| Livestock Research for Rural Development 27 (3) 2015 | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
Four halophytes from El Oued (Atriplex halimus L., Sueda mollis, Tamarix aphylla, Zygophyllum album) which are preferentially grazed by camels and hay vetch-oats, a reference control substrate, were analyzed to determine their nutritional value for camels. Our study is based on the precise chemical characterization of plants and the evaluation of their nutritional potential by measuring the fermentability in vitro by ruminal microbiota camels.
The results of our work show that Algerian saline ecosystems are rich in good forage quality plants with moderate levels of crude protein and minerals (Atriplex halimus and Sueda mollis), and more or less acceptable rates indigestible fiber and secondary substances (Tamarix aphylla, Zygophyllum album).
The measurement of gas production shows that the ruminal microflora camel is very effective in the digestive and metabolic utilisation of rations, unlike most publications for ruminants that mention that in vitro gas production was negatively influenced by the fiber content of foods and the level of secondary compounds.
Keywords: arid region, chemical composition of plant, digestibility, forage, dromedary, nutritional value, rangelands, Sahara, vegetation
Rangeland in North Africa covers an area of 130 million hectares (Ben M'hamed 1990). In Algeria, this area accounts for approximately 31.615-32.400 million hectares (Abdelguerfi et al 1996), most of which is located in the arid and semi-arid areas, (Makkar et al 1993). Despite the severe weather conditions in these regions (low rainfall, high temperatures, salinity ...), some naturalized species, including halophytes survive with forms of extraordinary adaptations (LeHouérou 2001). These plants are very appreciated by the dromedary or "desert ship" which presents food relief, and monetary utility of the nomad. One of the major problems that limit the development of camel breeding is diet, which is based on local feed resources. Despite the importance that the resources that populate the dry land ecosystems have in animal nutrition and protection of the environment, they have not, however, received the attention they deserve. Indeed, there is some work that can see the great power of this animal trait among which include Chaibou (2005) in Mali, Correra (2006) in Mauritania and Algeria, Oulad Belkhir (1989 ), Longo et al (2007), Chehma (2005) Chehma and Longo (2004) Chehma et al (2008), and Chehma et Youcef (2009), Chehma et al (2010).
In this work, we were interested in assessing the nutritional value of halophytes collected from camel's courses in the arid regions of Algeria, by determining their chemical composition and estimation of the metabolic activity of the camel ruminal microbiota to them in vitro. The aim is to assess the possibility of their use as a component of food rations in camel breeding and selection of the most interesting fodder plants nutritionally.
Plant material Sampling is performed in a salty area course named Benguecha (common Taleb El-Arbitraitors El Oued Province). The choice of the studied plants that form the herbaceous layer of the camel route was done according to their abundance during the winter of 2013. The identification of these plants was made with the help of the work of Quézel and Santa (1962), Ozenda (1991) and Nègre (1961). According to the methodology of the "hand plucking method", only the plant parts (tender branches, leaves, flowers, and fruits) really grazed by camel have been collected. After identification, each of the 4 samples thus formed; Atriplex halimus (Amaranthaceae), Sueda mollis (Amaranthaceae), Tamarix aphylla (Tamaricaceae), and Zygophyllum album (Zygophyllaceae) was dried in a ventilated oven, ground and stored for analysis.
The chemical analyzes of forages perform according to standards described by AOAC (14, method ID 942.05). All measurements were done in triplicate.
The dry matter (DM), organic matter (OM) and ash were determined according to Sauvant et al (1988). The nitrogen assay was performed according to the Kjeldahl method. The procedure of Van Soest et al (1981) was applied to determine the neutral fiber (NDF), acid fiber (ADF) and lignin (ADL). The wet digestion with nitric and perchloric (Elmer, 1994) was made to obtain extracts for the determination of mineral elements (Ca, Mg, K, NaCl) using atomic absorption spectrophotometry flame. Secondary substances identified in the context of this work are: total phenols (TP), total tannins (TT) and oxalates. The content of total phenols is determined by a spectrophotometric method, the method described by Makkar et al. (1993), based on the principle of the redox and use of Folin-Ciocalteu reagent or Folin-Denis reagent. The tannins are distinguished from non tannins with a solid matrix (PVPP) (method of Makkar 2003). Analysis of the condensed tannins (proanthocyanidins) is made according to the technique (Porter et al., 1986) with modifications of Makkar (2003), using as standard quebracho tannins. Oxalates are determined by titration with KMnO4 solution 0.002N after their dissociation in a solution of HCl 0.25 N and precipitation in the presence of a precipitating agent.
To measure the amount of gas produced by the different plant samples, the fermentation was conducted according to the technique of calibrated glass syringes described by Menke and Steingass (1988). This technique allows information about the process of fermentation in the rumen by measuring the volume of the product gas from the fermentation of plant material sample dried in the presence of artificial saliva and the inoculum subject to all anaerobiosis and at a temperature of 39 °C. After 24 hours of incubation the gases produced and corrected by the gases produced by the inoculum in control tubes were used to calculate the organic matter digestibility (OMD) using the following regression equation (Menke and Steingass 1988):
OMD (%) = 185.3 + + 9.239GP 0.540MAT
Statistical analysis of the results was performed using SPSS Version 20.0 software. To highlight the existence of significant differences between ecotypes for the studied parameters, variance analysis method was used, supplemented by "Duncan" test to compare means between groups. Correlations between different parameters were analyzed with the test "Pearson Correlations".
The chemical composition of halophytes collected and selected in El Oued region, as well as the vetch-oat hay is presented in Table 1. The table shows that examination of all substrates contains high tenors and slightly different in dry matter (DM). A. halimus has a higher DM content and significantly similar to vetch hay oats (935.08 and 934.56 g / kg, respectively) (P> 0.05) followed by T. aphylla (802.82 g / kg), and Z. album (721,92g / kg), while the lowest rate in DM is recorded in S. mollis (602.85 g / kg). The arid geographic area of the forage where the plants are found explains this low humidity.
| Table 1. Dry matter content and chemical composition (% DM) of halophytes collected from El Oued region | |||||
| A. halimus | S. mollis | T. aphylla | Z. album | vetch-oat hay | |
| DM (g/kg) | 935,08d | 602,85a | 802,82c | 721,92b | 934,56d |
| O M | 802,06b | 832.6e | 819,26d | 783,98a | 808,66c |
| CP (g/kgMS) | 150,4d | 162,5e | 87,2b | 70,4a | 114,6c |
| NaCl | 12,26d | 10,28c | 9,36b | 10,68c | 1,41a |
| K+ | 1,25d | 1,45e | 0,72b | 0,82c | 0,3a |
| Ca2+ | 2d | 1,9d | 0,8b | 1c | 0,2a |
| Mg2+ | 1,2c | 1,4e | 0,49b | 0,58b | 0,12a |
| NDF | 40,59a | 51,42b | 62,41d | 77,70e | 55,88c |
| ADF | 28,15a | 35,46b | 45,95d | 53,11e | 40,6c |
| ADL | 7,3a | 8,9b | 13,09d | 14,83e | 9,37c |
| Ash | 18,05c | 15,96b | 18,30c | 19,95d | 5,86a |
| abcdeMeans in the same row without common letter are different at P<0.05DM= Dry matter, CP= Crude protein, OM= organic matter, NDF=Neutral detergent fiber, ADF= Acid detergent fiber, ADL=Acid detergent lignin | |||||
With the exception of the hay-oats vetch, all substrates were characterized by their high ash content. The Amaranthaceae (S. mollis and A. halimus) are the busiest salt (10.3 and 12.26% of dry matter, respectively) followed by Z. album (9%) and T. aphylla (8%). The K+ content were for the majority of species less than or around 1% of the dry matter of the consumable part. The calcium content is from 1.5 to twice higher than that of magnesium. The Amaranthaceae are the richest in these bivalent (1.9 to 2% by Ca2+ and 1.2 and 1.4 Mg2+, respectively for A. halimus and S. mollis). The mineral composition of feed results from the combined action of several factors; the vegetative phase of the plant, the environmental conditions and operating modes. (Jarrige et al 1995; Chehma 2005; Chehma and Youcef 2009).
As to the contents of crude protein (CP), we note that it is significantly variable between substrates (P<0.05). However and for all forages, CP levels are comparable to arid forage, apparently with no geographically specific relationship: Western Tunisians (55 to 221 g / kg DM, Guasmi-Boubaker et al 2005), arid Egyptian areas (124-185 g / kg DM, Salem et al 2005), West African regions (137-212 g / Kg DM, Rittner and Reed 1992), East Africa (156-275 g / kg DM, Nshalai et al 1994), the tropics (211 g / kg DM, Larbi et al 1994).
In general, substrates studied have a different composition parietal (P <0.05). For the NDF fraction which represents the total wall (cellulose + hemicelluloses + lignin), it varies between 40.59% and 77.7% DM, while the ADF fraction varies between 28.15 and 53.11%. The highest value is noted for Z. album and the lowest is recorded for A. halimus (P <0.05). Indeed, according to Kellems and Church (2001), plants with NDF and ADF, respectively, from 70 to 88% and from 39 to 67% are classified as low-quality forage species. High levels of NDF fraction in these plants could be explained by environmental conditions in the region of El Oued (high temperature and low precipitation). Pascual et al(2000) indicate that high temperatures and low precipitation tend to increase the parietal fraction (NDF) and reduce the soluble content of plants. Against all odds, the reference substrate, vetch oats, contains an intermediate rate of about 55.88% DM. These results are similar to the work available in literature (Ammar et al 2005; Gazmi- Boubaker et al 2005; Pascual et al 2000).
| Table 2. Levels of secondary compounds (% DM) and salt-tolerant forages collected from El Oued region | ||||
| Substrats | Total oxalates | Total phenols | Total tannins | Condensed tannins |
| A. halimus | 8,86a | 1,85b | 0,1a | 0,030b |
| S. mollis | 18,89b | 4,59c | 3,83d | 0,056c |
| T. aphylla | TRACES | 7,53d | 1,73c | 0,060c |
| Z. album | TRACES | 0,10a | 0,02a | 0,009a |
| Vesce-avoine | TRACES | 0,11a | 0,25b | 0,01a |
| abcdMeans in the same column without common letter are different at P<0.05 | ||||
The average secondary compounds content of halophytes collected and selected in El Oued region, as well as the vetch-oat hay is shown in Table 3. In fact, high levels of these compounds depreciate forage quality. The levels of total phenols are variable depending on the species, T. aphylla being the richest species in total polyphenols (7.53% of the dry matter), Z. album and vetch hay oats are the poorest species and have significantly similar values (P <0.05). The levels of phenolic compounds found in this study, according to some authors (Frutos et al., 2002; Khanal and Subba, 2001), may have a limited effect on the availability of nutrients from forage for ruminal microbiota. A similar trend is observed for total tannins (TT), the highest concentration is found in S. mollis (3.83% DM) and the lowest content in A. halimus (0.1% DM) (P <0.05). Oxalates are accumulated at much higher levels in the Amaranthaceae S. mollis is the species most rich in oxalate, while Z. album and T. aphylla contains traces of oxalate. While condensed tannins (CT), are absent or detected only trace amounts in most studied forages. Higher results in secondary compound were obtained in the work of Ammar et al (2009), Alvarez et al (2005) for shrubs in northern Spain. The results achieved in our work on TT and TC are similar to the values of forages in arid areas of northern Egypt (Salem et al., 2006), for fodder collected in the arid regions of Southern Sudan (El-Fadel Seed et al 2000) for African fodder from the east (Abdulerzak et al 2000).
The biological parameters measured on the species studied, which were incubated in calibrated syringes are recorded in Table 3. Each value is the average of 3 repetitions. The volume of gas produced (GP) in the syringes is lower in the 2 Amaranthaceae (150.96 ml and 141,83ml / 0.2 g DM for A. halimus and S. mollis) than T. aphylla and Z. album, the latter has the highest value (190,983ml / 0.2g MS). Thus, the degradability of organic matter, estimated from gas production is variable depending on the species, S. mollis is the species most degradable. The variation of gas production is related to the composition of the substrates and the variable contents of secondary compounds according to the species and the botanical family. However, unexpected results are observed for hay vetch oats which has a value similar to that of S. mollis despite the low levels of cell wall constituents and secondary compounds. Indeed, halophytes prove well be fermented by the rumen microbiota camel, unlike most publications that mention that in vitro gas production is negatively influenced by the fiber content of foods (Apori et al 1998; Fructos et al 2004; Getachew et al 2000).
| Table 3. Gas production (GP) and digestibility of organic matter (DOM) of the test plants | ||
| Substrates | GP (ml) | DOM |
| A. halimus | 150,96b | 47,24b |
| S. mollis | 141,83a | 45,61a |
| T. boveana | 185,7c | 53,31c |
| Z. album | 190,9d | 54,19c |
| Vesce-avoine | 142,2a | 45,42a |
| abcd Means in the same column without common letter are different at P<0.05 | ||
The correlation coefficients among the nutrient values of secondary substances and quantities of gas produced are reported in Table 4 in the form of a triangular matrix. Here we present examples of correlations between the different parameters are studied by focusing more on the correlations with NaCl and gas production. The array analysis shows that the ash percentage (r = 0.937; p = 0.0001) increases with the percentage of NaCl. Similarly, there is a positive correlation between the accumulation of NaCl in the aerial part of the plant and the percentages of K+ cations (r = 0.799; p = 0.01), Ca2+ (r = 0.818; p = 0.01) and Mg2+ (r = 0.743; p = 0.01). Furthermore, the presence of NaCl in the edible part of the plant is negatively related, but without statistical significance fractions NDF and ADF. The total nitrogenous matter is not connected with gas production reflecting the low contribution of nitrogen content in gas production, a situation reported by many authors (Aregheore 2000; Khazaal et al 1993; Long et al 1999). Thus, the components in NDF, ADF and ADL are positively and significantly correlated with the production of gas. These results are contradictory to the work carried out on ruminants (Areghoreb 2000; Khazaal et al 1995).
So, camels are more effective in the digestive and metabolic utilization ration compared to conventional ruminants, particularly nitrogen and parietal compounds, probably because of the specific microflora contained pre stomachs Camels (Jouany 2003; Longo et al 2007). Negative and non-significant correlation was also observed between the production of gas and its oxalate content. Several studies show that this compound is strongly accumulated in halophytes in response to salt stress (Nyman et al 1989; Guo et al 2005). This compound has been considered by several authors as an anti-nutrient, its presence reduces the availability of calcium and sometimes other items (Weaver et al 1987; Nakata and McConn 2007).
This study aimed to estimate the nutritive value of halophytes collected from camel's courses in the arid regions of Algeria. Analysis of the chemical composition of the substrates reveals that they contain moderate amounts in CP. They are very rich in parietal composed and contain low concentrations of lignin. The evaluation of the in vitro fermentability of the substrates by the ruminal microflora shows that these substrates are efficiently degradable by the ruminal microflora dromedary, and the presence of large quantities of salt does not affect their degradability. However, these substrates can be used for camel diets in areas with salt soil.
| Table 4. Correlation matrix between nutritional, anti-nutritional and biological parameters. | ||||||||||||||||
| OM | CP | NaCl | K+ | Ca2+ | Mg2+ | NDF | ADF | ADL | Ash | TO | TP | TT | CT | GP | DOM | |
| DM | -0,347 | 0,038 | -0,395 | -0,522* | -0,353 | -0,461 | -0,365 | -0,297 | -0,333 | -0,430 | -0,525 * | -0,339 | -0,751 ** | -0,445 | -0,172 | -0,123 |
| OM | 0,497 | -0,090 | 0,328 | 0,206 | 0,360 | -0,464 | -0,416 | -0,421 | -0,202 | 0,606* | 0,699 ** | 0,869 ** | 0,806 ** | -0,487 | -0,512 | |
| CP | -0,052 | 0,498 | 0,506 | 0,583 * | -0,847 ** | -0,877 ** | -0,934 ** | -0,371 | 0,770 ** | -0,100 | 0,369 | 0,144 | -0,941 ** | -0,963 ** | ||
| NaCl | 0,799 ** | 0,818 | 0,743 ** | -0,064 | -0,147 | 0,087 | 0,937 ** | 0,409 | 0,308 | 0,186 | 0,394 | 0,354 * | 0,267 | |||
| K+ | 0,976 ** | 0,984 ** | -0,429 | -0,529 * | -0,375 | 0,592 | 0,868 ** | 0,281 | 0,546 | 0,507 | -0,222 | -0,310 | ||||
| Ca2+ | 0,968 ** | -0,498 | -0,604 * | -0,439 | 0,597* | 0,803 ** | 0,176 | 0,375 | 0,400 | -0,229 | -0,317 | |||||
| Mg2+ | -0,514 | -0,606 | -0,473 | 0,504 | 0,896 ** | 0,245 | 0,541 * | 0,496 | -0,321 | -0,406 | ||||||
| NDF | 0,981* | 0,985 ** | 0,237 | -0,578 * | -0,124 | -0,189 | -0,295 | 0,785 ** | 0,812 ** | |||||||
| ADF | 0,962 ** | 0,166 | -0,649 ** | -0,047 | -0,186 | -0,248 | 0,787 ** | 0,819 * | ||||||||
| ADL | 0,403 | -0,610 * | 0,093 | -0,164 | -0,114 | 0,639 ** | 0,565 ** | |||||||||
| Ash | 0,147 | 0,353 | 0,103 | 0,350 | -0,603 ** | -0,699 ** | ||||||||||
| TO | 0,227 | 0,734 ** | 0,503 | 0,199 | 0,157 | |||||||||||
| TP | 0,669 | 0,944 ** | 0,276 | 0,323 | ||||||||||||
| TT | 0,803 ** | -0,013 | -0,070 | |||||||||||||
| CT | 0,993 | |||||||||||||||
| GP |
1 ** |
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| DM: Dry matter, OM: organic matter, CP: Crude protein, NDF: Neutral detergent fiber, ADF: Acid detergent fiber, ADL: Acid detergent lignin, TO: Total oxalates, TP: Total phénols, TT: Total tanins, CT: Condensed tanins, GP: Gas production, DMO: Digestibility of organicmatter, *: P < 0,05, **: P < 0,01 | ||||||||||||||||
Abdelguerfi A, Si Ziani T, Kies N and Ouada M 1996 From autoecology to variability of media in Algeria: synthesis trial of works realised at the National Agronomic Institute El Harrach. Cahiers Options méditerranéennes, 18: 39-52.
Abdulrazak S A, Fujihara T, Ondiek JK, Orskov E R 2000 Nutritive evaluation of some acacia tree leaves from Kenya. Anim. Feed Sci. Technol. 85, 89-98.
Ammar H, Lopez S, Gonzalez J S 2005 Assessment of the digestibility of some Mediterranean shrubs by in vitro techniques. Anim. Feed Sci. Technol. 119, 323–331.
Ammar H, Lopez S, Kammoun M, Bodas R, Giraldez F G, Gonsalez J S 2009 Feeding quebracho tannins to sheep to enhances rumen fermentative activity to degrade browse shrubs. Anim. Feed Sci. Technol.149,1-15.
Alvarez del Pino M, Hervas G, Mantecon A R, Giraldez FJ, Frutos P 2005 Comparison of biological and chemical methods, and internal and external standards, for assaying tannins in Spanish shrub species. . J. Sci. Food Agric. 85, 583-590.
AOAC 1990 Official Methods of Analysis. 15th Edn. (Association of Official Analytical Chemists, INC, Va. USA).
Apori S O, Castro FB, Shand W J, Orskov E R 1998 Chemical composition, in sacco degradation and in vitro gas production of some Ghanaian browse plants. Anim. Feed Sci. Technol. 76, 129-137.
Aregheore E M 2000 Chemical composition and nutritive value of some tropical by-product feedstuffs for small ruminant in vivo and in vitro digestibility. Anim. Feed Sci. Technol. 85, 99-109.
Ben M’hamed M 1990 Forage shrub in North Africa-studies of the green belt of North Africa. ALESCO, Tunis, Tunisie, pp. 233.
Chaibou M 2005 Productivité zootechnique du désert : le cas du bassin laitier d’Agadez au Niger. Thèse en biologie intégrative, université de Montpellier II, 279 p. http://camelides.cirad.fr/fr/science/pdf/these_chaibou.pdf
Chehma A 2005 Etude floristique et nutritive des parcours camelins du Sahara septentrional algérien. Cas de la région de Ouargla et Ghardaïa. Thèse doctorat, université Badji Mokhtar, Annaba, Algérie, 178 p. http://camelides.cirad.fr/fr/science/pdf/these_chehma.pdf
Chehma A, Faye B, Bastinelli D 2010 Valeurs nutritionnelles des plantes vivaces des parcours sahariens algériens pour dromadaires. Fourrages, 204 : 263-268. http://www.afpf-asso.org/download.php?type=1&id=1818&statut=0
Chehma A, Faye B Djebar M R 2008 Productivité fourragère et capacité de change des parcours camelins du Sahara septentrionale algérien. Sécheresse, 19: 115-121.
Chehma A et Longo H F 2004 Bilan azoté et gain de poids chez le dromadaire et le mouton, alimentés à base de sous-produits de palmier dattier, de Drinn "Stipagrostis pungens" et de paille d’orge. Cahiers Agricultures, 13: 221-226. http://www.jle.com/fr/revues/agr/e-docs/bilan_azote_et_gain_de_poids_chez_le_dromadaire_et_le_mouton_alimentes_a_base_de_sousproduits_du_palmier_dattier_de_la_pa_262233/article.phtml?tab=texte
Chehma A, Youcef F 2009 Variations saisonnières des caractéristiques floristiques et de la composition chimique des parcours sahariens du sud est algérien. Sécheresse, 20 : 373-381. http://www.jle.com/fr/revues/sec/e-docs/variations_saisonnieres_des_caracteristiques_floristiques_et_de_la_composition_chimique_des_parcours_sahariens_du_sud_est_alger_282986/article.phtml?tab=download&pj_key=doc_attach_15059
Correra A 2006 Dynamique de l’utilisation des ressources fourragères par les dromadaires des pasteurs nomades du parc national du banc d’Arguin (Mauritanie). Thèse doctorat, Muséum National d’Histoire Naturelle, Paris, 247 p. http://camelides.cirad.fr/fr/science/pdf/these_correra_complet.pdf
Elmer P 1994 Analytical methods for atomic absorption spectrometry. The Perkin Elmer Corporation, USA.300pp. http://eecelabs.seas.wustl.edu/files/Flame%20AA%20Operating%20Manual.pdf
Fadel El-Seed A M A, Anim A E, Abdel Ati K, Sekine A, Hishinuma J, Hamana K 2000 Nutritive evaluation of some fodder tree species during dry season in central Sudan. Asian-Australian J. of Anim. Sci. 1, 844-850. http://www.ajas.info/upload/pdf/15_132.pdf
Frutos P, Hervas G, Ramos G, Giraldez F J, Mantecon A R 2002 Condensed tannin content of several shrub species from a mountain area in northern Spain, and its relationship to various indicators of nutritive value. Anim. Feed Sci. Technol. 95, 215–226. http://digital.csic.es/bitstream/10261/4805/3/Frutos_et_al_2002.pdf
Fructos P, Hervas G, Giraldez F J, Mantecon A R 2004 An in vitro study on the ability of polyethylene glycol to inhibit the effect of quebracho tannins and tannic acid on rumen fermentation in sheep, goats, cows and deers. Australian J. Agri. Research. 55(11), 1125-1132.
Gasmi-Boubaker A, Kayouli C, and Buldgen A 2005 In vitro gas production and its relationship to in situ disappearance and chemical composition of Mediterranean browse species. Anim. Feed Sci. Technol. 123, 303-311.
Getachew G, Makkar H P S and Becker K 2000 Tannins in tropical browse: effects on in vitro microbial fermentation and microbial protein synthesis in media containing different amounts of nitrogen. J. Agri. and Food chemistry. 148, 3581-3588.
Guo Z, Tan H, Zhu Z, Lu S, Zhou B 2005 Effect of intermediates on ascorbic acid and oxalate biosynthesis of rice and in relation to its stress resistance. Plant Physiology and Biochemistry. 43, 955-962.
Jarrige R, Ruckebusha Y, Demarquilly C 1995 Les herbivores ruminants. In: Nutrition des ruminants domestiques ingestion et digestion. Ed. INRA publications, Versailles, 905 p.
Jouany J P 2000 La digestion chez les camélidés. Comparaison avec les ruminants. 2000. INRA production animale .13,165-176. https://www6.inra.fr/productions-animales/content/download/4052/41861/version/2/file/Prod_Anim_2000_13_3_02.pdf
Kellems R O, Church D C 2001 Livestock feeds and feeding. Prentice Hall, Englewood Cliffs, NJ. 654 pp.
Khanal R C, Subba D B 2001 Nutritional evaluation of leaves from some major fodder trees cultivated in the hills of Nepal. Anim. Feed Sci. Technol. 92, 161-165.
Khazaal K, Dentinho M T, Riberio J M and Orskov E R 1993 A comparison of gas production during incubation with rumen contents in vitro and nylon bag degradability as predictors of the apparent digestibility in vivo and the voluntary intake of hays. Animal Production, 57: 105-112.
Khazaal K, Dentinho M T , Riberio J M , Orskov E R 1995 Prediction of apparent digestibility and voluntary intake of hay fed to sheep: Comparison between using fibre components, in vitro digestibility or characteristics of gas production or nylon bag degradation. Anim. Sci. 61, 527-538.
Larbi A, Smith J W, Kurdi I O, Adekunle I O , Raji A M and ladipo D O 1998 Chemical composition, rumen degradation and gas production characteristics of some multipurpose fodder trees and shrubs during wet and dry seasons in the humids tropics. Anim. Feed Sci. Technol. 72, 81-96.
LE HOUÉROU H N 2001 Biogeography of the arid steppeland north of the Sahara. Journal of Arid Environments, 48, 103-128.
Long R J, Apori S O, Castro F B and Orskov E R 1999 Feed value of native forages of the Tibetan Plateau of China. Animal Feed Science and Technology, 80: 101-113.
Longo H F, Siboukeur O, Chehma A 2007 Aspect nutritionnel des pâturages les plus appréciés par Camelus dromedarus en Algérie. Cahiers Agricultures, 16 : 477 - 483. http://www.jle.com/fr/revues/agr/e-docs/aspects_nutritionnels_des_paturages_les_plus_apprecies_par_camelus_dromedarius_en_algerie_276706/article.phtml?tab=download&pj_key=doc_attach_2355
Makkar H P S 2003 Quantification of Tannins: a laboratory Manual, 2nd edition, International Center for Agricultural Research in the dry areas, Allepo, Syria.
Makkar H P S, Blümmel M, Borowy N K and Becker K 1993 Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture.61, 161-165.
Menke K H Steingass H 1988 Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 28, 7-55.
Nakata P A, McConn M M 2007 Calcium oxalate content affects the nutritional availability of calcium from Medicago truncatula leaves. Plant Science . 172, 958-961.
Nègre R 1961 Petite flore des régions arides du Maroc Occidental. Ed. CNRS, Paris, 2 vol.
Nshalai I V, Siaw D E K A, Osuji P O 1994 The Relationship between gas production and chemical composition of 23 browses of the genus Sesbania. J. Sci. Food and Agri. 65, 13-20.
Nyman L P, Aritti J, Bradley T J 1989 Organic and inorganic constituents of salt tolerant Taro (Colocasia esculenta var antiquorum) tissues cultured in saline media. Environmental and experimental botany . 29(4) , 423-432.
Oulad Belkhir A 1989 Composition chimique et digestibilité in vitro des principaux pâturages consommés par le dromadaire dans quelques aires de distribution en Algérie. Mémoire Ing. INA, El Harrach, 65p.
Ozenda P 1991 Flore du Sahara. 3ème édition, complétée. CNRS, Paris, 662 p.
Pascual J J, Fernandez C , Diaz J R, Garces C, Rubert-Aleman J 2000 Voluntary intake and in vitro digestibility of different date-palm fractions by Murciano-Granadina (Capra Hirsus). J. Arid Environments. 45, 183-189.
Porter L W, Hrstich L N, Chan B G 1986 The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223–230.
Quézel P et Santa S 1962 Nouvelles flores de l’Algérie et des regions désertiques méridionales. Ed. CNRS, Paris, 2 vol., 1170 p.
Rittner U and Reed J D 1992 Phenolics and in vitro degradability of protein and fibre in West African browse. J. Sci. Food Agri. 58, 21-28.
Salem A Z M, Salem M Z M, El-Adawy M M and Robinson P H 2006 Nutritive evaluations of some browse tree foliages during the dry season, secondary compounds, feed intake and in vivo digestibility in sheep and goats. Anim. Feed Sci. Technol.127, 251-267.
Sauvant D 1988 La composition et l’analyse des aliments. In : Jarrige R. (ed), Alimentation des Bovins, Ovins et Caprins,INRA, Paris , 305-314.
Van Soest P J, Robertson J B, Lewis B A 1991 Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583-3597.
Weaver C M, Martin B R, Ebner J S, Krueger C A 1987 Oxalic acid decreases calcium absorption in rats, J. Nutr. 117, 1903 – 1906. http://jn.nutrition.org/content/117/11/1903.full.pdf
Received 6 February 2015; Accepted 21 February 2015; Published 3 March 2015