Nutritive value and anti-nutritional components of leaves of some salt-tolerant tree species

M R Al-Masri

Department of Agriculture, A.E.C.
P.O. Box 6091, Damascus, Syria
scientific@aec.org.sy

Abstract

The nutritive values of leaves of some salt-tolerant tree species (Tamarix articulata Vahl., Tamarix aphylla (L) Karst, Acacia ampliceps Maslin, Eucaliptus camaldulensis Dahnhard,, Casuarina equisetifolia L, Parkinsonia aculeate L.) were evaluated by determination of in vitro digestible organic matter (IVDOM), metabolizable energy (ME), net energy lactation (NEL) and the presence nutritional and anti-nutritional components.

The highest values of the crude protein, buffer soluble nitrogen and buffer soluble non-protein nitrogen and the lowest value of condensed tannins were obtained for P. aculeate. Leaves of E. camaldulensis contained lower concentrations (P<0.05) of crude protein and higher contents of anti-nutritional components than other tree species. The descending order (P<0.05) of the tree species on the basis of their crude protein content (g/kg DM) was P. aculeate (176)>A. ampliceps (145)>T. aphylla (142)>T. articulate (96)>C. equisetifolia (89)>E. camaldulensis (74). The ash content was high in C. equisetifolia, T. aphylla and A. ampliceps. The IVDOM, ME and NEL values ranged from 378-584 g/kg DM, 4.89-7.34 MJ/kg DM and 2.04-3.49 MJ/kg DM, respectively. The highest values of the IVDOM, ME and NEL were obtained for A. ampliceps. The IVDOM values were positively correlated with crude protein. Total phenols concentrations (g/kg DM) ranged from 18 in C. equisetifolia to 132 in E. camaldulensis. The addition of polyethylene glycol (PEG, 6000) to the plant samples incubated with rumen fluid at a ratio of (2:1 PEG:substrate) increased the values of  IVDOM, ME and NEL. The response to PEG treatment increased with increased concentration of phenolic compounds in the plant samples. Feeding of PEG with leaves of salt-tolerant tree species containing high levels of tannins can be helpful by increasing the organic matter digestibility and energy values. Leaves of P. aculeate, T. aphylla and A. ampliceps were rich in crude protein and therefore useful for supplementing low crude protein forage diets.

Key words: digestibility, energy, nutrient, polyethylene glycol, protein, tannin, waste

Introduction

In tropical and subtropical regions, ruminants feeding are largely dependent on pasture grasses and cereal crop residues so that a high level of ruminant production is not always possible. Correction of dietary deficiencies can increase microbial degradation of feed in the rumen and improve the animal's metabolic capacity to use energy, both of which increase the voluntary intake of digestible organic matter and ruminant production. Forages from shrubs and trees are used as dietary supplement to make up for dietary deficiencies in nitrogen, energy and minerals during regular feed shortages and droughts (Melagu et al 2003; Kumara Mahipala et al 2009) and to improve livestock performance (Abdulrazak et al 1996; Bensalem et al 2002). However, the use of tree and shrub leaves by herbivores is restricted by deterring mechanisms related to high tannin content (Rubanza et al 2003; Bakshi and Wadhwa 2004). The phenolic compounds (particularly tannins) in some trees and shrubs may bind to protein, thus rendering the protein undegradable by rumen microbes. Polyethylene glycol (PEG) is able to form complexes with tannins (Getachew et al 2000) and has been used to reduce tannin-protein complex formation or to release these complexes (Makkar et al 1995).

Salt-affected soils are widespread in Syria, resulting in large areas of agricultural land being withdrawn from agricultural production annually. Attempts are being made to make these areas productive again by utilizing available saline groundwater and salt-tolerant plants such as multipurpose tree species. Multipurpose tree species (Tamarix articulata Vahl., Tamarix aphylla (L) Karst, Acacia ampliceps Maslin, Eucaliptus camaldulensis Dahnhardt, Casuarina equisetifolia L., Parkinsonia aculeate L.) are widely used for reforestation in waste lands and considered as valuable plant sources in tropical agriculture and as an alternative forages for livestock. They are soil salt-tolerant trees and by tolerating saline water, save on usage of non-saline irrigation water, consequently reducing the cost of forage production (Khalifa et al 2003).

A. ampliceps and P. aculeate, a member of the Fabaceae family, are evergreen and leguminous trees. A. ampliceps is a fast growing tree, browsed well by cattle and widely used for reforestation of the arid and semi-arid areas in Asia. It is tolerant of alkaline, highly saline and waterlogged conditions. P. aculeate is a flowering tree native to the southwestern United States (western Texas, southern Arizona), Mexico, the Caribbean, south America, south to northern Argentina, and the Galápagos Islands. T. articulata and T. aphylla, members of the family Tamarieaceae, are evergreen and non-leguminous trees. T. articulata is a halophyte species native to the shores of south-west Europe and western Asia and grows well in salt affected soils. T. aphylla is a drought resistant well suited to arid and semi-arid rangelands. It grows quickly and is extremely tolerant of saline and alkaline soils native to Africa and Asia. C. equisetifolia, a member of the family Casuarinaceae, is an evergreen tree, tolerant of saline soils and grows on very dry soils subjected to difficult coastal conditions. E. camaldulensis is an evergreen forestry tree native to Australia, and belonging to the family Myrtaceae. It is tolerant of saline soils and acts as "biological pump" which contribute to dramatic change of water table through reducing the level of groundwater making the soil more suitable for agricultural production (Khalifa et al 2003). 

Objectives

The objectives of the present study were:

• To evaluate the leaves of some multipurpose tree species (T. articulata, T. aphylla, A. ampliceps, E. camaldulensis, C.  equisetifolia, P. aculeate) in terms of their contents of nitrogen forms, cell-wall constituents and nutritional and anti-nutritional components.
  
  
• To measure in vitro digestible organic matter and metabolizable energy of the leaves of tree species as well as their impact on and net energy lactation.
  
  
• To study the influence of polyethylene glycol on these parameters using a gas production technique.

Materials and Methods

Plant materials tested

Six tree species (T. articulata, T. aphylla, A. ampliceps, E. camaldulensis, C.  equisetifolia, P. aculeate) grown on a salty soil (salt concentration = 12.39 g/L, pH = 7.65 at 25-100 cm depth), located about 20 km east of Deir Ezzor (39^o 41.3 ^'E; 36.3 ^o 34.1 ^'N) in north-eastern Syria were selected. Tree species were 7 years old and irrigated by saline water (8.32-9.60 g/L). The leaf samples of each species with 4 replicates (3 trees each) were randomly and manually collected at the vegetative stage from different locations of the tree, dried at room temperature (20-25 ^oC) for one week, ground to pass a 1-mm sieve and stored frozen at -20 ^oC in sealed nylon bags for later analysis.

Determination of nutritional and anti-nutritional components

Standard methods as described in AOAC (1990) were used for determination of dry matter (DM), ash, ether extract (EE), crude protein (CP) and acid-detergent fibre (ADF). Neutral-detergent fibre (NDF) was determined by the method of Van Soest et al (1991), without the use of sodium sulfite and amylase. Both of NDF and ADF were not ash corrected. Acid-detergent residue was treated with 72% H₂SO₄ (w/w) for lignin estimation (Van Soest et al 1991). Non-fiber carbohydrate (NFC) was calculated as: NFC = DM – (CP + NDF + fat + ash) (Sniffen et al 1992).

Buffer soluble nitrogen (BS-N) and non-protein nitrogen (BS-NPN) were determined according to Makkar and Becker (1996). 50 mL of phosphate buffer (0.05 M, pH 7.0) in a centrifuge tube was added to 2.5 g sample and the contents were ultra-turraxed at 10 000 rpm for 4 x 3 min with intermittent cooling. The supernatant liquid was separated by centrifuging at 3500 g for 15 min. The buffer-soluble nitrogen was determined on aliquots of the supernatant by the Kjeldahl method. To other 10 mL aliquots an equal volume of 20% trichloroacetic acid was added; the mixture was kept overnight in a refrigerator and centrifuged at 3500 g for 15 min to collect the protein-free supernatant, aliquots of which were analyzed for non-protein nitrogen.

Total phenols (TP), hydrolysable tannins (HT) and condensed tannins (CT) were determined by spectrophotometric methods. Total phenols were quantified by Folin Cio-calteu reagent and hydrolysable tannins as the difference of phenolics before and after tannin removal from the extract using insoluble polyvinylpyrolidone (Makkar et al 1993). Condensed tannins were determined by the butanol-HCL method (Porter et al 1986).

Estimation of digestible organic matter, metabolizable energy and net energy lactation

In vitro digestible organic matter (IVDOM) and metabolizable energy (ME) and net energy lactation (NEL) were estimated according to the methods of Menke et al (1979) using a gas production technique, by incubating samples in 100 mL calibrated glass syringes at 39 ^oC with a rumen fluid mixture for 24 h, and with or without adding polyethylene glycol at a ratio of 2:1 PEG:substrate to study the biological activity of tannins (Makkar et al 1995). The equations used to estimate the IVDOM, ME and NEL values were:

IVDOM (g/kg DM)  =  (16.49 + 0.9042 (mL gas produced) + 0.0492 (protein g/kg DM) + 0.0387 (ash g/kg DM)) 10

ME (MJ/kg DM)  =  2.20  +  0.1357 (mL gas produced) + 0.0057 (protein g/kg DM) + 0.000286 (lipid g/kg DM)²

NEL (MJ/kg DM) = 0.54 + 0.0959 (mL gas produced) + 0.0038 (protein g/kg DM) + 0.0001733 (lipid  g/kg DM)²

The equations for roughages were chosen according to Menke and Steingass (1988). The volume of gas was based on that produced by incubating 200 mg of substrate for 24 h compared with that produced by the standard hay sample (Hohenheim University, Germany) used by Steingass and Menke (1986) to control quality of the rumen fluid.

The rumen fluid was collected before the morning feeding from 3 rumen-fistulated Awassi rams to avoid changes in rumen fluid activity during the experiment. The fistulated rams were principally fed on a roughage diet and received 162 g crude protein and 12.8 MJ ME per day. Rumen fluid samples were taken once every 7 days, 16 h after the last meal. The rumen fluid was homogenised and strained through 100-µm nylon cloth into a warm flask (39 ^oC) filled with CO₂. A total of 30 mL medium, consisting of 10 mL of rumen fluid and 20 mL of bicarbonate-mineral-distilled water mixture (1: 1: 2 by vol.), was pumped with an automatic pipette into the warmed syringes containing the samples (200 mg) and into the blank syringes. The syringes were shaken by hand for a couple of seconds, twice in the first hour and once again after 3, 6, and 8 h of incubation. Gas production from the experimental sample was recorded after 24 h of incubation and calculated by subtracting the volume of gas produced from the blank with or without the addition of PEG.

Data and statistical analyses

Results were subjected to analysis of variance (ANOVA) using a Statview-IV program (Abacus Concepts, Berkeley, CA, USA) and Fisher’s least significant difference test at the 0.05 level. Regression coefficients (R) between the studied parameters were calculated. 

Results

Generally there were considerable variations between the tree species in terms of chemical compositions and nitrogen forms (Table 1). Crude protein and ash contents (g/kg DM) ranged from 74-176 and 74-306, respectively. The crude protein content was highest in P. aculeate and lowest in E. camaldulensis. The descending order (P<0.05) of the tree species on the basis of their crude protein content was P. aculeate>A. ampliceps>T. aphylla>T. articulata>C. equisetifolia>E. camaldulensis. The ash content was high in C. equisetifolia, T. aphylla and A. ampliceps and low in T. articulata, E. camaldulensis and P. aculeate. The ether extract and NFC contents of E. camaldulensis were significantly (P<0.05) higher than the other tree leaves. The lowest value of NFC was obtained for A. ampliceps. NDF contents ranged from 322 g/kg DM in E. camaldulensis to 576 g/kg DM in T. articulata. T. articulata had the highest content of ADF and lignin and C. equisetifolia the lowest content of lignin compared with other species.

Soluble nitrogen forms and phenolic contents varied (P<0.05) between tree species (Table 2) with the E. camaldulensis having the highest concentrations of phenolics and lowest concentrations of BS-N and BS-NBN. The BS-N and BS-NPN contents (g/kg DM) ranged from 1.1-11.8 and 1.0-4.9, respectively.  P. aculeate had the highest content of the BS-N and BS-NPN and the lowest concentration of condensed tannins. Total phenols (TP) concentrations (g/kg DM) ranged from 18 in C. equisetifolia to 132 in E. camaldulensis. T. aphylla, P. aculeate and C. equisetifolia had the lowest (P<0.05) content of condensed tannins compared with other species. The hydrolysable tannins (HT) content was highest in E. camaldulensis and lowest in A. ampliceps and C. equisetifolia. The TP and HT concentrations were negatively correlated with CP (R = -0.48; P<0.05 and R = -0.65; P<0.05, respectively), BS-NPN (R = -0.68; P<0.001 and R = -0.82; P<0.001, respectively) and BS-N (R = -0.55; P<0.01).

The tree species varied widely in gas production, IVDOM, ME and NEL (Table 3). A. ampliceps had the highest values of the IVDOM, ME, NEL. IVDOM in the leaves of studied species decreased (P<0.05) in order of A. ampliceps> T. aphylla> C. equisetifolia or P. aculeate> E. camaldulensis>  T. articulata. There was a positive effect of added PEG on the values of IVDOM, ME and NEL. The IVDOM values were negatively correlated with NDF (R = -0.49; P<0.05), ADF (R = -0.68; P<0.002), lignin (R = -0.77; P<0.001) and HT concentrations (R = -0.53; P<0.02) but positively correlated with CP and BS-NPN (R = 0.58; P<0.01). The ME and NEL values were negatively correlated with lignin concentrations (R = -0.56; P<0.01) in all studied species.

Discussion

The differences in IVDOM, ME and NEL values of studied tree species reflect different contents of nutritive components in the experimental samples. The results indicated that the IVDOM, ME and NEL values of tree leaves are negatively correlated with the cell wall contents but positively correlated with crude protein. Khanum et al (2007) indicated that the feedstuffs (wheat straw, grasses and crop residues) having different digestibility coefficients of organic matter showed differences in ME and that the ME values were very low in feedstuffs having high fiber and low protein contents. Alonso-Diaz et al (2009) indicated that NDF concentrations in leaves of tanniniferous trees (Lysiloma latisiliquum, Acacia pennatula, Piscidia piscpula) were negatively associated with in vitro dry matter digestibility (P<0.05). Lignocellulosic materials, particularly lignin, act as a physical barrier to microbial enzymes. It is generally agreed that the lignin concentration of forages is negatively related to the extent of digestion (Jung et al 1997). The lignin suppressing effect probably results from a reduction in attachment of ruminal microbes to feed particles and inhibition of microbial growth and microbial enzyme activity (McSweeny et al 2001).

The results indicated that CP contents were highest in P. aculeate, A. ampliceps and T. aphylla and lowest in the remaining studied species. Feedstuffs containing less than 80 g / kg DM of crude protein can not provide the minimum ammonia levels required by rumen microorganisms to support optimum activity (Norton 2003). The crude protein (74-145 g/kg DM) values in leaves of the experimental species (except P. aculeate; 176 g/kg DM) are lower than those (182 g/kg DM) reported by Sallam et al. (2008) for alfalfa hay as a commonly used forage for livestock. The BS-N concentration calculated as a percent of total nitrogen was lower (9%) in E. camaldulensis compared with P. aculeate (42%), indicating a lower solubility of nitrogen at the former species which included a large amount of phenolics.

Our results indicated that the content of ash (g/kg DM) was high in C. equisetifolia, T. aphylla and A. amplicepes which are extremely salt-tolerant species (Khalifa et al 2003). Kumara Mahipala et al (2009) and (Haddi et al 2003) reported that halophytes species (Atriplex amnicola, Atriplex nummularia, Rhagodia eremaea) and (Atriplex halimus, Salsola vermiculata, Sueada mollis) contained high concentrations of ash (157-179 g/kg DM) and (150-323 g/kg DM), respectively.

In our study, the metabolizable energy values (6.17-7.34 MJ/kg DM) in leaves of tree species, with the exception of T. articulate and C. equisetifolia, are comparable to those (6.9-7.6 MJ/kg DM) reported by Al-Masri (2007) for some range plants (Erodium cicutarium, Schismus arabicus, Alhagi camelorum, Salsola vermiculata). However, our IVDOM values (446-584 g/kg DM) of the studied species (except T. articulata) are analogous to those (523-681 g/kg DM) reported by Ammar et al (2005) for some Mediterranean browse species (Arbutus unedo, Calicotome villosa, Erica arborea, Myrtus communis, Phillyrea angustifolia, Pistacia lentiscus, Quercus suber). 

The CT concentration calculated as a percent of total phenols was high (50%) in A. ampliceps and low (3%) in T. aphylla, C. equisetifolia and P. aculeate. The HT percent of the total phenols was highest (80%) in E. camaldulensis compared with all the other species. Rubanza et al (2005) indicated that CT concentrations varied between Acacia species (A. angustissima, A. drepanolobium, A. nilotica, A. polyacantha, A. tortilis, A. Senegal), and ranged from 53 in Acacia nilotica to 98 g/kg DM in A. polyacantha. The CT content in the studied Acacia species (A. ampliceps) was 24 g/ kg DM. Getachew et al (2002) reported that plant samples containing total phenols and tannin levels (g tannic acid equivalent/kg DM) up to 40 and 20, respectively, are not expected to precipitate protein or cause increases in gas production upon addition of PEG to the in vitro gas production method and, therefore, are not likely to adversely affect ruminant productivity. Values of total condensed tannins exceeding 50 g/kg DM could inhibit microbial activity, depress dry matter digestibility (Kumar and Vaithiyanathan 1990) and reduce voluntary intake (Waghorn et al 1990). The high concentrations of total phenols (132 g/kg DM) and hydrolysable tannins (106 g/kg DM) in leaves of E. camaldulensis are comparable to those (122 g/kg DM and 89 g/kg DM, respectively) reported by Singh et al (2005) for Hippophae rhamnoides tree forage. The negative correlation between IVDOM and HT coinciding with observations of (Ammar et al 2005) for some Mediterranean browse and tree species which contained condensed tannins up to 360 g/kg DM. Pritchard et al (1988) indicated that the low intake and feed value of Acacia aneura leaf was related to its content of condensed tannins, which bound with the proteins in the leaves. Phenolic compounds depress in vitro gas production and that PEG treatment has a potential for improving gas production and fermentation of feedstuffs high in phenolics due to the binding of the phenolic compounds to the PEG (Tolera et al 1997). PEG treatment increased in vitro disappearing nitrogen of tree forages (Carissa spinarum, Hippophae rhamnoides, Quercus incana, Zizyphus jujube) (Singh et al 2005). Mbugua et al (2008) reported that addition of PEG to tannin-containing tree legumes (Calliandra calothyrsus, Acacia angustissima, Desmodium uncinatum, Desmodium intortum) significantly (P<0.05) improved the amount and the rate of gas production.

In our study, the addition of PEG in the fermentation process increased the IVDOM, ME and NEL values. This might be related to the high concentrations of tannins in the leaves of the tested tree species. The response to PEG treatment increased with increased concentration of phenolic compounds in the tree species. The highest increases in the values of IVDOM, ME and NEL as a result of PEG treatment were exhibited by E. camaldulensis and T. aphylla in comparison with other species (Table 4).

The increases in the values of IVDOM, ME and NEL were positively correlated with TP (R = 0.62; P<0.01) and HT (R = 0.48; P<0.05) concentrations. The degradability of protein in tannin-containing feeds is depressed, resulting in a low NH₃-N concentration. Addition of PEG results in increased levels of NH₃-N. A rapid degradation of nitrogen not matched with energy availability could lead to accumulation of NH₃-N in the in vitro system or to a high absorption of NH₃-N from the rumen in vivo. Synchronization of the rate of degradation of nitrogen and carbohydrate components in the rumen is extremely important for efficient utilization of rumen NH₃-N for synthesis of microbial protein. Therefore, utilization of browses with high tannin levels could be improved by inclusion of tannin-binding agents such as PEG and an additional energy source to trap the nitrogen resulting from fermentation. Addition of PEG can be advantageous if the tannin content of the feed is sufficiently high to the extent that it depresses microbial activity and digestibility of feeds drastically. On the other hand, addition of PEG to low-tannin feeds may result in negative effects by reducing the amount of undegraded protein and also by decreasing the efficiency of microbial protein synthesis (Getachew et al. 2000). 

Conclusions

Based on the results of this research it is concluded that:

• Leaves of P. aculeate, T. aphylla and A. ampliceps are suitable as nitrogen supplements for low crude protein forage diets for livestock in tropical regions. This is of economical benefit leading to a reduction in the cost of rations and consequently in the cost of livestock production.
  
  
• The addition of polyethylene glycol to the tree forages containing high levels of tannins increased the values of digestible organic matter, metabolizable energy and net energy lactation.

Acknowledgements

The author thanks the Director General and Head of Agriculture Department, A.E.C. of Syria, for their encouragement and financial support.    

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Received 26 November 2012; Accepted 12 December 2012; Published 5 February 2013

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