Evaluation of Carob (Ceratonia siliqua) and Honey Locust (Gleditsia triacanthos) Pods as a Feed for Sheep

Iranian Journal of Applied Animal Science

مقاله 9، دوره 8، شماره 2، شهریور 2018، صفحه 247-256   

نویسندگان

S. Medjekal^{* 1}؛ R. Bodas²؛ H. Bousseboua³؛ S. López⁴

¹Département de Microbiologie et Biochimie, Université Mohamed Boudiaf-M’sila, Faculté des Science, 2800 M’sila, Algérie

²Instituto Tecnológico Agrario de Castilla y León, Subdirección de Investigación y Tecnología, Valladolid, Spain

³Ecole Nationale Supérieure de Biotechnologie, Ali Mendjeli BP 66E RP 25100, Ali Mendjeli / Constantine, Algérie

⁴Departamento de Producción Animal, Instituto de Ganadería de Montaña (IGM) CSIC-Universidad de León, Universidad de León, León, Spain

چکیده

The nutritive value of Ceratonia siliqua and Gleditsia triacanthos pods was determined on the basis of their chemical composition, in vitro gas production and rumen fermentation end-products. Medicago sativa was used as a reference feed material. The studied samples showed differences in chemical composition and phenolic compounds. Crude protein (CP) content was particulary low (80 g/kg DM) in carob and higher in Medicago sativa and G. triacanthos pods with (159.79 and 121.56 g/kg DM, respectively). Inclusion of Polyethylene glycol (PEG) in fermentation medium results in a significant increase (P<0.05) of gas production in Ceratonia siliqua and Gleditsia triacanthos and no effect was observed with M. sativa. The highest values of gas production were observed for C. siliqua and G. triacanthos, whereas Medicago sativa had significantly low values. The highest asymptotic gas production was observed in Ceratonia siliqua and Gleditsia triacanthos (296.80 and 289.55 mL g^-1 DM, respectively), whereas Medicago sativa recorded the lowest value (243.64 mL g^-1 DM). The concentration of acetate differentiated two groups: Medicago sativa and Gleditsia triacanthos (86.58 and 66.32% respectively), while the fermentation of Ceratonia siliqua resulted in a lower acetate concentration (59.84%). Although there were noticeable differences among the three studied samples, Ceratonia siliqua and Gleditsia triacanthos pods showed better nutritional quality, indicating that they could be considered promising and interesting sources of feed for sheep during the dry season or as supplement to low quality diets.

کلیدواژه‌ها

carob؛ digestibility؛ honey locust pods؛ <i>in vitro</i> gas production؛ tannins

اصل مقاله

INTRODUCTION

The productivity of ruminant species in the most part of Algeria is limited by the low level energy and protein intake due to the lowest production of high quality forage especially during the summer season. Barley grain is the major source of supplemental feeding during the dry as well as reproductive seasons. However, prices of barley grain increased significantly due to substantial increase in international market price which put economical pressure on livestock owners. In addition, the area was under relatively long dry period which seriously impacted the production of range- land forge and increased the burden on livestock owners (Obeidata et al. 2011). Pods of several legume trees have been included in livestock diets in many parts of the world during critical periods of the year when quality and quantity of forages are restricted (Barakat et al. 2013). Among these, carob pods seem to be promising as a non-conventional feed resource which can be used for small ruminants feeding (Guessous et al. 1989). Carob bean is the fruit of Ceratonia siliqua, which belongs to the Leguminosae family. The tree has been extensively cultivated in most countries of the Mediterranean for years and in many areas of North America. Carob pods are mostly used in the food industry for carob bean gum and locust bean gum (Battle and Tous 1997; El Hajaji et al. 2013). Some investigations explored carob pods as a readily available and inexpensive material for the production of bioethanol (Vourdoubas et al. 2002), and as a substrate for citric acid production (Roukas, 1998). Another promising feed for small ruminants in these regions, honey locust tree (Gleditsia triacanthos) is the one of introduced legume trees which were well adapted to almost parts of Algeria. This legume trees produce considerable amounts of pods every growing season. The pod yield can range from 12 to 27 kg per tree per year in young trees (Duke, 1983) to 87 kg per tree per year in adult trees (Papanastasis, 1996). Apparent seed digestibilities in sheep are reported to range between 75 to 90% (Small, 1983) and crude protein content of honey locust pods harvested in July and November ranged from 103 to 134 g kg^-1 DM (Pereira, 2000). Tannins are phenolic plant secondary compounds and are widely distributed through the plant kingdom, especially legumes and browses. Tannins are considered to have both adverse and beneficial effects, depending on chemical structure and concentration in diets (Piluzza et al. 2014). Adverse effects include reduction of feed intake, digestibility of fibre and nitrogen, and animal performance (Waghorn, 2008). Polyethylene glycol (PEG) binds condensed tannins reducing their biological activity. It has been used in these experiments to evaluate the effects of tannins. According to Yisehak et al. (2014) supplementation with PEG increased nutrient intake and total tract crude protein (CP), neutral detergent fibre (NDF) and acid detergent fibre (ADF) digestibility. The nutritive value of a ruminant feed is determined by the concentrations of its chemical components, as well as their rate and extent of digestion. Determining the digestibility of feeds in vivo is laborious, expensive and requires large quantities of feed. In vitro methods provide less expensive and more rapid alternatives. In addition, the gas production technique has been proved to be efficient in determining the nutritive value of feeds containing antinutritive factors (Kamalak et al. 2012). Therefore, the objective of this study was to evaluate carob and honey locust pods obtained from an arid region in Algeria to: (1) quantify chemical compositions and level of condensed tannin contents and (2) assess the effect of tannin activity on feed digestibility and nutrient availability in vitro using a PEG tannin bio-assay.

 

MATERIALS AND METHODS

Study area and sampling

This experiment was conducted using plant samples collected from M’sila (N 35˚ 26’ 07.9’’-E 004˚ 20’ 52.8’’, 398 m altitude) (Figure 1). M’sila is in north central Algeria, in the Saharan Atlas region, at the northern edge of Saharan Desert between the Atlas Mountains and the el-Hodna depression and salt lake. According to Köppen classification, the climate of this region is BWh (dry desert climate), characterized by high temperatures ranging between 24 and 41 ˚C, and scarce and erratic annual precipitations for a total of 100 and 250 mm/year. Carob and honey locust pods were handly collected by from at least 10 different trees for each substrat. Samples were collected during the dry season, because this is the time of the year when these plants may be more important. Then, samples were immediately freeze-dried and milled in a hammer mill using a 1 mm sieve.

 

Chemical analysis

The oven dried samples were ground in a Willey Mill to pass through 1 mm sieve for the determination of chemical composition. Feed samples were analysed for dry matter (DM) following the method of AOAC (2000). Nitrogen was determined using the micro-Kjeldahl method (AOAC, 2000). Crude protein (CP) was calculated as N × 6.25. The neutral detergent fiber (NDF), acid detergent fiber (ADF) and acid detergent lignin (ADL) were analyzed according to Van Soest et al. (1991) using the ANKOM Fiber Analyzer (ANKOM Technology, Fairport, NY). Sodium sulphite was added to the solution for the NDF determination. Fibre fractions were expressed including residual ash. Samples were also analyzed for phenolic compounds following the procedures described by Makkar (2003). Total condensed tannins of dried pods were determined by butanol-HCl method as described by Makkar (2003). The concentrations of phenols were expressed in g tannic acid equivalent/kg DM, whereas the concentration of condensed tannins was expressed in g quebracho equivalent/kg DM. All chemical analyses were performed in triplicate.

 

In vitro studies

Rumen fluid was obtained from four mature Merino sheep (body weight 49.04±4.23 kg) fitted with permanent rumen fistula (60 mm diameter) maintained in cages and fed ad- libitum lucerne hay (CP 167 g, NDF 502 g, ADF 355 g and ADL 71 g/kg DM) and had free access to water and a mineral/vitamin block. A sample of rumen contents was withdrawn prior to morning feeding, transferred into thermos flasks and taken immediately to the laboratory. Rumen fluid from the four sheep was mixed, strained through various layers of cheesecloth and kept at 39 ˚C under a CO₂ atmosphere (Ammar et al. 2004). The rumen fluid was diluted (1:4 v/v) with a culture medium containing macro- and micro-mineral solutions, resazurin and a bicarbonate buffer solution and prepared as described by Menke and Steingass (1988). The medium was kept at 39 ˚C and saturated with CO₂. Oxygen in the medium was reduced by the addition of a solution containing cysteine hydrochloride and Na₂S as described by Van Soest et al. (1966). The method used for gas production measurements was as described by Theodorou et al. (1994). About 500 mg of each sample were incubated in 50 mL of diluted rumen fluid (10 mL mixed rumen fluid+40 mL medium prepared under a CO₂ constant flow) in 120 mL serum bottles pre-warmed at 39 ˚C and flushed with CO₂. Six bottles containing only diluted rumen fluid were incubated as blanks and used to compensate for gas production in the absence of substrate. All the bottles were crimped with aluminium caps and placed in the incubator at 39 ˚C, being shaken at regular times. Volume of gas produced in each bottle was recorded at 3, 6, 9, 12, 16, 21, 26, 31, 36, 48, 60, 72, 96, 120 and 144 h after inoculation time, using a pressure transducer (Delta Ohm DTP704-2BGI, Herter Instruments SL, Barcelona). In order to estimate the fermentation kinetic parameters, gas production data were fitted using the exponential model proposed by France et al. (2000):

G= A [1-e^-c(t-L)]

Where:

G (mLg^-1): cumulative gas production at time t.

A (mLg^-1): asymptotic gas production.

c (/h^-1): fractional rate of gas production.

L (h): lag time.

The energy value and digestibility of feedstuffs were calculated from the amount of gas produced at 24 h of incubation with supplementary analyses of crude protein and ash, as follows (Menke and Steingass, 1988).

ME (MJ/kg DM)= 2.2 + 0.136 × G24 + 0.057 × CP + 0.029 × CP²

OMD (%)= 14.88 + 0.889 × G24 + 0.45 × CP + 0.0651 × Ash

Where:

ME: metabolizable energy.

G24: 24 h net gas production (mL/200 mg DM).

CP: crude protein (% of DM).

OMD: organic matter digestibility.

Ash: ash (% of DM).

The gas production technique described above was used for the effect of PEG effect. Incubations were carried out in serum bottles with or without the addition of 500 mg PEG. Ground samples (300 mg) were weighed out into serum bottles, kept at approximately 39 ˚C and flushed with CO₂ before use. Two bottles were used for each substrate with each inoculum source one for each treatment (with or without PEG). Bottles were tightly closed and placed in the incubator at 39 ˚C, being shaken at regular times. The volume of gas produced in each bottle was recorded at 6, 12, 24 and 48 h after inoculation time, using a pressure transducer. Gas production was corrected by subtracting the volume of gas produced from blank cultures. The gas production technique described above was also used for volatile fatty acids determination. After 24 h of incubation, bottles were swirled in ice to stop fermentation, and then opened. A sample of supernatant (0.8 ml) was added to 0.5 ml of deproteinizing solution (20 g metaphosphoric and 4 g crotonic acid/l 0.5N HCl) for volatile fatty acid (VFA, s) analysis. The VFA were determined by GC using a Perkin-Elmer Autosystem XL GC (Perkin-Elmer Inc., USA), equipped with a semicapillary TR-FFAP (30 m×0.53 mm×1 m) column (Supelco, USA), flame Ionization detector (FID) and an auto-sampler. Temperatures were 140 °C in the column and 250 ˚C both in the injector and the detector, and carrier gas (He) flux was 13 mL/min. Each sample was injected automatically with a split ratio of 1/3. Chromatograms were integrated using software Star Chromatography Workstation 6.2 (Varian Inc., USA).

 

Statistical analysis

One way analysis of variance (Steel and Torrie, 1997) was performed on chemical composition, gas production, fermentation kinetics parameters, metabolizable energy, organic matter digestibility and volatile fatty acids data. Tukey’s test was used for the multiple comparison of means (P<0.05). Analysis of variance between different variables were performed using SAS software package (SAS, 2000).

 

RESULTS AND DISCUSSION

Chemical composition

The chemical composition and phenolics contents of Gleditschia triacanthos (G. triacanthos), Ceratonia siliqua (C. siliqua ) pods and Medicago sativa (M. sativa) are in Table 1. Dry matter content of C. siliqua were higher (P<0.05) than those of G. triacanthos and M. sativa hay. The ash content was lowest (P<0.05) in G. triacanthos and C. siliqua and highest in M. sativa (P<0.05). The highest crude protein and NDF contents were in M. sativa. Among the studied samples, NDF content was highest (P<0.05) in M. sativa followed by G. triacanthos and C. siliqua which did not differ.

 

Figure 1 The study area

 

 

Table 1 Chemical composition (g kg^–1 dry matter) of the three studied samples

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the means.

 

M. sativa had more (P<0.05) ADF than the other studied samples. C. siliqua had the highest (P<0.05) ADL content while contents were lowest (P<0.05) in M. sativa and G. triacanthos,C. siliqua and G. triacanthos had the highest (P<0.05) total extractable phenols (TEP) and total condensed tannins (TCT) than those of M. sativa. Natural grasslands associated with trees and / or shrubs have a considerable role in ruminant feeding in extensive Mediterranean production systems, such as the one in the semi-arid region in Algeria. Legume trees or shrubs, such as C. siliqua and G. triacanthos can be used to supplement the available feedstuff during the periods of feed scarcity that are common in Mediterranean areas (Chassany and Flamant, 1996). In the present study, CP content was particulary low (80 g/kg DM) in carob pods in agreement with data reported by other authors (Silanikove et al. 1996; Silanikove et al. 2006). It is well known that carob pods, although rich in water soluble sugars (WSS), has a very low crude protein content, and contains hight levels of tannins, mainly of the condensed type, which minimize its nutritional value (Marakis et al. 1997). As expected, the CP content was higher in the M. sativa and G. triacanthos pods. Legumenous shrubs and and trees have been used as feedstuffs for livestock in many regions of the world, mainly because of their high protein content (Ammar et al. 2004) throughout the year that can be attributed to the ability of these plants to fix atmospheric nitrogen (Ammar et al. 2005), suggesting the possibility that G. triacanthos pods may be used as a dry season feed supplement to low quality diets. All of the samples studied herein contained high fibre (NDF, ADF) and ADL content. Similar results were reported for these samples and other Algerian and Mediterranean fodder shrubs (Frutos et al. 2002; Bruno-Soares and Abreu, 2003; Getachew et al. 2004; Boufennara et al. 2012). Consent with results for lignin content of carob pods (175.89 g/kg DM), Khazaal and Orskove, (1994) reported high values in samples harvested in different maturity stage (Arbutus andrachronoids, Cistus incanus and Arbutus unedo) with 182.8, 171.3 and 163.5 g/kg DM). According to Wilson and Kennedy, (1996), lignin is mainly found in the xylem in which the lignin concentrations reach levels which render cells copmpetely indigestible. In contrast, lignin concentration in other tissues are low making them almost completely digestible. Concentration of phenolics varied widely among studied samples. The analysis of specific tannins is an indication of the presence of some anti-nutritive factors in feedstuff. It has been reported that plants with more than (60 g/kg DM) free condensed tannin are less palatable and digestible than forages with lower concentrations of this chemicals, although there is more protein to by-pass the rumen and higher nitrogen retention (Terrill et al. 1992). However, animals that regularly consume tannineferous feedstuffs adapt to minimize detrimental effects of tannins, due to extra mastication, large amounts of saliva and rumen fermentation (Salem et al. 2001). Odenyo and Osuji, (1998) identified some tannins tolerant ruminal bacterial strains from enriched cultures of rumen microflora of goats to establish a medium containing high concentrations of crude tannins extract or tannic acid. A strain of the anerobe Selenomonas ruminantium, subspices ruminantium, capable growing on tannic acid or condensed tannin as a sole energy source, has been isolated from ruminal contents of feral goats browsing tannin-rich foliage (Skene and Brooker, 1995).

 

Effect of PEG on in vitro gas production

Inclusion of PEG in fermentation of the three studied samples (Table 2) results in a significant increase (P<0.0001) of gas production in C. siliqua and G. triacanthos and no effect was observed with M. sativa. In addition, the increase in gas production upon the addition of PEG, compared with that without PEG, for C. siliqua and G. triacanthos varied widely (P<0.05), being particularly high in C. siliqua (165.28 mL/g DM) and (133.06 mL/g DM) in G. triacanthos. Inclusion of PEG in fermentation of studied samples (Table 2) results in a significant increase (P<0.0001) of gas production in C. siliqua and G. triacanthos species and no effect was recorded within M. sativa. This may be due to the influence of PEG on the anti-nutritional factors contained in these samples such as condensed tannins. It is well established that the incorporation of PEG in the diet has beneficial effects, particularly for tanniniferous feeds having of 5-10 % contents of condensed tannins (Silanikove et al. 1996; Silanikove et al. 1997; Ben Salem et al. 2002). The PEG inactivation of tannins increases voluntary feed untake, availability of nutrients and decreases microbial inhibition in degrading the tanniniferous feeds, which in turn increases the performance of animals (Bhat et al. 2013). The increased GP when samples were incubated with PEG were also reported for different forages by other authors. Arhab et al. (2009) evaluated the influence of tannins present in arid zone forages from Algeria including Aristida pulmosa, Astragalus gombiformis, Genista saharae and vetch-oat hay on in vitro gas production (GP). They found that inclusion of PEG resulted in an overall increase in GP (20.2%). Moreover, the increase in GP when samples were incubated with PEG were also reported by others (Singh et al. 2005; Boufennara et al. 2013; Elahi et al. 2014). Bakhshizadeh and Taghizadeh (2013) determine the effect of PEG inclusion during in vitro incubation on GP they reported an increased GP at all incubation times than control; however, there was no significant increase in GP within levels of PEG. Therefore, tannins which bind strongly with dietary and endogenous protein would need to be counteracted with a competitive agent such as PEG. The addition of PEG, which has a relatively low cost, improves nutritional value of C. siliqua and G. triacanthos pods testified by an increased level of GP. 

 

In vitro gas production kinetics

Data of in vitro fermentation kinetics are shown in Table 3. The highest values of gas production, C and G₂₄ were observed for C. siliqua and G. triacanthos, whereas M. sativa had significantly low values. Similar trends were observed for the in vitro fermentation kinetics estimated from the gas production curves. Figure 2 shows the cumulative gas production profiles of the three different samples that were incubated in buffered rumen fluid. For the three samples studied heirin, fermentation started readily without lag time. The highest asymptotic gas production was observed in C. siliqua and G. triacanthos (296.80 and 289.55 mL g^-1 DM, respectively), whereas M. sativa recorded the lowest value (243.64 mL g^-1 DM). The estimated metabolizable energy (ME), and organic matter digestibility (OMD) are presented in Table 3. The ME contents were particularly higher in M. sativa, while C. siliqua and G. triacanthos had significantly lower values of ME (13.35 and 11.48 MJ kg^-1 DM; respectively). The OMD of C. siliqua was slightly higher than that of G. triacanthosand M. sativa. The use of the in vitro gas production methodology to estimate digestion of feeds is based on the well established relationship between the feed digestibility and in vitro gas production, in combination with the feed chemical composition (Menke and Steingass, 1988; López, 2005). In the present study, the main value of this technique was to detect differences between fermentative activity in rumen fluid of sheep when carob and honey locust pods with different tannin contents were incubated. This technique is considered more sensitive to detect such differences than other in vitro gravimetric technique (Williams, 2000).

 

Table 2 In vitro gas production (mL/g DM) of the three studied samples, without (-) polyethylene glycol (PEG) or with (+) PEG

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the means.

 

Figure 2 Cumulative gas production profiles

 

 

Table 3 In vitro fermentation kinetics of the three studied samples (estimated from gas production curves)

 

A: asymptotic gas production; c: fractional rate of gas production; L: lag time; G₂₄: 24 h net gas production; ME: metabolizable energy and OMD: organic matter digestibility.

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the means.

 

Moreover, the gas production technique allows the monitoring of the kinitics of fermentation of the feed over long incubation period without the need to use a large number of tubes to terminate treatment after different incubation periods (Khazaal and Orskove, 1994). In the current experiment, the highest cumulative gas production after 144 h of incubation (Figure 2)was observed for carob pods (296.80 mL g^-1 DM) and the lowest was obtained with M. sativa (234.64 mL g^-1 DM). The high cell wall contents in M. sativa could have accounted for the limited substrate degradation and fermentation, and consequently for the low gas production observed. These results suggest that both carob and honey locust pods can be used as feeds for ruminants. Since, carob pods were explored as a readily available and inexpensive material for the production of bioethanol (Vourdoubas et al. 2002), and as a substrate for citric acid production (Roukas, 1998). The C. siliqua pods show a high level of total sugar (around 470 g kg^-1 DM) and low values of CP and crude fibre (about 54 and 75 g kg^-1 DM, respectively) (Tous and Battle, 1990). Similarly, according to Bruno-Soares and Abreu, (2003) in G. triacanthos pods, the major components in DM (about 600 g kg^-1 DM) are neutral detergent fiber (310 g kg^-1 DM) and total sugars (290 g kg^-1 DM) where sucrose represents about 750 g kg^-1 DM. Our results suggest that these samples would be also a highly fermentable feedstuff in the rumen that could represent a substantial supply of energy to the animal. Adequately combined with a source of degradable N, it can favor the synthesis of microbial protein in the rumen (Boufennra et al. 2016). When feedstuffs are incubated in vitro, gas is produced mainly from the fermentation of carbohydrates (Blummel and Orskov, 1993), with a small contribution from the fermentation of protein or fat (Wolin, 1960). The slightly variation among plants samples in their fermentation of gas production, and ME and OMD mostly may be attributed to their variable nutrient and secondary compounds contents (Mbugua et al. 2008). Chemical composition and in vitro fermentation and digestibility are largely affected by plant species, plant morphological fraction, environmental factors, and maturity stage (Salem, 2005; Medjekal et al. 2015). Generally, as cell wall (fibre) increases, digestibility and energy content decrease (Van Soest, 1994). Our results were in line with those reported by Bruno-Suares and Abreu, (2003), Karabulut et al. (2006) and Obeidata et al. (2011), who observed higher digestibility of date pulp with lower cell-wall content. Hence, the supplementation of poor quality roughages with pods such carob and honey locust, which is commonly used by smallholder farmers, is likely to improve the performance of animals by supplying protein and soluble carbohydrates or energy (Nurfeta et al. 2008).

 

Fermentation end-products

There were differences (P<0.001) among the three studied samples in total and individual VFA concentration and acetate to propionate ratio after 24 h of incubation (Table 4). The lowest total VFA concentration was with M. sativa (68.98 mmol L^-1) and the highest with C. siliqua (89.10 mmol L^-1), whereas G. triacanthos showed an intermediate value (80.77mmol L^-1). The concentration of acetate (major fatty acid) differentiated two groups: M. sativa and G. triacanthos (86.58 and 66.32% respectively), while the fermentation of C. siliqua resulted in a lower acetate concentration (59.84%). On the other hand concentrations of propionate were higher in C. siliqua and G. triacanthos and lower M. sativa. M. sativa produced the highest molar proportions of isovalerate and valerate, whereas the acetate/propionate ratios were significantly different between treatments (P<0.0024). Acetate to propionate ratios ranged from 2.06 in C. siliqua to 3.36 in M. sativa. The variation in the in vitro gas production of studied samples was directly related to differences in other fermentation end-products (total VFA production). In the present experiment, the concentration of acetate (major fatty acid) differentiated two groups: M. sativa and G. triacanthos (86.58 and 66.32% respectively), while the fermentation of C. siliqua resulted in a lower acetate concentration (59.84%). The proportions of the dominant VFA produced in the rumen vary with diet, microbial growth rates, level of feeding, and rumen pH (Lopez et al. 2000). Degradation of fibrous or cellulosic materials is likely to produce a higher molar proportion of acetate and a lower proportion of propionate. However, feed with low fibre content would be expected to result in a reduction in the acetate: propionate ratio during rumen fermentation (Moss et al. 2000; Medjekal et al. 2016). Propionate is a useful end product of fermentation for ruminant because of it can be used for glucose synthesis (Leng et al. 1967) and is associated with higher efficiency of energy retention and utilisation in the rumen (Armstrong and Blaxter, 1957). Acetate is mostly unchanged by the liver and supplies the main source of energy by either being oxidized to ATP or stored in long chain fatty acids. Acetate and butyrate are the significant contributors to long chain fatty acids production for tissue deposition or secretion in milk (Madrid et al. 2002). Consistent with our results, Bouazza et al. (2014) reported differences in VFA and methane production from the rumen fermentation of Algerian Acacia tree foliage. The most fermentable plant species (Astragalus gombo or M. sativa) led to higher production of both fermentation gas and VFA. Moreover, Medjekal et al. (2016) reported differences (P<0.05) in pH and VFA production at 24-hour incubations of browse species of Algerian arid and semi-arid areas, with pH ranging from 6.29 (straw) to 6.73 (Hedysarum coronarium), total VFA from 1.16 (Stipa tenacissima) to 3.59 (Astragalus gombo) mmol/g dry matter (DM) incubated and the acetate:propionate ratio from 3.06 (straw) to 5.81 (Ononis natrix). According to Getachew et al. (2004), a high acetate:propionate ratio is an idication of fermentation of structural carbohydrates and thus of more fibrous feed. Furthermore, acetate to propionate ratio reduction in the rumen has been described as a common feature of several antimethanogenic compounds, wich indicates a concurrent decrease of methane formation and shift in ruminal fermentation (Albengres Abecia et al. 2012).

 

Table 4 Total (mmol L^‑1) production of volatile fatty acids, molar proportions (%), and acetate to propionate ratio (A:P) after 24 h of in vitro incubation

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the means.

 

The acetate to propionate ratios observed with our samples are within the range of values reported in other in vitro studies (Brown et al. 2002; Albengres Abecia et al. 2012; Medjekal et al. 2016).

 

CONCLUSION

Chemical composition and in vitro gas production can be considered useful indicators for the preliminary evaluation of likely nutritive value of previously uninvestigated plants samples. Our study suggest the possibility that C. siliqua and G. triacanthos pods may be used as a dry season feed supplement to low quality diets. Asreported by other authors, the addition of PEG inactivated the effects of tannins. Further studies are beaded to understand when the addition of PEG is useful in vivoto improve the nutritional value of both carob and honey locust pods.

 

ACKNOWLEDGEMENT

Financial support received from the Junta de Castilla y León, Spain is gratefully acknowledged. Medjekal S. gratefully acknowledge the receipt of a Study and Doctoral Research Abroad Fellowship funded by the Algerian Ministry of Higher Education and Scientific Research to conduct the experimental work of his PhD projects at the University of León (Spain).

مراجع

Albengres Abecia L., Toral P.G., Martín-García A.I., Martínez G., Tomkins N.W., Molina-Alcaide E., Newbold C.J. and Yáñez-Ruiz D.R. (2012). Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats. J. Dairy Sci. 95, 2027-2036.

Ammar H., Lopez S. and 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., Gonzalez J.S. and Ranilla M.J. (2004). Seasonal variations in the chemical composition and in vitro digestibility of some Spanish leguminous shrub species. Anim. Feed Sci. Technol. 115, 327-340.

AOAC. (2000). Official Methods of Analysis. 17^th Ed. Association of Official Analytical Chemists, Arlington, Washington, D.C. Arhab R., Macheboeuf D., Aggoun M., Bousseboua H., Viala D. and Besle J.M. (2009). Effect of polyethylene glycol on in vitro gas production and digestibility of tannin containing feedstuffs from North African arid zone. Trop. Subtrop. Agroecosyst. 10, 475-486.

Armstrong D.G. and Blaxter K.L. (1957). The utilization of acetic, propionic and butyric acids by fattening sheep. Br. J. Nutr. 11, 413-425.

Bakhshizadeh S. and Taghizadeh A. (2013). The effect of polyethylene glycol (6000) supplementation on in vitro kinetics of red grape pomace. Int. J. Agric. 3, 523-528.

Barakat N.A., Laudadio V., Cazzato E. and Tufarelli V. (2013). Potential contribution of retama raetam (Forssk.) Webb and Berthel as a forage shrub in Sinai, Egypt. Arid Land Res. Manag. 27, 257-271.

Battle I. and Tous J. (1997). Carob tree. Ceratonia siliqua Promoting the Conservation and Use of Underutilized and Neglected Crops. 17. Institute of Plant Genetics and Crop Plant Research. Gatersleben/International Plant Genetic Resources Institute, Rome, Italy.

Ben Salem H., Nefzaoui A. and Ben Salem L. (2002). Supplementation of Acacia cyanophylla foliage-based diets with barley or shrubs from arid areas (Opuntia ficus-indica f. inermis and Atriplex nummularia) on growth and digestibility in lambs. Anim. Feed Sci. Technol. 96(1), 15-30.

Bhat K.T., Kannan A. and Sharma P.O. (2013). Value addition of feed and fodder by alleviating the antinutritional effects of tannins. Agric. Res. 2, 189-206.

Blummel M. and Orskov E.R. (1993). Comparison of in vitro gas production and nylon bag degradability of roughages in predicting of food intake in cattle. Anim. Feed Sci. Technol. 40, 109-119.

Bouazza L., Boufennara S., Bodas R., Bousseboua H., Tejido M.L., Ammar H. and Lopez S. (2014). Methane production from the rumen fermentation of Algerian: Acacia tree foliage. Forage resources and ecosystem services provided by mountain and Mediterranean grasslands and rangelands. Options Méditerranéennes Series A. 109, 797-800.

Boufennara S., Bouazza L., López S., Bousseboua H. and Bodas R. (2013). Feeding and management strategies to improve livestock productivity, welfare and product quality under climate change Zaragoza. Options Méditerranéennes Series A. 107, 283-287.

Boufennara S., Lopez S., Bousseboua H., Bodas R. and Bouazza L. (2012). Chemical composition and digestibility of some browse plant species collected from Algerian arid rangelands. Spanish J. Agric. Res. 10, 88-98.

Brown V.E., Rymer C., Agnew R.E. and Givens D.I. (2002). Relationship between in vitro gas production profiles of forages and in vivo rumen fermentation patterns in beef steers fed those forages. Anim. Feed Sci. Technol. 98, 13-24.

Bruno-Soares A.M. and Abreu J.M. (2003). Merit of Gleditsia triacanthos pods in animal feeding: Chemical composition and nutritional evaluation. Anim. Feed Sci. Technol. 107(1), 151-160.

Chassany J.P. and Flamant J.C. (1996). Contexte économique, social et institutionnel de la question pastorale et des systèmes d’élevage extensif en régions méditerranéennes. Pp. 15-32 in The Optimal Exploitation of Marginal Mediterranean Areas by Extensive Ruminant Production Systems. N. Zervas and J. Boyazoglu, Eds. EAAP Publication, Rome, Italy.

Duke J.A. (1983). Handbook of Energy Crops. Department of Agronomy Purdue University, US. Available at: http://www.hort.purdue.edu.

El Hajaji H., Farah A., Ennabili A., Bousta D., Greche H., El Bali B. and Lachkar M. (2013). Etude comparative de la composition minérale des constituants de trois catégories de Ceratonia siliqua (comparative study of the mineral composition of the constituents of three varieties of Ceratonia siliqua). J. Mater. Environ. Sci. 4(2), 165-170.

Elahi M.Y., Nia M.M., Salem A.Z.M., Mansouri H., Olivares-Perez J. and Kholif A.E. (2014). Effect of polyethylene glycol on in vitro gas production kinetics of Prosopis cineraria leaves at different growth stages. Italian J. Anim. Sci. 13, 363-368.

France J., Dijkstra J., Dhanoa M.S., Lopez S. and Bannink A. (2000). Estimating the extent of degradation of ruminant feeds from a description of their gas production profiles observed in vitro: Derivation of models and other mathematical considerations. Br. J. Nutr. 83, 143-150.

Frutos P., Hervas G., Ramos G., Giraldez F.J. and 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.

Getachew G., Robinson P.H., DePeters E.J. and Taylor S.J. (2004). Relationships between chemical composition, dry matter degradation and in vitro gas production of several ruminant feeds. Anim. Feed Sci. Technol. 111, 57-71.

Guessous F., Rihani N., Kabbali A. and Johnson W.L. (1989). Improving feeding systems for sheep in a Mediterranean rain-fed cereals/livestock area of Morocco. J. Anim. Sci. 67, 3080-3086.

Kamalak A., Guven I., Kaplan M., Boga M., Atalay A.I. and Ozkan C.O. (2012). Potential nutritive value of honey locust (Gleditsia triacanthos) pods from different growing sites for ruminants. J. Agric. Sci. Technol. 14, 115-126.

Karabulut A., Canbolat O. and Kamalak A. (2006). Evaluation of carob, Ceratonia siliqua pods as a feed for sheep. Livest. Rese. Rural Dev. Available at: http://www.lrrd.org/lrrd18/7/kara18104.htm.

Khazaal K. and Ørskov E.R. (1994). The in vitro gas production technique: An investigation on its potential use with insoluble polyvinylpolypyrrolidone for the assessment of phenolics-related antinutritive factors in browse species. Anim. Feed Sci. Technol. 47, 305-320.

Leng R.A., Steel J.W. and Luick J.R. (1967). Contribution of propionate to glucose synthesis in sheep. Biochem. J. 103, 785-790.

López S. (2005). In vitro and in situ techniques for estimating digestibility. Pp.87-121 in Quantitative Aspects of Ruminant Digestion and Metabolism. J. Dijkstra, J.M. Forbes and J. France, Eds. CAB International, Wallingford, United Kigdom.

López S., Dijkstra J. and France J. (2000). Prediction of energy supply in ruminants, with emphasis on forages. Pp. 63-94 in Forage Evaluation in Ruminant Nutrition. D.I. Givens, E. Owens, R.F.E. Axford and H.M. Omed, Eds. CAB International, Washington, United Kigdom.

Madrid J., Megías M.D. and Hernández F. (2002). In vitro determination of ruminal dry matter and cell wall degradation, and production of fermentation end-products of various by-products. Anim. Res. 51, 189-199.

Makkar H.P.S. (2003). Quantification of Tannins in Tree and Shrub Foliage. Kluwer Academic Publishers, Dordrecht, Netherlands.

Marakis S., Lambraki M., Marakis G. and Roussous S. (1997). Enrichment of deseeded crob pod with protein and sucrose or fructose by solid state fermentation. Pp. 235-236 in Advances in Solid State Fermentation. S. Roussos, B.K. Lonsane, M. Raimbault and G. Viniegra-Gonzalez, Eds. Springer Science, Media Dordrecht, Netherlands.

Mbugua D.M., Kiruiro E.M. and Pell A.N. (2008). In vitro fermentation of intact and fractionated tropical herbaceous and tree legumes containing tannins and alkaloids. Anim. Feed Sci. Technol. 146(1), 1-20.

Medjekal S., Ghadbane M. and Bousseboua H. (2015). Impact of season of harvest on potential nutritive value, methane production and condensed tannins content of calobota saharae in m´sila, north-central Algeria. J. Polish Agric. Univ. 18(2), 1-9.

Medjekal S., Ghadbane M., Bodas R., Bousseboua H. and López S. (2016). Volatile fatty acids and methane production from browse species of Algerian arid and semi-arid areas. J. Appl. Anim. Res. 4, 1-6.

Menke K.H. and 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.

Moss A.R., Jouany J.P. and Newbold C.J. (2000). Methane production by ruminants: its contribution to global warming. Annl Zoot. 49, 231-253.

Nurfeta A., Tolera A., Eik L.O. and Sundstøl F. (2008). The supplementary value of different parts of enset (Ensete ventricosum) to sheep fed wheat straw and Desmodium intortum hay. Livest. Sci. 119(1), 22-30.

Obeidata B.S., Alrababah M.A., Abdullah A.Y., Alhamad M.N., Gharaibeh M.A., Rababah T.M. and Abu Ishmais M.A. (2011). Growth performance and carcass characteristics of Awassi lambs fed diets containing carob pods (Ceratonia siliqua). Small Rumin. Res. 96, 149-154.

Odenyo A.A. and Osuji P.O. (1998). Tannin-tolerant ruminal bacteria from East African ruminants. Canadian J. Microbiol. 44(9), 905-909.

Papanastasis V. (1996). Selection and utilization of cultivated fodder trees and shrubs in the Mediterranean production systems. Pp. 85 in Proc. Int. Symp. Organ. HSAP and EAAP. Ioannina, Greece.

Pereira B.A.M. (2000). Aspects of nutritive value of Gleditsia triacanthos pods as fodder for ruminants. Implications in the interest of the species to improve the pastoral systems in center and South of Portugal. MS Thesis. Technical University of Lisbon, Lisbon, Portugal.

Piluzza G., Sulas L. and Bullitta S. (2014). Tannins in forage plants and their rolein animal husbandry and environmental sustainability: A review. Grass and Forage. Sci. 69, 32-48.

Roukas T. (1998). Citric acid production from carob pod by solid-state fermentation. Enzyme. Microb. Technol. 24, 54-59.

Roukas T. (1998). Carob pod: A new substrate for citric acid production by Aspergillus niger. Appl. Biochem. Biotechnol. 74(1), 43-53.

Salem A.Z.M. (2005). Impact of season of harvest on in vitro gas production and dry matter degradability of Acacia saligna leaves with inoculums from three ruminant species. Anim. Feed Sci. Technol. 123, 67-79.

Salem A.Z.M., González J.S., López S. and Ranilla M.J. (2001). Evolución de la respuesta en la producción unilateral de saliva parotidea a la inclusión de quebracho en la dieta en ganado ovino y caprino. Pp. 322-324 in Proc. Asoc. Interprof. Para el Desarrollo Agrario (AIDA), Zaragoza, Spain.

SAS Institute. (2000). SAS^®/STAT Software, Release 8.1. SAS Institute, Inc., Cary, NC. USA.

Silanikove N., Gilboa N. and Nitsan Z. (1997). Interactions among tannins, supplementation, and polyethylene glycol in goats fed oak leaves. Anim. Sci. 64, 479-483.

Silanikove N., Gilboa N., Nir I., Perevolotsky A. and Nitsan Z. (1996). Effect of a daily supplementation of polyethylene glycol on intake and digestion of tannin-containing leaves (Quercus calliprinos, Pistacia lentiscus and Ceratonia siliqua) by goats. J. Agric. Food Chem. 44, 199-205.

Silanikove N., Landau S., Or D., Kababya D., Bruckental I. and Nitsan Z. (2006). Analytical approach and effect of condensed tannins in carob pods (Ceratonia siliqua) on feed intake, digestive and metabolic responses of kids. Livest. Sci. 99, 29-38.

Singh B., Sahoo A., Sharma R. and Bhat T.K. (2005). Effect of polethylene glycol on gas production parameters and nitrogen disappearance of some tree forages. Anim. Feed Sci. Technol. 123(1), 351-364.

Skene I.K. and Brooker J.D. (1995). Characterisation of tannin acylhydrolase activity in the ruminal bacterium Selenomonas ruminantium. Anaerobe. 1, 321-327.

Small M. (1983). Honeylocust pods and the digestion of protein by sheep. Agrofor. Rev. 4, 6-7.

Steel R.G. and Torrie J.H. (1997). Principles and Procedures of Statistics. A Biometrical Approach, McGraw-Hill Co., New York.

Terrill T.H., Rowan A.M., Douglas G.B. and Barry T.N. (1992). Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. J. Sci. Food Agric. 58, 321-329.

Theodorou M.K., Willams B.A., Dhanoa M.S., McAllan A.B. and France J. (1994). A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim. Feed Sci. Technol. 48, 185-197.

Tous J. and Batlle I. (1990). El Algarrobo. Mundi-Prensa, Madrid, Spain.

Van Soest P.J. (1994). Nutritional Ecology of the Ruminant. Cornell University Press, Ithaca, New York.

Van Soest P.J., Robertson J.B. and 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.

Van Soest P.J., Wine R.H. and Moore L.A. (1966). Estimation of the true digestibility of forages by the in vitro digestion of cell walls. Pp. 438-441 in Proc. 10^th Int. Grassland Congr. Helsinki, Finland.

Vourdoubas J., Makris D., Kefalas P. and Kaliakatsos J. (2002). Studies on the productionof bioethanol from carob. Pp. 489-493 in Proc. 12^th European Conf. Technol. Exhibit. Biomass Energy, Indust. Clim. Protec. Amsterdam, Netherlands.

Waghorn G. (2008). Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production-progress and challenges. Anim. Feed Sci. Technol. 147, 116-139.

Williams B.A. (2000). Cumulative gas production techniques for forage evaluation. Pp 189-213 in Forage Evaluation in Ruminant Nutrition. D.I. Givens, E. Owen, R.F.E. Axford and H.M. Omed, Eds. CABI Publishing, Wallingford, United Kigdom.

Wilson J.R. and Kennedy P.M. (1996). Plant and animal constraints to voluntary feed intake associated with fibre characteristics and particle breakdown and passage in ruminants. Aust. J. Agric. Res. 47, 199-225.

Wolin M.J. (1960). A theoretical rumen fermentation balance. J. Dairy Sci. 43, 1452-1459.

Yisehak K., De Boever J.L. and Janssens G.P. (2014). The effect of supplementing leaves of four tannin-rich plant species with polyethylene glycol on digestibility and zootechnical performance of zebu bulls (Bosindicus). J. Anim. Physiol. Anim. Nutr. 98, 417-423.