Kinetics of gas production of fodder of Moringa oleifera Lam grown in tropical dry forest areas from Colombia

  • I. I. GarcíaEmail author
  • J. Mora-Delgado
  • J. Estrada
  • R. Piñeros
Open Access


Moringa oleifera is considered as an alternative to improve the availability and quality of forage for feeding ruminants in tropical areas. Nutritional quality and gas production were evaluated analyzing the fodder of cultivars of M. oleifera from different Colombian provenances. Samples of leaves and thin stems were taken during the dry season from three cultivars (Flandes, Armero and Palmira). Bromatological analysis was determined in the laboratory of Animal Nutrition at the National University of Colombia—Palmira; gas production kinetics was determined using the syringes test during 72 h. Values obtained were used to run a Gompertz model building kinetic curves of gas production. To compare the mean test Tukey HSD (P < 0.05) was applied. Results suggest acceptable fiber contents: FDN (35.67, 41.99, 27.45%); FDA (22.28, 24.98, 15.04%); LDA (4.04, 4.95, 2.50%), respectively. The time to inflection point (HIP, hours) was 134 for Flandes, 24.01 for Amero and 19.34 for Palmira; Flandes’ HIP indicates that the test should be longer than 72 h to confirm this value. The volume of gas at inflection point (GIP, ml) was very similar for the three accessions (61.27; 78.80 and 69.98 for Flandes, Amero and Palmira respectively). The highest maximum gas production rate (MRGP, ml/h) found was 10.1 for Armero cultivar. Lower Lag phase (LPh or microbial establishment, h) was 12.12 h in Palmira. Our conclusion is that the bromatological quality of M. oleifera and gas production differs in fodder of different origins, probably caused by differences in management and soil conditions.


Feeding Bromatology Dry matter Ruminants Digestibility 


Moringa oleífera (Lam) is considered a species of great ecological plasticity, since it is located in different soil, rainfall, precipitation, temperature and altitude conditions (Arias 2014). It is a fast-growing tree (3 to 5 m the first year); it is resistant to drought (minimum 250 mm of annual precipitation); it thrives in a temperature range of 25–40 °C, and even tolerates up to 48 °C, and − 1 °C it is very versatile except for waterlogged conditions (Nouman et al. 2014). Among its uses, the forage stands out by virtue of its nutritional characteristics (23 and 9% crude protein, and 79 and 57% digestibility for leaves and stems, respectively) and the high yield of fresh biomass (526 t ha−1 per year, with 900 plants); the leaves and flowers are rich in proteins, minerals and vitamins, and are also a source of human food; pods, seeds and roots are also edible (Espinosa-Martínez 2010). Pérez (2010) stated that Moringa oleifera (Lam) is an alternative for the production of forage of high protein content for animal feeding, due to its adaptability and low production cost.

M. oleifera can be used as a protein supplement to a basal diet with low quality forage (P. maximum); it results in a highly significant increase in dry mater (DM) consumption (Reyes et al. 2009). It has been reported that fresh and dry moringa leaves exhibit crude protein (CP) contents between 6.7 and 27.1%, respectively. Likewise, Mendieta-Araica et al. (2011) reported 29.2% in moringa leaves, while Araujo-Febres (2005) and Ferreira et al. (2008) reported 33.25%. Also, lower neutral detergent fiber (NDF) and acid detergent fiber (ADF) contents were recorded in moringa fodder leaves, which show better fodder quality (Nouman et al. 2014). However, the differences between the values reported by different authors should be considered; they may be due to the parts of the plant collected, its phenological status, the period of the year in which they were collected, the frequency of cut and the environment in which the collected material grew (Edwards et al. 2012).

A parameter that allows to evaluate the impact of the consumption of M. oleifera in ruminal kinetics is the evaluation of DM degradation and the ruminal gas production. Thus, gas production techniques allow researchers to determine the extent and kinetics of food degradation through the volume of gas produced during the fermentation process (Theodorou et al. 1994). These techniques have been of great interest and their use has increased thanks to the ease and usefulness of data on the kinetics of digestion of both soluble and insoluble fractions in diets based on forages (Getachew et al. 1998). The measurement of cumulative gas production has been proposed as an indicator of carbon metabolism, focusing on the accumulation of the final products of fermentation: CO2, CH4 and volatile fatty acids (VFA).

This system has the advantage that the final product that is measured (gas) is a direct result of the microbial metabolism, instead of registering the disappearance of the substrate. In addition, the formation of fermented final products can be monitored at short intervals of time and, therefore, the fermentation kinetics can be accurately described (Bruni 2001). The measurement of gas production using the fermentation test in syringes implemented in the studies of Ruiz et al. (2005) and Boudry et al. (2003) following the procedures described by Menke et al. (1979), is a suitable method for studying this type of process. Furthermore, this method is ideal for comparative studies as it generates data from digestion kinetics by measuring the fermentation of the food instead of its disappearance (Alvarez 2009).

The use of the in vitro gas production technique, as a tool for the evaluation of food for ruminants, assumes that the gas produced during fermentation is proportional to the digested dry matter and the digestion of the food implies the fermentation of different fractions along the time, and consequently the relation Gas Produced/Disappeared Substrate, could change throughout the fermentation for the same food (Jaurena et al. 2006).

Some studies suggest that gas production profiles reflect a sequence of fermentation processes, which throughout the incubation time begin at a high fermentation rate, followed by a declination phase. Thus, a two-step approach and a multiphasic model have the best goodness fit with these processes (Wang et al. 2011). While sigmoidal shapes indicate that rate of gas production increased firstly, reached maximum rate and then decreased, which might suggest a close relationship with increased microbial activities during the early stages of incubation (Wang et al. 2011; Groot et al. 1996).

In this study, the bromatological quality and the gas production in the digestibility of fodder samples from three different cultivars of Moringa oleifera Lam were determined, using the syringes methodology.

Materials and methods

Fodder origin and sample preparation

Samples of Moringa forage were harvested at pre-flowering stage (leaves and thin stems; 0.5 average ratio) from three cultivars, located in the municipalities of Armero (Ar), Flandes (Fl) and Palmira (Pl), during dry season. These were identified as cultivars Armero, Flandes and Palmira, respectively (Table 1). Fodder was harvested at vegetative state (40 cm above ground level). After that, the samples were chopped into pieces of three cm using an electrical grass chopper.
Table 1

Characteristics of localities of provenance at fodder of M. oleifera


Soil type and fertility

Physics and meteorological characteristics

Flandes (Fl)

Soil inceptisols; clayey (> 387%); saturation of bases with high contents of Ca, Mg and K (> 6.0; > 1.2; 0.3 me/100 g); medium DM values (1.5–3.0), high contents of P (> 45 ppm); pH close to neutrality and slightly acidic (5,6–7,0)

304 meters above sea level; flat topography; precipitation 1300 mm per year; average temperature 28 °C

Coordinates: 4°15′01.80″N; 74°50′72.23″W

Armero (Ar)

Soil Typic Ustropepts; clayey (> 387%); saturated soils with high contents of Ca, Mg and K (> 6.0; > 2.4; 0.3) high contents of P (> 45 ppm): medium DM values (1.5–3.0); slightly acidic pH (5,6–6,5)

275 meters above sea level; flat topography; precipitation 1738 mm per year; average temperature 26 °C

Coordinates: 5°00′25.63″N; 74°54′15″W

Palmira (Pl)

Soil Epiquert ustico; high in clay (> 75%); high saturation of bases (85%) with high contents of Ca, Mg and K (24.1, 5.8, 0.54); high P contents (84 ppm): medium DM values (2.3%), pH close to neutrality and slightly basic (7.4)

1000 meters above sea level; flat topography; precipitation 1532 mm per year; average temperature 24 °C

Coordinates: 02°06′N and 65°03′W

Sources: Castro (1996), Holguín et al. (2015) and Acosta et al. (1997)

Analytical assessments

Samples were dried using a forced air oven at 60 °C until constant weight (for 48 h). Analyses were carried out in the Nutrition Laboratory of the Universidad Nacional de Colombia-Palmira and Nutrition Laboratory of Universidad de Caldas. The samples of each cultivar were processed in triplicate, following the procedures proposed by the Association of Official Agricultural Chemists (AOAC 1990): crude protein (CP) by the Micro-Kjeldahl method; NDF and ADF and lignin, following the sequence described by Van Soest and McQueen (1973) and van Soest et al. (1991); ether extract (EE) by soxhlet extraction; the gross energy (GE) was determined in adiabatic calorimetric pump. The ash content was determined by direct incineration of the dried material in a muffle furnace at 500 °C as per the AOAC (2005). Digestibility of DM was estimated by formula of Mertens (1987).

Kinetics of gas production

This was carried out following the methodology described by Boudry et al. (2003). A total of 15 syringes of 100 ml capacity and emboli were marked and greased with Vaseline one day before the fermentation test. After that, 200 mg of dried samples from each M. oleifera cultivar was harvested and placed inside each syringe; then they were taken to the stove at 39 °C until the day of the test. Thus, four solutions were prepared: A (Micro Minerals), B (Micro Buffer), C (Macro Minerals) and D (Oxidizer Reduction Indicator). On the day of the test, 450 ml of ruminal fluid was collected from two Brahman breed cattle fistulas, fed with commercial concentrate, mineralized salt and star grass (Cynodon plectostachyus). This was done at CIAT International Center for Tropical Agriculture 10 min from the laboratory, whereupon the liquid was transported in a thermos flask at 39 °C. In the laboratory, the inoculum was filtered and kept in a water bath at 39 °C under CO2 gassing.

Afterwards, a fifth solution E was prepared, corresponding to the buffer solution (common bicarbonate and phosphate solution, reducing agent, nitrogen source, minerals, and resazurin as an indicator of redox potential).

Next, the inoculum (ruminal fluid) was mixed with the buffer solution (E) in a glass vessel with constant CO2 gassing. Each syringe was filled with 30 ml of the buffer solution mixed with the inoculum; air trapped within each was extracted, pressing the plunger until it reached the top of the content: thus, they were closed with the security clip to avoid solution losses; at this time, the first volume reading (V0) was made and the water bath was taken at 39 °C with slight agitation.

The volume reading (mm Hg) of the syringes was carried out at 2, 5, 8, 12, 16, 20, 24, 48 and 72 h after inoculation. It should be noted that the fermentation of forages in syringes should be carried out for 144 h because only at this time the gas production curve stabilizes; lower fiber content such as Moringa fermentation can be carried out until 72 h (Ruiz et al. 2005).

When the level of the plunger exceeded 60 ml, all the gas contained in the syringe was removed and the plunger was placed in the initial position. Three replicates were made for each cultivar; in addition, there were three syringes containing medium and inoculum without substrate (blanks) and three syringes containing a known raw material (reference), which is useful to determine if there are errors in the test procedures.

The average gas recorded in the blanks, which normally corresponds to 13–27% of the final reading, is subtracted from the total gas produced by the evaluated substrates, thus obtaining the total gas actually derived from the substrate fermentation (Pell and Schofield 1993; Schofield 2000).

Regression model

A logistic regression was used to model gas accumulation, where parameters α, β, and δ, were estimated by non-linear regression analysis (see Eq. 1) using the SAS version 9.4. licensed to Universidad de Caldas
$$ Y = \frac{\alpha }{{1 + \beta *exp\left( { - \delta *X} \right)}} $$
where Y is the accumulated gas production at a time x, rapidly degradable fraction, α is the maximum gas production, β gas production rate or difference between the initial gas and the final gas at a time x, δ Lag time.

The parameters alpha (α), beta (β), and delta (δ) were converted into parameters with biological significance. For the purposes of this study, the parameters are: time to point of inflection (HPI, hours), gas inflection point (GPI ml), maximum gas production rate (TMPG, ml/h), and lag phase (FL or microbial accommodation h). To estimate the biological parameters, the following equations were used: HPI = b/c (Eq. 2); GPI = a/e (Eq. 3); TMPG = (a*c)/e (Eq. 4); and FL = ((b/c) − (1/c)) (Eq. 5); where e is Euler’s number, which equals approximately 2.718281828459.

Statistical analysis

Descriptive statistics were applied to the proximal analysis of the accessions. Later, to analyze the gas production from each cultivar samples, an analysis of variance was performed and to compare the means, the Tukey DSH test was applied (P < 0.05).

Results and discussion

Proximal analysis

The three types of fodder show significant differences in dry matter content, with a higher value in Palmira samples. Similar, the PC content showed significant differences, obtaining in Palmira the highest value, followed by Flandes and Armero. There were no differences for the EE content. The gross energy at Palmira and Flandes have statistical differences with respect to Armero, being higher in the Armero cultivar (Table 2).
Table 2

Bromatological analysis of Moringa oleifera fodder from different cultivars


Dry matter (%)

Crude protein (%)

Ether extract (%)

Gross energy (Kcal)


23.19 ± 0.836a

17.97 ± 0.16 b

8.06 ± 0.43 a

3831.8 ± 5 a


25.92 ± 0.085c

12.89 ± 0.32 a

10.47 ± 0.77a

5059.8 ± 4b


24.78 ± 0.085b

18.70 ± 0.61 b

8.29 ± 1.50 a

4986.1 ± 8 a

Averages with a common letter between rows are not significantly different (P > 0.05)

The percentage of cell wall was greater for the Armero cultivar followed by Flandes and Palmira, and the same trend was found for FDA and LDA, with statistical differences between them. For hemicellulose, no significant differences were found; in cellulose the Armero cultivar was statistically higher compared to the other two cultivars. The estimated data show that Palmira cultivar had a significant higher digestibility with respect to other fodder (P < 0.0001) (Table 3). Following an inverse trend to fiber values, the estimated digestibility of dry matter was higher for Palmira, followed by Flandes and Armero.
Table 3

Fiber content and digestibility of three Moringa oleifera fodder cultivars


NDF (%)

ADF (%)

ADL (%)

Hemicellulose (%)

Cellulose (%)

DDMe (%)


35.70 ± 0.06b

22.30 ± 0.05b

4.04 ± 0.19b

13.39 ± 0.96 ab

17.85 ± 0.71b

71.5 ± 1.4b


41.96 ± 2.94c

24.98 ± 0.30c

4.95 ± 0.03c

17.01 ± 3.24b

20.03 ± 0.27 c

69,4 ± 0.0c


27.63 ± 0.11a

15.04 ± 1.80a

2.50 ± 0.38a

12.41 ± 1.92 a

12.55 ± 1.43a

77.2 ± 0.2a

Averages with a common letter between rows are not significantly different (P > 0.05)

NDF neutral detergent fiber, ADF acid detergent fiber, ADL acid detergent lignin, DDMe Digestibility of Dry Matter (estimate)

Gas production kinetics

Figure 1 shows the gas production accumulated by OM fermentation during the 72-hour incubation period. Cumulative gas production was characterized by an increase with the time of exposure of the samples to the attack of microorganisms, with average values of 56.9; 146.1 and 137.0 ml/gr of DM, for Flandes, Armero and Palmira, respectively. The Tukey test showed statistical differences (P < 0.0001).
Fig. 1

Predicted cumulative gas production of fodder from three different cultivars of M. oleifera per gram of incubated organic matter

This may be related to the energy of the fodders evaluated; in fact, in Table 2 we can see that the Armero and Palmira cultivars are the ones with the highest energetic values presented.

On the other hand, it is known that in the advanced hours of fermentation, when soluble sugars are depleted, cellulolytic bacteria and lignolytic fungi begin to act on the cell wall, inducing greater methanogenesis, thus, substrates with higher NDF and ADF (Armero) will induce greater gas production. In contrast, the Flandes forage has a low level of gross energy and an intermediate level of NDF, which is likely to affect low gas production.

The potential fermentation of the substrate at cultivar Amero, under the incubation conditions (asymptote of the curve) in the Logistic model corresponds to 214,21 ml/gr DM (parameter α), with a latency phase or fermentation delay of 0, 13 h (parameter δ) and a fermentation rate of 3.08 ml h−1 (Table 4).
Table 4

Parameters of the Logistic model for the production of gas observed at different fodder cultiars of Moringa oleifera









































HIP time to inflection point (h), GIP gas to the inflection point (ml), MRGP maximum rate of gas production (ml/h−1), LPh lag phase (h)

The parameters found when applying the Logistic model indicate a greater amount of soluble or rapidly degradable fraction in the accession Armero, followed by Palmira and Flandes; however, the soluble fraction has very close values among the three accessions.

The same occurred with the GIP parameter, where cultivar Ar showed higher values than the other fodder. In the same sense, higher value of the maximum gas production rate (MRGP, ml/h) found was 10,1 for Armero, but this value was very close to cultivar Palmira. Cultivar Flandes had the longest time of inflection point (HPI) for about 134 h and the same trend for microbial colonization time (LPh; 115.9) with a significant delay versus other cultivars. This value in Flandes substrate indicates that the trial should be carried out more than 72 h in order to find the LPh. The volume of gas at the inflection point (GIP, ml) was very close for the three fodder types and the Lag phase (LPh or microbial establishment, h).

The variation in bromatological results observed could be attributed to differences in the growing conditions, mainly to the soil fertility and previous management practices of the soils. Also, the quality of fodder could be influenced by environmental conditions at the time of sampling. Although samples were obtained during the dry season on the three sites, the intensity of dry conditions maybe was not similar; perhaps, those conditions could have influenced the fodder chemical composition.

In general terms, the data of CP obtained in this work are close to those provided by other studies; it has been reported that fodder quality of mixed stem and leaves of moringa as tree and fodder crop exhibit CP contents between 16.41 and 15,31%, respectively (Nouman et al. 2014). In our study, the CP data are higher for the cultivar located in a higher altitudinal belt, unlike the cultivars established in lower lands. In this regard, a study under conditions similar to the Palmira cultivar, in terms of altitudinal range and environmental temperature, allows us to see that the forage of moringa harvested at 45 days produced a percentage of CP of 18%, unlike a cultivar located in lowlands (450 masl) which presented only 16% CP (Ramirez 2016).

The EE values found are slightly higher than those reported by other authors, which normally range from 3.76 to 5.32% (Guevara and Rovira 2012; Valarezo and Ochoa 2013). It should be noted that these high values of EE, as an indicator of fat content, is what makes it possible to classify M. oleifera as an oleaginous plant (Gonzalez 2018), for which fat values are much higher than those of other forage plants.

The NDF and ADF values found in this study coincide with a large number of reports, ranging between 27 and 45% for ADF and around 40% for NDF (Foidl 2000; Mendieta-Araika et al. 2011; Rodríguez et al. 2014); however, exceptional reports have been found with much lower fiber values in leaves of cultivars under subtropical conditions of 11.40% 8.49% and 1.8% based DM of NDF, NDA and NDL, respectively (Moyo et al. 2011).

According to Linn and Martin (1999), the FDA content also correlates negatively with the food digestibility, since this fraction contains cell wall components such as lignin that inhibit the action of ruminal microorganisms for its own degradation. This partly explains the lower nutritional value of tropical forages. Of the different components of FDA, lignin is the one that is most associated with depression in DM digestibility, but other factors could be involved, as possible connections to low molecular weight molecules (Ferrerira et al. 2013).

About gas production, protein stoichiometrically contributes less to gas production than carbohydrates, so it is well known that the CP level of a substrate correlates negatively with the resulting gas production (Getachew et al. 2000); in this sense, leaves of M. oleifera (Lam) contain considerable amounts of crude protein, but they are mostly insoluble and have low in vitro digestibility (Texeira et al. 2014). However, the higher production of gas is related to a greater availability of fermentable substrate by ruminal microorganisms (Rodríguez et al. 2014); that fermentable substrate is reflected in a greater amount of gross energy of fodder. Different studies suggest that the release of gas from a food incubated in vitro with ruminal inoculum is related to the energy value of the food (Menke et al. 1979; Mtui et al. 2009; Maheri-Sis et al. 2008). In addition, it is evident that in the early hours of fermentation a portion of the substrate containing soluble sugars ferments immediately, but generally they only represent a small portion of potentially digestible materials (Stefanon et al. 1996). After that, with colonization of fiber by cellulolytic bacteria and their degradation, an increase of gas production is achieved (Dhanoa et al. 2000). Perhaps, the interaction between a high availability of soluble carbohydrates, expressed in the high values of gross energy, interacting with cellulolytic activity on the cell wall explains the higher gas production of Armero fodder.

Specifically, with regard to the gas production of M. oleifera, different studies have shown higher gas production in advanced phases of the fermentation, which makes the accumulation to show a progressive tendency and mark the inflection point of the curve in advanced hours. Rodriguez et al. (2014) evaluated Moringa oleifera (Lam) and other woody forage species with the technique of Theodorou et al. (1994), reporting that in the initial phase of fermentation (16 h) M. oleifera and Morus alba had the highest values of gas accumulation, reaching 108.6 and 111.5 ml/g respectively; its production was also high in the final phase (96 h) when compared to the other species analyzed (162.4 and 197.6, respectively). In our study, the values obtained were close to those reported in the literature, but higher values were obtained in the Armero cultivar that exceeds 200 ml/gr.

In a study with M. oleifera, Rodriguez et al. (2014) showed a high value of gas production potential (parameter A) that reached 147.46 ml/gr, below those reached in our study. In addition, the microbial efficiency expressed by parameter C (0.149) in the Gompetz model run in the Rodriguez study was close to the parameter δ of the Armero and Palmira cultivars obtained in this study.

Parameter δ is a reflection of the growth of ruminal microorganisms and the accessibility of microbial enzymes to the nutrients of a food (Getachew et al. 2000); this is so because, for the substrate to be degraded in the rumen, it must undergo an attachment process by rumen bacteria, known as colonization time or lag time, which allows enzymes to reach the substrate (Peripolli et al. 2016). In this study, the origin of fodder affected the colonization time of bacteria to the rapidly degradable fraction of feed. The lower value of these parameters in the Fl cultivar could be related to their high content of energy, which constitutes a driver for metabolism of microorganisms and access of enzymes to the substrate and, therefore, a shorter time for the start of the microbial activity. In general terms, the behavior of these parameters, in the case of moringa, could be related to their higher content of easily fermented carbohydrates (Akinfemi et al. 2009).

Olivera et al. (2013) evaluated Moringa oleifera (Lam) cultivars, from three areas of the municipality of Camagüey (Cuba) and found significant differences in gas production (P < 0.05) between provenances at 12, 24 and 96 h of incubation.

Rodriguez, et al., 2014, found that the microbial efficiency and the maximum speed of gas production, for M. oleifera was greater than for the other species, However, the inflection point of the sigmoidal curve that describes the changes in velocity of in vitro gas production over time, indicated that the Vmax was reached at shorter times for M. oleifera (9 h).


Higher production of gas is related to a higher gross energy levels, but also, higher levels of cell wall could be related with microbial activity of cellulolytic microorganism, increasing the gas production.

It is concluded that a variation in the results between fodder from different moringa cultivars can be observed, which can be attributed to the differences in the cultivation conditions, mainly to the quality and management of the soils; possibly this is affected by the agro climatic and edaphic conditions in which the crop develops.



To Universidad del Tolima by the study commission Granted; to Universidad de Caldas for the advice received from its researchers.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


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Authors and Affiliations

  1. 1.Department of Livestock Production, Livestock-Agroforestry Systems Research GroupUniversidad del TolimaIbagueColombia
  2. 2.Department of Production Systems, Biology of Livestock Production Research GroupUniversidad de CaldasManizalesColombia

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