J. Dairy Sci. 89:4005-4013
© American Dairy Science Association, 2006.
A Meta-Analysis of the Effects of Lactobacillus buchneri on the Fermentation and Aerobic Stability of Corn and Grass and Small-Grain Silages
D. H. Kleinschmit and
L. Kung, Jr.1
Department of Animal and Food Science, University of Delaware, Newark 19716-2150
1 Corresponding author: lksilage{at}udel.edu
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ABSTRACT
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The results of adding Lactobacillus buchneri to silages from 43 experiments in 23 sources reporting standard errors were summarized using meta-analysis. The effects of inoculation were summarized by type of crop (corn or grass and small grains) and the treatments were classified into the following categories: 1) untreated silage with nothing applied (LB0), 2) silage treated with L. buchneri at 
100,000 cfu/g of fresh forage (LB1), and 3) silage treated with L. buchneri at > 100,000 cfu/g (LB2). In both types of crops, inoculation with L. buchneri decreased concentrations of lactic acid, and this response was dose-dependent in corn but not in grass and small-grain silages. Treatment with L. buchneri markedly increased the concentrations of acetic acid in both crops in a dose-dependent manner. The numbers of yeasts were lower in silages treated with LB1 and further decreased in silages treated with LB2 compared with untreated silages. Untreated corn silage spoiled after 25 h of exposure to air but corn silage treated with LB1 did not spoil until 35 h, and this stability was further enhanced to 503 h with LB2. In grass and small-grain silages, yeasts were nearly undetectable; however, inoculation improved aerobic stability in a dose-dependent manner (206, 226, and 245 h for LB0, LB1, and LB2, respectively). The recovery of DM after ensiling was lower for LB2 (94.5%) when compared with LB0 (95.5%) in corn silage and was lower for both LB1 (94.8%) and LB2 (95.3%) when compared with LB0 (96.6%) in grass and small-grain silages.
Key Words: aerobic stability • silage • Lactobacillus buchneri
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INTRODUCTION
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Exposure to air during feeding and storage can cause silages to spoil. Yeasts that are able to metabolize lactic acid are the primary initiators of spoilage, which leads to an increase in silage pH. This change in the silage environment allows for the growth of opportunistic bacteria and fungi, causing further spoilage (Woolford, 1990). Spoiled silage results in a decrease in net farm income because it represents a loss of nutrients and because animals fed spoiled silage are less productive. Muck (1996) was the first to suggest that inoculation with Lactobacillus buchneri might improve the aerobic stability of silages. Since that time, a considerable amount of research has been conducted with this micro-organism, which apparently improves the aerobic stability of silages via the anaerobic conversion of lactic acid to acetic acid (Oude Elferink et al., 2001). Critics of this approach to improving the aerobic stability of silages have often raised several concerns. First, some have been skeptical regarding the ability of microbial inoculation to alter the process of fermentation and improve aerobic stability (Kung et al., 2003a). Second, some contend that high concentrations of acetic acid in silages have the potential to reduce DM intake in animals consuming these silages (Anil et al., 1993); thus, inoculation with L. buchneri could compromise animal performance. Last, many have questioned the efficacy of inoculation with heterolactic acid bacteria because these microbes have less efficient pathways that can lead to large losses in DM (Pahlow et al., 2003). Our objective was thus to summarize experiments that have investigated the effects of L. buchneri on silage fermentation, DM recovery, and the aerobic stability of whole-plant corn silages and grass and small-grain silages using a meta-analytical technique.
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MATERIALS AND METHODS
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In this summary, the experiments were separated into those that had examined whole-plant corn silage or silage from grass and small grains. Grass and small grains were included in the same data set because the data in this review indicated similar fermentation profiles. Experiments were excluded for lack of data if silages were ensiled for less than 56 d. The studies summarized in this review are listed in Table 1
. Only studies from the literature that reported standard errors of the mean were used, which included peer-reviewed journals, meeting abstracts, conference proceedings, and a thesis. Data that evaluated the effect of L. buchneri on the fermentation and aerobic stability of corn silage were taken from 26 experiments in 15 research studies (Table 1). For grass and small-grain silages, which included barley, sorghum, wheat, ryegrass, and pea:wheat mixtures, data from 17 experiments in 10 research studies were used (Table 1). For both types of crops, treatments were classified into the following categories: 1) untreated corn silage with no inoculant applied (LB0), 2) corn silage treated with L. buchneri at 1 x 105 cfu/g of fresh forage (LB1), and 3) corn silage treated with L. buchneri at > 1 x 105 cfu/g (LB2). These treatments were divided as such because the suggested application rate of microbial inoculants is usually 100,000 cfu/g; however, in some of the previous research with L. buchneri, this application rate was found to be ineffective in altering the fermentation and improving aerobic stability but increasing the dose had marked results (Ranjit et al., 1999; Ranjit and Kung, 2000; Ranjit et al., 2002). Aerobic stability was measured in generally the same manner for all of the studies and was defined as the number of hours silage was exposed to air before a 2°C rise in temperature above the ambient temperature, although some defined it as the number of hours silage was exposed to air before a 1°C rise in temperature (Table 1).
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Table 1. Citable literature summarized in this review of the fermentation and aerobic stability of silages treated with Lactobacillus buchneri using a meta-analysis
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The chemical composition of the silages was reported on a DM basis, and the populations of yeasts were reported on a log10 basis. The aerobic stability from each study was converted to log10 prior to statistical analysis because the variances in the data were not normally distributed. Aerobic stability is reported in the tables as both log10 and hours, and the results of this variable will be discussed as hours because this value is readily applied to the field. Statistical analysis was performed using the MIXED procedure (Littell et al., 1996) of SAS (SAS Institute, 1999). The statistical model was Y = treatment + study + residual error, with treatment being a fixed effect and study being a random effect. The inverse of the variance of each study was used as the weighted variable (St-Pierre, 2001). Orthogonal contrasts were designed to test for the effect of untreated vs. treated with L. buchneri (LB0 vs. LB1 and LB2) and a low inoculation rate vs. a high inoculation rate (LB1 vs. LB2). Significant differences among means were declared at P < 0.05 and tendencies were discussed at P < 0.10. A regression investigating the numbers of yeasts in relation to the concentration of acetic acid in silages was performed as described by St-Pierre (2001). The relationship for DM content and the resulting lactic acid:acetic acid ratio in the silages was determined with a simple linear regression using PROC REG (SAS Institute, 1999) instead of a meta-analysis because the statistical analysis of this measure generally was not conducted in the individual studies and the standard errors were therefore unknown.
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RESULTS
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Corn Silage
The chemical and microbial composition, DM recovery, and aerobic stability of corn silages are shown in Table 2. The DM content was similar among treatments (approximately 31%). Corn silages treated with L. buchnerii had greater (P < 0.01) pH values (3.75 and 3.88 for LB1 and LB2, respectively) compared with untreated silage (3.70). The pH was further increased (P < 0.01) when corn silage was treated with the higher dose of L. buchneri compared with the lower dose. Compared with LB0 (6.59%), treated silages [LB1 (5.87%) and LB2 (4.79%)] had lower (P < 0.01) concentrations of lactic acid, and the concentration of this acid was further lessened (P < 0.01) in silages treated with the higher rate of application. Silages that were treated with L. buchneri had greater (P < 0.01) concentrations of acetic acid when compared with LB0 (2.18%). Silages treated with LB2 (3.89%) had greater (P < 0.01) concentrations of acetic acid compared with the lower application dose of LB1 (2.63%). The concentrations of propionic acid, ethanol, ammonia-N, and water-soluble carbohydrates (WSC) were unaffected by inoculation. Inoculation with L. buchneri (95.5 and 94.5% for LB1 and LB2, respectively) decreased (P < 0.05) the DM recovery in silages compared with LB0 (95.5%). Treating corn silage with the higher application rate of L. buchneri decreased (P < 0.01) DM recovery compared with the lower application rate. Treating silages with L. buchneri at the lower rate (3.10 log10 cfu/g) decreased (P < 0.01) the numbers of yeasts 10-fold compared with LB0 (4.18 log10 cfu/g). Increasing the inoculation rate of L. buchneri (LB2 = 1.88 log10 cfu/g) further lessened (P < 0.02) the numbers of yeasts in corn silages compared with LB1. Inoculation with LB2 (503 h) markedly increased (P < 0.01) the aerobic stability of corn silage compared with LB1 (35 h) and LB0 (25 h). There was a negative relationship (R2 = 0.68, P < 0.01) between numbers of yeasts in corn silages and their concentrations of acetic acid (Figure 1) and no relationship between DM content and the resulting lactate:acetate ratio of untreated and treated corn silage (data not shown).
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Table 2. The effects of Lactobacillus buchneri1 on the chemical (DM basis) and microbial composition, DM recovery, and aerobic stability of corn silage
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Figure 1. Relationship between the concentrations of acetic acid (DM basis) and numbers of yeasts in corn silages. The database was composed of untreated corn silage, corn silage treated with Lactobacillus buchneri at 100,000 cfu/g of fresh forage, and corn silage treated with L. buchneri at > 100,000 cfu/g (P < 0.01).
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Grass and Small-Grain Silages
The chemical and microbial composition, DM recovery, and aerobic stability of grass and small-grain silages are shown in Table 3. The DM content was similar among all treatments (approximately 32%). Inoculation with L. buchneri increased (P < 0.01) the pH in silages (4.19 vs. an average of 4.41), and this was caused by the lower (P < 0.01) concentrations of lactic acid in these silages (7.32 vs. an average 2.89%). Conversely, treatment with L. buchneri (3.59 and 4.31% for LB1 and LB2, respectively) markedly increased (P < 0.01) the concentrations of acetic acid compared with LB0 (1.38%), with LB2 having the greatest (P < 0.02) concentration of this acid. All silages contained propionic acid, and inoculation with L. buchneri increased (P < 0.02) the concentrations of this acid compared with untreated silage (0.16, 0.66, and 0.71% for LB0, LB1, and LB2, respectively). The concentrations of ethanol in silages treated with L. buchneri (0.86 and 0.84% for LB1 and LB2, respectively) were greater (P < 0.01) than those in untreated silage (0.44%). The ammonia-N concentrations of the silages were unaffected by treatment (average of 0.317%). Silages treated with L. buchneri (1.36 and 0.96% for LB1 and LB2, respectively) had lower (P < 0.01) concentrations of WSC compared with the untreated silages (2.08%). Inoculation with L. buchneri decreased (P < 0.01) the recovery of DM relative to LB0 (96.6 vs. an average of 95.1%); however, the inoculation rate had no effect. Yeasts were almost undetectable in all silages, yet treating silages with L. buchneri improved (P < 0.01) aerobic stability compared with LB0 (206, 226, and 245 h for LB0, LB1, and LB2, respectively). Furthermore, increasing the application rate of L. buchneri improved (P < 0.03) aerobic stability. A relationship was not found between the numbers of yeasts and the concentrations of acetic acid in these silages because yeasts were nearly undetectable in all silages regardless of treatment. There was a weak positive relationship (R2 = 0.29, P < 0.01) between silage DM from grass and small-grain silages that were treated and the resulting lactic acid:acetic acid ratio (Figure 2), but this relationship was not observed in untreated silages (data not shown).
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Table 3. The effects of Lactobacillus buchneri1 on the chemical (DM basis) and microbial composition, DM recovery, and aerobic stability of grass and small-grain silages
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Figure 2. Correlation between silage percent DM and the ratio of lactic acid:acetic acid in grass and small-grain silages treated with
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DISCUSSION
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Lactobacillus buchneri is an obligate heterolactic acid bacterium that has been used as a silage inoculant to enhance the aerobic stability in a variety of silages via the anaerobic degradation of lactic acid to acetic acid. In the studies summarized in this analysis, inoculation with L. buchneri decreased the concentrations of lactic acid and increased the concentrations of acetic acid in all silages. As expected, this resulted in treated silages with higher pH. Increasing the rate of inoculation had a greater impact on the reduction in concentration of lactic acid in corn than on the reaction in grass and small-grain silages. The increase in acetic acid from inoculation with L. buchneri was greater as the application rate increased in both types of crops. However, the increase was of a moderate nature because the concentration of acetic acid was only 3.88% even with the highest level of application. Calculations were made to compare the estimated amount of acetic acid that should have been produced if 1 mol of lactic acid was converted to 0.48 mol of acetic acid by L. buchneri, as reported by Oude Elferink et al. (2001). The increases in concentrations of acetic acid in LB1 treatments for both corn and grass and small-grain silages were very Lactobacillus buchneri (P < 0.01). close to what was expected (2.53% expected and 2.63% actual in corn silage, and 3.45% expected and 3.59% actual in grass and small-grain silages). However, treatment with LB2 resulted in approximately 0.8 to 0.9% more acetic acid than was projected in both types of silages, and the reason for this finding is unknown. In corn silage, the changes in lactic and acetic acids resulted in a decrease in the ratios of lactic acid:acetic acid in untreated corn silage from approximately 3.0:1 to 2.3:1 and 1.3:1, for the low and high dose of L. buchneri, respectively. Practical recommendations in the field have suggested a desirable lactic acid:acetic acid ratio of more than 3:1 (Kung and Stokes, 2001), which would be an indication of a more dominant homolactic fermentation. However, it is now evident that silages treated with L. buchneri should not be held to this standard. In untreated grass and small-grain silages, the ratio of lactic acid:acetic acid was 5.3:1, and was markedly decreased to 0.8:1 for LB1 and further decreased to 0.6:1 for LB2. The actual concentration of acetic acid for grass and small-grain silages treated with LB2 was 4.31%. The positive relationship between silage DM from grass and small-grain silages that were inoculated and the resulting lactic acid:acetic acid ratio did not exist for untreated grass and small-grain silages or for corn silages. Specifically, Driehuis et al. (2001) found that the effects of L. buchneri on fermentation end-products in ryegrass increased as DM content decreased (range of 24.0 to 42.1% DM); however, a similar study has not been conducted with corn silage. It is unclear why such large inversions in the lactic acid:acetic acid ratio occurred in the treated grass and small-grain crops but not in treated corn silages, and the reasons for this difference should be investigated in the future.
Acetic acid has good antifungal properties, and increases in this acid should inhibit the growth of yeasts in silages (Woolford, 1975). In the summarized experiments, treatment of corn silage with the lower application rates of L. buchneri resulted in a 10-fold decrease in numbers of yeasts compared with the untreated silage, and treatment with LB2 decreased the numbers of yeasts more than 100-fold. Associated with these lower numbers of yeasts was an improvement in aerobic stability, but the effect was markedly greater (> 500 h of stability) in corn silage treated with the higher application rate (LB2). The relationship between numbers of yeasts in all corn silages and their concentrations of acetic are shown in Figure 2
. For small-grain and grass silages, yeasts were low even in untreated silages and aerobic stability was thus relatively high. However, addition of L. buchneri improved the aerobic stability of these silages by inhibiting the growth of yeasts from the environment after aerobic exposure, and the effect was greater at the higher level of application than at the lower rate of application. In corn and small-grain and grass silages, the aerobic stability of all silages was greater than the time that silage would normally be exposed to air in a feed bunk (i.e., more than 12 to 24 h). However, air is known to penetrate the silage mass before feeding and during prolonged storage. Therefore, situations may result in exposure to air well before actual feeding (e.g., rips in plastic, leaking silo doors, air penetrating between the plastic and silage, etc.); thus, the actual hours of aerobic stability should be viewed as relative.
Lactobacillus buchneri may also produce other antimicrobial substances that may be responsible for improved aerobic stability. For example, a bacteriocin, Buchnericin LB, was reported to be present in L. buchneri (Yildirim, 2001). This bacteriocin adsorbed to gram-positive bacteria but was unable to have the same effect on gram-negative bacteria, possibly due to a lack of receptors on these later organisms (Yildirim et al., 2002). To date, bacteriocins produced by strains of L. buchneri used as silage inoculants have not been identified.
Lactobacillus buchneri also produces 1,2-propanediol during the metabolism of lactic acid to acetic acid (Oude Elferink et al., 2001); however, it was not included in the meta-analysis because too few studies had reported its concentration. Concentrations of 1,2-propanediol as high as 2 to 4% of the DM have been reported in some studies (Driehuis et al., 2001; Nishino et al., 2002, 2003a, Nishino et al., b). This finding could have some implications when transition cows are fed large amounts of these silages, because 1,2-propanediol is often fed to prevent ketosis. This compound may also be converted to propionic acid by organisms other than L. buchneri (Driehuis et al., 1999a). Krooneman et al. (2002) isolated Lactobacillus diolivorans from silage and reported that it was capable of converting 1,2-propanediol to equimolar portions of 1-propanol and propionic acid, the latter being highly antimycotic. However, this conversion to propionic acid appears to be inconsistent in silages. For example, Driehuis et al. (2001) detected high amounts of propionic acid and 1-propanol in ryegrass silage treated with L. buchneri when ensiled at 23% DM. However, these end-products were not detected in treated rye-grass silage ensiled at 35% DM; instead, large quantities of 1,2-propanediol were detected in treated silage. In this summary, inoculation with L. buchneri did not affect the concentration of propionic acid in corn silage, but both levels of inoculation (LB1 and LB2) increased the concentration of this acid in grass and small-grain silages equally, indicating that the presence of organisms capable of converting 1,2-propanediol to propionic acid may be crop specific. Similarly, inoculation had no effect on the concentrations of ethanol or WSC in corn silage but appeared to stimulate ethanol production in grass and small-grain silages to a much greater extent than that theoretically expected. The observation that L. buchneri increased the concentration of ethanol in grass and small-grain but not corn silages may be explained by 2 theories. First, L. buchneri may have stimulated the production of ethanol in corn silage, as observed in grass and small-grain silages. However, this effect may have been masked by ethanol produced by the greater numbers of yeasts in corn silage, which were practically nonexistent in grass and small-grain silages. Second, treating grass and small-grain silage with L. buchneri decreased the concentration of WSC but no effect was observed in corn silage. Lactobacillus buchneri has a greater affinity for metabolizing lactic acid when the pH is at 3.8 (similar to corn silage) than when the pH is at 4.3 (similar to grass and small-grain silage; Oude Elferink et al., 2001). As a result, L. buchneri may utilize WSC more readily in silages, such as grass and small-grain silage, that are stored at a pH > 4.0. This may also increase the ethanol production in these silages because L. buchneri ferments WSC in a heterolactic fashion (Oude Elferink et al., 2001). These observations including the large inversions of lactic acid:acetic acid collectively emphasize that unknown factors specific to different crops and DM contents may affect how silages ferment when they are inoculated with L. buchneri, and such factors should be investigated further.
Preliminary concerns relative to the potential of large losses of DM from silages treated with L. buchneri because of its heterolactic nature do not appear to be substantiated by the results of the meta-analyses. The loss of DM in corn silage by the higher application of L. buchneri was 1 percentage point greater than for untreated silage. This occurrence was also observed in the grass and small-grain silages in that inoculation with L. buchneri, regardless of the application rate, increased the loss of DM by about 1.5 percentage points. Relative to the potential beneficial effects of improved aerobic stability during storage and feeding, those losses were small.
Concerns that high concentrations of acetic acid in silages treated with L. buchneri may depress intake could not be addressed by the meta-analysis because of the low number of studies. However, available research has shown that when cattle (Driehuis et al., 1999b; Kendall et al. 2002; Taylor et al., 2002; Kung et al., 2003b) and sheep (Ranjit et al., 2002) are fed silages treated with L. buchneri, DMI is not affected. Insufficient numbers of studies were available at the time of this review to perform a robust meta-analysis for the effects of L. buchneri on high-moisture corn and legume silages. In addition, at the time of this review L. buchneri was being sold commercially in combination with homolactic acid bacteria, but there were insufficient numbers of studies with this combination of bacteria to include them in the current meta-analysis.
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CONCLUSIONS
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The effects on the fermentation of corn and grass and small-grain silages when treated with L. buchneri were consistent in some but not all quantitative measurements, and certain responses appeared to be crop specific. In general, inoculation decreased the pH, concentrations of lactic acid, and numbers of yeasts, whereas it increased concentrations of acetic acid and aerobic stability in both types of crops. The higher rate of inoculation with L. buchneri was more consistently effective in corn silages than in grass and small-grain silages. This summary did not directly address the concern that silages that are high in acetic acid could reduce animal intake. However, it did show that the increases in the concentration of acetic acid by inoculation with L. buchneri are moderate. Inoculation increased the concentrations of propionic acid and ethanol and decreased the concentrations of WSC in grass and small-grain silages but not corn silages, suggesting a crop-specific effect. Although DM losses attributable to inoculation were significant, they were numerically small. The aerobic stability of silages was consistently improved with inoculation, and this effect was greater with an increasing rate of application for all crops.
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ACKNOWLEDGEMENTS
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The authors thank Normand St-Pierre of The Ohio State University for his assistance with statistical analyses.
Received for publication September 7, 2005.
Accepted for publication May 6, 2006.
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ABSTRACT
INTRODUCTION
