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The effect of a condensed tannin-containing forage on methane emission by goats¹

E (Kika) de la Garza American Institute for Goat Research, Langston University, Langston, OK 73050

	Abstract

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The objective of this study was to compare methane emission by goats consuming the condensed tannin-containing forage sericea lespedeza (Les-pedeza cuneata) or a mixture of crabgrass (Digitaria ischaemum) and Kentucky 31 tall fescue (Festuca arundinacea). Two groups of 12 Angora does (initial average BW = 41.5 ± 2.7 kg) that previously grazed a pasture of sericea lespedeza or crabgrass/tall fescue for approximately 4 mo were used. After 1 wk of adaptation to metabolism cages, gas exchange was measured for 24 h in an open-circuit respiration calorimetry system with four head boxes. Forage harvested daily from the previously grazed pastures was consumed ad libitum. Crude protein concentration was 10.3 and 13.0%, IVDMD was 64.5 and 75.3%, and the level of condensed tannins was 17.7 and 0.5% for sericea lespedeza and crabgrass/tall fescue, respectively. Dry matter intake (1.11 vs. 0.67 kg/d) and digestible DMI (estimated from IVDMD; 0.71 vs. 0.51 kg/d) were greater (P < 0.01) for sericea lespedeza than for crabgrass/tall fescue. Ruminal ammonia N (3.7 and 9.9 mg/dL; P < 0.001) and plasma urea-N concentrations (16.7 and 20.9 mg/dL; P = 0.07) were lower for sericea lespedeza than for crabgrass/tall fescue. Concentrations of individual and total VFA and the acetate-to-propionate ratio in ruminal fluid did not differ between treatments (P > 0.19). Despite higher DMI by goats fed sericea lespedeza, daily energy expenditure (409 vs. 431 kJ/kg BW^0.75), heart rate (70 vs. 73 beats/min), and the ratio of energy expenditure to heart rate (5.82 vs. 5.94) did not differ between sericea lespedeza and crabgrass/tall fescue, respectively (P > 0.13). Methane emission expressed as both quantity per day or relative to DMI was lower (P <0.001) for sericea lespedeza than for crabgrass/tall fescue (7.4 vs. 10.6 g/d and 6.9 vs. 16.2 g/kg DMI). Substantial differences between the forages in condensed tannins concentration and methane emission by Angora goats suggest that condensed tannins decreased methane emission.

Key Words: Condensed Tannins • Energy Expenditure • Goats • Methane

	Introduction

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There have been recent reports of lower methane emissions by ruminants consuming forages containing low or moderate vs. negligible levels of condensed tannins (CT), determined in vitro and in vivo with cattle (Roth et al., 2001; Woodward et al., 2001, 2002). Condensed tannins are found in a multitude of plants around the globe. Therefore, if established that CT can consistently and on a long-term basis decrease methane production by ruminants, there is potential for widespread use and marked effect.

Effects of CT in ruminants vary with the type of tannin or plant source. One CT-containing plant prevalent in many areas of the United States is sericea lespedeza (Lespedeza cuneata). Similar to variation among plants and CT, different ruminant species vary in responses to CT. Compared with other ruminants, goats are relatively less affected by antinutritional factors in many plants because of factors such as differences in salivary proteins (Foley et al., 1999). Therefore, in addition to the potential direct importance to goat farming, studying effects of feeding plants containing CT to goats has merit with respect to reasonable expectations of similar effects with cattle and sheep. However, with cattle and sheep, it is expected that magnitudes of change in methane emission and intake of plants high in CT may be different than with goats. The objective of this experiment was to compare the effect of sericea lespedeza, containing CT, with a mixture of forages having a negligible concentration of CT on methane emission by goats.

	Materials and Methods

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The Langston University Animal Care Committee approved the experimental protocol. Twenty-four Angora does (41.5 ± 2.7 kg BW) were allocated to two treatments: consumption of sericea lespedeza or crab-grass/tall fescue forage. Twelve does had previously grazed a predominantly sericea lespedeza pasture (1 ha) for 4 mo, and the other 12 does had grazed a pasture (1 ha) with crabgrass (Digitaria ischaemum) and Kentucky 31 tall fescue (Festuca arundinacea) forages (approximately 1:1 mixture). The initial allocation of does to the two pasture treatments was random. In the present experiment, does remained on the same forage treatments, but with different housing and feeding conditions. The experiment was conducted in early September through mid-October of 2002, and all forage harvested and fed consisted of regrowth vegetation. One week before measurements started, goats were placed in metabolism cages (1.05 m x 0.55 m) in an enclosed facility, to which they had previous exposure. During adjustment to metabolic cages and measurement periods, goats were fed forage harvested daily using a small self-propelled sickle bar mower (BCS 850, BCS, Harvard, MA), at an approximate height of 6 cm, from pastures previously grazed. Animals were fed for ad libitum intake at 0830, 1200, and 1700 daily, with forages offered at approximately 110% of consumption on the preceding few days. Angora does had free access to water during the adjustment to metabolic cages, and water was provided four times daily during the 24-h measurement period.

After adjustment to metabolic cages, does were randomly allocated to six animal sets, each consisting of two does that had grazed sericea lespedeza and two from the crabgrass/tall fescue pasture. The sets were randomly assigned to six measurement days. For a 24-h period, goats were placed in a four-animal head box open-circuit respiration calorimetry system (Sable System Int., Henderson, NV) with continued ad libitum consumption. Before gas exchange measurements, CO₂ production and O₂ consumption were checked via an ethanol burn test (101.3 ± 1.1 and 100.3 ± 1.6% of expected CO₂ production and O₂ consumption, respectively). Analyzers were calibrated with gases of known concentrations. The Brouwer (1965) equation, without including urinary N, was used to calculate energy expenditure.

In addition to gas exchange measurement, heart rate was monitored with stick-on ECG electrodes attached to the chest just behind and slightly below the left elbow and at the base of the jugular groove on the right side of the neck. The human S610 heart rate monitor system of Polar Electro (Woodbury, NY) was used, with measures taken at 1-min intervals. Heart rate was measured because of its relationship to energy expenditure (Brosh et al., 1998) and as a part of a broader effort to characterize potential factors, such as diet, that might influence this relationship in goats. Immediately after gas exchange and heart rate measurements and before feeding at approximately 0800, ruminal fluid was sampled via stomach tube and blood via jugular venipuncture. Blood was collected into a 7-mL tube containing sodium heparin (Becton Dickinson, Vaccutainer Systems, Rutherford, NJ), which was immediately chilled in an ice bath, transported to the laboratory, and centrifuged at 1,500 xg and 4°C for 20 min. Plasma was stored at –20°C until analyses. Five milliliters of ruminal fluid was mixed with 1 mL of 25% (wt/vol) metaphosphoric acid and used for VFA analysis; another 5 mL of ruminal fluid was mixed with 2 mL of 50% HCl and used for ammonia-N analysis. Forage offered and orts were weighed daily to measure DMI.

Dietary forage samples collected daily during the measurement period were frozen, lyophilized, and ground to pass a 1-mm screen. The DM content was determined by drying at 95°C for 17 h. The Kjeldahl digestion method was used for CP analysis, and the concentration of OM was determined by ashing in a muffle furnace at 550°C for 12 h (AOAC, 1990). Concentrations of NDF, ADF (nonsequential), and IVDMD were determined by the Filter Bag Technique of AN-KOM Technology Corp. (Fairport, NY). Ruminal fluid for IVDMD was collected in the morning from four ruminally fistulated goats grazing a warm-season grass-based pasture. In vitro DM digestion was determined with 48 h of incubation using a DaisyII system (Ankom Technology Corp.), with residual DM assessed as NDF. The CT concentration in sericea lespedeza and crab-grass/tall fescue forages was determined with the butanol-HCl colorimetric procedure of Terrill et al. (1992), using CT extracted (Sephadex LH-20, Sigma Chemical Co., St. Louis, MO) from sericea lespedeza as the standard (Jackson et al., 1996).

Plasma urea-N was quantified as described by Chaney and Marbach (1962). Ruminal fluid samples were analyzed for VFA (Goetsch and Galyean, 1983) and ammonia-N (Chaney and Marbach, 1962a). Volatile fatty acids analysis entailed centrifugation of the ruminal fluid/metaphosphoric acid solution for 20 min at 10,000 xg. Supernatant fluid was subjected to gas chromatography (Hewlett-Packard Co., Avondale, PA) using a 1.98 m x4 mm i.d. glass column packed with 15% SP-1200 plus 1% H₃PO₄ on 100/120 Chromosorb W AW (Supelco Inc., Bellefonte, PA). Data were analyzed as a completely randomized design experiment by GLM procedures of SAS (Version 8e, SAS Inst., Inc., Cary, NC), with the model consisting of treatment.

	Results

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The concentrations of CP, NDF, ADF, and IVDMD were generally lower for sericea lespedeza than for crab-grass/tall fescue (Table 1), but the concentration of CT in sericea lespedeza was higher. Body weight did not differ between treatments (P = 0.46), but goats offered sericea lespedeza had higher DMI and digestible DMI (P < 0.01) than those fed crabgrass/tall fescue forage (Table 2). Methane production (g/d) was lower (P < 0.001) for goats fed sericea lespedeza than for the crab-grass/tall fescue forage diet. When methane emission was expressed per unit of DMI or digestible DMI, methane production was much lower for sericea lespedeza than the for crabgrass/tall fescue forage (P < 0.001). Daily energy expenditure, heart rate, and the ratio of energy expenditure to heart rate did not differ between treatments (P > 0.13). Molar concentrations of ruminal VFA were not affected by treatment (Table 3; P > 0.19); however, the concentration of ammonia-N in ruminal fluid was lower (P < 0.001) for sericea lespedeza than for crabgrass/tall fescue. Moreover, plasma urea-N concentration tended to be lower (P = 0.06) for the sericea lespedeza than for the crabgrass/tall fescue diet.

	Discussion

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Based on IVDMD, and assuming complete digestion of cell solubles, it would seem that NDF in sericea lespedeza was of very low digestibility (i.e., 40.1%) compared with crabgrass/tall fescue NDF (i.e., 55.7%). Legumes typically have higher lignin concentrations than grasses, and forage fed in this experiment was sampled after the major warm-season growing period of sericea lespedeza. These factors suggest low digestibility of NDF of sericea lespedeza; however, lignin of legumes influences digestibility of other cell wall constituents less adversely than lignin of grasses (Traxler et. al., 1998). Therefore, this predicted digestibility of sericea lespedeza NDF seems lower than expected. In this regard, as mentioned subsequently, it is possible that CT in sericea lespedeza negatively affected in vitro digestion; however, it is unknown whether similar effects occurred in vivo in animals of this experiment fed sericea lespedeza. Concentrations of NDF and ADF in sericea lespedeza were similar, which probably relates to the presence of CT. Van Soest (1994) reported that CT are partially soluble in neutral detergent but precipitate as tannin-protein complexes in acid detergent.

The difference between treatments in DMI was of similar magnitude to that observed previously while the does were grazing (1.9 and 1.6 kg of DM/d for sericea lespedeza and crabgrass/tall fescue, respectively; Min et al., 2004). Likewise, there are other reports of relatively high intake of forage containing CT. For example, Woodward et al. (2001) noted greater intake by dairy cows of CT-containing Lotus corniculatus and pedunculatus than of ryegrass. Athanasiadou et al. (2001) reported an increased consumption of a high-protein diet by sheep when quebracho CT were included at 6% of the diet (fresh weight basis). However, there are also reports of intake of CT-containing forage being similar to or lower than that of forage low in CT (Barry and McNabb, 1999; Landau et al., 2000; Woodward et al., 2001). These varied results probably reflect different dietary levels of CT, as well as variation among plants in CT biological activity (Min et al., 2003).

Instances when forage CT positively affected feed intake, and also when intake was not influenced but animal performance was improved, are most likely because of increased intestinal AA absorption resulting from low to moderate binding of protein by CT (Waghorn et al., 1987). Observations of decreased forage intake seem to be the result of excessive protein binding by CT, resulting in deleterious effects on ruminal and/or intestinal digestion, nutrient absorption, or endogenous protein loss (Barry and Duncan, 1984). In the present experiment, because intake was greater for sericea lespedeza vs. crabgrass/tall fescue, and because performance was greater for sericea lespedeza in the preceding 4 mo of grazing (Min et al., 2003), it would seem that protein binding of sericea lespedeza CT increased intestinal AA absorption (Waghorn, 1996) without severely depressing digestion or adversely affecting other physiological conditions. Increased intestinal AA absorption and decreased ruminal protein degradation are supported by lower concentrations of ammonia-N in ruminal fluid and urea-N in plasma of goats fed sericea lespedeza, with much greater differences between forages than expected based on the ratio of forage CP concentration to IVDMD (i.e., 0.160 and 0.173 for sericea lespedeza and crabgrass/tall fescue, respectively). In support of this idea, Molan et al. (2001) and Min et al. (2000, 2002), using in vitro and in situ techniques, respectively, showed that for CT-containing plants there was decreased ruminal degradation of plant protein to ammonia compared with CT-free plants because of slower rates of both solubilization and degradation. Similarly, in vitro ruminal protein degradation rate and predicted ruminal escape protein were 27 and 18%/h for white clover (Trifolium repens L.) compared with 1 and 96%/h for sericea lespedeza (L. cuneata var. Dum.-Cours), respectively (Broderick and Albrecht, 1997). Min et al. (1998) noted that ewes grazing the CT-containing forage Lotus corniculatus had lower ruminal ammonia and blood urea concentrations than ewes grazing CT-free forage, with no difference in VFA concentration.

Other sources of CT, when included in diets at low levels compared with sericea lespedeza of this experiment, have adversely affected intake or digestion (Barry and McNabb, 1999; Landau et al., 2000). Therefore, based on the high level of hydrolyzed CT in sericea lespedeza, and the high intake compared with crab-grass/tall fescue, it would seem that potential adverse effects of sericea lespedeza CT are relatively low on a per-unit-of-CT basis.

The degree to which methane emission was less for sericea lespedeza compared with crabgrass/tall fescue on an absolute basis (i.e., 30%) became much greater when expressed relative to intake of total (57%) and digestible DMI (50%). Somewhat smaller differences have been previously observed. For example, Woodward et al. (2001) reported that in sheep, methane emission relative to digestible DMI was decreased by 24 to 29% when the CT-containing forage Lotus pedunculatus was fed compared with ryegrass or lucerne. A similar decrease (23%) in methane emission relative to DMI was observed by the same authors when cows were fed Lotus corniculatus silage compared with ryegrass silage. Differences between studies may be attributable to different levels of CT, with a higher concentration in sericea lespedeza (17.7% CT) of the present experiment, compared with Lotus pedunculatus (8% CT) or Lotus corniculatus (2.6% CT) of these other studies.

Methane emission relative to DE intake is typically less for legumes vs. grasses (Benchaar et al., 2001). In addition, methane emission per unit of total or DE intake decreases with increasing level of intake (Johnson and Johnson, 1995). Although it is not possible to definitively partition the contribution of CT to the difference in methane emission in this experiment, the magnitude of difference and relatively small possible influences of other factors suggest an effect of CT.

	Implications

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These results suggest the potential for condensed tannins in forages such as sericea lespedeza to minimize methane emission by ruminants, in addition to other benefits when not included at a high percentage of the diet, such as increased intestinal amino acid absorption. Research is needed to identify the mode of action of condensed tannins in decreasing methane emission, as well as to characterize effects of different types and levels of condensed tannins to develop practical means of exploitation.

	Footnotes

 
¹ This research was supported by USDA Project Number 00-38814-9500. Appreciation is expressed to farm and laboratory personnel of the E (Kika) de la Garza American Institute for Goat Research for their assistance.

³ Current address: Texas A & M Agric. Res. and Ext. Center, P.O. Box 1658, Vernon, TX 76385.

² Correspondence: P.O. Box 730 (phone: 405-466-3836; fax: 405-466-3138; e-mail: rpuchala{at}luresext.edu).

Received for publication February 9, 2004. Accepted for publication October 11, 2004.

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