Seasonal changes in cell wall digestion of eight browse species from northeastern Mexico

J G Moya-Rodríguez, R G Ramírez and R Foroughbakhch

Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, Apartado Postal 142, Sucursal F, San Nicolás de los Garza, Nuevo León, 66451, México.

roqramir@fcb.uanl.mx

Abstract

Leaves from Acacia wrightii, Bumelia celastrina, Castela texana, Forestiera angustifolia, Karwinskia humboldtiana, Larrea tridentata, Schaefferia cuneifolia and Zanthoxylum fagara were evaluated to estimate the seasonal dynamics of the in situ digestibility of the cell wall (CW). Nylon bags (5 x 10 cm; 53 µm of pore size) with 4 g of sample of each species were incubated in rumen fistulated sheep, which were fed Medicago sativa hay. In all plants, the soluble fraction of the CW (a, %), the insoluble fraction of the CW (b, %) and the effective degradability of the cell wall (EDCW, %) were higher in winter than in other seasons. Only F. angustifolia (63.8) and K. humboldtiana (59.3) had annual mean EDCW values higher than M. sativa hay (51.7). Bumelia celastrina (34.0) was lowest in EDCW. The hemicellulose content in evaluated browse species was positively correlated with EDCW; however, lignin was negatively correlated with the ruminal digestion of the CW.

From the results obtained in this study, plants such as F. angustifolia and K. humboldtiana can be considered as good feeds for grazing ruminants during all seasons of the year, and C. texana, L. tridentata and Z. fagara as appropriate during winter.

Keywords: Browse plants, cell wall degradability, northeastern Mexico

Introduction

In general, the quality of a diet for grazing ruminants depends upon the species present in the range, the amount of forage available, and the nutritional quality of the plant species. The type of species present in the range depends on their adaptation for survival (Nelson and Mosler 1994). The selectivity of the plant species by grazing animals may be affected by the presence of some anti-nutritional compounds found in the foliage. The most common compounds are lignin and condensed tannins. Generally, lignin is high in browse plants and has a negative effect upon the total organic matter digestibility (Van Soest 1993). The condensed tannins negatively affect the nutritional status of ruminants consuming forage with high content of browse plants, reducing the ruminal digestion of protein and cell wall (Holechek et al 1990). Studies carried out with browse plants from northeastern Mexico have shown that the amount of cell wall present in those plants is similar or inferior to that of Medicago sativa hay which is considered an excellent feed for ruminants (Foroughbakhck et al 1997; Ramirez et al 2000).

This study was carried out with the objectives to estimate and compare seasonally the non linear parameters of digestion and effective degradability of cell wall of eight native shrubs that grow in northeastern Mexico. Medicago sativa hay was used in this study as reference plant of high nutritive value.

Materials and Methods

Study area

The study was carried out in three different sites (counties) located in Nuevo Leon, Mexico: Mina, El Carmen and Hualahuises. Mina is located at 26° 03' north latitude and 100º 35' 30’’ west longitude. The dominant plant community is represented by shrubby vegetation which is characterized by species varying in height (from 1 to 3 m). The climate is typically semi-arid with annual mean temperature of 21.4 ºC and with an annual precipitation of 278 mm. The soil is calcareous, with a pH of 7.8, of fine texture and low organic matter content (Foroughbakhch 1992). The Carmen is located at 25º 57' north latitude and 100º 20' west longitude. The plant community is represented by shrubby vegetation. The climate is semi-arid with rains in summer, the annual mean temperature is about 21.4 ºC, and the annual total precipitation is 694 mm. The soil is calcareous, of alluvial origin, of loamy texture, with medium quantity of organic matter and with a pH of 7.5. Hualahuises is located at 24º 55' north latitude and 99º 42' 30´´ west longitude, and the plant cover is characterized by shrubby vegetation. The climate is semi-arid with rains in summer, the annual mean temperature is 22.3 ºC and the annual precipitation is 749 mm. The soil is from coluvial origin, of loamy texture, with medium quantity of organic matter and with a pH of 7.7. During the year of study (1999) the highest precipitation occurred in the summer season, being 100 mm in Mina, 287 mm in Carmen and 494 mm in Hualahuises (Foroughbakhch 1992).

Collection and chemical analysis of samples

Shrubs that are selected by ruminants in northeastern Mexico (Ramírez et al 1993) such as Acacia wrightii Benth, Bumelia celastrina H.B.K., Castela texana T. & G. Rose, Forestiera angustifolia Torr., Karwinskia humboldtiana (R. & S.) Zucc., Larrea tridentata DC., Schaefferia cuneifolia Gray., and Zanthoxylum fagara (L) Sarg., were collected in winter (February 27 to March 5), spring (June 1 to 9), summer (August 21 to 29) and autumn (November 26 to December 4) of 1999. The selection of the material consisted of simple random sampling where leaves were collected from at least 10 plants of each species in each season of the year. Samples were dried in the shade until constant weight, and were ground in a Wiley mill to pass through a 2 mm screen. Samples for each plant and each season (in quadruplicate) were analysed for organic matter (OM) and crude protein (CP) according to the procedures described by AOAC (1997). Cell wall (CW), cellulose, hemicellulose and lignin were determined with the method of Goering and Soest (1970), and condensed tannins by the vainillin-HCl method of Burns (1971) as modified by Price et al (1978). The nutritional data were previously reported by Moya-Rodriguez et al (2002)

Degradability of cell wall

The rate of disappearance of the cell wall of the evaluated species and M. sativa hay was measured by the nylon bag technique, using rumen cannulated Pelibuey sheep (about 45 kg live weight). During the trial, sheep were fed alfalfa hay ad libitum. Four grammes of ground material were placed in the bags (5 x 10 cm, with pore size of 53 mm) and suspended in the ventral part of the rumen of sheep. The bags were removed from the rumen after 4, 8, 12, 24, 36 and 48 h incubation, and washed in cold water until the water became clear. The zero time disappearance was obtained by washing un-incubated bags. The bags were dried in an oven at 60^oC for 48 h.

The dry matter losses in each incubation period were used in the following equation from Ørskov and McDonald (1979):

p = a + b (1 - e^-ct)

where P is the percentage of disappearance of the CW at time t, a is the soluble fraction of the sample that is lost during washing, b is the insoluble fraction that is degraded slowly in the rumen, c is a constant rate of disappearance of the fraction b, and t is the incubation time.

The non-linear parameters a, b and c, and the effective degradability of the cell wall (EDCW) = (a+b)c/(c+k)[e^-(c+k)T] were calculated using the computer program Neway (McDonald 1981): where k represents the outflow rate from the rumen and T is the lag time. The EDCW values of browse leaves and M. sativa were estimated using an outflow rate of 2%/h.

Statistical analysis

The values related with the seasonal variation of the nutrients and degradability characteristics of the cell wall of the plants were analyzed using a Complete Randomized Block Design, where the Blocks were the seasons and browse plants the treatments. Simple linear correlation coefficients between the chemical composition, reported by Moya-Gonzalez et al (2002) and the non-linear parameters of in situ digestibility and effective degradability of cell wall in studied browse plants were also estimated (Zar 1996).

Results and discussion

The soluble fraction of the cell wall that is lost during washing of the nylon bags (a) was higher during winter than in autumn. Only plants such as F. angustifolia and K. humboldtiana had a higher soluble fraction than alfalfa hay. S. cuneifolia was similar to the alfalfa hay (Table 1). The insoluble but degradable fraction of the cell wall (b) was higher in most plants during summer and autumn, than in spring and winter. With the exception of L. tridentata and S. cuneifolia, all plants had annual mean values of (b) higher than alfalfa hay. The potential degradability of the cell wall (a + b) was higher in summer and autumn than in winter and spring. With the exception of B. celastrina, L. tridentata and S. cuneifolia, all plants had annual mean potential degradability values of the cell wall higher than alfalfa hay. With the exception of K. humboldtiana and Z. fagara, the degradation rate of the cell wall (c), was higher during winter than in summer and autumn (Table 1).

Tabla 1. Seasonal changes of non-linear parameters of in situ digestibility of the cell wall in browse species from northeastern Mexico
	*M. sativa*	*A. wrightii*	*B. celastrina*	*C. texana*	*F. angustifolia*	*K. humboldtiana*	*L. tridentata*	*S. cuneifolia*	*Z. fagara*
Fraction a, %
Winter	26.0^a	23.9^a	12.1^a	21.6^a	34.0^a	25.1^b	26.2^a	20.1^a	11.1^a
Spring	23.1^b	13.6^c	17.3^a	21.7^a	34.1^a	32.0^a	25.0^a	21.8^a	0.0^b
Summer	21.7^b	17.8^b	17.8^a	14.6^b	28.0^b	20.8^c	16.1^b	23.2^a	1.7^b
Autumn	20.8^b	0.1^d	0.0^b	11.0^c	28.5^b	26.8^b	0.0^c	21.2^a	0.0^b
Mean	22.6	13.8	11.8	17.2	31.1	23.7	16.8	21.7	3.2
SE	±0.9	±0.9	±2.1	±1.0	±1.8	±0.9	±1.3	±1.1	±1.1
Fraction b, %
Winter	40.7^a	41.6^b	68.5^a	52.9^b	49.8^b	61.6^b	56.1^a	36.3^b	67.2^{a b}
Spring	42.2^a	51.7^ab	28.4^b	23.5^c	43.5^b	49.9^c	13.0^b	41.0^b	75.4^a
Summer	45.8^a	68.1^a	33.6^b	52.5^b	66.9^a	73.5^a	44.8^a	42.7^b	48.4^b
Autumn	45.8^a	57.0^{a b}	66.8^a	76.4^a	64.5^a	60.1^b	46.0^a	51.3^a	77.6^a
Mean	43.6	54.6	49.3	51.3	56.1	56.3	40.0	42.8	67.1
SE	±4.2	±7.8	±10.4	±4.8	±4.3	±3.7	±9.1	±2.4	±8.4
Fraction a+b, %
Winter	66.7^a	65.5^{a b}	80.6^a	74.5^ab	83.8^{a b}	86.7^b	72.2^a	57.1^c	78.3^a
Spring	65.2^bc	65.3^ab	45.7	45.2^c	77.6^b	81.9^b	39.2^b	62.8^{b c}	75.4^a
Summer	67.6^{a b}	86.0^a	51.4^b	67. ^b	94.9^a	94.3^a	69.8^a	65.9^b	50.0^b
Autumn	66.6^c	57.1^b	66.8^{a b}	87.4^a	92.9^a	86.9^b	46.0^{a b}	72.5^a	77.6^a
Mean	68.9	68.4	61.1	68.5	87.3	79.9	56.8	64.6	70.3
SE	±3.6	±8.4	±9.3	±4.9	±4.0	±3.3	±8.5	±2.0	±7.7
abcd Means with the same letter superscript are not different (P‹0.05); a = soluble fraction of cell wall; b = degradable fraction of cell wall; a+b = potential degradability of cell wall.

The lignin content of the leaves negatively affected the soluble fraction of the leaves (Table 2); however, hemicellulose content was positively associated with the soluble fraction. The cell wall and lignin content were negatively correlated to the (b) value, but the hemicellulose content was positively correlated. The fibre content and the lignin concentration negatively affected the potential degradability of the cell wall, but the hemicellulose content was positively correlated with this component. Condensed tannins were negatively related with the degradation rate of the cell wall but not with the other components. In general, the correlations were relatively low for all the relationships.

Table 2. Simple linear correlation coefficients between chemical composition and non-linear parameters of digestibility and effective degradability of cell wall in browse species from northeastern Mexico
	Organic matter	Crude protein	Cell wall	Cellulose	Hemicell.	Lignin	Condensed tannins
a	- 0.09	0.03	-0.45**	-0.01	0.47**	-0.20*	- 0.02
b	0.17*	0.08	- 0.39**	- 0.13	0.36**	- 0.22*	0.02
a+b	0.13	0.10	-0.38*	- 0.13	0.45**	- 0.21*	0.01
c	- 0.28*	- 0.003	-0.12	- 0.10	0.11	-0.19*	- 0.23**
EDCW	- 0.11	0.23*	-0.39**	- 0.12	0.67**	- 0.22*	- 0.11
(P< 0.05); *(P< 0.01); Hemicell = hemicellulose;; a = soluble fraction of CW; b = degradable fraction of CW; a+b = potential degradability of CW; c = degradation rate of CW; EDCW = effective degradability calculated considering a rumen outflow rate of 2 %/h

The lag time (time required for the ruminal microbes to initiate the cell wall degradation varied between 3 and 4 hours in most plants and seasons of the year (Table 3). The effective degradability (EDCW) of the cell wall was highest during winter for all the browse plants with lowest values during summer and autumn (Table 3). Only F. angustifolia and K. humboldtiana had annual mean values of EDCW higher than M. sativa hay. Bumelia celastrina had the lowest mean value of EDCW.

As was to be expected, the content of cell wall and of lignin were negatively correlated to EDCW. Conversely, the hemicellulose content was positively correlated to EDCW.

The negative effect of lignin upon cell wall digestibility has been reported by many authors. Ramirez et al (2000) studied the effect of cell wall and its derivatives (lignin and condensed tannins) upon degradability of 15 browse plants from northeastern Mexico, and reported that lignin content negatively influenced the EDCW. This finding was also observed by Singh et al (1989) who reported that high levels of lignin in browse plants from India reduced EDCW. Also, Foroughbakhch et al (1998) reported that high levels of lignin affected the EDCW in forage from shrub plants from northeastern Mexico. Hatfield (1993) concluded that lignification of plant cell walls has long been correlated with decreased digestibility but the responsible mechanism has not been established. There is increasing speculation that the utilisation of forage cell wall components as an energy source is regulated by the cross-linked nature of cell wall components (Jung and Deetz 1993).

Table 3. Seasonal dynamics of the degradation rate, fase lag and effective degradability of the cell wall in browse species from northeastern Mexico
	*M. sativa*	*A. wrightii*	*B. celastrina*	*C. texana*	*F. angustifolia*	*K. humboldtiana*	*L. tridentata*	*S. cuneifolia*	*Z. fagara*
	Fraction c, %/hour
Winter	6.1^a	4.9^a	4.9^a	8.1^a	5.1^b	3.9^a	7.4^a	10.7^a	5.7^a
Spring	4.9^ab	3.6^ab	3.6^ab	4.2^b	4.5^a	3.8^a	3.9^b	5.1^b	3.1^a
Summer	5.6^ab	1.4^b	1.5^b	2.1^c	3.1^c	2.1^a	4.4^ab	3.2^c	4.7^a
Autumn	3.2^b	2.5^ab	1.4^b	1.2^c	1.4^c	3.3^a	3.2^b	2.3^c	3.0^a
Mean	4.9	3.1	2.8	3.9	4.5	3.3	4.7	5.3	4.1
SE	±0.9	±0.9	±0.8	±0.5	±0.8	±0.6	±1.0	±0.4	±1.1
	Lag time, hours
Winter	3.0^b	3.0^b	2.6^a	3.1^ab	3.5^a	3.8^ab	3.2^a	4.1^ab	3.5^ab
Spring	4.2^a	4.6^a	3.4^a	4.6^a	4.3^a	5.6^a	3.7^a	4.3^a	4.9^a
Summer	3.7^a	4.4^a	3.2^a	2.8^b	3.2^a	3.8^b	3.2^a	3.5^b	2.7^b
Autumn	3.3^b	3.8^b	3.2^a	3.4^ab	3.5^a	4.5^ab	3.0^b	3.7^ab	3.0^b
Mean	3.5	3.9	3.1	3.5	3.6	4.4	3.4	3.9	3.5
SE	±0.3	±0.9	±0.6	±0.6	±0.8	±0.6	±0.5	±0.2	±0.6
	Effective degradability, %
Winter	54.1^a	48.2^a	39.2^a	54.2^a	66.4^a	61.3^a	52.1^a	49.0^a	55.2^a
Spring	50.1^c	43.2^ab	36.0^a	39.4^b	66.3^a	60.9^a	35.7^b	48.6^a	40.7^b
Summer	53.0^b	43.1^b	36.0^a	39.7^b	66.0^a	55.2^b	48.3^a	47.7^ab	33.8^c
Autumn	49.5^c	29.9^c	24.7 ^b	36.4^b	56.5^b	59.6^c	27.4^c	46.4^b	40.9^b
Mean	51.7	41.1	34.0	42.4	63.8	59.3	40.9	47.9	42.7
SE	±0.9	±1.6	±1.7	±1.3	±1.5	±1.3	±2.4	±0.7	±1.3
a b c d Means within rows with the same letter superscript are not different (P‹0.05); Effective degradability was calculated considering a rumen outflow rate of 2 %/h

Conclusions

In this study, the cell wall of plants was more digested during the winter than in other seasons of the year. The lignin content negatively affected the effective degradability of cell wall, and the hemicellulose content positively influenced the EDCW. F. angustifolia and K. humboldtiana had effective degradability values higher than M. sativa hay, thus they can be considered as good feeds for ruminants in all seasons of the year. C. texana, L. tridentata and Z. fagara appear to be appropriate for use during winter.

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Received 6 February 2002

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