Bromatological characterization of yacon silage in the tropical highlands of Colombia

J J Lopera-Marín^1,2, J Angulo-Arizala¹, E Murgueitio Restrepo² and L Mahecha-Ledesma¹

¹ Universidad de Antioquia, Grupo de Investigación en Ciencias Agrarias - GRICA, Ciudadela Robledo, Carrera 75 No. 65 - 87. Medellín, Colombia
joaquin.angulo@udea.edu.co
² Centro para la Investigación en Sistemas Sostenibles de Producción Agropecuaria (CIPAV), Grupo de Investigación CIPAV, Carrera 25 No 6-62 Cali, Colombia

Abstract

The aim of this research was to examine the nutritional value of yacon (Smallanthus sonchifolius) silage using different plant fractions in three mixtures. The study was conducted at the "Cien Años de Soledad" farm (geographic coordinates: 6° 26' 45.49" N and 75° 32' 43.20" W), which is in the municipality of Rionegro, eastern Antioquia (Colombia). A total of eighteen treatments were evaluated in a 3x3x2 factorial design, with three mixtures (inclusion) of the plant components: 100 % stems and leaves (M1), 50 % stem and leaves, and 50 % tubers (M2), and 75 % stems and leaves, with 25 % of tubers (M3); three evaluation times after sealing 15, 25 and 35 days; and the addition or not of lactic acid bacteria. The effect of factors and interactions was evaluated on the content of dry matter, digestibility, crude protein, soluble protein, ether extract, crude fiber, NDF, ADF, sugars, starches, and non-structural carbohydrates by analysis of variance. The silage mixtures of yacon that included proportions of tubers (M2 and M3) showed the best nutritional values in terms of digestibility, fiber, crude and soluble protein, starches, and non-structural carbohydrates (p<0.05). This would suggest that yacon could be a local forage plant with the potential for strategic supplementation of ruminants in the tropical highlands of Colombia and the Andean region.

Key words: silo additive, supplementation, sustainable livestock, tropical forage, tuber, yacon

Introduction

In Colombia and other Latin American countries, dairy farming in the highland tropics is confronted with the challenge of adapting to climate change and contributing to mitigating its effects. In addition, there is the responsibility of using natural resources sustainably throughout the entire production process. One possible strategy for creating more efficient and sustainable models for feeding cattle could be to research new resources that are rich in protein, energy, vitamins, and minerals. This could help to reduce the importation of expensive feed stuck for producers, which often has a considerable ecological footprint, such as cereals and soybeans.

The advances reached with Tithonia diversifolia (Hemsl.) A. Gray must be added to other shrubs and crops suitable to the agroecological conditions of the tropical mountains (Chará et al 2019; Angulo-Arizala et al 2022; Rodríguez-Badilla y Riaño Jiménez 2022; Castaño-Jiménez et al 2023). Silage is a food conservation method based on the anaerobic fermentation process, which has the potential to preserve fodder chemical quality for long periods (Vanegas y Codero-Ahiman 2019; Moreno Poveda et al 2020). One of its main advantages is the possibility of using undervalued and new local resources that are important for ruminant nutrition. This could be a strategy for supplementation in times of shortage of fodder or to partially replace balanced foods (Sossa Sánchez et al 2017).

A local resource with the potential to be used in silage is the yacon Smallanthus sonchifolius (Poep. & Endl) H. Robinson, a plant of the Asteraceae family, originally from high zones of the Andean region. This ancestral plant is cultivated for domestic uses in small areas from the center and south of Colombia to the north of Argentina, at altitudes between 1800 and 2800 meters above sea level (González Leguizamon 2018; Sáenz Torres et al 2016).

The yacon offers multiple benefits for nutrition and human health. Its tubercles roots (tubers), stems, and leaves have also been used ancestrally to feed small domestic animal species (Sáenz 2019). One of its principal attributes is the presence of different types of sugars, especially fructooligosaccharides (FOS) or oligofructans (represented between 40 and 70%), in which the inulin is highlighted. This polysaccharide has a sugar flavor but is not toxic or digestible to monogastric, which is why people who have diabetes can consume it (Moreno Díaz et al 2019). Instead, yacon´s carbohydrates including oligosaccharides as well as inulins and fructooligosaccharides can be used by ruminants due to their microorganism in rumen (Pinzón Rodríguez y Lemus Gámez 2017).

Other advantages of the yacon are the low cost of the crop and the possibility of contributing to the generation of complementary incomes in sustainable production systems (Lopera-Marín et al 2020). For this characteristic, the yacon is profiled as a local resource for strategic supplementation in livestock systems, especially dairy cows (Valentová y Ulrichová 2003).

This investigation evaluated the bromatological quality of yacon silage (S. sonchifolius) elaborated with different plant fractions in high colombian tropic conditions. The vision for the future is to offer a new alternative for strategic supplementation in dairy livestock systems through mixed forage banks, intensive silvopastoral systems, forage hedges, and other land uses that can contribute to the conservation of fragile high mountain ecosystems.

Materials and methods

Location

The research was done on the farm called “Cien Años de Soledad” (geographic coordinates: 6° 26' 45.49" N y 75° 32' 43.20" W) located in Rionegro east of Antioquia (Colombia). The experimental area is between 2200 and 2350 m altitude, with annual precipitation of 2200 mm and an average temperature of 17.7 ºC (maximum 22.5 ºC – minimum 12.8 ºC). According to Holdridge's classification, the life zone is identified as a low-mounted wet forest (Holdridge 1966).

Establishment, cultivation management, and harvesting of fodder

The cultivation of yacon was established from basal propagules (agamic or vegetative seed) in 117 m². Soil preparation was done by manual tillage, without soil correctives or fertilization. Three hundred ninety-nine yacon individuals were planted with 0.8 m between grooves and 0.6 m between plants. The yacon was harvested 7.5 months after planting. All the harvested leaves, stems, and tubers were intended to prepare the silages described below.

Photo 1. Yacon rhizomes and tubers. Photo: Jhon Jairo Lopera	Photo 2. Harvested yacon tubers. Photo: Jhon Jairo Lopera

Treatments and experimental design

This research evaluated the 18 treatments resulting from a factorial structure 3 x 3 x 2. Were used:

1. Three mixtures of the inclusion of components from the plant in the silage: 100 % stems and leaves (M1), 50 % stems and leaves, with 50 % tubers (M2), and 75 % stems and leaves, with 25 % tubers (M3).
   
   
2. Three post-sealing evaluation times: 15, 25, and 35 days.
   
   
3. Silage with and without the addition of acid-lactic bacteria (commercial product in water-soluble powder with Lactobacillus plantarum, Lactobacillus brevis, Pediococcus acidilactici, and Streptococcus diacetylactis,manufactured by Bentoli Agricultural Products in Texas - United States).

Silage preparation

According to the evaluated treatment, the yacon plant fraction (roots or tubers, stems, and leaves) was used in different proportions. The harvested material was partially dried in the shade for six hours, after which it was chopped using a three-blade electric-powered straw chopper (Penagos brand, manufactured by Penagos Hermanos y Compañía SAS in Quimbaya - Colombia) until fragments with a maximum length of 2 cm were obtained. For all treatments, diluted molasses was added to water, equivalent to 2 % of the silage weight. Treatments that included acid-lactic bacteria were added 1 g of commercial water-soluble powder per 10 kg of prepared silage.

The matter was packed manually in silo bags of polyethylene prime manufactured in Bogotá - Colombia by Plastilene Soluciones SAS. These guarantee uniform thickness and high resistance to the sealing (barrier of O₂) and stacking, as well as the possibility of compacting the forage during the bag filling. Were filled 54 bags with silage (three bags per treatment, and each one was 10 kg). They were labelled with information on each treatment, mixture, and addition or not of acid-lactic bacteria of commercial origin, as well as the estimated fermentation time.

The bags were sealed with polypropylene strings after the air was manually extracted through compacting. Each bag was covered with a triple layer of vinipel paper and stored in a warehouse on wooden pallets.

Photo 3. Crop, preparation and storage of yacon silage. Photo: Jhon Jairo Lopera

Evaluated variables

The bromatological characterization of the silage was realized through near-infrared spectroscopy (NIRS) in the Integrated Laboratory of Animal Nutrition, Biochemistry and Pastures and Fodder of the Faculty of Agricultural Sciences – the University of Antioquia (Mark: FOSS; Model: DS 2500F; Working software: ISIscan Nova DS2500F; Software version: 10.2.3.9) (Rivera Rivera et al 2018; Pereira et al 2023). For this process, the samples were dried at 70 ºC for 16 hours, ground to a diameter of 1 mm in a Cyclotec mill, and read in a DS 2500F equipment, using quartz buckets with approximately 12 g of the ground material. The results predicted by NIRS yielded information on the percentage of dry matter (DM), digestibility of dry matter, crude protein (CP), soluble protein (SP), ether extract (EE), crude fiber (CF), neutral detergent fiber (NDF), acid detergent fiber (ADF), sugars, starches, and non-structural carbohydrates (NSC). All variables were analyzed on a dry matter basis.

The pH was determined through a pH-meter (pH METER LT-YK21PH c with range 0 ~ 14 pH, manufactured by twilight in Monterrey - México). For this process was necessary the construction of a manual press made of stainless steel. This press was introduced 15 g of silage, and the silage fluid was subsequently extracted, which was subjected to pH evaluation. The pH-meter was heated with a pH 7.00 and pH 4.00 solution.

Statistics analysis

The information was collected under a factorial arrangement structure 3 x 3 x 2 (three treatments, three times, and two additives). The obtained data were analyzed according to the following mathematical model:

Y_ijkl = µ + M_j + T_k + A_l + MT_jk + TA_kl + MA_jl + MTA_jkl + EE_ijkl

Where:

Y_ijkl = variable response

µ = general mean

M_j = j-th effect of the mixture in different proportions of the plant components in silage (M1, M2 and M3)

T_k = k-th time effect (15, 25, 35 days)

A_l = l-th effect of the additive (without and with)

MT_jk = jk-th effect of the interaction between mixing and time

TA_kl = kl-th effect of the interaction between time and additive

MA_jl = jl-th effect of the interaction between mixture and additive

MTA_jkl = jkl-th effect of mixing interaction, time and additive

EE_ijkl = experimental error. They distributed N (0.1) σ²

R Project software version 4.4.1 (R Core Team 2024) was used for information analysis. The variance of analysis (ANOVA) was performed using the lme (linear mixed effect models) function of the nlme package (linear and nonlinear mixed effect models). In case of rejection of the null hypothesis in the ANOVA (p<0.05), the Tukey mean separation test was used.

Results and discussion

The pH is an analytical indicator used to evaluate the quality of silage. It can be affected by the type of matter that is used, the size of the particle, and the fermentable potential (Reyes-Gutiérrez et al 2018). The pH descends during the fermenting phase when the microorganisms (own of the ensiled matter and additions) produce lactic acid from the fermentable carbohydrates (Hartinger et al 2019).

This study observed an effect related to the proportions of plant parts used to prepare silage. The greater inclusion of tuber, the lower the pH (p<0.05), compared to the treatment without tuber inclusion (100 % leaves and stems) (Table 1). Likewise, a decrease (p<0.05) in pH was observed over the evaluation time, going from 4.4 at 15 to 4.21 at 30 days. Similar pH values were found in silages of C. purpureus x C. glaucum (hybrid OM-22) and Moringa oleifera, when 25 and 50 % of sweet potato tubers (Ipomoea batatas L.) were included (Rodríguez et al 2020).

One possible explanation for the descent in the pH that happens when the proportion of tubers increases is more NSC that some bacteria degrade to produce lactic acid. Similar results were obtained when ensiled king grass was with cassava roots (López-Herrera et al 2019a). The absence of an additive effect in the pH might be due to the activity of lactic-fermenter microorganisms present previously in the fermented matter, as was described by Keshri et al (2018).

The pH values recorded in this research (4 to 5) are in a range characterized by good-quality silos and well-conserved. The pH values above five can indicate less nutritional silage caused by proteolytic bacteria like Clostridium or Bacillus, which degrade proteins of the matter (Pinzón Rodríguez y Lemus Gámez 2017). The pH values less than or equal to 3.9 indicate a more intense fermentative process that tends to promote the lactic fermentation. Though this can reduce losses by the anaerobic decomposition in the silage, the registers down of the optimal are associated with lower animal consumption (López-Herrera et al 2019b).

The differences in the content of DM (Table 1) were significant (p<0.05), and the DM decreased with the addition of more tuber mixture. The silage DM remained constant between 15 and 25 days, but it significantly declined when the matter was uncovered 35 days later (p<0.05). The DM content registered in the evaluated silages is considered low compared to the 30 to 35 % registered in the other silages (Ashbell y Weinberg 2001). In the current study, the M1 had a DM content of 16.79 % higher than the ones observed in M3 and M2 (15.29 % and 14.08 %, respectively). It should be noted that M2 contained 50% of tubers in the prepared silage, influencing a higher humidity content. The DM values are consistent with the mixtures that are made.

A study made in Cuba (Rodríguez et al 2020) registered a loss of 14 points of DM when they included 50 % of boniato tubers (L. batatas) in silages of C. purpureus x C. glaucum (hybrid OM-22) and M. oleifera. The same tendency was observed in this study. A silage study made with 100 % of yacon leave found 16.39±0.13 % of DM, similar values to the ones found in this evaluation for M1 (Pinzón Rodríguez y Lemus Gámez 2017). Those results suggest the convenience of drying the matter before the ensilage process. In the present investigation, a partially dried of 6 hours was made. A prolonged process (>10 hours) can probably improve the final content of DM in the silages (Sánchez Matta 2005). In a study where sugar beet ( Beta vulgaris L.) silage was evaluated, DM results were low (<15%), and these are lower than the values reported in the present evaluation (Nieto-Sierra et al 2020).

A study made in Japan used lactic acid bacteria (Lactobacillus plantarum). Dried beet pulp is looking to improve the nutritional quality of the yacon waste (tubercles, stems, and leaves) during the ensilage process (Wang et al 2019); the DM values for the control and treatment with bacteria were 12.3 and 12.6 %, respectively. The present study obtained higher values with and without additives application (15.54 and 15.22 %), with no statistical difference between the two treatments.

Considering the significant interaction, A x T (Figure 1b), the current study results suggest that the opening time of the silage should not exceed 25 days. If lactic acid bacteria are used, they are enough to increase the content of DM at 25 days, but not at 15 or 35 days.

(a)	(b)
Figure 1. Significant interactions for the % of dry matter (DM): mixture x additive (a); additive x time (b)

The CP content decreased significantly as the proportion of leaves-stems was reduced and increased the proportion of tubers in the silage (p<0.05) (Table 1). This result was expected, considering that the CP content in the leaves and stems almost duplicates the content of the tubers. In silages made with king grass and cassava, it was registered to decrease the protein of the silage when the proportion of the tubers e was increased (López-Herrera et al 2019a). The CP values found in the current study are lower than those reported by Pinzón Rodríguez y Lemus Gámez (2017) when they used 100 % yacon leaf (18.69±1.85), likewise the percentage of ash (15.00±0.01). This could be due to the harvested product not being fertilized by the yacon used in this study.

Silage opening time also affected CP content, which was higher at 35 days than at 25 and 15 days, while SP only increased at 35 days (Table 1). This information may be related with the proteolysis process, which is reduced by the presence of NSC, especially in the mixtures with different proportions of tubers (M2 and M3) and a probable decrease in the production of ammonia nitrogen that was no measured in the current study (Rodríguez et al 2020).

Adding lactic acid bacteria decreases the content of CP in the ensilage with no effect on the SP. Additives (such as bacteria), besides being used to improve the fermentative process conditions, are also an alternative to partially replace the dried vegetable material before being ensiled (Llatas Llaja 2019). This author mentions that the additives can negatively affect the CP in materials like stems and other thick particles with high humidity contents and without the correct wilting before silage. In the current study, lactic acid bacteria increased the CP to 25. For day 35, there was no significant difference between adding or not adding, and the CP values were lower (Figure 1b). This contrasts with the information given by Mariadhas Valan et al (2014) and Sánchez Matta (2005), who claim that the addition of additives (bacteria) improves the compositional quality of the silage.

Contrary to what occurred with CP, the SP content increased to the extent that there was a more significant proportion of tubers in the mixtures (p<0.05). This effect is also related to the high sugar content (including NSC) of yacon tuber (M2 and M3) (Hernández et al 2020). However, the data obtained in M1 and M2 of the present work show SP values lower than 60 %, and they are profiled as foods rich in protein surplus, with the possible effect of reducing the production of enteric methane (Porsavatdy et al 2016; Sossa Sánchez et al 2017). This may be supported by the balance of fermented feeds in the duodenum and large intestine about the rumen, where the acetogenic elimination of hydrogen in the fermentative degradation probably occurs (Hung et al 2020).

The CP showed a significant difference (p<0.05) in the interaction M x A, where only M3 had the highest content of this fraction without the additive application (Figure 2a). In the interaction A x T (Figure 2b), it was founded higher values of CP on the 15 and 25 days (p<0.05) without the application of additive. The same variable indicates triple interaction (p<0.05) (Figure 3). The SP in the interaction M x A (Figure 4a) was different (p<0.05) in the M2 without the application of lactic acid bacteria, while the M3 was the one with a higher additive (p<0.05). The M1 was not affected by the application or any of it. To the interaction M x T (Figure 4b), all the mixtures were different on day 35 (p<0.05).

(a)	(b)
Figure 2. Significant interactions for the % crude protein (CP): mixture x additive (a); additive x time (b)

(a)	(b)
Figure 3. Significant interaction for the % crude protein (CP): mixture x additive x time

(a)	(b)
Figure 4. Significant interactions for the % of soluble protein (SP): mixture x additive (a); mixture x time (b)

The digestibility of dry matter of the silage (Table 2) did not present significant differences between M2 and M3 (80.30 and 78.51 %, respectively), but both were different from M1, which showed a lower percentage of digestibility (70.45 %). The obtained results generally showed high digestibility, which can be attributed to the high content of NSC, whose availability may be higher for ruminal microorganisms (González Bermeo 2018). The same author references that the high percentages of digestibility are associated with the low presence of fibers, especially NDF, which stimulates a higher consumption of DM. The digestibility of the silage found in the current study was higher than the one described by Pinzón Rodríguez y Lemus Gámez (2017) (50.60±0.14 %). In a study where the silage of four forages (Cratylia argentea, Hibiscus rosa-sinensis, Trichanthera gigantea and Tithonia diversifolia) was evaluated, the values of in situ DM degradability at 72 hours (p<0.05) were 67.56, 69.70, 67.09 and 62.80, respectively (Roa y Galeano 2015). The values for H. rosa-sinensis are very close to those reported in this study for M1.

The values of the EE (Table 2) were similar in M1 and M3 (2.23 and 2.14 %), but both were different (p<0.05) to M2 (1.74 %). The decrease in M2 can be related to the proportion of tubers (50 %) richer in soluble sugars. In evaluations of silages made only with yacon leaves, and in some cases with orange peel, higher values were found (between 4.38±0.03 and 4.66±0,22 %) (Pinzón Rodríguez y Lemus Gámez 2017). Regarding the sealing time, the obtained values were similar between the 25 and 35 days (2.00 and 2.19 %) but differed (p<0.05) between days 15 and 35. The lowest values on day 15 can be related to this aerobic phase of silage and loss of carbohydrate glycolysis process; with a higher fermentation time, the process tends to improve (Vanegas Ruiz y Codero-Ahiman 2019).

The values of NDF obtained in this investigation (Table 2) decrease with the increase of yacon tubers proportion. No statistical differences were found between M2 and M3 (28.71 and 28.58 %, respectively), but these treatments were different (p<0.05) than M1 (37.56 %). This may be associated with acid hydrolysis of hemicellulose in the metabolism of microbial sucrose during the fermentation process (Hartinger et al 2019). A similar behavior was observed by Rodríguez et al (2020) by incorporating 25 and 50 % of tubers of C. purpureus x C. glaucum (hybrid OM-22) and M. oleifera, where the increase of tuber proportion was associated with the decrease of NDF.

The NSC includes, among others, sugars and starches (NRC 2001). In the current research, the yacon silages, including 25 and 50 % of the tuber, had higher sugar contents and NSC and registered a relation of 1.86 and 1.89, respectively (Table 3). An investigation about silages where potato tubers were included in different proportions next to grasses was found to increase the proportion of NSC and starches, especially physically useful ones. A good indicator of this balance is obtaining a relation of 2:1 between NSC and NDF.

The percentage of sugars decreases with the increase in fermentation time (p<0.05), probably due to the acidic hydrolysis of hemicellulose during the fermentation process (Table 3) (Hartinger et al 2019). The starches showed an opposite behavior (p<0.05) during the same times, with higher percentages on days 25 and 35 (11.28 and 13.53 %, respectively) (Table 3). This may be influenced by the fermentation of the water-soluble carbohydrates of the ensiled material by the bacteria at the beginning of the process (Rodríguez-Oliva et al 2022). Likewise, the excellent compaction of the ensiled material probably limited the increase in temperature, reduced the intensity of the glycolysis process, and avoided losses in this fraction. The addition of lactic acid bacteria accomplishes the objective of growing the concentration of sugars (p<0.05), providing energy to microorganisms that intervene in the fermentation process, and improving the chemical characteristics of the silage (Noguera et al 2006). For the same variable in Figure 5a and 5b, interactions are shown in M x A and M x T, respectively.

(a)	(b)
Figure 5. Significant interactions for the % of sugars: mixture x additive (a); mixture x time (b)

Most of the analyzed variables related to the compositional quality of silage did not show the effect of bacteria in the fermentative process. In some cases, adding commercial additives based on bacteria L. plantarum, L. brevis, P. acidilactici and S. diacetylactis was associated with lower nutritional quality silage. This suggests that some lactic acid bacteria must be identified in the yacon silage. Although the fermentation that occurred in this process was probably hetero fructose (acid-lactic fermentation), the results may be associated with the yacon is differentiated sugar profile, characterized by the presence of fructooligosaccharides, including inulin (Sáenz Torres et al 2016). This FOS presents acid-lactic fermentation; however, the results may indicate that the used bacteria in the experiment were not the most appropriate or specific to improve this process.

Conclusions

In this investigation, the treatment with a higher proportion of yacon tubers (M3 and M2) showed the best results, especially in higher digestibility and EE. They were also the high in NSC value and the low in NDF content. This could help reduce the problems associated with lack of energy in the diet and increase DM consumption in livestock dairy farms in the tropical highlands of Colombia.

All treatments showed low levels of dry matter, especially the mixtures that include tubers. This requires the perfection of a wilting or drying process for this fraction of the plant. On the other hand, aerial forage (stems and leaves) may be used as it is a source of food for dairy cows and can be conserved using the silage technique, improving its quality by including 25% of tubers in the same plant.

Generally, the additive based on lactic acid bacteria did not positively affect the yacon silage. It is necessary to identify specific bacteria that have improved silage chemical characteristics and are rich in sugars like FOS or oligofructose, which are present in yacon. One route is to explore additives from epiphytic flora that can contribute to fermentation in forages with low DM content and reduce nutrient loss during silage making. However, the present research has shown silage with good compositional quality, without additive application in the mixtures with aerial forage and tubercles, on the 35 days of sealing.

Acknowledgments

Authors thanks to farm “Cien Años de Soledad” (Jhon Dairo Valencia Manrique and Andrés Camilo Marín) for helping in the process and development of the different activities of preparation and planting of the crop, as well as taking data in each growing cycle and at harvest time. To Zoraida Calle Díaz (Biol., MSc.) for support in the statistical analysis and the leadership program ELTI (Environmental Leadership & Training Initiative) for the collaboration in the final edition of the text. To Manuela Cruz Sánchez and Claudia Patricia Sossa (CIPAV researchers) for the support taking information process.

This research is part of the doctoral thesis "Productive evaluation of intensive silvopastoral systems (ISPS) in high tropical dairy, with supplementation of creole fodder resources and lipid sources." Financed by the GRICA Group of the University of Antioquia (through sustainability resources), CIPAV (through the support received by Minciencias and the Autonomous Patrimony National Fund for the Financing of Science, Technology and Innovation Francisco José de Caldas, through the plan to strengthen Innovation for Resilience and Climate Change Mitigation in the Livestock Agriculture Landscapes of Colombia, code 3307100270685, contract 006-2020), and the Sapiencia Fund - Medellín Higher Education Agency (Mayor's Office of Medellín, Antioquia, Colombia).

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