Seasonal changes in chemical composition and in vitro gas production of six plants from Eastern Algerian arid regions

M-L Haddi, H Arab*, F Yacoub*, J-L Hornick**, F Rollin** and S Mehennaoui*

Faculté des Sciences de la Nature, Université de Constantine, Route Ain El Bey, 25000 Constantine, Algeria
*Laboratoire LRESPA, Département des Sciences Vétérinaires, Université de Batna, Algeria
**Faculty of Veterinary Medicine, University of Liège, Belgium
haddil@yahoo.com

Abstract

Seasonal variations of nutritive value of six important plants from Algerian arid regions were investigated. Edible aerial parts were monthly sampled, when available, from October 2002 to July 2003 and their chemical composition and their in vitro gas production (GP) parameters evaluated using a logistic model. Metabolisable energy (ME) and organic matter digestibility (OMD) were also estimated. Arid plants were three halophytes shrubs (Atriplex halimus, Salsola vermiculata and Sueada mollis), one tree fodder (Tamarix africana) and two herbaceous plants (Cynodon dactylon and Cyperus conglomeratus). Three semi-arid forages (green wheat Triticum aestivum, green leguminous Hedysarum coronarium) and commercial mixed hay were used for comparison.

Organic matter (OM), crude protein (CP), neutral detergent fibre (NDF), calcium, GP kinetic parameters, ME and OMD were significantly lower (P<0.05) for arid plants and their NDF, ADF and ADL contents (480 ± 215, 281 ± 150 and 76.3 ± 45.0 g/kg DM, respectively) were not significantly affected by the season. CP content was significantly lower (P<0.05) in summer (108± 4.1 g/kg DM). Within arid plants, seasonal changes were significant for DM (P<0.001), CP (P<0.001), copper (P<0.05), phosphorus (P<0.0001), ME (P<0.001) and OMD (P<0.001). Maximum rate of GP (r_m) for arid feeds occurred in winter (0.049 h^-1, January) with the lower value in autumn (0.025 h^-1, October), while the highest asymptotic GP “b” was reached in winter (February: 277 ml/g OM). Seasonal changes were highly significant for b, t₁ (half time of b), t_m (time needed for r_m), r_m, GP at 24 h (b₂₄), GP at 48 h (b₄₈) and GP at 96 h (b₉₆). Depending on the season, some arid plants were better fermented in winter: Atriplex halimus in January (r_m=0.069 h^-1), Sueada mollis in February (0.052 h^-1), Tamarix africana in January (0.062 h^-1); others in spring: Cynodon dactylon in March (0.037 h^-1) and Cyperus conglomeratus in May (0.055 h^-1), while Salsola vermiculata reached its r_m in summer (0.056 h^-1, in July),). ADL content was negatively correlated to GP (-0.27≤r≤-0.34), ME (r=-0.50) and OMD (r=-0.35) only for arid plants. Cu content (10.0 mg/Kg DM; CV: 24.6 %) was positively correlated to the constant of fitting curve “c” (r=0.38) and GP (r=0.19). P content was essentially correlated to the GP (0.18≤r≤0.34). Arid plants, except Salsola vermiculata, have better nutritional characteristics in winter and spring, the wet and cold seasons.

Keywords: arid shrubs, Atriplex, Cynodon, Cyperus, Salsola, Sueada, Tamarix

Introduction

 The contribution of the native pastures to the nutritional requirements of domestic animals is essential in the Eastern Algerian arid zones. Chenopodiaceous shrubs like Atriplex, Salsola and Sueada, and herbaceous plants like Cynodon dactylon are the main forage plants. Atriplex spp. is a world spread halophyte shrub especially in salty soils. Their various agronomic and nutritional aspects are well characterized (Haddi et al 2002; El Waziry 2007). In the cold season (from October to March), part of the 19 millions of sheep move to the arid pastures where dromedaries and other domestics animals live all the year. So the stoking rate arises and subsequently becomes detrimental for forage plants and the local environment where the ranging is essentially extensive due to the scarcity of water and feeds. Scare and irregular precipitations, excessive temperatures, drought, salinity and evapotranspiration in the arid regions influence the life cycle and annual regrowth of xerophytes plants. Incidence of these factors on nutritional value of arid browses is not yet established. The potential feeding value and the nutritive characteristics of available browses in the natural pastures of salty arid regions remains poorly investigated. Understanding if the domestic animals meet their needs in terms of energy, nitrogen and mineral nutrients in these regions, can help to manage better the animal production and can ovoid possible nutritional deficits and their consequences on animal health. Our objective was to evaluate the seasonal changes of the nutritive value, by the determination of chemical composition and the in vitro gas production kinetics of six important plants browsed in the salty arid region in South-East Algeria. In order to rank these arid plants, partial comparison was made with three semi arid forages. Arid plants nutritionally evaluated here were only part of numerous plants daily browsed by domestic ruminants in the concerned region.

Material and methods 

Plant material and sampling areas

Six arid plants were collected monthly (when available) from the South-East Biskra from October 2002 to July 2003. Only edible green aerial parts, from 15 to 25 cm of length, were manually clipped from three halophytes shrubs (Atriplex halimus, Salsola vermiculata and Sueada mollis), one tree fodder (Tamarix africana) and two herbaceous plants: Cynodon dactylon and Cyperus conglomeratus. For several reasons, particularly the overgrazing, edible green aerial parts of arid plants were not quantitatively available all the time in the pasture and consequently it was not easy to find enough plant material at each sampling. Semi arid forages, used for comparison, were collected once in spring 2003 at Constantine (280 Km at North Biskra) and included green wheat plant, green leguminous Sulla (Hedysarum coronarium) and one commercial mixed hay. As reported by Lemnaouar (2001), mixed hay was the cheapest forage composed by several herbaceous dried plants and sold around the year in the market. The sampling site of arid plants was 5 m below sea level and is characterized by high salinity of soil. Average annual precipitation is 140 mm (Hirche et al 2007) concentrated during 30-40 days in the cold season, from the ending of autumn to the beginning of spring. The area is considered arid on the UNESCO classification scale (Pagot 1992).

Analytical methods

Chemical analysis of feeds

Whole plants were dried in air forced oven at 55° C for 72 h. Then, leaves and stems were manually separated for Atriplex halimus, Salsola vermiculata, Sueada mollis and Tamarix africana. For the others arid browses separation was not applicable. Semi arid forages were evaluated as whole plants. Samples were milled to pass 1 mm screen and stored in polypropylene bottles at room temperature for subsequent analysis. Dry matter (DM), ash, crude protein (CP), ether extract (fat) were determined using the AOAC procedures (AOAC 1990). Calcium, copper and manganese were determined using an atomic absorption spectrophotometer after wet digestion in nitric and perchloric acid and ashing. Phosphorus was determined by the phospho-molybdate reaction method using a photo flame spectrophotometer. Contents of neutral detergent fibre (NDF), acid detergent fibre (ADF) were analyzed according to Van Soest et al (1991), without α-amylase and sodium sulphite and expressed free of ash. Acid detergent lignin (72% H₂SO₄ , ADL) and acid insoluble ash (ASHINS) were determined following Robertson and Van Soest (1981). All samples were analyzed in duplicate.

Rumen fluid collection and in vitro gas production trials

Rumen content of slaughtered dromedaries was chosen for its appropriate in vitro gas production characteristics (Haddi et al 1999).The donor animals were adult males browsing in the same arid region of plant sampling, weekly transported from Biskra to municipal slaughterhouse at Constantine. The whole rumen content was collected in pre-warmed thermos, tightly closed and immediately transported to the laboratory. For in vitro trials, 200 ± 10 mg of dried samples were placed in 100 ml calibrated glass syringes witch were greased with Vaseline and pre-warmed. In a Wolfe flask, 1 volume of strained rumen fluid was mixed with 2 volumes of artificial saliva (Menke and Steingass 1988) at 39°C in water bath under free oxygen CO₂ flux. Syringes were filled with 30 ml of the mixture, degassed and incubated at 39°C. Evolved gas was read every two hours in the first 24 h and every 6 h thereafter. The content of syringes was gently homogenised at each reading. Each batch for all samples was repeated twice in a different weeks and three syringes of blank (containing no feeds) were included. Cumulative gas was corrected for the blank and expressed in millilitres of gas produced (GP) per gram of organic matter (OM).

Data analysis

Corrected gas data were fitted to the monophasic logisitic model according to Groot et al (1996), g(t) = b/(1+(t₁/t)^c), where “t” is the time of in vitro incubation in hour, g(t) the cumulative gas produced expressed in ml/g OM, “b” the asymptotic gas production, t₁ the time required to reach 50% of b, “c” an unitless constant reflecting the shape of the fitting curve. The fractional rate r(t) of GP was computed as follow r(t)=c.t^c-1/(t₁^c+t^c) (hour^-1) and its maximum (r_m) was reached when d(r(t))/dt=0 at t_rm, the time of maximum rate of GP. Gas production was also estimated at 24 h of incubation (b₂₄), 48 h (b₄₈) and 96 h (b₉₆). Using cumulative gas (ml) produced by 200 mg DM of feed at 24 h and the content of CP (g/kg DM), metabolisable energy (ME) and organic matter digestibility (OMD) were estimated using the following regression equations of Menke and Steingass (1988) for roughage feeds:

ME _{(Mega Joules/Kg DM)} =2.2+0.1357*GP _{(ml/200 mg DM)} +0.0057*CP _{(g/kg DM)} +0.0002859*CP²;

OMD _{(g/Kg DM)} = 24.91+0.7222*GP _{(ml/200 mg DM)} +0.0815* CP _{(g/kg DM)}.

In order to evaluate the effect of various factors, data were subjected to analysis of variance using the following general linear model:

Y_i = µ + F_i + e_i,

Where:

Y_i = observation,
µ = population mean,
F_i = factor (plant species, location, morphological fraction or season) effect and
e_i the residual error.

Means were separated using the Student Newman Keuls multiple range test in the GLM procedure of the SAS statistics software (SAS 2003). The correlation analysis and the non linear fitting were performed using the corresponding procedures of the same software.

Results 

Seasonal variation of chemical constituents

Arid plants seemed to maintain constant the major part of their nutritional constituents around the year (table 1).

Seasonal variations were not significant (P>0.05) for organic matter, acid insoluble ash, ether extract, cell wall content (NDF), lignocellulosic content of cell wall (ADF) and for acid lignin (ADL), but significant (P<0.001) for only few chemical constituents: DM, CP, P and Cu (Table 2). The highest contents of DM were reached in the driest seasons, summer and autumn (380 and 361 g/kg of fresh matter, respectively). Summer was also a season with lowest CP (108 g /kg DM) and Cu (8.3 mg/kg DM) contents. Winter, a cold and humid season, seemed to be better for CP and P (145 g and 2.8 g/Kg DM, respectively). Cu content was significantly low in summer but relatively constant elsewhere.

Chemical constituents of the morphological fractions

Morphological composition of arid plants  significantly (P<0.001) affected the contents of all nutrients, excepted Cu. Leaves have a highest content of EE, CP, Ca, P and a lowest content of ADF (138 g/kg DM). ADF and ADL were significantly higher for stems which have also significantly less ASHINS, EE, CP and Mn than leaves. OM content of stems was significantly higher than leaves but similar to whole plants (table 1).

Whole plant refers here only to herbaceous species (Cyperus conglomeratus and Cynodon dactylon) for which stems and leaves are difficult to separate in our context. DM, ASHINS, NDF and Mn were high in these plants, but their ADL content was significantly lower than leaves and stems of the arid plants.

Chemical constituents of arid species

Arid plants belong to different categories: shrubs, tree fodders and herbaceous plants, and showed different nutritional contents. Nutritional differences between plant species were large, in terms of CV,0 for ADL, Mn, ASHINS and ADF, but limited for OM. Herbaceous plants were less lignified than shrubs: Cyperus conglomeratus was the less lignified and Tamarix africana, was the more lignified.

Compared to semi arid forages, arid plants showed significantly less OM (P<0.001), CP (P<0.05) and Ca (P<0.001). Nevertheless, arid and semi-arid forages have comparable contents of DM, ASHINS, EE, NDF, ADF, ADL, P, Cu and Mn (P>0.05) (Tables 3 and 4).

Average CP of arid plants content was 132 (g/kg DM) and ranged from 103 for Cynodon dactylon to 148 for Sueada mollis, and its seasonal variation was significant (P<0.001) (table 1).

However this content referred only to edible green aerial parts of arid plants. Figures 1a to 1e show the CP content variation during the period of study. For Cyperus conglomeratus, CP content increased irregularly from autumn (November) to spring (May), culminating in March (174 ± 1.0) (figure 1a to 1e) and then decreased. The highest CP content for Cynodon dactylon was also observed in spring (May: 132.1 ± 2.3) (figure 1a).

Figure 1a.  Crude protein change of Cyperus conglomeratus and Cynodon dactylon from October to July, g/kg DM	Figure 1b. Crude protein change of leaves and stems of Sueada mollis from October to July, g/kg DM

For this graminaceous herb, CP content increased first from October to December and then from February to May. From June to October CP content was the lowest and nearly constant.

Stems of Sueada mollis were less rich in CP than leaves and their content ranged from 65.9 in May to 118 in November (figure 1b). For leaves, CP decreased constantly from December (236 ± 6.3 g/kg DM), to May (177 ± 4.8) and then increased from May to July. For Tamarix africana CP content also decreased from autumn to summer for leaves and stems (figure 1c).

In this tree fodder the lowest CP content was observed during July with 104 ± 7.6 for leaves and 90.4 ± 14.1 for stems. Salsola vermiculata and Atriplex halimus showed a nearly similar seasonal change of CP content, for both leaves and stems (figures 1d and 1e).

Apart from Sueada mollis, CP contents of arid plants decreased in the warm and dry seasons and increased in the cold and humid seasons. However, lignin and all the structural constituents remained unchanged between the seasons.

In vitro gas production parameters

Seasonal variation of kinetic parameters of GP

Characteristics of in vitro gas production are shown in tables 5 and 6.

Arid plants species were differently degraded by ruminal microflora and their kinetic parameters were significantly different (P<0.001). Effect of the season was significant for all in vitro kinetic parameters, excepted t_1, the time needed for half GP and r_m, the maximum rate of gas production. The lowest values of c, b, t_m and b₉₆ were reached in summer. In this season arid feeds gave less gas (b: 198 ml/g OM, P<0.05) and the maximum rate was reached faster after only 12.3 h of incubation. Comparable t₁ were needed for the half gas production, and ranged from 23.2 h in winter to 28.2 h in autumn. Asymptotic gas production b ranged from 198.4 in summer to 238 ml/g OM in winter but remained lower than semi arid feeds: 330 ml/g OM, (table 6). Arid plants produced gas with comparable r_m, witch ranged from 0.044 in winter to 0.039 h^-1 in autumn but remained lower than semi arid forages (0.078 h^-1). Kinetic parameter c varied significantly (P<0.05) from 1.5 in summer to 1.7 in the other seasons.

All kinetic parameters were also significantly affected by morphology (excepted t₁) and species (table 5). Gas productions b, b₂₄, b₄₈ and b₉₆ were higher for herbaceous whole plants Cyperus conglomeratus and Cynodon dactylon, but leaves and stems of shrubs were fermented at higher r_m (0.044–0.046 h^-1). For leaves, c and t_m were significantly higher (1.8 and 18.1 h, respectively). Leaves and stems of shrubs and herbaceous whole plants reached t₁ between 22.4 and 26.4 h and were not significantly different (P<0.05). Within the six arid species, Atriplex halimus had high c, t₁, t_m and r_m but its GP were lower than Cyperus conglomeratus and Cynodon dactylon. Cyperus conglomeratus had the highest gas production b, b₂₄, b₄₈ and b₉₆ but a lower t₁ and t_m, all positive features for its nutritive value. In contrast, Salsola vermiculata was characterised by a high t₁ and t_m and by a low GP and r_m, a negative aspects for animal nutrition. Sueada mollis showed the significantly lower GP (b, b₂₄, b₄₈ and b₉₆) than others shrubs. Its r_m was reached 12.8 h after the beginning of incubation, but its t₁ was reached later at 28.1 h. Tamarix africana showed the lowest t_m (8.9 h) and a comparable amount of gas at 24 h (b₂₄) than Atriplex halimus.

Semi arid forages differed significantly only by their GP. Green wheat had the highest GP followed by green Sulla and commercial mixed hay. Differences between arid and semi arid feeds were significant for all the kinetic parameters, excepted the parameter c. Mixed hay was the nearest to arid plants in terms of GP (table 6).

Figures 2a to 2e show the seasonal changes of r_m of in vitro gas production for arid plants between October 2002 and July 2003.

Different trends of r_m were observed within species and their morphological fractions. Arid plants reached their maximum rate of in vitro GP between January and May, excepted Salsola vermiculata with an exactly opposite trend.

Table 7 shows the significant relationships between chemical constituents and kinetic parameters of gas production, for arid plants.

Correlation coefficients of Pearson, ranged from -0.16 for t₁ and ADF to 0.61 for b and Mn. The cell wall content (NDF) was correlated to all kinetic parameters of gas production, excepted r_m: negatively to c, t₁, tm b₄₈ and b₉₆ and positively to b and b₂₄. A part from the negative correlation between t₁ and Ca, all significant relationships between mineral contents and kinetic parameters were positive. Acid insoluble ash was positively correlated with GP (0.29 ≤ r ≤0.43) but ADL was acid lignin content was negatively correlated to GP at any incubation time.

According to regression equations for roughages (Menke and Steingass 1988), metabolisable energy (MJ/Kg DM) and organic matter digestibility (g/Kg DM) were estimated (table 8).  

ME energy of arid plant ranged from 5.01 (in summer) to 5.58 MJ (winter-spring). Compared to semi arid forages and as for all others nutritional aspects, aridplants showed a significantly (P<0.05) lower ME and OMD. Winter and spring have a higher but not different from autumn (P>0.05). While leaves and stems showed a similar ME and OMD, whole plants of Cyperus conglomeratus and Cynodon dactylon have a highest value of ME and OMD (5.96 and 552, respectively). Studying mature Cynodon dactylon in Brazil, Nogueira Filho et al (2000), reported a similar value for ME (5.76 MJ/kg DM), but a lower value for OMD (409 g/kg DM). Atriplex halimus, a completely sampled shrubs from October to July, had its highest ME a nd OMD values in February (6.4 and 574.0 respectively), with an increasing trend from December to March and a decreasing one from  March to June both for leaves and stems (figures 3a and 3b).

But leaves of Atriplex halimus reached the highest ME value in March. Valderrábano et al (1996), reported similar ME value (7.5 MJ/Kg DM) in Northern regions of the Mediterranean sea. Salsola vermiculata showed the highest ME and OMD values in December, with a decreasing trend from December to May, both for leaves and stems (data not showen). Similarly, Sueada mollis had its highest ME and OMD values in December, with continuous decreasing trend from December to May. Tamarix africana had its highest ME and OMD values in November (6.24; 584), Cyperus conglomeratus in May (8.19; 695) and Cynodon dactylon also in May (6.81; 611).

Discussion 

Nutritional of arid plants were wholly lower than semi arid forages. Among the later, mixed hay was the nearest feed to arid plants. These characteristics were discrete during autumn, an intermediate season, then increased during the cold and wet seasons (winter and spring) and finally decreased from June to October during warm and dry seasons. Salsola vermiculata, an abundant halophyte shrub presented a reverse trend and gave a better nutritional and kinetic characteristics in the warm and dry season maybe for its bitter taste during the regrowth in the cold and humid seasons. In arid regions, plant forages grow at low density and became difficult to harvest for sampling, especially green edible aerial parts. In attempt to evaluate the density of some halophyte shrubs in the same area in April 1999 (unpublished data), we find, in the very dense zone, 0.7 tons/hectare for Atriplex halimus, 0.5 t/ha for Salsola vermiculata, 0.2 t/ha for Tamarix africana and 0.06 t/ha for Sueada mollis. However, only few percents for this biomass are edible.

Leaves of arid shrubs were less fibrous than stems. Lignocellulosic content (express as ADF) was more abundant in stems witch also were more lignified than leaves and herbaceous whole plants. In fact, Cyperus conglomeratus and Cynodon dactylon, have the lowest ADL contents, and are generally intensively browsed and rapidly exhausted from pasture like many others herbaceous plants. Surprisingly, edible aerial parts of arid shrubs have a lower ADL content than a whole semi arid leguminous Sulla (76.3 vs. 110 g/kg DM) and have less NDF fibres than many cereal straws, as reported by Wanapat et al (1989). In any case, arid browses were less ligneous than some Mediterranean shrubs (Ammar et al 2005). Arid plants evaluated in this study can supply adequate mineral level for Ca, P, Cu and Mn for maintenance needs for ruminants (Ca: 4.0, P: 3.0 g/kg DM, Mn: 50.0 and Cu 10.0 mg /Kg DM) according to Andrieu and Demarquilly (1987). However, positive correlations between P content and GP indicate a stimulatory effect of increasing P concentration on cell content degradation and consequently on the amount of gas produced. Probably a higher mineral content is needed for used ruminal microflora. For phosphorus, Komisarczuk-Bony and Durand (1991) suggested that 5 g/kg ODM were required for ruminants fed on roughages; consequently, less than 50% of P is supply by our arid plants. CP contents of studied arid plants were valuable and comparable with some woody plant foliages from African semi-arid regions as reported by Breman and Kessler (1995). ME and OMD were low for arid plants and if we assume that 10 g microbial protein are produced per 1 MJ of ME intake (AFRC 1993); only 50-60 g of microbial protein can be synthesized per Kg of DM, in the rumen. Current results are concordant with those from previous study conducted in the same area from March to June 1996 (Haddi et al 2003). In this study whole plant of Salsola vermiculata, Atriplex halimus, Sueada mollis and two others shrubs showed their best nutritive characteristics in spring, even with significant differences between species. Chemical aspects seemed less affected than kinetic parameters by the season, suggesting that the rumen microflora encountered additional constraints linked to physical structure of plant tissues or toxic substances witch change during the life cycle of plants.

Conclusion 

Arid plants and semi arid forages differed mainly by their in vitro degradation parameters witch reflect not only the chemical aspects but also others characterics related to the tissues structure elaborated as an adaptive response to the arid context. The fact that maximum rate (r_m) of in vitro degradation of the arid browses was similar around the year can be assigned to the constant fibrous but not highly lignified structure of arid cell wall.

Arid plants are for essential importance in supporting basic nutritional requirements of domestic ruminants in the arid regions. They are fibrous but not ligneous and their nutritive constituents were low compared to those of semi arid zones. However, arid plants can reveal their nutritive potential (minerals, energy and nitrogen) through their leaves during the wet and cold season, when several thousand ovine are browsing in these regions. Plant species and morphological composition were the discriminatory factors for the nutritive value essentially for chenopodium shrubs and tree fodder. Many different factors like precipitation regimen, specific growth cycle of each arid plant, animal browsing pressure, anti-nutritional substances, etc.., can influence their nutritive value and deserve further investigations.

Acknowledgments 

This study was supported by University of Constantine (Algeria) and University of Liege (Belgium) through the CUD-PIP collaborative project “Health and production of ruminants in East Algeria”, funded by General Directory of Cooperation and Development (GDCD, Brussels). The first author would thank Dr. D Pizzighello (University of Padua, Italy) for assistance during statistical analysis and Dr. A Boukerrou (Veterinary Regional Laboratory, Constantine) for laboratory facilities.

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Received 2 May 2008; Accepted 12 March 2009; Published 18 April 2009

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