Animal Science

Inclusion of different levels of Ricinus communis L leaf blade meal in whole diets for sheep

J. Zamora¹ 
http://orcid.org/0000-0001-6565-3959

A. del Viento² 
http://orcid.org/0000-0001-9564-7971

L. Barrientos³ 
http://orcid.org/0000-0003-4451-8410

J.M. Palma^{2  *} 
http://orcid.org/0000-0001-6061-546X

¹Facultad de Medicina Veterinaria y Zootecnia. Universidad de Colima, km. 40, Autopista Colima-Manzanillo, Crucero de Tecomán, Tecomán, Colima. C.P. 28100

²Centro Universitario de Investigación y Desarrollo Agropecuario (CUIDA) y FCBA. Universidad de Colima. Gonzalo de Sandoval, Número 444 Col, Las Víboras, Colima, México. C.P. 28045

³Departamento de Madera, Celulosa y Papel. CUCEI. Universidad de Guadalajara

Abstract

To evaluate different inclusion levels (0, 15, 30 and 45%) of Ricinus communis leaf blade (LHRc) in whole sheep diets, four animals, with an initial weight of 27.37 ± 1.70 kg were housed in individual cages. Periods of 20 days were used. The first 15 days were used for diet adaptation, and the last five for measurement. A 4 x 4 Latin square design was applied, with Tukey test (P <0.05) for the multiple analysis of means, plus the linear regression analysis. Variables total food intake (TFI/kg DM), leaf intake (g DM Ricinus communis/kg LW), daily weight gain (DWG/kg), food efficiency (FE/kg) and registration of poisoning signs, were studied. There was a statistical difference (P <0.05) in all variables. The best results were for 0% of Ricinus communis leaf blade (total feed intake 1,332 kg DM/day, daily weight gain 0.315 kg/day and food efficiency 0.254 kg), with respect to 45% of LHRc (total food intake 0.881 kg DM/day, 12.2 g DM of Ricinus communis/kg LW, daily weight gain 0.090 kg/day and food efficiency 0.096 kg). There was presence of diarrhea in this treatment, without compromising the life of animals. The rest of treatments shared statistical similarity. The inclusion of Ricinus communis leaf blade meal had a negative influence on dry matter intake of sheep, with a remarkable reduction in the 45% level, where there was also the presence of diarrhea, without causing deaths.

Key words: forage; arboreal; tropic; sheep

In Mexico, it is common to use high diets with grains (corn, sorghum and soy bean) in sheep intensive estabulated systems, to achieve maximum weight gain, which shortens the length of stay, although this implies a high investment and dependence on inputs (^{Salinas 2015}).

Given these conditions, it is necessary to look for local alternatives that allow the substitution of these inputs to develop resilient livestock systems. The search for the use of unconventional foods, such as trees and shrubs, represents an option under tropical conditions, for the boosting silvopastoral systems (^{Palma et al. 2019}).

An unconventional forage resource is Ricinus communis L. (HRc), a shrub species considered as a protein-energy food (^{Ramírez et al. 2017}), with high ruminal degradability (^{Lara et al. 2016} and ^{Palma 2018}) and low levels of fiber fractions, comparable with alfalfa (^{Ramírez et al. 2017}), which has also shown promising results in the development of sheep (^{Zamora et al. 2020}). However, it is mostly used for biofuel production (^{Cuellar-Sánchez et al. 2016}).

The use of Ricinus communis forage in intensive estabulated systems constitutes an alternative for the substitution of corn, sorghum and soy bean in whole diets, destined for mutton production in Mexico.

Therefore, the objective of this study was to evaluate different inclusion levels of Ricinus communis leaf blade meal in whole diets intended for sheep.

Materials and Methods

The study was carried out at MAPRIC's facilities, located in Libramiento Sur Colima-Coquimatlán, km 5, Colima, Mexico. The prevailing climatic conditions are characterized by a mean temperature of 25.8 °C, a maximum of 33.1 °C and a minimum of 18.6 °C. Pluvial precipitation is 823.1 mm and altitude of 500 m a.s.l., so warm subhumid climate is predominant (^{García 2004}).

Animals were housed in individual metabolic cages. Four Dorper x Pelibuey F1 animals were used, with initial LW of 27.37 ± 1.70 kg, which were not castrated, immunized (Adbac 11), dewormed (IVER MAX GOLD) and vitaminized (vitamin E and Selenium).

R. communis leaf blade (LHRc), of wild origin, was manually collected, without any restriction regarding physiological state of the plant. The collected material was dried in the sun, and processed in a forage grinder (Xalapa MA-460), with a 1.27 cm sieve to obtain the meal.

Four different inclusion levels of LHRc leaf blade meal were evaluated (0, 15, 30 and 45%) in isoenergetic and isoprotein integral diets (CP 15%, ME 11.72 MJ kg DM) (table 1), for a period of 20 d (15 for adaptation and five for measurements during four periods).

Table 1 Composition of whole diets for sheep with different inclusion levels of Ricinus communis L leaf blade meal (LHRc) 

Ingredients	Inclusion level, %
	0	15	30	45
LHRc	0.0	15.0	30.0	45.0
Soy bean paste	15.0	5.5	6.0	0.0
Broken corn	32.5	30.0	22.5	17.0
Sorghum	30.0	30.0	22.5	17.0
Sugar cane stick	10.0	5.0	5.2	2.0
Bypass fat	5.0	4.0	3.5	5.0
Molasses	3.0	6.0	8.0	12.0
Urea	1.5	1.5	3.0	0.0
Salt	1.0	1.0	1.0	10.0
Sodium bicarbonate	1.0	1.0	0.0	0.0
Mineral premix	1.0	1.0	1.0	1.0
Total	100.0	100.0	100	100.0

Variables total food intake (TFI, kg DM/d) and intake index (kg DM / LW0.75) were evaluated, as well as leaf intake (g DM Ricinus communis/kg LW), daily weight gain (DWG, g DM/d), food conversion (FC), food efficiency (FE) and signs of intoxication.

All animals were fed twice a day (8:00 am and 5:00 pm), and a rejection of 5% was considered. Water was offered ad libitum.

Two samples were taken from each treatment, as well as LHRc to perform the proximal chemical analysis (^{AOAC 1990}), from which the nitrogen-free extract (NFE), total digestible nutrients (TDN), digestible energy (DE) and metabolizable energy (ME) were determined (figure 1). In addition, fiber fractions were calculated (^{van Soest 1963}) and non-fibrous carbohydrates were estimated (^{Mertens 2003}) in whole diets.

$NFE=DM100-\left(CP+SE+CF+ASH\right)$

$TDN=\sum (NFE\left(0.9\right)+CP\left(0.8\right)+SE\left(0.9\right)\left(2.25\right)+CF(0.5)$

$DE=TDN\left(4.409\right)/100$

$ME=DE\left(0.82\right)$

NFE-nitrogen-free extract, TDN-total digestible nutrients, DE-digestible energy, ME-metabolizable energy

A phytochemical screening was performed, according to the methodology proposed by ^{Joseph et al. (2013)} for alkaloids, flavonoids, saponins, tannins and quinones. All tests were conducted in duplicate. To report the results, the qualitative crossover system was used to specify the presence or absence of metabolite groups. The criteria abundant presence (+++), medium (++), slight (+) and absence (-) were followed.

ANDEVA statistical analysis was used, with a 4x4 Latin square design. For comparison of means, Tukey test (P <0.05) was used. Linear regression analysis was applied for TFI (kg DM/d), leaf intake (g DM Ricinus communis/kg LW) and DWG. Statistix 8.0 software was used.

Results and Discussion

Table 2 shows the proximal chemical analysis, fiber fractions, estimated energy values for Ricinus communis (Rc) leaf and whole diets under study, and the phytochemical screening in the Ricinus communis leaf.

Table 2 Proximal chemical analysis and parts of fiber in whole diets destined for sheep, with different inclusion levels of Ricinus communis L leaf blade meal (LHRc) 

Components		Inclusion level of LHRc (%)
	LHRc	0	15	30	45
Dry matter (%)	87.15	86.99	86.00	86.00	85.31
Crude protein (%)	22.59	18.80	14.84	15.02	13.89
Ether extract (%)	3.37	2.30	2.82	3.33	3.88
Ashes (%)	9.49	6.64	6.33	6.99	8.97
Neutral detergent fiber (%)	22.72	26.35	20.92	21.44	19.79
Acid detergent fiber (%)	11.61	10.18	7.63	9.07	8.10
Non-fibrous carbohydrates	58.17	54.09	44.91	46.78	46.53
Lignin (%)	3.31	2.59	2.04	2.47	2.47
Nitrogen-free extract (%)	55.12	66.16	71.42	69.70	67.94
Total digestible nutrients	79.22	82.29	84.16	83.97	82.78
Digestible energy* (MJ/kg DM)	14.60	15.15	15.48	15.44	15.23
Metabolizable energy (MJ/kg DM)	11.92	12.43	12.72	12.68	12.51
Alkaloids	+
Flavonoids	+
Saponins	+++
Tannins	+
Quinones	-

*Determined from total digestible nutrients

Abundant presence (+++), medium presence (++), slight presence (+) and absence (-)

The value of Ricinus communis meal was lower in CP and ME (table 2) with respect to that reported in studies of ^{Ramírez et al. (2017)}, who reported CP content of 27% and ME of 11.72 MJ/kg DM as a reference value for the production of integral diets, which caused modifications in their protein content, without altering their energy level.

This difference in nutritional quality can be explained by the type of leaf collected, due to the variability that can exist after harvesting wild material. There is no control regarding regrowth age and phenological stage, since there are few studies that address nutritional characterization based on plant age (^{Ramírez et al. 2017}).

In the case of Ricinus communis leaf, it contained abundant saponins and a slight presence of alkaloids, flavonoids and tannins, as well as the absence of quinones. These results are similar to those reported by ^{Suurbaar et al. (2017)}, although these authors indicated a slight presence of saponins.

Several authors have pointed out the abundant existence of alkaloids, mainly ricinine, a metabolite that can generate toxicity with neurological symptoms (^{Riet-Correa et al. 2017} and ^{Brito et al. 2019}). Spontaneous intoxication has also been reported due to its leaf intake (^{Bianchi et al. 2018}). However, according to ^{Brito et al. (2019)}, this phenomenon is unusual, an aspect that, in this study, was only associated with the presentation of diarrhea with the highest level of inclusion.

Table 3 shows the results of different inclusion levels of Ricinus communis leaf in integral diets, considering the evaluated variables. Regarding dry matter intake in its different expressions, it decreased significantly in control treatment with respect to that with 45% of inclusion of Ricinus communis forage, as the maximum inclusion level. This performance affected weight gain, because the lowest productive performance was obtained with this treatment, and this had a negative impact on efficiency. An outstanding aspect is that animals consuming treatments with 0 and 45% of inclusion presented mechanical diarrhea in the first three days of ingestion. This situation lasted until the seventh day for the treatment with 45% of inclusion of Ricinus communis leaves, and was maintained with soft feces. This phenomenon that was found in all the experimental periods. This episode did not occur in the rest of the treatments, which shared statistical similarity among them. It should be mentioned that there was no poisoning or death at any Ricinus communis inclusion level.

Table 3 Dry matter intake and productive performance of sheep fed whole diets with different inclusion levels of Ricinus communis L leaf blade meal 

Variable	Treatments
	0	15	30	45	SE ±	P
Total DM intake (kg)	1.332^a	1.123^ab	1.105^ab	0.881^b	0.052	0.009
Intake (kg DM/kg LW0.75)	0.080^a	0.070^ab	0.074^ab	0.061^b	0.003	0.041
Intake index (%)	3.21^a	2.83^ab	3.00^ab	2.50^b	0.11	0.038
R. communis intake (gDM/kg LW)	0.00^c	4.65^b	10.18^a	12.20^a	1.18	0.001
DWG (kg)	0.315^a	0.145^ab	0.200^ab	0.090^b	0.030	0.038
Food conversion	4.185	8.895	6.740	8.453	1.874	0.692
FE (kg)	0.255^a	0.136^ab	0.173^ab	0.096^b	0.026	0.053

^a,bDifferent letter in the same row indicate statistical difference (Tukey test p<0.05). MSE = mean standard error

The use of high grain diets is a common practice in intensive estabulated systems. Therefore, the search for alternatives with local resources represents a challenge, because this type of diet was practically 3.5 times better in DWG with respect to the level of 45% of Ricinus communis, explained by the decrease of intake, which was 1.5 times lower with the presence of diarrhea and soft feces. This phenomenon is related to purgative effects due to the presence of ricin (toxalbumin) and ricinine (alkaloid) in leaves, as pointed out by ^{Hussein et al. (2015)}.

The main secondary metabolite of leaf is ricinine, an alkaloid that generates acute neurological symptoms (^{Riet-Correa et al. 2017} and ^{Brito et al. 2019}) with intoxication, three to six hours post-ingestion. There are signs of dehydration, sialorrhea, dyspnea, ataxia, chewing movements, lateral head and neck deviation, incoordination, hesitant walking, and, in some cases, tympanism. Depending on these symptoms, which persist from 2 to 16 hours, animals may recover or die. For these neurological disorders to occur, sheep must consume from 10 to 20 g DM / kg LW, according to an experimental evaluation (^{Döbereiner et al. 1981}). This performance did not occur in the present study.

Another type of poisoning occurs with seeds. Its main secondary metabolite is toxalbumin ricin, which is highly toxic. Its ingestion is associated with a gastroenteric type picture, with the presence of diarrhea, foul-smelling stools and blackish brown color in the perianal region in hinder limbs, as well as apathy, dehydration, abdominal pain, ruminal stasis and weakness. It can even cause death (^{Aslani et al. 2007} and ^{Alburquerque et al. 2014}), when seed intake was accidental or, in some cases, induced by forage deficit, due to drought.

Ricinus communis leaf also contains ricinine (^{Vasco-Leal et al. 2020}), which can be associated with the presence of diarrhea. It is known that this metabolite stimulate the effect of the small intestine, which increases peristalsis with a laxative action and the evacuation of liquid feces, without pain or colics (^{Herrera and Gutiérrez 2003}), as confirmed in the present study.

It is known that food intake of animals is multifactorial, since it includes nutritional state, individual expression, prior knowledge of the food to its nature, in terms of quality, taste, color, smell and chemical content of the plant, as factors that influence on its selection and intake (^{Villalba et al. 2015}).

Low food intake was associated with the sudden supply of this unconventional forage, leading to learning and adaptation. In this regard, ^{Lara et al. (2016)} observed an increasing adaptation to obtain a gradual increase in its ingestion. These authors recorded 3.8 g DM Rc / kg LW at 9 d, with increases of 9.5 and 18.9 g DM Rc/kg LW, at 25 and 30 d, respectively when replacing the base diet. Problems of diarrhea, poisoning or death were not registered. In this study, maximum mean intake was 12.2 g DM Rc/kg LW for the highest inclusion level used, but without adapting to it.

Another explanation for low intake with the 45% inclusion level of R. communis was associated with an ingestion restriction, due to its combination with molasses. ^{Lara (2015)} alluded to this issue, finding a negative effect of up to four times, of R. communis leaf intake combined with molasses, compared to the ingestion of leaf alone. According to ^{Obumselu et al. (2011)}, this phenomenon is related to astringency for this forage.

This astringency deals with the presence of saponins (^{Das et al. 2012}), which generates a bitter taste. In sheep, it is associated with the ability to detect toxins, resulting in a negative hedonic taste, when selecting food (^{Ginane et al. 2011}). These aspects should be evaluated in future experiments, to avoid restriction of this type of whole diet or in the possible generation of ruminal activators, which allow supplementation restriction, from non-conventional foods (^{Rodríguez and Palma 2018}).

Ruminal degradability of Ricinus communis forage is high, like its passage rate (^{Ramírez et al. 2017} and ^{Palma 2018}). This can be related to the high availability of fermentable carbohydrates, which caused diarrhea, associated with ruminal acidosis, as a consequence of microbial fermentation in the whole diet. With the inclusion of 45% of Ricinus communis forage, the use of sodium bicarbonate was not considered. Therefore, low acid detergent fiber content and particle size influenced on the lack of effective fiber, which avoids the problem of acidosis (^{Bach and Calsamiglia 2006}).

In pregnant ewes, consuming forage diets based on sugar cane top, intake was also affected, with the use of 20% of Ricinus communis forage and compare it with alfalfa (^{Ramírez-Navarro et al. 2020}). This inclusion level affected intake by 18%, in a first stage that did not consider the adaptation period. After this phase, intake was affected between 4 and 6%, although it did not affect productive parameters or generated intoxication, abortions or deaths in females. It did not cause damage to their offspring in the periods studied either.

Regarding linear regression analysis, these results can be considered as preliminary, in terms of weight gain. This aspect should be addressed in future studies, having a direct inverse relationship for intake and weight gain. As the inclusion level of Ricinus communis forage increased, these indicators decreased (TFI y = -9.142x + 1315.6, P = 0.004 and R2 = 0.455; DWG y = -0.004x + 0.281, P = 0.014 and R2 = 0.362). For the intake of g DM of Ricinus communis/kg LW, there was a positive linear regression (y = 0.282x + 0.163, P = 0.001 and R2 = 0.809), although with undesirable effects, as observed with the highest intake of Ricinus communis.

This type of study enables the development of strategies that allow the inclusion of this unconventional forage in the feeding of ruminants in new technological schemes, aimed at the development of agroforestry systems in general (^{Sánchez et al. 2016}), and of silvopastoral or agro-silvopastoral systems, in particular (^{Palma 2018}).

It is concluded that Ricinus communis L. leaf blade meal has a negative effect on food intake, as part of whole rations destined for sheep. Specifically, when levels of 45% are used, in which animals presented diarrhea and soft feces, without other intoxication signs or death.

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Received: September 11, 2020; Accepted: October 10, 2020

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Los autores declaran no presentar conflicto de intereses

Los autores declaran presentar contribución igualitaria en la concepción de la investigación, obtención y procesamiento de los datos y redacción del documento