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Abanico veterinario

On-line version ISSN 2448-6132Print version ISSN 2007-428X

Abanico vet vol.11  Tepic Jan./Dec. 2021  Epub Oct 11, 2021 

Original Article

Fermentative quality and methane production in corn stubble silage with fermented and unfermented nopal cactus

Elia Araiza-Rosales1

Adolfo González-Arreola2

Gerardo Pámanes-Carrasco1

Manuel Murillo-Ortiz2

Rafael Jiménez-Ocampo3

Esperanza Herrera-Torres*  4

1CONACYT-Universidad Juárez del Estado de Durango, Durango, México. C.P. 34000.

2Facultad de Medicina Veterinaria y Zootecnia, Universidad Juárez del Estado de Durango. Durango, México.

3Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Durango. Km 4.5 Carretera Durango- Mezquital. Durango, México.

4Instituto Tecnológico del Valle del Guadiana-Tecnológico Nacional de México. Durango, México.


The objetive of this research was to evaluate the nutritive and fermentative quality and methane emissions in corn stubble silages with nopal (Opuntia ficus-indica), for which three experimental treatments were evaluated, T1: corn fodder; T2: 75 % corn stubble + 25 % nopal; and T3: 75 % corn stubble + 25 % fermented nopal. Twenty-one microsilos (7 per treatment) were prepared in plastic containers and left to ferment for 30 days. At the end of fermentation, the chemical composition, fermentation parameters, gas production and methane (CH4) were evaluated. Dry matter (DM), crude protein (CP), neutral detergent fiber (NDF) and acid detergent fiber (ADF) contents were different among treatments (p<0.05); CP content increased 44 % with the addition of fermented cactus (T3). Ammonia nitrogen, lactic acid and volatile fatty acids values were different among treatments (p<0.05). Maximum gas production (Gmax) and CH4 concentration decreased 32 % and 49 % at T3, respectively. The addition of cactus and fermented cactus to corn stubble silage increases protein content. In addition, it reduces ruminal methane synthesis in vitro.

Keywords: fermentation; corn stubble; greenhouse gases; silage


El objetivo de esta investigación fue evaluar la calidad nutritiva, fermentativa y la emisión de metano en ensilajes de rastrojo de maíz con nopal (Opuntia ficus-indica), para lo cual se evaluaron tres tratamientos experimentales, T1: forraje de maíz; T2: 75 % rastrojo de maíz + 25 % nopal y T3: 75 % rastrojo de maíz + 25 % nopal fermentado. Se elaboraron 21 micro-silos (7 por tratamiento) en recipientes de plástico y se dejaron fermentar por 30 días. Al término de la fermentación se evaluó la composición química, los parámetros de fermentación, producción de gas y metano (CH4). Los contenidos de materia seca (MS), proteína cruda (PC), fibra detergente neutro (FDN) y fibra detergente ácida (FDA) fueron diferentes entre los tratamientos (p<0.05); el contenido de PC incrementó 44 % al adicionar nopal fermentado (T3). Los valores de nitrógeno amoniacal, ácido láctico y ácidos grasos volátiles fueron diferentes entre tratamientos (p<0.05). La máxima producción de gas (Gmax) y la concentración de CH4 disminuyeron 32 % y 49 % en T3, respectivamente. La adición de nopal y nopal fermentado a ensilados con rastrojo de maíz incrementa el contenido de proteína. Además, reduce la síntesis de metano ruminal in vitro.

Palabras clave: fermentación; rastrojo de maíz; gases efecto invernadero; ensilaje


In northern Mexico, extreme temperatures and prolonged drought have caused a decrease in forage production. Thus, small producers have found it necessary to use forage resources that represent a low nutrient supply for ruminants to counteract the dry season (López-Inzunza et al., 2017). Thus, corn (Zea mays) stubble has been used as a forage source in arid and semiarid areas in the north of the country as a shearing in the production of grains for human consumption (SAGARPA, 2009). Under these production conditions, nopal cactus emerges as an alternative in livestock feed (Flores-Hernández et al., 2017). Nopal cactus (Opuntia spp.) is an important plant resource in northern Mexico; it is considered a natural water store and it is very efficient in water consumption (Orona- Castillo et al., 2008). Additionally, nopal provides digestible energy, water and vitamins to the animal during the dry season (Dubeux et al., 2018).

In addition, compared to other annual forages, nopal uses less water for its production and growth (Flores-Hernández et al. 2019). However, its low protein content (4 % DM) limits its use as a sole forage source. Due to the above, it is recommended to apply different biotechnological processes that help increase its protein content; for example, solid-state fermentation (SSF) (Herrera et al., 2017). The SSF process increases the protein content of the substrate by increasing the unicellular protein in the cell wall of the microorganisms. The most commonly used microorganisms are Saccharomyces cerevisiae yeasts and some Kluyveromyces species ((Van Markis et al., 2006). On the other hand, the ensiling process can serve to decrease the problems of cattle feeding and face the shortage of forage in the dry season (Castro et al., 2016). This process inhibits the growth of pathogenic microorganisms by decreasing the pH, due to the presence of lactic acid bacteria (LAB), which allows preserving the freshness and nutritional characteristics of forages for later use (Mokoboki et al., 2016). Due to the above, the objective of this work was to evaluate the nutritional quality and in vitro gas production of corn stubble silages with the addition of cactus and fermented cactus.


Study area

The study was carried out at the Faculty of Veterinary Medicine and Animal Husbandry of the University of Juárez, Durango State. Forage nopal variety AV6 was randomly harvested from a cultivated nopal plantation, located next to the Faculty and within Durango municipality, Mexico.

Solid state fermentation (SSF) and preparation of microsilos

The nopal cactus stalks were cut into pieces of approximately 1 cm2 using a stainless steel knife and placed in 19 l plastic containers, where they were inoculated with Sacharomyces cerevisiae (1% m/m). The fermentation process was carried out for 48 h at 25 ºC. Treatments consisted of including cactus and fermented cactus to corn fodder, as shown in Table 1. Experimental microsilos were prepared with chopped corn forage without grain, and in mature state with a particle size of 2 to 4 cm (Variety: Hybrid 21/20) (T1, n=7), corn stover with fresh nopal (T2, n=7). Besides prepared with corn stubble with fermented nopal (T3, n=7) in plastic containers (30 cm diameter × 50 cm high), hermetically sealed for 30 d. After this time, the microsilos were opened for later analysis.

Table 1 Ingredients proportions in experimental treatments 

(%) T1 T2 T3
Corn stubble 100 75 75
Unfermented nopal -- 25 --
Fermented nopal -- -- 25

Fermentative variables

Once the microsilos were opened, the following variables were evaluated: pH (Hanna instruments, model HI 83142); lactic acid according to Borshchevskaya et al. (2016); as well as volatile fatty acid and ammonia nitrogen (NH3-N) contents, using the procedures proposed by Galyean (2010).

Chemical analysis

Samples from each experimental microsilos were dried in a forced air oven at 55 °C for 72 h; subsequently, the particle size was reduced to 1 mm in a Wileymil mill (Arthur H Thomas, Philadelphia, PA, USA), to determine the dry matter (DM) contents (method 934.01). Crude protein (CP) concentrations were determined by the micro-Kjeldhal technique (method 920.87), using the conversion factor (6.25) (AOAC, 2010). The concentration of NDF, ADF were obtained according to the procedures proposed by Van Soest (1991) and the gas production parameters according to the technique described by Menke and Steingass (1988).

Gas in vitro production

Approximately 1 g of sample from each experimental microsilo was placed in glass modules in a pressure transducer equipment, ANKOM brand. In addition, it was incubated in triplicate with a 2:1 solution of ruminal buffer-liquid solution, according to the procedure described by Murillo-Ortiz et al. (2018). Incubations were carried out from 0 to 96 h and recording pressure values at the same time. The gas production kinetics was estimated using the Gompertz function (Murillo-Ortiz et al., 2018), according to the following equation:

GP = Gmax ∗ exp[−A ∗ exp(−kt)]

Where GP= gas production at time t (ml), Gmax= maximum gas production (ml), k= constant gas production rate (h-1) and A= lag phase (h). From the 24 h incubation, the valve was opened to release gas for 2 s from each module. The gas released from each module was connected to a portable CH4 and CO2 analyzer through a tube to measure the concentration of these gases according to the procedures established by the manufacturer (GEMTM5000, LANDTEC, USA).

In vitro fermentation parameters

To evaluate fermentation parameters, 1 g of sample was placed in nylon bags (ANKOM, F500 nylon bags; ANKOM, 2018), pre-weighed and placed inside ANKOM modules and incubated in triplicate with buffer solution: ruminal fluid, in a 2:1 ratio according to Murillo- Ortiz et al. (2018)). After 24 h of continuous fermentation, the modules were opened and immediately pH was measured (Hanna instruments, model HI 83142). The bags were removed from the modules and were washed with distilled water and dried at 65°C for 48 h. In vitro digestibility of dry matter (IVDDM) was calculated based on the difference in dry matter content of the substrate before and after incubation. Additionally and approximately 1.0 ml of the filtrate was centrifuged at 3,000×g for 5 min; then, 500 μl of the supernatant liquid was acidified with 150 μl of 25 % metaphosphoric acid to evaluate volatile fatty acids. Also approximately 1.0 ml of the filtrate was placed in tubes and was acidified with 30 μl of 50 % v/v sulfuric acid to determine N-NH3 (Galyean, 2010).

Statistical analysis

The data obtained were analyzed with a completely randomized design, using the GLM procedures of SAS (2010). Means were compared with Tukey's multiple range test and declared significant differences when P≤0.05.


Chemical composition.

Dry matter (DM) content decreased with the inclusion of corn stubble (P<0.05, Table 2). Silages containing stubble and nopal (t2 and t3) presented adequate DM contents, since according to Pineda-Cordero (2016) silages containing between 30 and 35 % DM are considered of good quality. In addition, the moisture present in silages determines the type of fermentation that took place during the ensiling process. Other factors that determine fermentation quality are the soluble carbohydrates present and the buffering capacity of the forage used (Bernal et al., 2002).

Table 2 Chemical composition of corn stubble silages added with nopal cactus 

(%) T1 T2 T3 SEM
Dry Matter 42.0±0.29 a 35.9±0.48b 35.5±0.26b 0.25
Crude protein 6.2±0.55c 8.9±0.10b 11.1±0.05a 0.05
Neutral detergent fiber 53.2±2.31b 63.1±0.08a 58.8±0.12ab 1.09
Acid detergent fiber 23.6±0.06c 37.6±0.05a 35.3±0.73b 0.34
Digestibility of dry matter 61.8±2.44 58.4±1.98 64.1±2.20 1.81

a,bDifferent letters in the same row indicate differences (P<0.05). SEM=standard error of the mean, n=3.

Crude protein (CP) concentration was different among treatments (P<0.05, Table 2). The addition of cactus and fermented cactus increased 43.54 % and 79 % the CP concentration in silages, respectively, compared to t1. The increases at t2 and t3 are due to the initial protein content in the corn stubble before ensiling (mature green forage contained 4.9 %, while the stubble contained 5.2 % CP; results not shown) and to the proliferation of cellular protein from the Saccharomyces cereviseae yeast used to ferment the nopal. However, Alhanafi et al. (2019)) recorded a lower CP content in silages of Opuntia ficus, indica added with Atriplex (6.41 %); compared to t2 of this study.

The concentration of neutral detergent fiber (NDF) was lower in T1 (P<0.05, Table 2); an increase of 18% was observed in T2. This increase is due to the presence of corn stubble, which has a high amount of fiber; however, part of the hemicellulose is hydrolyzed during the ensiling process. At this stage, pentoses are released and they are fermented into lactic acid and acetic acid (McDonald et al., 2002).

Likewise, acid detergent fiber (ADF) content showed the same behavior; ADF increased 59 and 49 % at T2 and T3, respectively (P<0.05, Table 2). In the same way, the increases in ADF were attributed to the presence of corn stubble at T2 and T3. Nevertheless, NDF and ADF contents were within the range of good quality forages.

Fermentation parameters of silage process

The pH values were higher in t2 and t3, with respect to t1 (P<0.05, Table 3); however, all were within the ideal values, which is indicative of a good fermentation and conservation process. It is worth mentioning that the speed with which a silage achieves a pH <4.0 guarantees silage stability and reduces nutrient loss by secondary fermentations, or by bacterial and fungal contamination (Ha Vu et al., 2019).

Table 3 Fermentation parameters of corn stubble silage with cactus addition 

(%) T1 T2 T3 SEM
Dry Matter 42.0±0.29a 35.9±0.48b 35.5±0.26b 0.25
Crude protein 6.2±0.55c 8.9±0.10b 11.1±0.05a 0.05
Neutral detergent fiber 53.2±2.31b 63.1±0.08a 58.8±0.12ab 1.09
Acid detergent fiber 23.6±0.06c 37.6±0.05a 35.3±0.73b 0.34
Digestibility of dry matter 61.8±2.44 58.4±1.98 64.1±2.20 1.81

a,bDifferent letters in the same row indicate differences (P<0.05). SEM=standard error of the mean. N-NH3 =ammonia nitrogen, n=3.

The concentration of ammonia nitrogen in the silages increased with the cactus and fermented cactus inclusion (P<0.05, Table 3). This increase recorded in t2 and t3 silages could have been caused by an increase in protein degrading microorganisms (Berumen et al., 2015; Ruangyote and Metha, 2018), or also the use of corn stover reduces the amount of soluble carbohydrates and therefore increases protein degradation (Herremans et al., 2019). However, to classify a silage as good quality, the maximum ammonia nitrogen concentration should be 7-20 % of total nitrogen (Sánchez and García, 2017); therefore, the experimental silages obtained values that are within this range and therefore indicate that an adequate fermentation process was carried out.

The concentration of acetic acid was different between treatments (P<0.05, Table 3). Volatile fatty acids are the product of fermentations induced by the presence of coliform bacteria that transform lactic acid into acetic and butyric acid, and are present in manure and soil. According to Kung et al. (2018), acetic acid concentrations are between 0.5 and 2.0%, when DM content is 45 to 55 %; therefore, the values obtained in this work are within the range for good quality silages (0.5-1.1 %). Propionic acid values were different among treatments (P<0.05, Table 4). The results obtained in this study are equal to those reported by González et al., (2019) in corn silage with cactus and fermented cactus (4.0%). Butyric acid concentrations were higher in silages containing stubble (P<0.05, Table 3); however, these values indicate that there was adequate fermentation. In addition, Da Silva et al. (2020) report lower propionic acid values in cactus silages with gliricidia. According to the lactic and butyric acid values obtained in the silages of this study, it can be inferred that the inclusion of cactus and fermented cactus in the stubble promotes an increase in lactic acid and a decrease in butyric acid, which results in silages with good fermentative and nutritional quality.

Ruminal fermentation parameters

N-NH3 concentration was lower in t1, compared to t2 and t3 (P<0.05, Table 4). The inclusion of cactus and fermented cactus in the stubble silages promoted an increase of 48 % and 27.7 % in N-NH3, respectively. Changes in this variable indicate that proteolysis is taking place and it increased due to crude protein increase in the silage by the addition of stubble and fermented nopal. However, there are studies that affirm that increases in N-NH3 concentration are because the protein is not incorporated into microbial protein synthesis, which would reflect an energy loss in the ruminant (Rodríguez et al., 2007). On the contrary, other authors also found increases for N-NH3 when crude protein content was increased through the addition of urea in pineapple silages (López-Herrera et al., 2014). Additionally, these results agree with those obtained by Pinho et al. (2017) in nopal silages (17 mg/dL) at 9 h of incubation. Thus, in this study, the N-NH3 concentrations recorded in all treatments presented adequate levels higher than 5 mg/dL, which allows guaranteeing microbial protein synthesis (Rodríguez et al., 2007).

Table 4 In vitro ruminal fermentation parameters of corn stubble silage added with nopal cactus 

T1 T2 T3 SEM
pH 6.8±0.008 6.9±0.17 6.9±0.03 0.01
N-NH3 (mg/dL) 11.9±1.08b 17.7±0.43a 15.2±0.08a 0.55
Acetic Acid (%) 53.3±0.89a 52.1±0.48a 46.5±0.43b 0.52
Propionic Acid (%) 27.1±0.72b 30.6±0.31a 32.1±0.45a 0.43
Butyric Acid (%) 14.7±0.05a 12.6±0.13b 14.7±0.05a 0.07

a,b Different letters in the same row indicate differences (P<0.05). SEM=standard error of the mean. N-NH3 ammoniacal nitrogen; n=3.

On the other hand, acetic acid concentration decreased and propionate concentration increased in corn stubble and fermented cactus silage (P<0.05; Table 4), compared to t1 and t2. In this sense, a decrease in acetic acid concentration at t2 and t3 is closely related to a decrease in the fermentation of structural carbohydrates (NDF and ADF). Thus, since structural carbohydrates have the highest concentration in the nutrients of t2 and t3, it is suggested that adequate fermentation is not taking place (Van Soest, 1994). However, Sánchez et al. (2014) also detected a decrease in acetate concentration and an increase in ruminal propionate. Regularly, the production rate of propionate and other AGV is directly related to the consumption of fermentable substrates from the diet, which favors propionate synthesis from microbial fermentation by amylolytic bacteria (Van Soest, 1994).

Maximum gas production (Gmax) was higher at t1 (P<0.05; Table 5). The inclusion of cactus and fermented cactus in silages with corn stubble decreased maximum gas production 31.9 % and 48.7 %, respectively. The values obtained in this study are lower than those reported in leucaena and star grass (234 and 154 ml/g, respectively) by Naranjo et al. (2016). Similarly, González et al. (2019) recorded higher Gmax values in corn silages with nopal (176 ml). The decrease in gas production observed in this study is attributed to the decrease in dry matter digestibility at t2 and t3, as a result of the addition of corn stubble that NDF and ADF values are higher than those recorded at t1. As previously mentioned, the presence of structural carbohydrates prevents adequate fermentation, which is reflected in gas production.

Table 5 Gas kinetic parameters of corn stubble silage with nopal added 

Parameters T1 T2 T3 SEM
Gmax (ml/g DM) 124.8±8.48a 94.6±6.50b 84.0±1.75b 5.10
A (h) 4.2±0.21a 2.7±0.03b 4.4±0.04a 0.10
K(%/h) 0.08±0.001 0.07±0.007 0.09±0.003 0.003
Methane (ml/g DM) 9.7±0.29a 7.3±0.29b 6.5±0.16b 0.21
CO2 (ml/g DM) 59.0±4.49a 49.8±0.75ab 44.7±0.70b 2.17
Methane:CO2 ratio 0.16±0.010 a 0.14±0.003 b 0.14±0.005 b 0.014

a,bDifferent letters in the same row indicate significant difference (P<0.05). SEM=standard error of the mean; Gmax: maximum gas production; k represents the specific gas production rate; A is the latency period before gas production starts (lag phase).

On the other hand, the dormancy period "A" decreased 55 % at t2 (stubble + nopal silage). To explain this result, variables that were not considered in this study, such as soluble carbohydrate content or lignin, must be taken into account, since the faster onset of fermentation depends on these. In this sense, López-Inzunza et al. (2017) reported longer dormancy times for silages with higher ADF content, with respect to NDF content in silages with pineapple stubble; these authors showed structural carbohydrate concentrations and dormancy times similar to those reported in this study (72 % NDF and an A of 3.8 h). Moreover, the A values obtained in this study are also similar to those recorded by González et al. (2019) in corn forage silages with nopal cactus. Additionally, methane production decreased 32 and 49 % in silages that included nopal and fermented nopal, respectively (P<0.05; Table 5). Similarly, the methane: CO2 ratio also decreased with the addition of fermented nopal and nopal without fermented, as well as corn stubble. This variable is closely related to ruminal methane synthesis. Higher values in this ratio suggest an increase in ruminal methane synthesis through the CO2 reduction pathway (Murillo et al., 2018). Thus, although a reduction in methane and CO2 production is closely related to a decrease in the fermentative quality of t2 and t3 silages, this reduction also suggests changes or even an inhibition in methanogenic populations (Tavendale et al., 2005. In addition, the decrease in methane is directly related to an increase in ruminal.


The addition of nopal and fermented nopal to corn stubble silages increases crude protein content by 43 and 79 %, respectively. In addition, the use of nopal and fermented nopal in corn stubble silages reduces ruminal methane synthesis in vitro. On the contrary, the presence of corn stubble increases the structural carbohydrate content of the silage, which compromises ruminal fermentation and gas production in vitro; however, in vivo studies are recommended to confirm these results.


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Code: e2021-01.

Received: January 21, 2021; Accepted: April 28, 2021

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