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EVALUATION OF DRIED MAO POMACE (ANTIDESMA BUNIUS LINN.) AND LACTIC ACID BACTERIA AS ADDITIVES TO ENSILE STYLO LEGUME (STYLOSANTHES GUIANENSIS CIAT184).

Byline: S. Bureenok, N. Pitiwittayakul, C. Yuangklang, K. Vasupen, B. Saenmahayak, Y. Kawamoto and J. T. Schonewille

Keywords: Fermentation quality, Lactobacillus paraplantarum, Phenolics, Silage.

INTRODUCTION

It is generally accepted that, amongst others (McDonald et al., 1991), the water soluble carbohydrate (WSC) content of forages is important to ensure the rapid production of lactic acid (Zhang et al., 1997; Tamada et al., 1999) in order to ensure a good quality silage. Stylo (Stylosanthes guianensis CIAT184) is a legume of practical interest in tropical countries (Phaikaew and Hare, 2005). However, Stylo contains low amounts of WSC (Bureenok et al., 2016) which hinders the process of ensiling (Liu et al., 2011, 2012). Therefore, addition of WSC to fresh Stylo prior to ensiling would likely be required to facilitate the growth of lactic acid bacteria (LAB) and ensure the rapid production of lactic acid (LA) to obtain a stable, nutritious silage. Dried mao (Antidesma bunius Linn.) pomace is a by-product of mao wine or juice processing from Mao Luang seeds and widely available in the North-East of Thailand, i.e. around 75 tons/year (Samappito and Butkhup, 2008).

Dried mao pomace (DMP) may be a good source of WSC (Table 1) to facilitate the ensiling of Stylo. However, DMP also has a high content of total phenolics which have the capacity to inhibit the growth of various bacteria including gram positive bacteria (Butkhup and Samappito, 2011), thereby, potentially hindering the establishment of a stable silage. In addition to the WSC content, the number of epiphytic LAB on forages also are important to ensure the rapid establishment of a stable silage. It has been shown that the addition of fermented juice of epiphytic LAB (FJLB) from tropical forages such as Napier grass (Bureenok et al., 2006) and Guinea grass (Bureenok et al., 2005) improved the quality of the respective silages. The latter two studies indicate that the number of epiphytic LAB on Napier and Guinea grass may be sub-optimal for ensiling purposes.

Recently, Bureenok et al. (2016) demonstrated that the treatment of fresh Stylo with FJLB resulted in palatable, stable silage (pH<4.3) but the ensiling process of Stylo not treated with FJLB, was not evaluated. The presented study aimed to evaluate the efficacy of DMP, either or not in combination with additional LAB in the form of either FJLB or Lactobacillus paraplantarum (LPP). The latter was selected because in a wide variety of forages it appears to be the most dominant epiphytic LAB (Liu et al., 2012; Pang et al., 2011, 2012; Wang et al., 2017; Zhang et al., 2017).

MATERIALS AND METHODS

Experimental forages: The experiment was conducted at the Rajamangala University of Technology-Isan Sakon Nakhon Campus, Thailand in 2014. Stylo was grown with no fertilizer and harvested 60 days after regrowth and chopped to approximately 2-4 cm with a forage cutter and subsequently sampled to determine its nutrient composition (Table 1). Then, the six experimental silages were prepared immediately after cutting with the treatments arranged in a 2 x 3 factorial fashion, i.e. forage with or without additional DMP and with or without additional LAB from either FJLB or the isolated strain. The applied doses of forage specific FJLB and the isolated strain (Lactobacillus paraplantarum, LPP) were log 5.89 and 5.56 colony forming units (cfu) g-1 fresh forage, respectively. DMP was applied at a level of 100 g kg-1 fresh forage.

Thereafter, ~100 g fresh material of each silage treatment, was packed in plastic pouches (20.32 x 33 cm, 120 u thickness; M-PLASPACK, Bangkok, Thailand) and sealed with a vacuum sealer. For each sampling day and each experimental forage, three replicate pouches (n=3) were prepared and all pouches were kept at ambient temperature (27-30AdegC).

Preparation of FJLB and LPP: Fermented juice of LAB (FJLB) was made from fresh Stylo as described by Bureenok et al. (2011). Then, MRS agar plates were inoculated with samples from FJLB and subsequently incubated anaerobically at 35AdegC for 2 days. Thereafter, LPP was isolated and subsequently cultured on MRS broth at 37AdegC for 24 h. The 16S rDNA sequence of the type strains in the database of EzTaxon-eserver (http://eztaxon-e.ezbiocloud.net/) was used to compare with the 16S rRNA gene sequence of the isolated strain from FJLB (Kim et al., 2012).

Collection of samples: Upon arrival from the local processing plant, mao pomace was dried at 60AdegC in hot air oven and stored at ambient temperature (27-30AdegC) until the analysis of its nutrient composition and polyphenol content. Silage samples were taken at 1, 3, 5, 7, 14, 21 and 30 days to assess the ensiling characteristics of the forages. Subsamples (~20 g fresh material) of silage were mixed with distilled water (70 mL) and placed in a refrigerator at 4AdegC for 12 h. Then, the extract was filtered and the pH of the filtrate was recorded. The filtrate was stored at -20AdegC until the analysis of LA, volatile fatty acids (VFAs) and ammonia-N (NH3-N). Subsamples of ~ 10 g were taken to assess LAB counts. Directly after sampling, 90 mL of a sterilized 0.85% NaCl was added and the samples were thoroughly mixed. Thereafter, serial dilutions (10-1-10-8) were made and LAB were counted on MRS agar and incubated at 35AdegC for 2 days (Kozaki et al., 1992).

The remaining part of the silage in each pouch was dried at 60AdegC (48 h) and subsequently ground (1-mm screen) and kept until the analysis of nutrient composition and total polyphenol content.

Chemical analysis: Lactic acid and VFA were measured using HPLC. The steam distillation technique was used to determine NH3-N content (Cai, 2004). Total nitrogen (N) of silage was determined according to procedures set by the AOAC (method 981.10, 1995) and converted to crude protein (CP) by multiply 6.25 as a factor. The ash contents were determined according procedures set by the AOAC (method 938.08, 1995). Neutral detergent fiber (NDF) was determined by the method of Van Soest et al. (1991) and expressed exclusive of residual ash. The WSC content was determined as described by Dubois et al. (1956). The total phenolics content was determined by the method of Waterhouse (2005).

Statistical analysis: All data of Stylo legume after 30 days of ensiling were subjected to ANOVA using SAS (1994), based on the model:

Yij = u + DMPi + LABj+ (DMP x LAB)ij + eij

where Yij = response variable, u = overall mean, DMPi = Dried mao pomace (i = yes or no), LABj = Lactic acid bacteria (j = no or FJLB or LPP), (DMP x LAB)ij = interaction term between DMP and LAB and eij= residual error. Furthermore, LAB counts and selected fermentation characteristics (LA, pH and NH3-N) at the different time points were subjected to ANOVA with repeated measures using the model already described. Tukey's test was used to test the different effects of the treatment.

Table 1. Chemical composition and pH of fresh Stylo and dried mao pomace (DMP).

###Stylo###DMP

Dry matter(DM, g kg-1)###284###883

Crude protein (g kg-1 DM)###122###70

Neutral detergentfibre (g kg-1 DM)1###496###402

Acid detergent fiber(g kg-1 DM)1###304###235

Hemicellulose (g kg-1 DM)###193###167

Water soluble carbohydrates (g kg-1 DM)###45###188

Total phenolic content (g kg-1 DM)2###nd###110

pH###5.56###3.70

Table 2. Selected indices of fermentation and chemical composition in Stylo legume after 30 days of ensiling with (yes) or without (no) dried mao pomace (DMP) and either without (no) or with fermented juice of epiphytic lactic acid bacteria (FJLB) or Lactobacillus paraplantarum (LPP).

Added DMP###No###Yes###SEM###P-values

Added LAB###No###FJLB###LPP###No###FJLB###LPP###DMP###LAB###DMPxLAB

Fermentation Characteristics

LAB (log cfu g-1 FM)###6.39###6.76###6.22###6.96###6.66###6.60###0.02###0.075###0.221###0.184

Lactic acid (g kg-1 DM) 11.0d###34.5bc###40.2abc###29.1c###50.8ab###59.3a###3.45###<0.001###<0.001###0.850

TFa (g kg-1 DM)###29.6c###50.2b###56.8b###47.7b###76.0a###77.6a###2.39###0.007###0.008###0.809

LA/Tfa###0.38b###0.69a###0.71a###0.62a###0.67a###0.76a###0.02###0.052###0.001###0.012

HAc/Tfa###0.37###0.25###0.24###0.35###0.32###0.22###0.02###0.480###0.132###0.631

HBut/TFa###0.21a###0.03b###0.02b###bdl###bdl###bdl###0.01###<0.001###<0.001###0.999

NH3-N (g kg-1 total N)###89.0a###81.7a###74.8a###36.5b###42.7b###34.4b###3.43###<0.001###0.059###0.128

pH###4.76a###4.44b###4.38b###3.73c###3.76c###3.68c###0.06###<0.001###0.008###0.018

Chemical composition

DM (g kg-1)###269b###240c###236c###337a###329a###343a###2.35###<0.001###0.020###0.018

CP (g kg-1 DM)###116c###121ab###117c###122ab###123a###118bc###0.37###0.090###0.009###0.026

NDF (g kg-1 DM)###573###572###564###549###544###560###5.22###0.106###0.954###0.610

Total phenolics###4.41c###4.20c###5.93bc###7.11ab###8.55a###5.76bc###0.22###<0.001###0.477###0.004

(mg gallic acid g-1 DM)

RESULTS

Fermentation characteristics and chemical composition: After 30 days of ensiling, all treatments had no effect on the number of LAB in the silages (Table 2). On average, the addition of DMP caused a 1.6 times increase (P < 0.001) in the LA content of the silages while the use of either FJLB or LPP caused on average a 2.3 times increase of the LA content (P < 0.001). The total content of fermentation acids (TFa) was not affected (P = 0.809) by DMP x LAB (Table 2). The addition of both DMP and LAB increased TFa (P a$? 0.008) by 47.3 and 68.5%, respectively. The LA fraction of TFa was influenced by DMP x LAB due to the low values found in the silage that was neither treated with DMP nor LAB (P = 0.012). The acetic acid (HAc) fraction of TFa was similar for all treatments (P [greater than or equal to] 0.132) and for all treatments combined, a mean value of 0.37 was found.

The use of DMP depressed the fractions of both propionic and butyric acid (HBut) of the silages and the fraction of HBut was depressed below the detection limit. In case silages were not treated with DMP, HBut fractions were lower (P < 0.001) when LAB were added, irrespective of the source of LAB. The NH3-N contents were not affected by DMP x LAB (P = 0.128). The use of DMP caused a 54% decrease in NH3-N values (P < 0.001) but addition of LPP only tended to decrease the NH3-N content (P = 0.059). The silage pH was affected by a significant interaction between DMP and LAB. The lowest pH's (P < 0.001) were found in the DMP treated silages and the use of FJLB or LPP did not affect the pH in those silages (P = 0.018). In contrast, the use of either FJLB or LPP resulted in almost 5% lower pH values (P = 0.008) in the silages without DMP.

Due to its high DM content, the addition of DMP increased (P < 0.001) the DM contents of the silages (Table 2) while LAB reduced (P = 0.020) the DM contents. However, the reduction of DM contents only occurred when LAB were added to the silages without DMP (P = 0.018). The use of FJLB, but not LPP, caused higher (P = 0.009) CP contents in silages. This effect of FJLB, however, was only observed in silages without DMP (P = 0.026). The NDF contents were found to be similar between the silages (P [greater than or equal to] 0.106). Addition of LAB did not affect (P = 0.477) the total phenolic content of the silages. Across the LAB treatments, the use of DMP caused a 1.47 fold increase (P < 0.001) of the content of total phenolics but the use of both DMP and LPP decreased the content of total phenolics of the silages (P = 0.004).

Time courses on selected indices of fermentation: Besides the NH3-N content (Fig.1, panels G and H), LAB counts, LA concentrations and pH of the experimental silages were not affected by the three-way interactions between DMP, LAB and time (P [greater than or equal to] 0.122) and are therefore not reported. The LAB counts were affected by time (P < 0.001) and the use of DMP caused a minor, but significant (P < 0.001), difference in LAB counts in the course of time (Fig. 1, panel A). Likewise, time patterns of LAB counts were found to be significantly (P < 0.001) affected by the addition of LAB (Fig. 1, panel B). The LA concentrations also were found to be affected by time (P < 0.001). However, the LA concentrations continued to rise after 15 days of ensiling when DMP was used while LA concentrations remained almost similar in case Stylo was ensiled without DMP (Fig. 1, panel C, P = 0.008). Likewise, LA concentrations increased with time after 10 days of fermentation in the case LAB was used (Fig. 1, panel D, P = 0.011).

Silage pH was affected by time (P< 0.001) but not by DMP x time (Fig. 1, panel E, P [greater than or equal to] 0.463) while a trend (P = 0.070) was observed for LAB x time (Fig. 1, panel F). A three-way interaction between DMP, LAB and time was observed for silage NH3-N contents (data not shown, P < 0.001). Both the addition of DMP and LAB caused different (P < 0.001) time courses of NH3-N (Fig. 1, panels G and H).

DISCUSSION

During the first week of ensiling, the addition of DMP caused a reduction in LAB counts. This observation is most likely explained by the fact that DMP has a high content of total phenolics because Butkhup and Samappito (2011) have demonstrated that such compounds inhibit bacterial growth including gram positive bacteria. However, the depressant effect of DMP on LAB counts was found to be relatively small and did not affect LA contents. Numerically, LA contents were even higher when DMP was used as an additive. Perhaps, the high WSC content of DMP stimulated the production of LA, thereby, counteracting the depressant effect of total phenolics on LAB counts. On the other hand, it must be taken into account that the use of DMP not only provided WCS but also increased the DM content of the silage. It is well known that higher DM contents of silage improve the process of ensiling (McDonald et al., 1991).

Clearly, the current data do not causally explain the higher LA contents of the silages treated with DMP. Across time, both FJLB and LPP were found to be equally effective in raising the mean LA content of silage, irrespective the use of DMP. This result appears to be in contrast with the observation that the fraction of LA of total fermentation acids (TFa), after 30 d of ensiling, was influenced by DMP x LAB. This apparent discrepancy can probably be explained by the different time patterns of the LA content during the 30 d ensiling period (Fig. 1, panel C). The influence of the last two LA values on the mean LA content of silage treated with DMP, was probably too small to significantly influence the interaction between DMP and LAB on the mean LA content. Dried mao pomace versus FJLB and LPP, was found to be a more effective additive to produce sufficient LA to reduce silage pH.

This result is in line with the current observation that TFa after 30 days of ensiling was higher when DMP was applied. These results support the idea that the WSC content of Stylo limits the process of LA formation. Furthermore, the silages treated with DMP had low NH3-N contents (i.e. < 43 g/kg total N). Perhaps, current pH values have inhibited the growth of proteolytic Clostridia, thereby, preventing the formation of ammonia (Umana et al., 1991). Umana et al. (1991) suggested that well preserved silages should contain pH values < 4.5 and NH3-N 0.70, < 0.20, and < 0.025, respectively (Ojeda et al., 1991). The current results show that a good silage quality was already achieved when DMP instead of FJLB or LPP was used as silage additive. In case DMP was added, the values with respect to pH, NH3-N and butyric acid (Umana et al., 1991; Ojeda et al., 1991) were already met.

However, in the silages treated with DMP, LA/TFa was found to be on average 0.69 and this was associated with an average HAc of total TFa fraction of 0.30. Even though the aerobic stability of the silages is not specifically evaluated in the current study, the relative high HAc fractions may indicate that the aerobic stability of the silage (Weinberg et al., 1993; Danner et al., 2003) was somewhat compromised. On the other hand, the pH and DM contents of the DMP silages were on average 3.7 and 336 g kg-1, respectively and this combination of silage pH and DM content generally ensures a sufficient stability of the silage (McDonald et al., 1991). The current data cannot explain the relatively high fraction of HAc of total TFa. However, it is likely not related to the DMP as the fractions of HAc were high in all silages. Stylo contains approximately 200 g hemicellulose/kg DM and it can be speculated that the HAc originated from hemicellulose acetyl groups (Bergen et al., 1991).

Further research, however, is warranted to substantiate this suggestion. The addition of DMP was associated with virtually zero HBut contents which can be explained by the low pH values of the silages in question. The DMP silages had pH values < 4.0 and such low pH values are known to inhibit the growth of clostridia species and thereby the production of HBut (Lindgren et al., 1985). Next to DMP, the addition of either FJLB or LPP also increased the TFa content of the silages. Although caution is warranted to generalize this result, it can be speculated that the number of epiphytic LAB in Stylo, next to its low WSC content, also limit the process of fermentation during ensiling. This is in an agreement with results of Bureenok et al. (2005, 2006) who suggested that the application of FJLB to tropical forages such as Napier grass and Guinea grass, improved the quality of the respective silages.

In legumes, low levels of butyrate are commonly observed (Ward, 2008) but in the current study, the fraction of HBut of TFa was much too high (Ojeda et al., 1991) when Stylo was ensiled without LAB and DMP. The epiphytic LAB in Stylo may be heterolactic bacteria and produce also a weak acid such as acetic acid. The production of HAc prevents a rapid decline of the pH during ensiling (Liu et al., 2012) thereby hindering the growth of Clostridia species (Kaiser and Weiss, 1997) so as to keep HBut/total fermentation acids < 0.025 (Ojeda et al., 1991).

Conclusions: Ensiling of Stylo without DMP or LAB leads to inferior silage quality. The use of DMP as a silage additive to Stylo results in a good quality silage, irrespective the use of LAB in the form of FJLB or LPP.

Acknowledgments: The Commission on Higher Education and Thailand Research Fund (TRF) are greatly appreciated for funding this project (MRG5580045).

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