which registered a digestibility similar to that of the control feed.

Table 5 Nutritive value of beet pulps evaluated in fattening rabbits. 

Indicators Origin of BP SE P value
BP1 BP2 BP3 BP4 BP5
DP (%) 4.5a 3.8a 5ab 4.2a 6.6b 0.6 0.03
DE (MJ kg-1 DM) 14.1bc 14.5c 12.3ab 11.8a 14.2c 0.6 0.01

DP = digestible protein; DE = digestible energy; SE = standard error

The digestible energy content of pulps was in the range of digestible energy values reported for this by-product by other authors (table 5), which average value in rabbits is 12.52 MJ kg-1 DM(Papadomichelakis et al. 2004),that is higher than the digestible energy content of alfalfa (Medicago sativa), the source of fiber most commonly used in rabbit diets, in which the average content was reported as 8.9 MJ kg-1 DM (Fernández-Carmona et al. 1998), and represents 56.7 % of the gross energy contained in the diets intake by the rabbit (Machado et al. 2012).

But the origin of the BP also significantly affects the DE values (P <0.05). Other studies have found high variability of the digestible energy content of BP used in rabbit feeding (9.6 to 14.2 MJ kg-1 DM), attributed to the type of basal diet or the inclusion level of this by-product in the diet (de Blas and Carabaño, 1996). From the available information, these authors suggested a value of 10.5 MJ kg-1 DM for this by-product, for an inclusion level of 15 %; suggesting that this by-product be considered as an energy concentrate for rabbits, due to its highly digestible fiber content (de Blas et al. 2003). However, that value may vary according to the type of basal diet and the inclusion level in the diet. At 15 % of inclusion, the digestible energy is 9.6 MJ kg-1 DM (García et al. 1993); while at 40 % of replacement, the value increases to 12.3 MJ kg-1 DM (Maertens and d Groote 1984); and when the pulp is offered alone, the value reaches 14.2 MJ kg-1 DM (Martínez and Fernández 1980), evidencing that the digestible energy content of BP varies in direct relation to the replacement level. However, replacements levels above 30 % are not recommended because it affects the intake and yield of rabbits (García et al. 1993 and de Blas and Carabaño 1996).

In this study, the same basal diet and a single inclusion level of BP have been used, but a great variability in the digestibility coefficients has also been obtained, which seems to show that the origin of the BP also affects the DE value, which seems logical given the differences in chemical composition of BP, especially with the different contents in fibrous fractions and, possibly, also with the chemical nature of them.

The BP5 registered a high DE content and showed the highest digestibility coefficients of all fibrous fractions, both soluble and insoluble, which could be linked to plant origin, since it is the only BP obtained from varieties that are collected in summer and present the highest differences in the type of fibers they contain (Arce et al. 2019).

The lowest DE values correspond to BP3 and 4, which also correspond to the lowest digestibility coefficients of insoluble fibers and, in the case of BP4, also soluble fiber (table 3). The low degradability of the NDF of BP3 with respect to the BP1 and BP2 and of the FSND of BP4 compared to the BP1, BP2 and BP3, all varieties harvested in winter, contradicts its composition in these fractions and with the high degradability values reported by other authors (Fernández-Carmona et al. 1996 and de Blas et al. 2002), and could be due to particularities of the industrial extraction process in these industries (Arce et al. 2019).

The increases in the digestibility coefficients found in this study against the control feed are consistent with all the studies carried until now, where it has been shown that BP is a by-product of easy digestion by the microbial flora of the caecum, reaching digestibility values higher than 80 %, as a result of the rapid degradation of sugars and pectins and their low lignin content (Gidenne, 2003).

Despite the limited information on the digestibility of BP fiber, there is a consensus that this component is very important in the fermentation efficiency and caecal health of the rabbit (García et al. 2000, Belenguer et al. 2012, de Blas 2013 and Gidenne 2015). The incorporation of moderate levels of soluble fiber in feed, by incorporating BP, improves the morphology and functionality of the intestinal mucosa of the rabbit (El Abed et al. 2011). This positive effect could be related to both its contribution in soluble fiber and its content of insoluble fermentable fiber, especially at the ileal level (Abad-Guamán et al. 2015). The hydrolysis of the fibrous fractions releases sugars of low molecular weight in the small intestine (Pedersen et al. 2015), and the use of these oligosaccharides-disaccharides derived from the fiber degradation allows the microbiota profile to be modified and improves in some cases the health of animals (Ocasio Vega et al. 2015, 2018a).

However, the interpretation of results is complicated as the complexity of compounds that are included in the fibrous fractions, and that give rise to other concepts, such as total dietary fiber (TDF), insoluble dietary fiber and soluble fiber (SF) is more fully known and its importance in the nutrition and digestive health of rabbits (Trocino et al. 2013), where soluble fiber is part of TDF that includes pectic substances, β-glucans, fructans and gums, and excludes the starch and the neutral detergent fiber (Hall 2003).

Based on the average gross energy value of BP (GE = 17,781 ± 0.198 MJ kg-1DM), estimated in accordance with the Nehring and Haenlein (1973) equation, and its average digestible energy value (DE = 12,757 ± 0.787 MJ kg-1 DM) obtained in the test, it is estimated that this by-product has a high efficiency of gross energy use (k = 0.717 ± 0.044, CV 6.1 %), confirming its goodness as an energy source for the rabbit; which is logical, since it is formed by a high proportion of soluble fiber that promotes the caecal fermentation and improves digestibility in the rabbit (Falcao-E-Cunha et al. 2004, Gómez-Conde et al. 2009, Xiccato et al. 2011 and Maertens et al. 2014).

CONCLUSIONS

The BP is a good source of fiber to include in feed for rabbits, but poor in protein. Its inclusion at 20 % in a conventional feed increases the digestibility coefficients of all fibrous fractions and decreases those of the BP, although the effect is variable depending on the origin of BP, which also influences on its nutritional value, both in content in DE as in DP. It is recommended to include beet pulp in rations for rabbits, as they generally improve their digestibility coefficients.

ACKNOWLEDGMENTS

To the Universidad Técnica de Oruro, Instituto de Ciencia y Tecnología Animal de la Universitat Politècnica de Valencia and the office of Acción Internacional de la Universidad Politécnica de Valencia for the financial support of the research

REFERENCIAS

Abad-Guamán, R. Carabaño, R. Gómez-Conde, M. S. & García, J. 2015. Effect of type of fiber, site of fermentation, and method of analysis on digestibility of soluble and insoluble fiber in rabbits. J. Anim. Sci. 93 (6): 2860-2871. doi:10.2527/jas2014-8767, ISSN:1525-3163 (web) [ Links ]

Abad-Guamán, R., Delgado, R., Ocasio Vega, C., Nicodemus, N., Carabaño, R. & García, J. 2017. Fibra soluble y fermentable para mejorar salud intestinal en conejos. Boletín de Cunicultura 186: 38-40. ISSN: 1696-6074 [ Links ]

AOAC. 2016. Official methods of analysis of AOAC International. 20th ed., Rockville, MD: AOAC International, ISBN: 978-0-935584-87-5, Available: Available: http://www.directtextbook.com/isbn/9780935584875 , [Consulted: June 22, 2018]. [ Links ]

Arce O., Alagón G., Ródenas L., Martínez-Paredes E., Moya V.J., Pascual J.J., & Cervera C. 2019. Efecto de la época de cosecha en las características químicas de la pulpa se remolacha azucarera (Beta vulgaris) granulada. Nota técnica. Cuban J. Agric. Sci., 53 (1): 1-7, ISSN: 2079-3480 [ Links ]

Badiola, I., de Rozas, A., González, J. Aloy, N. García, J. & Carabaño, R. 2016. Recent advances in ERE in growing rabbits. In: Proceedings 11th World Rabbit Congress. Eds. Qin, Y., F. Li, T. Gidenne. 15-18 June, Qingdao, China. ISSN 2308-1910 [ Links ]

Bäuerl, C., Collado, M.C., Zúñiga, M., Blas, E. & Pérez Martínez, G. 2014. Changes in cecal microbiota and mucosal gene expression revealed new aspects of epizootic rabbit enteropathy. PloS One 9:e105707. doi:10.1371/journal.pone.0105707, ISSN: 1932-6203 [ Links ]

Belenguer, A., Abecia, L., Belanche, A., Milne, E. & Balcells, J., 2012. Effect of carbohydrate source on microbial nitrogen recycling in growing rabbits. Livest. Sci., 150 (1-3): 94-101. https://doi.org/10.1016/j.livsci.2012.08.005, ISSN‎: ‎1871-1413 [ Links ]

Carabaño, R., De Blas, C., García, J., Nicodemus, N. & Pérez de Ayala, P. 1997. Necesidades de fibra. XIII Curso de Especialización FEDNA. Madrid. 16 p. [ Links ]

Carabaño, R. & Fraga, M.J., 1992. The use of local feeds for rabbits. Options Mediterranéennes - Série Séminaires Nº 17, 141 - 158. ISSN: 1811-3419 [ Links ]

Cobos, A., 1993. Influencia de la dieta en la composición lipídica de la carne de conejos. PhD. Thesis. Universidad Complutense de Madrid. 256 pp. [ Links ]

de Blas, J. C. 2013. Nutritional impact on health and performance in intensively reared rabbits. Animal, 7 (s1): 102-111. doi: 10.1017/S1751731112000213, ISSN: 1751-732X (Online) [ Links ]

de Blas, C. & Carabaño, R. 1996. A Review on the Energy value of Sugar Beet Pulp for Rabbits. World Rabbit Sci., 4 (1), 33-36. https://doi.org/10.4995/wrs.1996.268, ISSN: 1257-5011 [ Links ]

de Blas, C., García, J., Gómez-Conde, S. & Carabaño, R. 2002. Restricciones a la formulación de piensos para minimizar la patología digestiva en conejos. XVIII curso de especialización FEDNA, Barcelona, FEDNA, 163: 73- 93 [ Links ]

de Blas, C. & Mateos, G.G. 2010. Feed formulation. En: de Blas, C., and Wiseman, J. (eds). Nutrition of the Rabbit, 2nd Edition. Cabi, Cambridge. 222-232. ISBN 978-1-84593-669-3 [ Links ]

De Blas, C., Mateos, G.G. and García-Rebollar, P. 2003. Tablas FEDNA de composición y valor nutritivo de alimentos para la fabricación de piensos compuestos. Segunda edición. FEDNA, Madrid: 296-299. [ Links ]

De Blas, C. & Villamide, M. J. 1990. Nutritive value of beet pulp for rabbits. Anim. Feed Sci. Tech., 31 (3-4), 239-246. https://doi.org/10.1016/0377-8401(90)90128-U, ISSN: 0377-8401 [ Links ]

de Rozas, A.M.P., Carabaño, R., García, J., Rosell, J., Cano, J. V.D., García, J.B., Rosell, J., Díaz, J.V., Barbé, J., Pascual, J.J. & Badiola, I. 2005. Etiopatogenia de la enteropatía epizoótica del conejo. In: Actas XXX Symposium de Cunicultura: Valladolid, 19 y 20 de mayo de 2005: 167-174. [ Links ]

EGRAN. 2001. Technical note: Attemps to harmonize chemical analyses of feeds and faeces for rabbit feed evaluation. World Rabbit Sci., 9 (2): 57-64. https://doi.org/10.4995/wrs.2001.446, ISSN: 1257-5011 [ Links ]

El Abed, N., Delgado, R., Abad, R, C. Romero, C., Villamide, M. J., Menoyo, D., Carabaño, R. & García, J. 2011. Soluble and insoluble fibre from sugar beet pulp enhance intestinal mucosa morphology in young rabbits. In: Proc. 62nd Annual meeting of the European Federation (Stavanger, Norway) of Animal Science, Book of abstracts. Wageningen Academic Publishers, Wageningen, The Netherlands. p. 159. DOI: 10.3920/978-90-8686-731-8, ISBN: 978-90-8686-177-4 [ Links ]

Falcao-E-Cunha, L., Peres, H., Freire, J. P. & Castro-Solla, L. 2004. Effects of alfalfa, wheat bran or beet pulp, with or without sunflower oil, on caecal fermentation and on digestibility in the rabbit. Anim. Feed Sci. Tech., 117 (1-2): 131-149. https://doi.org/10.1016/j.anifeedsci.2004.07.014, ISSN: 0377-8401 [ Links ]

Fernández-Carmona, J., Bernat, F., Cervera, C. & Pascual, J. J. 1998. High lucerne diets for growing rabbits. World Rabbit Sci., 6 (2): 237-240. https://doi.org/10.4995/wrs.1998.350, ISSN: 1257-5011 [ Links ]

Fernández-Carmona, J., Cervera, C. & Blas, E. 1996. Prediction of the energy value of rabbits feeds varyng widely in fibre content. Anim. Feed Sci. Tech., 64 (1): 61-75. https://doi.org/10.1016/S0377-8401(96)01041-3, ISSN: 0377-8401 [ Links ]

Fraga, M., Pérez, de Ayala, P., Carabaño, R. & De Blas, J C. 2011. Effect of type of fiber on the rate of passage and on the contribution of soft feces to nutrient intake of finishing rabbits. J. Anim. Sci. , 69 (4): 1566-1574. https://doi.org/10.2527/1991.6941566x, ISSN:1525-3163 (web) [ Links ]

Garcia, G., Galvez, J. F. & de Blas, J. C. 1993. Effect of substitution of sugar beet pulp for barley in diets for finishing rabbits on growth performance and on energy and nitrogen efficiency. J. Anim. Sci., 71 (7): 1823-1830. https://doi.org/10.2527/1993.7171823x, ISSN:1525-3163 (web) [ Links ]

García, J., Carabaño, R. , Pérez -Alba, L. & de Blas, J. C. 2000. Effect of fiber source on cecal fermentation and nitrogen recycled through cecotrophy in rabbits. J. Anim. Sci., 78 (3): 638-646. https://doi.org/10.2527/2000.783638x, ISSN:1525-3163 (web) [ Links ]

Gidenne, T. 2003. Fibres in rabbit feeding for digestive troubles prevention: respective role of low-digested and digestible fibre. Livest. Prod. Sci., 81 (2-3):105-117. https://doi.org/10.1016/S0301-6226(02)00301-9, ISSN: 0301-6226 [ Links ]

Gidenne, T. 2015. Dietary fibres in the nutrition of the growing rabbit and recommendations to preserve digestive health: a review. Animal, 9 (2): 227-242. https://doi.org/10.1017/S1751731114002729, ISSN: 1751-732X (Online) [ Links ]

Gidenne, T., Carabaño, R., García, J. & de Blas, C. 2010. Fibre digestion. En: de Blas, C. , and Wiseman, J. (eds). Nutrition of the Rabbit, 2nd Edition. Cabi, Cambridge. 66-82. ISBN 978-1-84593-669-3 [ Links ]

Gidenne, T. & Jehl, N. 1996. Replacement of starch by digestible fibre in the feed for the growing rabbit. 1. Consequences for digestibility and rate of passage. Anim. Feed Sci. Tech., 61 (1-3): 183-192. https://doi.org/10.1016/0377-8401(95)00937-X, ISSN: 0377-8401 [ Links ]

Gómez-Conde, M. S., Garcia, J., Chamorro, S., Eiras, P., Rebollar, P. G., Pérez de Rozas, A., Badiola, I., de Blas, C. & Carabaño, R. 2007. Neutral detergent-soluble fiber improves gut barrier function in twenty-five-day-old weaned rabbits. J. Anim. Sci., 85 (12): 3313-3321. https://doi.org/10.2527/jas.2006-777, ISSN:1525-3163 (web) [ Links ]

Gómez-Conde, M.S., Pérez de Rozas, A., Badiola, I., Perez-Alba, L., de Blas, C., Carabaño, R. & García, J. 2009. Effect of neutral detergent soluble fibre on digestion, intestinal microbiota and performance in twenty five day old weaned rabbits. Livest. Sci., 125 (2):192-198. DOI: 10.1016/j.livsci.2009.04.010, ISSN‎: ‎1871-1413 [ Links ]

Hall, M.B. 2003. Challenges with nonfiber carbohydrate methods. J. Anim. Sci., 81 (12): 3226-3232. https://doi.org/10.2527/2003.81123226x, ISSN:1525-3163 (web) [ Links ]

Machado, L. C., Ferreira, W. M. & Scapinello, C. 2012. Apparent digestibility of simplified and semi-simplified diets, with and without addition of enzymes, and nutritional value of fibrous sources for rabbits. R. Bras. Zootec., 41 (7): 1662-1670. http://dx.doi.org/10.1590/S1516-35982012000700015, ISSN 1806-9290 (On line) [ Links ]

Maertens, L. & de Groote, G. 1984. Digestibility and digestible energy of a number of feedstuffs for rabbits. In: Proc. 3rd World Rabbit Congress, pp 244-251, Roma. [ Links ]

Maertens, L., Guermah, H. & Trocino, A. 2014. Dehydrated chicory pulp as an alternative soluble fibre source in diets for growing rabbits. World Rabbit Sci., 22 (2): 97-104. https://doi.org/10.4995/wrs.2014.1540, ISSN: 1257-5011 [ Links ]

Martínez, J. & Fernández, J. 1980. Composition, digestibility, nutrive value and relation among them of several feeds for rabbits. In: Proc. 2nd World Rabbit Congress, pp 214-223. Barcelona. [ Links ]

Martínez-Vallespín, B., Navarrete, C., Martínez-Paredes, E., Ródenas, L., Cervera, C. & Blas, E. 2011. Determinación de la Fibra Soluble en Detergente Neutro: Modificaciones del Método Original. In: Proc. AIDA. XIV Jornadas sobre Producción Animal, 1. Zaragoza, 291-293. ISBN Obra C.: 978-84-615-0062-8 [ Links ]

Martínez-Vallespín, B., Martínez-Paredes, E., Ródenas, L., Moya, V.J., Cervera, C., Pascual, J.J. & Blas, E. 2013. Partial replacement of starch with acid detergent fiber and/or neutral detergent soluble fiber at two protein levels: Effects on ileal apparent digestibility and caecal environment of growing rabbits. Livest. Sci., 154 (1-3): 123-130. https://doi.org/10.1016/j.livsci.2013.02.012, ISSN‎: ‎1871-1413 [ Links ]

Nehring, K. & Haenlein, G. F. W. 1973. Feed evaluation and ration calculation based on net energy fat. J. Anim. Sci., 36 (5): 949-964. ISSN: 1525-3163 (web) [ Links ]

Ocasio-Vega, C., Abad-Guamán, R., Delgado, R., Carabaño, R. , Carro, M. D. & García, J. 2018a. Effect of cellobiose supplementation and dietary soluble fibre content on in vitro caecal fermentation of carbohydrate-rich substrates in rabbits. Archives Anim. Nutr., 72 (3): 221-238. https://doi.org/10.1080/1745039X.2018.1458459, ISSN: 1745-039X [ Links ]

Ocasio-Vega, C., Abad Guamán, R., Kimiaeitalab, M.V., Kühn, G., Vanegas, J., Delgado, R., Menoyo, D., Nicodemus, N., Carro, M.D, Carabaño, R. M. & García, J. 2015. Efecto del nivel de fibra soluble y de la suplementación con celobiosa sobre los rendimientos productivos en conejos en cebo. In: "XL Symposium de Cunicultura de ASESCU", 28-25 de mayo de 2015, Santiago de Compostela. p. 4. ISBN: 978-84-92928-42-2 [ Links ]

Ocasio-Vega, C., Delgado, R., Abad-Guamán, R., Carabaño, R. , Carro, M.D., Menoyo, D. & García, J. 2018b. The effect of cellobiose on the health status of growing rabbits depends on the dietary level of soluble fiber. J. Anim. Sci. , 96 (5), 1806-1817. doi: 10.1093/jas/sky106, ISSN: 1525-3163 (web) [ Links ]

Papadomichelakis, G., Fegeros, K. & Papadopoulos, G. 2004. Digestibility and nutritive value of sugar beet pulp, soybean hulls, wheat bran and citrus pulp in rabbits. Epitheorese-Zootehnikes-Epistemes, 32:15-27. ISSN: 1413-5736 [ Links ]

Pedersen, M.B., Yu, S., Arent, S., Dalsgaard, S., Bach Knudsen, K.E. & Lærke, H.N. 2015. Xylanase increased the ileal digestibility of nonstarch polysaccharides and concentration of low molecular weight nondigestible carbohydrates in pigs fed high levels of wheat distillers dried grains with solubles. J. Anim Sci. 93 (6): 2885-2893. doi: 10.2527/jas.2014-8829, ISSN: 1525-3163 [ Links ]

Pérez , J. M., Lebas, F., Gidenne, T., Maertens, L., Xiccato, G., Parigi-Bini, R., Dalle Zotte, A., Cossu, M. E., Carazzolo, A., Villamide, M. J., Carabaño, R. , Fraga, M. J., Ramos, M. A., Cervera, C., Blas, E., Fernandez, J., Falcao E Cunha, L. & Bengala Freire, J. 1995. European reference method for in vivo determination of diet digestibility in rabbits. World Rabbit Sci. , 3 (1): 41-43. https://doi.org/10.4995/wrs.1995.239, ISSN: 1257-5011 [ Links ]

Santoma, G. 1989. Últimos avances en la alimentación del conejo. Boletín de cunicultura, 46: 19 - 39. ISSN: 1696-6074 [ Links ]

SAS. 2010. User’s guide: statistics version 9.2. (32) Statistical Analysis Systems Institute Inc., Cary (North Caroline, USA). [ Links ]

Trocino, A., Garcia, J., Carabaño, R. & Xiccato, G. 2013. A metaanalysis on the role of soluble fibre in diets for growing rabbits. World Rabbit Sci., 21 (1): 1-15. http://dx.doi.org/10.4995/wrs.2013.1285, ISSN: 1257-5011 [ Links ]

Villamide, M.J., Maertens, L., Cervera, C., Perez, J.M. & Xiccato, G. 2001. A critical approach of the calculation procedures to be used in digestibility determination of feed ingredients for rabbits. World Rabbit Sci., 9 (1): 19-25. https://doi.org/10.4995/wrs.2001.442, ISSN: 1257-5011 [ Links ]

Xiccato, G., Trocino, A., Majolini, D., Fragkiadakis, M. & Tazzoli, M. 2011. Effect of decreasing dietary protein level and replacing starch with soluble fibre on digestive physiology and performance of growing rabbits. Animal, 5 (8): 1179-1187. doi: 10.1017/S1751731111000243, ISSN: 1751-732X (Online). [ Links ]

Received: February 05, 2019; Accepted: June 24, 2019

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