Short-term use of monensin and tannins as feed additives on digestibility and methanogenesis in cattle

ABSTRACT

The objective was to assess the effects short-term use of monensin and Acacia mearnsii tannins as feed additives on nutrient intake, digestibility, and CH₄ production in cattle. Six rumen-cannulated Holstein cows were distributed in two 3×3 Latin square experimental design, and each experimental period lasted 21 days. The basal diet was composed of corn silage and concentrate in a 50:50 dry matter (DM) basis proportion. Treatments were control, monensin (18 mg kg⁻¹ of DM), and tannin-rich extract from Acacia mearnsii (total tannins equivalent to 6 g kg⁻¹ of DM). Nutrient intake and apparent digestibility coefficients were not affected by the addition of monensin or tannins to diets. However, tannins showed a tendency to reduce crude protein digestibility. Monensin decreased CH₄ emission by 25.6% (g kg⁻¹ of body weight) compared with the control treatment. Monensin is more effective than Acacia mearnsii tannins in reducing CH₄ emissions in the short term, considering a diet of the same roughage:concentrate proportion for cattle.

Keywords:
animal nutrition; gas production; methane; ruminants

Introduction

Methane gas and its environmental effects, particularly on the greenhouse effect, have been increasingly studied, and strategies for emission reduction are increasingly sought (Guan et al., 2006; Wanapat et al., 2015). Methane is a byproduct of the ruminant digestive process and, depending on the components of the diets, its production might represent an energy loss of feed intake up to 2-12% (Johnson and Johnson, 1995).

Feed additives such as monensin are widely used to improve feed efficiency of ruminants; however, the use of this ionophore was banned by many countries, and alternatives have been studied (Wanapat et al., 2015), among them the use of Acacia mearnsii tannins (Carulla et al., 2005; Grainger et al., 2009). The extraction of tannins from Acacia mearnsii occurs on an industrial scale in Brazil, because they are widely used in leather tanning, effluent treatment, and in the food sector. Polyphenolic compounds are the main active substances of tannins, which can be classified into hydrolyzable (HT) and condensed (CT), depending on the molecule structural arrangement and the reactivity. Goel and Makkar (2012) highlighted that tannins have great potential to reduce CH₄ production; however, more research on cows is needed to know the best dosage without decreasing organic matter digestibility and animal production.

Studies carried out with monensin or tannins on enteric CH₄ mitigation demonstrated that additive effectiveness depends on the source and its dietary levels (Oliveira et al., 2005) and species and physiological state of the animals (Makkar, 2003a). According to Johnson and Johnson (1995), after a short-term use (30 days), CH₄ production levels return to those observed before monensin administration, probably due to the ability of the microbiota to adapt to the ionophore. Rumen microbes can adapt to tanniniferous diets by increasing the proportion of tannin-resistant bacteria in the rumen, therefore, mitigating the inhibitory effects of these secondary plant compounds (Smith et al., 2005). Staerfl et al. (2012) showed that Acacia mearnsii tannin extract might be useful to mitigate enteric CH₄ formation in maize silage-based diets in the long term (nine months). Therefore, it is important to evaluate its short-term effectiveness.

The hypothesis of this study is that the inclusion of monensin or low dose tannin extracts from Acacia mearnsii as feed additives in the short term can reduce methanogenesis without altering digestibility. The objective was to compare low-dose tannins to the known monensin effect on intake, digestibility, and methanogenesis in cattle.

Material and Methods

The trial was conducted in Pirassununga, state of São Paulo, southeastern Brazil (21°59′45″S, 47°25′37″ W, and 625 m above sea level). All procedures involving animal care were conducted in accordance with the Institutional Animal Care and Use Committee Guidelines (case no. 8580120514).

Six rumen-cannulated dry Holstein cows (average body weight [BW] = 784±87 kg) were randomly allocated in individual stalls with sand bed, fans, and ad libitum access to feed and water. The feed was offered twice daily at 08:00 and 16:00 h as a total mixed ration in a 50:50 (dry matter [DM] basis) roughage to concentrate ratio. The basal diet was formulated to meet NRC (2001) nutrient requirements recommended for dry cows (Table 1). Before the beginning of the experiment, the animals were fed only corn silage.

Table 1
Ingredients and chemical composition (DM basis) of the basal diet

Item		Basal diet
Ingredient (g kg−1 of DM)
	Corn silage	500
	Dry ground corn grain	347
	Soybean meal	122
	White salt	5
	Dicalcium phosphate	1
	Limestone	5
	Vitamin and mineral premix1	20
Chemical composition (g kg−1 of DM)
	Dry matter (g kg−1)	531
	Ash	76
	Ether extract	35
	Crude protein	120
	Neutral detergent fiber	271
	Acid detergent fiber	144
	Non-fibrous carbohydrates	498
	Total digestible nutrients	799

• ¹
  Composition of vitamin and mineral premix per kilogram of product: 200 g of Ca; 60 g of P; 20 g of S; 20 g of Mg; 70 g of Na; 15 mg of Co; 700 mg of Cu; 700 mg of Fe; 40 mg of I; 1,600 mg of Mn; 19 mg of Se; 2,500 mg of Zn; 200,000 IU of vitamin A; 50,000 IU of vitamin D3; 1,500 IU of vitamin E.

The experimental design was two 3×3 Latin squares with three treatments, and each experimental period of 21 days. The experimental diet was supplemented with the following feed additives: control (no additives), monensin (addition of 300 mg of sodium monensin per animal per day – equivalent to 18 mg kg⁻¹ of DM; Rumensin® 200, Elanco Animal Health, Brazil), or tannin (addition of 100 g tannin extract per animal per day – total tannins equivalent to 6 g kg⁻¹ of DM; tannin-rich extract obtained from Acacia-black, Acacia mearnsii; Veronese & Cia Ltda, Caxias do Sul, Brazil). The total phenol concentrations (895 g kg⁻¹ of extract) were determined by the Folin-Ciocalteau reagent method (Makkar, 2003b), and total tannins were estimated according to Makkar et al. (1993) as the difference in total phenol concentration before and after treatment with insoluble polyvinylpolypyrrolidone (873 g kg⁻¹ in tannic acid equivalents). The CT concentrations were determined according to Makkar (2003b) by the butanol-HCl method (339 g kg⁻¹ in leucocyanidin equivalents). The ionophore monensin was selected as strategy to decrease CH₄ emission to be a feasible feed additive commonly used in beef and dairy production (Guan et al., 2006). The additives were hand-mixed with concentrate mixture first, then with corn silage to obtain the total mixed diet.

The monensin dose was chosen based on the review of Beauchemin et al. (2008). According to these authors, who evaluated the same additive of this study, doses of 15 mg kg⁻¹ of DM do not affect the CH₄ production, but doses of 15 to 20 mg kg⁻¹ of DM can reduce the total CH₄ production in dairy cattle. Grainger et al. (2009), using 9 g kg⁻¹ DM of Acacia mearnsii CT extract, observed reduction in feed intake. Perna Junior (2018) used different levels of total tannins (0, 5, 10, and 15 g kg⁻¹ of DM), the same additive of this study, and found linear reduction for neutral detergent fiber (NDF), organic matter (OM), and crude protein (CP) digestibility. Therefore, to minimize the negative effect on DM intake (DMI) and digestibility, a lower level of supplementation was used in this study (total tannins equivalent to 6 g kg⁻¹ of DM or CT equivalent to 2 g kg⁻¹ of DM). Soltan et al. (2017) reported that many phenolic compounds act against methanogens and may decrease CH₄ emission without affecting ruminal nutrient degradability or total digestibility. Additionally, a study with feedlot Holstein steers fed diets containing low HT or CT extract (6 g kg⁻¹ of DM) did not show any difference in tannin source on growth and DMI, but inclusion of tannins or its combination increased animal performance compared with the control treatment (Rivera-Méndez et al., 2017). Given this information, we did not use a purified source of CT as the basis for this study.

All feeders were examined every morning at 08.00 h. From the 15th to the 21st day of each period, the feed refusal of each cow was weighed and discounted from the offered in the bunker. The amount of diet offered was adjusted daily, allowing for a minimum of 5% and maximum of 10% of refusal throughout the experiment. This was multiplied by DM content of feed.

The total tract apparent digestibility of diet and its fractions were determined by chromium oxide (Cr₂O₃) marker as described in Bateman (1970). Briefly, chromium oxide (7.5 g) was provided through ruminal cannula at 08.00 and 16.00 h from day 5 until day 14. Fecal samples (200 g) were collected directly from the rectum of each cow twice daily from the 10th to 14th day. Digestibility was performed during this period so as not to interfere with CH₄ collection. The samples were placed in plastic bags and stored in a freezer at −20 °C for chemical analysis. The basal diet used in this trial was also sampled for further analysis.

At the end of each collection period, composite feed and feces samples were homogenized and dried in a forced-air oven at 55 °C for 72h. They were then ground in a mill (using a 1-mm sieve and placed in closed vessels) for subsequent determinations of the following: DM (method number 967.03; AOAC, 1990); ash (method number 923.03; AOAC, 1990); CP (method number 920.87; AOAC, 1990); ether extract (EE), determined gravimetrically after extraction using ether in a Soxhlet extractor (method number 920.85; AOAC, 1990); NDF assayed using heat stable amylase and acid detergent fiber (ADF) were analyzed according to Van Soest et al. (1991), both expressed excluding residual ash contents (Mertens, 2002).

Based on the feedstuff chemical composition, the nutrient digestibility was calculated as described: Digestibility (%) = 100 − [100 × (Cr₂O₃ on feed (%) / Cr₂O₃ on feces (%) × (Nutrient on feces (%) / Nutrient on feed (%)]. Non-fibrous carbohydrates (NFC) were calculated as proposed by Sniffen et al. (1992): NFC = 100 – (CP% + EE% + ash% + NDF%). Total digestible nutrients (TDN) were calculated by using the equation TDN = digestible CP + (2.25 × digestible EE) + digestible NDF + digestible NFC, according to NRC (2001).

To determine enteric CH₄, the sulfur hexafluoride (SF₆) tracer technique was used, as described by Johnson and Johnson (1995) and adapted in Brazil by Primavesi et al. (2004). Prior to the onset of methane collection, SF₆ permeation capsules, previously identified, were loaded and calibrated with constant and known release rates of SF₆ and then inserted in the rumen. The animals were adapted to the canisters during five days (10th to 14th) prior to collection, and then gas samples were collected over 24-h intervals for seven consecutive days, starting from the 15th experimental day. Concentrations of CH₄ and SF₆ were determined by gas chromatograph (HP6890, Agilent, Delaware, USA).

The CH₄ emission was calculated by dividing the release rate of SF₆ by the SF₆/CH₄ concentration ratio in the canisters. The potential emission of CH₄ was then expressed in several ways: grams per day (g day⁻¹); grams per hour (g h⁻¹); grams per kilogram of body weight (g kg⁻¹ of BW); grams per kilogram of metabolic weight (g kg⁻¹ of BW^0.75); grams per kilogram of dry matter intake (g kg⁻¹ of DMI); grams per kilogram of organic matter intake (g kg⁻¹ of OMI); grams per kilogram of digestible organic matter (g kg⁻¹ of DOM); percentage of gross energy lost as CH₄ (% GE), which considered the gross energy intake as calculated from the organic matter intake; and percentage of digestible energy lost as CH₄ (% DE). The conversion of CH₄ from grams to energy unit was performed according to the conversion factor, stated by Holter and Young (1992), in which CH₄ produces 0.0556 Mcal g⁻¹ when it is burned.

Data were statistically analyzed using the SAS software (Statistical Analysis System, version 9.3). Before the actual analysis, the data were analyzed for the presence of disparate information (“outliers”) and normality of residuals (Shapiro-Wilk). Individual observation was considered outlier when standard deviations in relation to mean was bigger than +3 or less than −3. When the normality assumption was not accepted, the logarithmic transformation or the square root was required. The data were analyzed according to the following model:

(1) $${\text{Y}}_{\text{ijkl}}=\text{μ}+{\text{T}}_{\text{i}}+{\text{P}}_{\text{j}}+{\text{S}}_{\text{k}}+{\text{A}}_{\text{l}}\left({\text{S}}_{\text{k}}\right)+{\text{ε}}_{\text{ijkl}}$$

in which Y_ijkl = dependent variable, μ = general mean, T_i = treatment effect (fixed effect), P_j = period effect (random effect), S_k = square effect (random effect), A_l(S_k) = animal within square effect (random effect), and ε_ijkl = random error associated with each observation.

The experimental unit was the animal within period, wherein each animal received a different treatment in each period. Therefore, there were six observations per treatment, totaling 18 experimental units. Treatments were evaluated by the least significance difference (LSD) test using 0.05 significance level.

Results

The DMI was not affected (P>0.05) when monensin or tannins were added to the diet. Treatments did not affect (P>0.05) intake of different nutrients, total tract apparent digestibility, and GE intake. However, tannins tended to reduce digestibility of CP (P = 0.08) by 2.8% compared with control (Table 2). Monensin decreased CH₄ emission (P<0.05) when expressed in g day⁻¹, g kg⁻¹ of BW, g kg⁻¹ of BW^0.75, and less energy was lost as CH₄ (MJ day⁻¹) compared with the control treatment (24.3, 25.6, 24.1, and 23.5%, respectively). Additionally, monensin tended to decrease (P = 0.09) CH₄ production in relation to the digested OM by 25% compared with the control (Table 3).

Table 2
Effect of short-term use of monensin and Acacia mearnsii tannins on feed intake and total tract apparent digestibility in cattle

Item		Treatment			SEM	P-value
		Control	Monensin	Tannin
Dry matter intake
	kg day−1	18.02	16.89	17.03	0.44	0.338
	g kg−1 of BW0.75	113.07	105.36	106.36	2.96	0.193
Daily nutrient intake (kg day−1)
	Organic matter	16.85	16.01	16.47	0.39	0.529
	Crude protein	2.15	2.03	2.09	0.05	0.488
	Neutral detergent fiber	5.78	5.49	5.65	0.13	0.497
	Acid detergent fiber	3.47	3.29	3.40	0.08	0.486
	Ether extract	0.56	0.53	0.55	0.01	0.466
	Gross energy (MJ day−1)	320.6	304.8	314.3	1.71	0.527
Total tract apparent digestibility (g g−1)
	Dry matter	0.816	0.833	0.798	0.101	0.307
	Organic matter	0.823	0.841	0.805	0.099	0.255
	Crude protein	0.796	0.820	0.774	0.090	0.082
	Neutral detergent fiber	0.740	0.752	0.702	0.160	0.362
	Acid detergent fiber	0.742	0.753	0.691	0.184	0.265
	Ether extract	0.875	0.895	0.872	0.066	0.157
	Gross energy	0.815	0.834	0.797	0.100	0.258

• BW^0.75 - metabolic body weight; SEM - standard error of the mean.
• Within rows, values with different letters are statistically different (P<0.05).

Table 3
Effect of short-term use of monensin and Acacia mearnsii tannins on methane production in cattle

CH4 production1	Treatment			SEM	P-value
	Control	Monensin	Tannin
g day−1	373.9a	282.9b	334.0ab	17.87	0.045
g kg−1 BW	0.43a	0.32b	0.38ab	0.01	0.037
g kg−1 BW0.75	2.32a	1.76b	2.08ab	0.09	0.038
g kg−1 DMI	20.69	16.81	19.93	0.96	0.200
g kg−1 OMI	22.07	17.74	20.54	0.98	0.182
g kg−1 DOM	38.92	29.17	38.69	2.03	0.099
% GE	6.43	5.22	6.18	0.30	0.209
% DE	11.76	8.82	12.00	0.62	0.084
MJ day−1	20.59a	15.75b	18.38ab	0.23	0.045

• SEM - standard error of the mean.
• ¹
  Methane emission in grams per day (g day⁻¹), grams per kilogram of body weight (g kg⁻¹ BW), grams per kilogram of metabolic weight (g kg⁻¹ BW^0.75), grams per kilogram of DM intake (g kg⁻¹ DMI), grams per kilogram of organic matter intake (g kg⁻¹ OMI), grams per kilogram of digestible organic matter (g kg⁻¹ DOM), percentage of gross energy lost as methane (% GE), percentage of digestible energy lost as methane (% DE).
• Within rows, values with different letters are statistically different (P<0.05).

Discussion

The present experiment showed that the use of monensin at 18 mg kg⁻¹ of DM does not influence changes in DMI and nutrient intake nor in digestibility, as shown by other studies (Oliveira et al., 2005; Fonseca et al., 2016). This fact is attributed to the action of monensin in altering the proportion of rumen microorganisms, and consequently, the proportion of short-chain fatty acids (SCFA) and byproducts (i.e., H₂, CO₂, CH₄) formed from feed fermentation (Nagaraja and Taylor, 1987), but without significantly affecting the digestion, passage rate, and feed intake (Bretschneider et al., 2008). Similar results were reported by other authors in bulls (Fonseca et al., 2016) and Holstein cows in lactation (Eifert et al., 2005).

As observed for monensin, the inclusion of tannin did not affect the intake and apparent digestibility of nutrients in cows. Studies demonstrated that CT in high concentrations in ruminant diets binds fiber, metal ions, polysaccharides, and proteins, and mainly, form complexes that hinder the action of ruminal bacteria, with consequent decreases in ruminal digestibility of nutrients (Grainger et al., 2009). Additionally, CT decreased total apparent digestibility and increased excretion of nutrients in feces (Carulla et al., 2005; Abdalla et al., 2007; Tiemann et al., 2008). However, in lower doses, tannins can act beneficially on feed digestion and rumen metabolism (Waghorn and Shelton, 1997), without altering intake and apparent digestibility of nutrients (Beauchemin et al., 2007). In the present study, even using a small amount of tannins, there was a tendency to reduce digestibility of CP by 2.8% compared with the control.

Formation of tannin-nutrient complexes, mainly with protein, may improve synchronization of available protein and energy for microbial protein production by improving the efficiency of synthesis (Makkar, 2003a). Furthermore, tannin-protein complexes of low pH (1.0 to 3.0), found in the abomasum of ruminants, are almost completely undone (Leinmüller et al., 1991), and protein are released and digested by gut proteases (Sliwinski et al., 2002). Thus, the tannin amount used in the present study was not sufficient to alter the intake and apparent digestibility of nutrients. Studies with tannin inclusion similar to the present study, for cows (Beauchemin et al., 2007) and lambs (Sliwinski et al., 2002), did not report alteration in intake and digestibility. However, studies that reported decrease of intake and/or digestibility offered greater amount of inclusion, just as in cows (Grainger et al., 2009) and in sheep (Carulla et al., 2005; Abdalla et al., 2007).

The dietary inclusion of monensin decreased CH₄ production, when expressed in g day⁻¹, g kg⁻¹ of BW, and g kg⁻¹ of BW^0.75, in relation to control by 24.3, 25.6, and 24.1%, respectively. Additionally, tannin-fed cows exhibited intermediate values of CH₄ production. According to Soltan et al. (2018), CH₄ emission is expressed in different ways, but determined CH₄ emission relative to the digested OM may become more persuading than determining CH₄ relative to the unit of the animal's daily production. In the present study, monensin, besides reducing CH₄ in relation to animal weight, showed tendency to reduce CH₄ by digested OM.

Monensin inhibits the growth of some gram-positive bacteria, such as Eubacterium, Lactobacillus, and Streptococcus, which produce acetic acid and other compounds such as H₂ (Chen and Wolin, 1979), and improves the growth of gram-negative bacteria, which produce propionic acid. Furthermore, there are indications that monensin has direct effect on ciliated protozoa by inhibiting its development and reducing the consequent production of H₂ (Hino, 1981; Russell and Strobel, 1989). Thus, the formation of ruminal CH₄ is lower due to the lack of H₂, the primary substrate for this synthesis (Buddle et al., 2011). Fonseca et al. (2016) found a decrease on daily CH₄ production in bulls when feeding monensin (22 mg kg⁻¹ of DM) at similar levels of the current study.

Studies suggest that tannins could act in two ways on methanogenesis: first, directly on methanogenic archaea by reducing CH₄ formation (Tavendale et al., 2005); second, by indirectly reducing the primary substrate for the CH₄ formation, mainly H₂ (Goel and Makkar, 2012). In the second case, tannins might form complexes with the feed (i.e., protein and fiber), preventing the action of bacteria, mainly cellulolytic (Bento et al., 2005), and consequently reducing the formation of acetic acid and other products such as H₂ and NH₃ (Tiemann et al., 2008). Carulla et al. (2005) fed sheep diets supplemented with Acacia mearnsii CT at dose of 25 g kg⁻¹ of DM and reported reduction in daily CH₄ production (L day⁻¹) by 7 and 12% reduction when CH₄ production was expressed in relation to DMI. However, the authors observed a decrease in digestibility by approximately 5%, suggesting that the tannins indeed form a complex with dietary nutrients, but probably in lower concentrations than at lower intensity without impairing the digestibility of nutrients. In fact, we observed in the present study that, when total tannins from Acacia mearnsii were used at dose of 6 g kg⁻¹ of DM, it did not interfere with digestibility of nutrients. However, the potential to reduce the CH₄ production was not efficient when compared with higher doses. Although not significant, doses of tannins used in the present study suggest that this is the starting point for reduction of CH₄ production in cattle.

Conclusions

Feed supplementation with monensin (18 mg kg⁻¹ of DM) or Acacia mearnsii extract (total tannins equivalent to 6 g kg⁻¹ of DM) in short-term use does not alter feed intake or the apparent digestibility of nutrients by cattle. At the levels of additives used, monensin is more effective than tannins in reducing CH₄ emissions in the short term.

Acknowledgments

The Universidade de São Paulo (USP) and Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA) for providing the infrastructure and staff necessary for this study. In addition, the authors express their appreciation to the Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for providing the financial support.

References

• AOAC - Association of Official Analytical Chemistry. 1990. Official methods of analysis. 15th ed. AOAC International, Arlington, VA.
• Abdalla, A. L.; Godoy, P. B.; Longo, C.; Araujo Neto, J. C.; Peçanha, M. R. S. R.; Bueno, I. C. S.; Vitti, D. M. S. S. and Sallam, S. M. A. 2007. Methane emission, protozoa and methanogens counts in sheep fed coconut oil or a Brazilian tannin-rich plant (Mimosa casealpineaefolia). Microbial Ecology in Health and Disease 19:33. https://doi.org/10.1080/08910600701231465
  » https://doi.org/10.1080/08910600701231465
• Bateman, J. V. 1970. Determinación de óxido crómico en alimento y heces - (H₂SO₄⁺ HClO₄); la digestibilidad aparente; prueba de digestibilidad. p.404-450. In: Nutrición animal. Manual de métodos analíticos. Bateman, J. V., ed. Herrero Hermano, México.
• Beauchemin, K. A.; McGinn, S. M.; Martinez, T. F. and McAllister, T. A. 2007. Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle. Journal of Animal Science 85:1990-1996. https://doi.org/10.2527/jas.2006-686
  » https://doi.org/10.2527/jas.2006-686
• Beauchemin, K. A.; Kreuzer, M.; O'Mara, F. and McAllister, T. A. 2008. Nutritional management for enteric methane abatement: a review. Australian Journal of Experimental Agriculture 48:21-27. https://doi.org/10.1071/EA07199
  » https://doi.org/10.1071/EA07199
• Bento, M. H. L.; Acamovic, T. and Makkar, H. P. S. 2005. The influence of tannin, pectin and polyethylene glycol on attachment of 15N-labelled rumen microorganisms to cellulose. Animal Feed Science and Technology 122:41-57. https://doi.org/10.1016/j.anifeedsci.2005.04.010
  » https://doi.org/10.1016/j.anifeedsci.2005.04.010
• Bretschneider, G.; Elizalde, J. C. and Pérez, F. A. 2008. The effect of feeding antibiotic growth promoters on the performance of beef cattle consuming forage-based diets: a review. Livestock Science 114:135-149. https://doi.org/10.1016/j.livsci.2007.12.017
  » https://doi.org/10.1016/j.livsci.2007.12.017
• Buddle, B. M.; Denis, M.; Attwood, G. T.; Altermann, E.; Janssen, P. H.; Ronimus, R. S.; Pinares-Patiño, C. S.; Muetzel, S. and Wedlock, D. N. 2011. Strategies to reduce methane emissions from farmed ruminants grazing on pasture. The Veterinary Journal 188:11-17.
• Carulla, J. E.; Kreuzer, M.; Machmuller, A. and Hess, H. D. 2005. Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Australian Journal of Agricultural Research 56:961-970. https://doi.org/10.1071/AR05022
  » https://doi.org/10.1071/AR05022
• Chen, M. and Wolin, M. J. 1979. Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Applied and Environmental Microbiology 38:72-77. https://doi.org/10.1128/AEM.38.1.72-77.1979
  » https://doi.org/10.1128/AEM.38.1.72-77.1979
• Eifert, E. C.; Lana, R. P.; Leão, M. I.; Arcuri, P. B.; Valadares Filho, S. C.; Leopoldino, W. M.; Oliveira, J. S. and Sampaio, C. B. 2005. Efeito da combinação de óleo de soja e monensina na dieta sobre o consumo de matéria seca e a digestão em vacas lactantes. Revista Brasileira de Zootecnia 34:297-308. https://doi.org/10.1590/S1516-35982005000100034
  » https://doi.org/10.1590/S1516-35982005000100034
• Fonseca, M. P.; Borges, A. L. C. C.; Silva, R. R.; Lage, H. F.; Ferreira, A. L.; Lopes, F. C. F.; Pancoti, C. G. and Rodrigues, J. A. S. 2016. Intake, apparent digestibility, and methane emission in bulls receiving a feed supplement of monensin, virginiamycin, or a combination. Animal Production Science 56:1041-1045. https://doi.org/10.1071/AN14742
  » https://doi.org/10.1071/AN14742
• Goel, G. and Makkar, H. P. S. 2012. Methane mitigation from ruminants using tannins and saponins. Tropical Animal Health and Production 44:729-739. https://doi.org/10.1007/s11250-011-9966-2
  » https://doi.org/10.1007/s11250-011-9966-2
• Grainger, C.; Clarke, T.; Auldist, M. J.; Beauchemin, K. A.; McGinn, S. M.; Waghorn, G. C. and Eckard, R. J. 2009. Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows. Canadian Journal of Animal Science 89:241-251. https://doi.org/10.4141/CJAS08110
  » https://doi.org/10.4141/CJAS08110
• Guan, H.; Wittenberg, K. M.; Ominski, K. H. and Krause, D. O. 2006. Efficacy of ionophores in cattle diets for mitigation of enteric methane. Journal of Animal Science 84:1896-1906. https://doi.org/10.2527/jas.2005-652
  » https://doi.org/10.2527/jas.2005-652
• Hino, T. 1981. Action of monensin on rumen protozoa. Japanese Society of Animal Science 52:171-179.
• Holter, J. B. and Young, A. J. 1992. Methane prediction in dry and lactating Holstein cows. Journal of Dairy Science 75:2165-2175. https://doi.org/10.3168/jds.S0022-0302(92)77976-4
  » https://doi.org/10.3168/jds.S0022-0302(92)77976-4
• Johnson, K. A. and Johnson, D. E. 1995. Methane emissions from cattle. Journal of Animal Science 73:2483-2492. https://doi.org/10.2527/1995.7382483x
  » https://doi.org/10.2527/1995.7382483x
• Leinmüller, E.; Steingass, H. and Menke, K. 1991. Tannin in ruminant feedstuffs. Animal Research and Development 33:9-62.
• Makkar, H. P. S.; Blümmel, M.; Borowy, N. K. and Becker, K. 1993. Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture 61:161-165. https://doi.org/10.1002/jsfa.2740610205
  » https://doi.org/10.1002/jsfa.2740610205
• Makkar, H. P. S. 2003a. Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin rich feeds. Small Ruminant Research 49:241-256. https://doi.org/10.1016/S0921-4488(03)00142-1
  » https://doi.org/10.1016/S0921-4488(03)00142-1
• Makkar, H. P. S. 2003b. Quantification of tannins in tree and shrub foliage: A laboratory manual. Springer, Netherlands. https://doi.org/10.1007/978-94-017-0273-7
  » https://doi.org/10.1007/978-94-017-0273-7
• Mertens, D. R. 2002. Gravimetric determination of amylase-treated neutral detergent fiber in feed with refluxing beakers or crucibles: Collaborative study. Journal AOAC International 85:1217-1240.
• Nagaraja, T. G. and Taylor, M. B. 1987. Susceptibility and resistance of ruminal bacteria to antimicrobial feed additives. Applied and Environmental Microbiology 53:1620-1625.
• NRC - National Research Council. 2001. Nutrient requirements of dairy cattle. 7th ed. National Academy Press, Washington, DC.
• Oliveira, M. V. M.; Lana, R. P.; Freitas, A. W. P.; Eifert, E. C.; Pereira, J. C.; Valadares Filho, S. C. and Pérez, J. R. O. 2005. Parâmetros ruminal, sangüíneo e urinário e digestibilidade de nutrientes em novilhas leiteiras recebendo diferentes níveis de monensina. Revista Brasileira de Zootecnia 34:2143-2154. https://doi.org/10.1590/S1516-35982005000600040
  » https://doi.org/10.1590/S1516-35982005000600040
• Perna Junior, F. 2018. Taninos como aditivo alimentar para mitigação das emissões de metano em ruminantes. Tese (D. Sc.). Universidade de São Paulo, Pirassununga. https://doi.org/10.11606/T.10.2018.tde-20082018-160632
  » https://doi.org/10.11606/T.10.2018.tde-20082018-160632
• Primavesi, O.; Frighetto, R. T. S.; Pedreira, M. S.; Lima, M. A.; Berchielli, T. T.; Demarchi, J. J. A. A.; Manella, M. Q.; Barbosa, P. F.; Johnson, K. A. and Westberg, H. H. 2004. Técnica do gás traçador SF₆ para medição de campo do metano ruminal em bovinos: adaptações para o Brasil. Embrapa Pecuária Sudeste, São Carlos.
• Rivera-Méndez, C.; Plascencia, A.; Torrentera, N. and Zinn, R. A. 2017. Effect of level and source of supplemental tannin on growth performance of steers during the late finishing phase. Journal of Applied Animal Research 45:199-203. https://doi.org/10.1080/09712119.2016.1141776
  » https://doi.org/10.1080/09712119.2016.1141776
• Russell, J. B. and Strobel, H. J. 1989. Effect of ionophores on ruminal fermentation. Applied and Environmental Microbiology 55:1-6.
• Sliwinski, B. J.; Soliva, C. R.; Machmuller, A. and Kreuzer, M. 2002. Efficacy of plant extracts rich in secondary constituents to modify rumen fermentation. Animal Feed Science and Technology 101:101-114. https://doi.org/10.1016/S0377-8401(02)00139-6
  » https://doi.org/10.1016/S0377-8401(02)00139-6
• Smith, A. H.; Zoetendal, E. and Mackie, R. I. 2005. Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microbial Ecology 50:197-205. https://doi.org/10.1007/s00248-004-0180-x
  » https://doi.org/10.1007/s00248-004-0180-x
• Sniffen, C. J.; O'Connor, J. D.; Van Soest, P. J.; Fox, D. G. and Russell, J. B. 1992. A net carbohydrate and protein system for evaluating cattle diets. II. Carbohydrate and protein availability. Journal of Animal Science 70:3562-3577. https://doi.org/10.2527/1992.70113562x
  » https://doi.org/10.2527/1992.70113562x
• Soltan, Y. A.; Morsy, A. S.; Lucas, R. C. and Abdalla, A. L. 2017. Potential of mimosine of Leucaena leucocephala for modulating ruminal nutrient degradability and methanogenesis. Animal Feed Science and Technology 223:30-41. https://doi.org/10.1016/j.anifeedsci.2016.11.003
  » https://doi.org/10.1016/j.anifeedsci.2016.11.003
• Soltan, Y. A.; Hashem, N. M.; Morsy, A. S.; El-Azrak, K. M.; Nour El-Din, A. and Sallam, S. M. 2018. Comparative effects of Moringa oleifera root bark and monensin supplementations on ruminal fermentation, nutrient digestibility and growth performance of growing lambs. Animal Feed Science and Technology 235:189-201. https://doi.org/10.1016/j.anifeedsci.2017.11.021
  » https://doi.org/10.1016/j.anifeedsci.2017.11.021
• Staerfl, S. M.; Zeitz, J. O.; Kreuzer, M. and Soliva, C. R. 2012. Methane conversion rate of bulls fattened on grass or maize silage as compared with the IPCC default values, and the long-term methane mitigation efficiency of adding acacia tannin, garlic, maca and lupine. Agriculture, Ecosystems and Environment 148:111-120. https://doi.org/10.1016/j.agee.2011.11.003
  » https://doi.org/10.1016/j.agee.2011.11.003
• Tavendale, M. H.; Meagher, L. P.; Pacheco, D.; Walker, N.; Attwood, G. T. and Sivakumaran, S. 2005. Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123-124:403-419. https://doi.org/10.1016/j.anifeedsci.2005.04.037
  » https://doi.org/10.1016/j.anifeedsci.2005.04.037
• Tiemann, T. T.; Lascano, C. E.; Wettstein, H. R.; Mayer, A. C.; Kreuzer, M. and Hess, H. D. 2008. Effect of the tropical tannin-rich shrub legumes Calliandra calothyrsus and Flemingia macrophylla on methane emission and nitrogen and energy balance in growing lambs. Animal 2:790-799. https://doi.org/10.1017/S1751731108001791
  » https://doi.org/10.1017/S1751731108001791
• Van Soest, P. J.; Robertson, J. B. and Lewis, B. A. 1991. Methods of dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74:3583-3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
  » https://doi.org/10.3168/jds.S0022-0302(91)78551-2
• Waghorn, G. C. and Shelton, I. D. 1997. Effect of condensed tannins in Lotus corniculatus on the nutritive value of pasture for sheep. The Journal of Agricultural Science 128:365-372. https://doi.org/10.1017/S0021859697004218
  » https://doi.org/10.1017/S0021859697004218
• Wanapat, M.; Cherdthong, A.; Phesatcha, K. and Kang, S. 2015. Dietary sources and their effects on animal production and environmental sustainability. Animal Nutrition 1:96-103. https://doi.org/10.1016/j.aninu.2015.07.004
  » https://doi.org/10.1016/j.aninu.2015.07.004

Publication Dates

• Publication in this collection
  22 May 2020
• Date of issue
  2020

History

• Received
  06 May 2019
• Accepted
  19 Feb 2020