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Cuban Journal of Agricultural Science

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

Cuban J. Agric. Sci. vol.52 no.4 Mayabeque Oct.-Dec. 2018  Epub Sep 21, 2018


Animal Science

Macroarchitecture of digestive organs in rabbits fed with varying levels of moringa (Moringa oleifera) forage meal

Y. Caro1  * 

Daymara Bustamante1 

L.E. Dihigo1 

J. Ly1 

1Instituto de Ciencia Animal, Apartado Postal 24, San José de las Lajas, Mayabeque, Cuba


Gastrointestinal morphology indices in 24 White New Zealand rabbits were examined, with an average weight of 2.0 kg, fattened ad libitum and randomly with varying levels (0.15 and 30 %) of moringa (Moringa oleifera) forage meal. There was not significant effect (P > 0.05) of the treatment on the relative content of fresh digesta (average, 116.7 g/kg live weight). The weight of the entire empty digestive tract seemed to slightly decrease in a significant way (R2, 0.884, P <0.040) with the introduction of moringa forage in the food (80.6, 79.8 and 76.1 g/kg live weight). There was not significant interdependence (P> 0.05) between the relative weight of fresh digesta and the tract of the evaluated rabbits. The moringa forage determined a longer small intestine (P <0.05) with a lower linear density (P> 0.10). It is concluded that the use of moringa forage meal to fatten rabbits can determine few changes in the gastrointestinal macroarchitecture of the animals.

Key words: rabbits; gastrointestinal tract; digestive organs; digesta


The use of tropical foliages in rabbit feeding is a subject of interest for countries in which conventional systems of rabbit production (McNitt et al. 2000) may not be sustainable if locally available foliar sources are not used (Dihigo et al. 2001, 2008, Phinmasan et al. 2004, Pok Samkol et al. 2005, Nieves 2008 and Nieves et al. 2009 a, b). Moringa (Moringa oleifera) is one of the tropical foliages that could be of interest to feed rabbits (Pérez et al. 2010). Moringa is a plant species whose foliage is characterized by having an appreciable protein level and, in turn, low cell wall content. This foliage usually has high in vitro ileal digestibility of N (Ly et al.2001 and Mireles et al. 2017).

The yields of moringa foliage, as well as its chemical composition, have motivated the study of its nutritional value in rabbits in different tropics regions, particularly when the food is supplied in granular form or in multi-blocks (Odeyinka et al. 2008, Nuhu 2010, Rodríguez 2010, Adenji and Lawal 2012 and Vivas 2014) and not as meal (Caro et al. 2018).

The gastrointestinal tract of rabbits has particularities that notably differentiate it from other farm animals. Its characteristics allow through the caecotrophy, the successful extraction of valuable nutrients from the forages that are supplied (Lebas et al. 1986 y Carabaño and Piquer 1998). From the morphological point of view, it has been found that the different digestive segments grow at different speeds, between three and seven weeks of age (Lebas and Laplace 1972). From the point of view of the influence of food ingested by the rabbit, different characteristics of the macroarchitecture of the gastrointestinal tract have been associated with feeding strategies and with the yield of the carcasses (Gidenne et al. 2012), so the traits of the digestive organs may also have a practical interest.

Under feeding conditions with tropical forages, there is little information about the interdependence between this type of rabbit feeding and the morphological characteristics of the alimentary canal of animals, especially when rabbits are fed with moringa foliage (Odeyinka et al. 2008, Dougnon et al. 2012 and Odetola et al. 2012).The objective of this study was to determine if there are changes in the gastrointestinal macroarchitecture of rabbits fed with varying levels of moringa forage meal in the diet.

Materials and Methods

The research was developed jointly in the Instituto de Ciencia Animal and in a non-state farm, of provincial reference, located in Madruga municipality, Mayabeque province, between June and August 2012.

The tree species Moringa oleifera accession Supergenius (India) was evaluated. This forage was obtained in the forage area from the Instituto de Ciencia Animal. It was established on typical red ferralitic soil, with rapid desiccation and uniform profile (Hernández et al. 1999).

Experimental procedure. In the Estación Experimental de Pastos y Forrajes "Miguel Sistach Naya", belonging to the Instituto de Ciencia Animal, the cultivation of M. oleifera var. Supergenius was established. The sowing was manually done, at a density of 100 000 plants/ha in a circumscribed area of 200 m2. For the forage processing, the whole plant was sampled and a second cut was carried out about 60 d after the previous cut. The cut of this forage was manually made, at a height of 30 cm above soil level. The process of drying the material was done in the shade for a period of five days, in order to reduce the humidity.

To facilitate the drying of this material, as well as undesired fermentative processes, it was preceded to turning three times a day with a rake, taking into account a bedding height less than 30 cm. Then, it was reduced to a 3 mm particle size, in a hammer mill and the meal was stored in 50 kg jute sacks until use.

Samples were taken from six sacks, previously homogenized. In order to obtain a representative mixture of approximately 1 kg, the contents of the sack were spread on a clean and flat surface for random sampling. The particle size was reduced to 1 mm in a hammer mill and then passed through a sieve of equal size to ensure a uniform size. The mixture was packed in glass bottles with a hermetic seal and stored at room temperature until further analysis (Herrera et al. 1986). The composition of the material under study is shown in table 1.

Animals and experimental diets. Twenty-four White New Zealand male rabbits of 45 d of age and initial live weight of ± 885 g were used. The animals were allocated in individual galvanized wire metal cages, equipped with a linear feeder and an automatic nipple drinker. The total duration of the experiment was 45 d.

Table 1 Proximal composition of moringa forage meal 

The composition of the experimental diets is shown in table 2. The diets were formulated according to the nutritional needs of protein and energy, established by Machado et al. (2011). They were isoproteic and isoenergetic. The treatments consisted on a control diet and the inclusion of 15 % and 30 % moringa forage meal. The diets were supplied as meal. During the experimental period the animals had food and water ad libitum. The food was offered in two portions (8:00 a.m. and 6:00 p.m.) daily.

Table 2 Chemical composition of experimental diets (percent in dry base) 

1 Each kg contains: vitamin A, 12 000 UI; vitamin D3, 2000 UI; vitamin B2,4160 UI, niacin, 16 700 UI, pantothenic acid , 8200 UI; vitamin B6, 3420 UI; folic acid, 0.98 g; vitamin B12, 16 mg; vitamin K, 1560 UI; vitamin E, 16 g; BHT, 8.50 g; cobalt, 0.75 g, copper; 3.50 g, iron, 9.86 g; manganese, 6.52 g; sodium, 0.87 g; zinc, 42.4 g; selenium, 6.60

Experimental procedure. The animals were slaughtered at the end of the period with 90 d of age and average weight ± 2.0 kg. After the laparatomy, the digestive tract was ligated in different places to avoid movements of digesta and four segments were isolated: stomach, small intestine, caecum and colon/ rectum. The organs were weighed full and empty. The difference between both weights was considered as the content of fresh digesta.

Morphometric indicators. The fresh weight of the gastrointestinal tract and each digestive organ was expressed as weight relative to live weight (g/kg) and percentage contribution of the digestive organs with respect to the total weight of the gastrointestinal tract (GIT), in %. The length of the intestinal segments was expressed relative to live weight (cm/kg), while the linear density was determined as relative weight of the intestines between their relative lengths (g/cm).

The digestive content of the stomach and caecal was expressed as relative weight to liveweight (g/kg) as well as the percentage contribution of the stomach and caecum with respect to the total weight of the GIT (%).

Experimental design and statistical analysis. A completely randomized design with three treatments and eight repetitions was used. The animal represented the experimental unit. The data of the evaluated indices were processed using the analysis of variance technique according to a simple classification, or regression (Steel et al. 1997). In the necessary cases, the means were compared by the Tukey test. Statistical packages of Minitab (2018) and InfoStat version 2012 (Di Rienzo et al. 2012) were used.

Results and Discussion

The data related to the weight of the full and empty digestive organs are shown in tables 3 and 4. In general, the preponderant role-played by the stomach and the caecum corresponded to their percentage contribution to the weight of the entire tract, which is already known (Lebas and Laplace 1972 and Carabaño and Piquer 1998).

The percentage contribution of the full stomach differed between treatments (table 3). The obtained results are comparable with those published by Diz (2013), who evaluated the inclusion of 20, 30 and 40 % of moringa forage meal in a commercial concentrate. In contrast, Dihigo et al. (2001) reported a decrease in the weight of this organ, with the inclusion of 30 and 45 % of sugarcane meal replacing alfalfa in diets for rabbits in fattening. Similarly, Albert (2006) observed a similar trend in guinea pigs that received erythrin forage meal, and explained that this effect could be given by the physical-chemical properties of the fibrous source under study and by the reduction of the digesta permanence.

Table 3 Relative weight (g fresh/kg live weight) and percentage contribution of full digestive organs of rabbits fed with moringa forage meal 

ab Means without common letter in the same row significantly differ from each other (P<0.05)

There was an increase in the percentage contribution of the caecum, as well as a decrease in the relative weight and in the percentage contribution of the empty colon/rectum (table 4) in the animals that intake moringa forage meal with respect to the control. De Blas et al. (2002) suggest that the level and type of dietary fiber influence on the accumulation of digesta in the caecum through its effect on intestinal motility. This performance is determined by the selective process of the fibrous particles that is performed in the caecal-colic segment, as part of the caecotrophy (Gidenne 1996).

Table 4 Relative weight (g fresh/kg live weight) and percentage contribution of empty digestive organs of rabbits fed with moringa forage meal 

ab Means without common letter in the same row significantly differ from each other (P<0.05)

Table 5 shows the longitudinal measurements of the different segments of the intestinal tract.

Table 5 Longitudinal measurements of empty digestive organs of rabbits fed with moringa forage meal 

ab Means without common letter in the same row significantly differ from each other (P<0.05)

The relative length of the small intestine did not differ (P> 0.05) between the treatments in which the different levels of moringa forage meal were included, but with 15 % of this forage differences were observed (P = 0.015) with respect to the control, in which the moringa was absent. In the moringa treatments, the linear density of colon/rectum was lower (P = 0.008). This could be due to the physical- chemical properties of the moringa forage meal. Yu and Chiou (1997) noted that the thickness of the muscle tunic increases because of the distension that causes high levels of fiber in the intestinal segments. In the particular case of moringa, a higher digestibility of the diet (Caro et al. 2018) could imply the presence of lower content of digesta in the posterior regions of the tract, modifying the gastrointestinal architecture as a whole.

Table 6 shows the results corresponding to the fresh digesta of rabbits.

With respect to the relative weight of digesta, this was significantly higher (P = 0.069) in the treatment with 15 % of moringa forage with respect to the control, while these two did not differ from that corresponding to 30 % of tree forage. The percentage contribution of the relative weight of the stomach content showed the same effect (P = 0.025). In contrast, the percent of the relative weight of caecal digesta expressed an opposite effect, with a lower value for 15 % of moringa forage in relation to the treatment without moringa (P = 0.084). This could reflect a change in the site of the gastrointestinal macroarchitecture where the digestive processes of rabbits fed with moringa forage meal take place, with greater importance for the gastric area with respect to the caecal. Dihigo (2007) observed a similar performance when evaluating the effect of different percentages of dehydrated citrus pulp and sugarcane meal on the morphophysiological indicators of the rabbit.

Table 6 Relative weight (fresh g/kg live weight)1 of the digesta content in the digestive organs of rabbits fed with moringa forage meal 

ab Means without common letter in the same row significantly differ from each other (P<0.05)

In this study, there was not significant interdependence (R2, 0.004, P> 0.05) between the relative weight of the fresh digesta and the empty segments of the entire digestive tract. Probably this effect was not significant (P> 0.05), due to the high variability found in this measure. There was also no significant effect of the treatment on the relative weight of all fresh digesta (average, 116.7 g/kg live weight). On the other hand, the relative weight of this tract seemed to slightly decrease in a linear way (R2, 0.884, P <0.040) with the introduction of moringa forage in the diet (figure 1).

Figure 1 Interdependence between moringa forage in diet and the digestive tract of rabbits in fattening (Syx, ± 6.46¸P<0.040). 

Knowing the gastrointestinal macroarchitecture of the rabbit could have immediate practical consequences, from the point of view not so much of the nutritional physiology as of the carcass yield of rabbits. In this sense, the data provided would be a contribution to this knowledge. It is known that in the rabbit there is an inverse relation between the carcass yield and the weight of the digestive organs (De Blas 1992, Lambertini et al. 2006 and Cornejo et al. 2016). As a demonstration, Kuzelov and Atanosoca (2011) found that the weight of the digestive tract could constitute 17.6 % of the animal weight. In the particular case of rabbits fed with moringa foliage, Dougnon et al. (2012) found that the digestive tract ponderally decreased with the increase of foliage in the food, while the opposite occurred with the carcass yield.

Although the evaluation of the carcasses was not an objective of this study, the data of the gastrointestinal macroarchitecture, from the point of view of the weight of the full digestive organs, could suggest, like those of Dougnon et al. (2012) advantages for a higher yield in the animals carcass. However, Nuhu (2010) found that while the carcass yield was 62 and 66 %, with 0 and 20 % of moringa leaves meal, these two treatments determined 16.4 and 16.3 g/kg of live weight for the weight of the full digestive tract. Due to the limited availability of results on this subject, it is obvious that more research is needed.

It is concluded that the use of moringa forage meal to fatten rabbits can determine few changes in the gastrointestinal macroarchitecture of animals. In this species, the digestive physiology of the use of tree forage from tropical nature, locally available, such as moringa, should be researched in detail.


Thanks to the rabbit breeder Gerardo Piloto for providing the animals and facilitating their facilities for the development of the research.


Adenji, A.A. & Lawal, M. 2012. Effects of replacing groundnut cake with Moringa oleifera leaf meal in the diets of grower rabbits. International Journal of Molecular Veterinary Research, 2(3):8-13. [ Links ]

Albert, A. 2006. Evaluación biofisiológica de las especies Trichantera gigantea; Morus alba y Erythrina poeppigiana en cuyes, en la región de Topes de Collantes. PhD Thesis. Instituto de Ciencia Animal, La Habana, Cuba. p. 40-53. [ Links ]

Carabaño, R. & Piquer, J. 1998. The digestive system of the rabbit. In: The Nutrition of the Rabbit (C. De Blas y J. Wiseman, editors). CAB International Publishing. Wallingford, p. 1-16. [ Links ]

Caro Y, Bustamante D, Dihigo L E & Ly J 2018: Digestibilidad aparente de nutrientes en dietas de forraje de Moringa oleifera para conejos en crecimiento. Livestock Research for Rural Development. Volume 30, Article #1. Retrieved February 7, 2018, Available: Available: ]

Cornejo, J.G., Rodríguez, L.T., Pro, A., González, F., Conde, V.F., Ramírez, M.E., López, E. & Hernández, A.S. 2016. Efecto del ayuno ante mortem en el rendimiento de la canal y calidad de la carne de conejo. Archivo de Zootecnia, 65(250):171-175. [ Links ]

De Blas, C. 1992. Factores que determinan el rendimiento y la calidad de la canal en conejos. Mundo Ganadero, 7:70-75. [ Links ]

De Blas, C., García, J. & Carabaño, R. 2002. Avances en nutrición de Conejos. Revisión a las principales peculiaridades sistema digestivo de los conejos, que son responsables, entre otras causas, de la complejidad de esta producción. In: XXVII Symposium de Cunicultura de ASESCU. Boletín de Cunicultura 122:1-9. [ Links ]

Dihigo, L. E. 2007. Caracterización físico-química de productos tropicales y su impacto en la morfofisiología digestiva del conejo. PhD Thesis. Instituto de Ciencia Animal, La Habana, Cuba. [ Links ]

Dihigo, L.E., Savón, L., Hernández, Y., Domínguez, M. & Martínez, M. 2008. Physicochemical characterization of mulberry (Morus alba), citrus (Citrus sinensis) pulp, and sugarcane (Saccharum officinarum) meals for the feeding of rabbits. Cuban Journal of Agricultural Science, 42(1): 65-68. [ Links ]

Dihigo, L.E., Savón, L., Orta, M. & Dormynich, F.S. 2001. Morphometric studies of the gastrointestinal tract and internal organs of rabbits consuming sugar cane meals. Cuban Journal of Agricultural Science , 35(4):361-365. [ Links ]

Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. & Robledo, C.W. InfoStat versión 2012. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available: ]

Diz, R. 2013. Comportamiento productivo de conejos que consumen harina de forraje de Moringa oleifera. Master Thesis. Instituto de Ciencia Animal. [ Links ]

Dougnon, T.J., Aboh, B.A., Kpodékon, T.M., Honvou, S. & Youssao, I. 2012. Effects of substitution of pellet of Moringa oleifera to commercial feed on rabbit’s digestion, growth performance and carcass trait. Journal of Applied Pharmaceutical Science, 2(9): 15-19. [ Links ]

Gidenne, T. 1996. Nutritional and ontogenic factors affecting rabbit caeco-colic digestive phisiology. In: Proceedings of 6th World Rabbit Congress. Tolouse, AFC/INRA p. 13-28. [ Links ]

Gidenne, T., Combes, S. & Fortun-Lamothe, L. 2012. Feed intake limitation strategies for the growing rabbit: effect on feeding behavior, welfare, performance, digestive physiology and health: a review. Animal 6(9): 1407-1419. [ Links ]

Hernández, A.; Pérez, J.M. & Busch, O. 1999. Nueva versión de la genética de los suelos de Cuba. Instituto de Suelos. AGROINFOR-MINAG. La Habana. Cuba. p. 64. [ Links ]

Herrera, R., González, S., García, M., Ríos, C. & Ojeda, F. 1986. Análisis químico del pasto. In: Los pastos en Cuba. Segunda Edición. EDICA. p. 701. [ Links ]

Kuzelov, A & Atanosova, E. 2011. Participation of main parts and internal organs in rabbit meat. Biotechnology in Animal Husbandry, 27(1):55-61. [ Links ]

Lambertini, L., Vignola, G., Badiani, A., Zaghini, G. & Formigoni, A. 2006. The effect of journey time and stocking density during transport on carcass and meat quality in rabbits. Meat Science, 72(4):641-646. [ Links ]

Lebas, F., Coudert, P., Rouvier, R. & De Rochambeau, H. 1986. The Rabbit. Husbandry, Health and Production. Roma, p. 235. [ Links ]

Lebas, F. & Laplace, J.P. 1972. Mensurations viscérales chez le lapin. 1. Croissance du foie, des reinset des divers segments intestinaux entre 3 et 11 semaines d´âge. Annales de Zootechnie, 81(1):37-47. [ Links ]

Ly, J, Samkol, P. & Preston, T. R. 2001. Nutritional evaluation of tropical leaves for pigs: Pepsin/pancreatin digestibility of thirteen plant species. Livestock Research for Rural Development . Volume 13, Article #48. Retrieved February 7, 2018, Available: Available: ]

Machado, L.C., Motta, W., Scapinello, C., Sangoi, M. & Castro, A. 2011. Manual de formulação de ração e suplementos para coelhos. Associação Científica Brasileira de Cunicultura. 24 p. ISBN 978- 85-912388-1-1. [ Links ]

McNitt, J., Patton, N., Lukefahn, S. & Cheecke, F. (2000). Rabbit Production. 8va ed. Interstate Publishers, Inc. 483 p. [ Links ]

Minitab. 2018. User´s Guide, Available: http://www.minitab.comLinks ]

Mireles, S., Moreno, E., Pok, Samkol, Caro, Y & Ly, J. 2017. Cut age and N balance in pigs fed with Moringa oleifera foliage meal. Cuban Journal of Agricultural Science , 51(2):191-196. [ Links ]

Nieves, D. 2008. Evaluación de recursos alimenticios tropicales alternativos para conejos (Oryctolagus cuniculus). Trabajo de grado presentado como requisito final para optar al título de Doctor en Ciencias Agrícolas. Universidad Central de Venezuela. 117 p. [ Links ]

Nieves, D., Moncada, I., Terán, O., González, C., Silva, L. & Ly, J. 2009a. Parámetros digestivos en conejos de engorde alimentados con dietas basadas en follajes tropicales. Digestibilidad ileal. Bioagro, 21(1): 33-40. [ Links ]

Nieves, D., Terán, O., Vivas, M., Arciniegas, G., González, C. & Ly, J. 2009b. Comportamiento productivo de conejos alimentados con dietas basadas en follajes tropicales. Revista Científica, FCV-LUZ. 19(2): 173-180. [ Links ]

Nuhu, F. 2010. Effect of moringa leaf meal (molm) on nutrient digestibility, growth, carcass and blood indices of weaner rabbits. A thesis submitted in partial fulfilment of the requirements for the award of Master of Science degree in Animal Nutrition. Kwame Nkrumah University of Science and Technology, Kumasi. 107 p. [ Links ]

Odetola, O.M., Adetola, O.O., Ijadunola, T.I., Adedeji, O.Y. & Adu, O.A. 2012. Utilization of moringa (Moringa oleifera) leaves meal as a replacement for soya bean meal in rabbit’s diets. Scholarly Journal of Agricultural Science, 2(3):309-313. [ Links ]

Odeyinka, S.M., Oyedele, O.J., Adeleke, T.O. & Odedire, T.A. 2008. Reproductive performance of rabbits fed Moringa oleifera as a replacement for Centrosema pubescens. In: 9th World Rabbit Congress. Verona, p. 411-415. [ Links ]

Pérez, A., Sámchez, T., Armengol, N. & Reyes, F. 2010. Características y potencialidades de Moringa oleifera Lamark. Una alternativa para la alimentación animal. Pastos y Forrajes, 33(4):1-20. [ Links ]

Phimmasan, H., Pok, Samkol & Ly, J. 2004. A note on the estimation of metabolites in hard faeces of rabbits. Revista Computadorizada de Producción Porcina, 11(1):38-42. [ Links ]

Pok Samkol, Bun Y & Ly J 2005. Physico-chemical properties of tropical tree leaves may influence its nutritive value for monogastric animal species. Revista Computadorizada de Producción Porcina , 12(1):31-34. [ Links ]

Rodríguez, W.J. 2010. Evaluación de bloques multinutricionales con tres niveles de follaje de teberinto como fuente proteica sobre el consumo y rendimiento en canal de conejos en la fase de engorde. El Salvador, San Salvador. 42 p. [ Links ]

Steel, R.G.D., Torrie, J.H. & Dickey, M. 1997. Principles and Procedures of Statistics. A Biometrical Approach. McGraw and Hill Book Company In Company (segunda edición). New York, p. 666. [ Links ]

Vivas, J.A. 2014. Efecto de la inclusion de harina de hojas de Moringa oleifera en la alimentación de conejos en desarrollo. Master Thesis. Universidad Nacional Agraria. Managua, 67 p. [ Links ]

Yu, B. & Chiou, W.S. 1997. The morphological changes of intestinal mucosa in growing rabbits. Laboratory Animals, 31: 254-263. [ Links ]

Received: March 21, 2018; Accepted: September 21, 2018

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