LARGE PARTICLE BREAKDOWN BY CATTLE EATING RYEGRASS AND ALFALFA
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1 LARGE PARTICLE BREAKDOWN BY CATTLE EATING RYEGRASS AND ALFALFA M. N. McLeod 1 and D. J. Minson: Brisbane, Queensland, Australia ABSTRACT The proportion of large particles (LP) broken down to small, insoluble particles by primary mastication (eating), rumination, digestion and detrition (rubbing) was determined for separated leaf and stem fractions of perennial ryegrass (Loliurn perenne) and alfalfa (Medicago sativa) fed to cattle cannulated at the esophagus. Large particles were defined as those particles retained during wet sieving on a screen with an aperture of 1.18 ram. Reduction in weight of particles caused by solubilizing or digestion was not considered to be particle breakdown per se, and particles were corrected for this loss in weight. The proportion of LP in the forage broken down by primary mastication was % (~ SE). Breakdown of LP by rumination was calculated from the weight of total particles regurgitated and the proportion of LP in the regurgitated and swallowed remasticated material. The weight of LP regurgitated was corrected for the dry matter lost by digestion using lignin ratio in the LP entering the rumen and of the regurgitated digesta. Rumination accounted for % of LP breakdown. Fecal loss accounted for % of the LP in forage. Breakdown of LP by digestion and detrition was calculated as % from the difference between the LP eaten and those broken down by primary mastication, rumination and passing out in the feces. The significance of these results for predicting voluntary intake from laboratory analysis is considered. (Key Words: Particle Size, Reduction, Forage, Steers, Intake, Digestibility.) I nt rod uet ion Voluntary intake by ruminants is limited by the quantity of forage particles and their rate of reduction in size within the rumen (Balch and Campling, 1962). Chewing during eating and during rumination is currently considered to be the only factor responsible for reducing the size of particles in the rumen (Ulyatt et al., 1986). Although microbial digestion makes a major contribution to reducing the dry weight of particles in the rumen and a small change in size in vitro (Murphy and Nicoletti, 1984), its contribution to particle size reduction in vivo is considered to be limited to a weakening of the forage cell-wall structure so that breakdown by rumination is facilitated (Ulyatt et al., 1986). The dismissal of digestion and detrition as potential mechanisms of large-particle breakdown in the rumen is rather surprising, because no attempt appears to have been made to determine whether chewing during eating and 1CSIRO, Div. of Tropical Crops and Pastures, Cunningham Laboratory, 306 Carmody Road, St. Lucia, Queensland 4067, Australia. Received January 12, Accepted November 5, rumination can account for au the breakdown of large particles (LP) in forage. This paper, which reports a study using four contrasting forage diets, aims at determining the proportion of large forage particles broken down by primary mastication (eating), rumination, digestion and detrition. Materials and Methods Pure swards of perennial ryegrass (Lolium perenne) and alfalfa (Medicago sativa) grown in southeast Queensland were cut at a vegetative stage, chopped to 2 to 4 cm lengths, dried at 100 ~ C and separated into leaf and stem fractions using a gravity seed separator (Laredo and Minson, 1973). The purity of the fractions was determined by hand separation into leaf lamina, leaf sheath and stem (including leaf petiole in the legume). Samples of the four diets were analyzed for neutral detergent fiber (ash-free, NDF; Van Soest and Wine, 1967), acid detergent fiber (ash-free, ADF), lignin (ash-free; Van 'Soest, 1963), and for N, P, Ca, S, K, Na, B, Cu, Mn and Zn by emission spectroscopy (Johnson and Simons, 1972). Other constituents of the plant were estimated as follows: hemicellulose = NDF (ash-free) - ADF (ash-free), cellulose = ADF (ash-free) -- lignin (ash-free) 992 J. Anim. Sci :
2 BREAKDOWN IN VIVO OF LARGE FORAGE PARTICLES 993 and neutral detergent soluble organic matter (NDSOM) = (NDF + feed-ash). Particle size of the four diets, digesta and feces was determined by the wet-sieving method described by Poppi et al. (1980). The method was modified to include the quantity of very small insoluble particles ("fines") that passed through the bottom (.15-mm) screen by collecting an aliquot of the water that circulated through the sieves and separating the particles by centrifugation. The particle size distribution in the sample was calculated as percentage (by weight) of the total weight of particles (including fines) present. Particle dry matter (DM) determined in this way did not include any water-soluble material. Large particles were defined as those particles that were retained on the top three sieves (4.75, 2.36 and 1.18 ram). These fractions had a high resistance to escape from the rumen of both sheep and cattle (Poppi et al., 1985). The four forages were fed to four mature Hereford steers (567 kg) with cannulas (40-mm diameter) at the esophagus. Steers were kept in metabolism cages and automatically fed 20% excess forage at hourly intervals using an automatic feeder (Minson and Cowper, 1977). Uneaten feed was automatically removed every hour, 5 min before fresh feed was offered. Water and salt (NaCI) were available continuously. The experimental treatment arrangement was a Latin square. Each steer was offered one of the four feeds during four periods, each lasting 15 d (7 d for adaptation and 8 d for measurements). The steers were weighed at the beginning and end of each period. Samples of feed, feed residues and feces were collected during the 8-d measurement period. Feces were stored at -5 ~ C until the end of the 8-d measurement period, when they were weighed and subsampled for DM determination. Samples of the masticated feed were obtained through the esophageal cannula and stored (-5 ~ C) before analysis for the proportion of LP as previously described. The proportion of dietary LP that was reduced to small particles by primary mastication (C) was calculated as fouows: Lp E - LP M C-- LP E where LPM = proportion by weight of LP in masticated feed partides swallowed and LPE = proportion by weight of LP in feed particles before eating. The quantity of LP broken down by primary mastication (P) and LP entering the rumen (A) was calculated as follows: P(g/d)=Fx C A(g/d)=F (1-C) and where F is the total quantity of LP eaten (g/d). The quantity of LP broken down by secondary mastication was determined by multiplying the quantity of LP regurgitated by the proportion of LP broken down during rumination. The quantity of forage LP regurgitated was calculated from the number of boll regurgitated each day, the average weight of these boll, the LP present and the extent to which the weight of the particles had been reduced by digestion. The number of boll regurgitated each day was determined by recording the characteristic pressure changes that occur in the esophagus using a pressure transducer connected to a chart recorder. Boll of regurgitated digesta (5.3 to 6.7% DM) were collected directly into a plastic container through an open esophageal cannula. Most of the regurgitated bolus appeared to be collected. For the measurement of breakdown of LP during chewing, the regurgitated digesta was allowed to pass into the mouth by dosing the esophageal cannula with the flat of the hand. A flexible plastic diverter tube (30 mm i.d.) was then inserted to divert the regurgitated digesta that was swallowed without chewing ("tail") and the boll of digesta that had undergone mastication. Some of the tail sample could not be collected, so no attempt was made to separate the tail from the chewed material. This swallowed material easily flowed through the diverter tube into a tared container. At least six replicates of regurgitated and returned digesta were collected from each steer for each feed. These were weighed and subsamples analyzed for DM, total particles (TP) and LP. The quantity of forage LP regurgitated in 24 h (R) was calculated from the number of boll regurgitated (B), their mean weight of DM, the proportion of this DM present as TP, the proportion of all particles that were present as large particles (LPr) and a correction for the loss in weight of the LP due to digestion in the rumen. The proportional loss in weight of LP
3 994 McLEOD AND MINSON by digestion was calculated from the lignin concentration in the LP entering the rumen (L a) and in the regurgitated feed (Lr). R (g/d) = B x mean bolus DM x TP LP r Lr/L a The quantity of LP broken down during rumination (S) was calculated from the weight of LP regurgitated (R) and the change in the proportion of the particles that were LP in the regurgitated digesta (LPr) and in the material returned to the rumen after mastication (LPs): R (LPr - LPs) S (g/d) = LPr The quantity of forage LP broken down by digestion (Di) plus detrition (Dr) was estimated as the difference between the quantity of LP eaten and the quantity of forage LP broken down by primary mastication (P), rumination (S) and the quantity of LP excreted in the feces (F) corrected for loss by digestion using the ratio of lignin in feed and feces LP: Di + Dr (g/d) = LP eaten - (P + S + F) The significance of differences between treatment means of the (4 x 4) Latin square design was measured by analysis of variance (Steel and Torrie, 1980). When the F test showed that differences between treatments were significant at the level of P <.05, Duncan's multiple range test was used to compare adjacent treatments when the treatments were arranged in order of magnitude. Results The four forages used in this study covered a fairly wide range of physical, chemical and nutritive values. Leaf varied from 9% to 90% and LP in the diet from 54% to 72% (Table 1). Cell contents, as measured by NDSOM, varied from 22% to 59%, and N varied from 1.6% to 3.4% (Table 1). Voluntary intake varied from 4,900 to 8,700 g/d, and digestibility of the DM varied from 51.8% to 66.9% (Table 2). The mean proportion of LP broken down to small particles during primary mastication was % (~ + SE; Table 2). This variation was due partly to a difference between the forages in breakdown of LP. The LP in the leaf fraction were broken to a greater extent than those in the stem fraction ( % vs %; P <.05), whereas the LP in the grass diets were broken to a greater extent than those in the legume diets ( % vs %; P <.05; Table 2). The net result of this difference in breakdown of LP was that, after masticating, the quantity of LP entering the rumen was not significantly different for the four forages (Table 2). The mean proportion of forage LP broken down by rumination was %. The only difference between the four forages was with the stem fraction of alfalfa, where breakdown of LP was 56.8%, compared with 46.8 to 48.6% for the other three forages (Table 3). This high breakdown of alfalfa stem during rumination was related to the low breakdown of LP during primary mastication. Breakdown of LP by digestion and detrition was calculated as the difference between the total LP eaten and the quantity broken down by mastication or passed out in the feces. The mean breakdown of LP to small particles by digestion and detrition was %. The difference between forages was small and not significant (Table 4). Discussion The importance of voluntary intake as a major factor limiting the nutritional value of forage probably was recognized first by Crampton (1957). This work stimulated studies on the mechanisms controlling voluntary intake, particularly the length of time forage particles were retained in the reticulo-rumen (rumen) and the concept that dietary residues must be reduced in particle size before they can pass out of the rumen (Balch and Campling, 1962). The main factor responsible for the reduction of food particles to a size sufficiently small to pass from the rumen was considered to be chewing during eating and rumination (Balch and Campling, 1962). The importance of physical breakdown was supported by the direct association between the total time spent in eating and ruminating each unit of forage with the rate at which digesta leaves the rumen (Freer et al., 1962) and, also, by the increase in voluntary intake found when roughages were ground and pelleted, a process that reduces the need for and extent of rumination (Minson, 1963). In this study, primary mastication during eating was found to be responsible for the breakdown of 25% of the LP in the forage, with breakdown being significantly higher in the leaf
4 BREAKDOWN IN VIVO OF LARGE FORAGE PARTICLES 995 TABLE 1. PHYSICAL CHARACTERISTICS a AND CHEMICAL COMPOSITION a OF THE FOUR CONTRASTING DIETS PRODUCED FROM FORAGES HARVESTED AT A VEGETATIVE STAGE OF GROWTH Measurement Leaf Stem Leaf Stem Physical characteristics Leaf, g/kg dry matter (DM) Stem, g/kg DM Total particles, g/kg DM b Large particles, g/kg DM Organic composition, g/kg DM NDSOM c NDF (ash-free) d ADF (ash-free) e Hemicellulose Cellulose Lignln Macroelements, g/kg DM Ash Nitrogen Phosphorus Calcium Sulfur Potassium Sodium Trace elements, mg/kg DM Copper Manganese Zinc O amean values of duplicate determinations. bdoes not include soluble DM removed during wet seiving. CNeutral detergent soluble organic matter. dneutral detergent fiber. eacid detergent fiber. TABLE 2. MEAN VOLUNTARY INTAKE AND DIGESTIBILITY OF DRY MATTER (DM) OF THE FOUR CONTRASTING FORAGES FED TO FOUR STEERS AND BREAKDOWN OF LARGE PARTICLES (LP) DURING PRIMARY MASTICATION Measurement Leaf Stem Leaf Stem SE c Intake of DM, g/d 8,712 a 7,038 ab 9,693 a 4,854 b 890 Digestible DM, % 54.1 ab 56.9 ab 66.9 b 51.8 a 4.0 Intake of LP, g/d 5,464 a 5,014 a 5,257 a 3,534 a 594 Proportion of LP eaten broken down, % 34.0 a 25.0 ab 26.5 a 16.7 b 2.7 LP entering rumen, g/d 3,605 a 3,758 a 3,865 a 2,943 a 345 a'bmeans in the same row without a common superscript differ (V <.05). CStandard error of mean; four observations per mean.
5 996 McLEOD AND MINSON Regurgitated digesta TABLE 3. LARGE PARTICLE (LP) BREAKDOWN IN FOUR FORAGES DURING RUMINATION BY FOUR STEERS Leaf Stem Leaf Stem SEd Number of boli/d (B) 572 a 504 ab 308 b 502 ab 56 Dry matter (DM) per bolus, g 27.8 a 24.4 a 30.4 a 27.3 a 3.8 Dry matter, g/d 15,902 a 12,298 a 9,363 a 13,705 a 2,452 LP in bolus, g/g DM.173 a.264 b.303 c.223 d.010 LP regurgitated, g/d 2,746 a 3,248 a 2,838 a 3,05 la 424 Digestion of LP from lignin ratio, % 30.3 a 18.O b 44.5 c 25.9 ab 3.5 Forage LP, R e, g/d 3,940 a 3,961 a 5,114 a 4,117 a 538 LP in total particles, regurgitated, % 21.5 a 31.8 b 36.6 b 33.6 b 1.6 Swallowed material after rumination, including "tail" LP in total particles, % 7.O a 12.4 ab 19.0 b 17.2 b 2.8 Proportion of LP regurgitated broken down, % 67.4 a 61.0 a 48.1 a 48.8 a 9.1 LP broken down by rumination, g/d 2,656 a 2,416 a 2,460 a 2,O09 a 512 Proportion of forage LP broken down by rumination, % 48.6 a 48.2 a 46.8 a 56.8 b 2.3 a'b'cmeans in the same row without a common superscript differ (P <.05). dstandard error of mean; four observations per mean. equantity of forage LP regurgitated after correction for loss of weight by digestion. fractions than in the stem fractions (Table 5). This level of breakdown by primary mastication is similar to values reported for mature temperature forages (30 to 40%; Lee and Pearce, 1984) and tropical forages (9 to 39%; Hendricksen et al., 1981; Poppi et al., 1981). Higher breakdowns have been found with temperate forages where more than 50% of the LP present were reduced to small particles (Gill et al., 1966; Reid et al., 1979; Ulyatt, 1983). This difference may have been caused by the high fiber and low digestibility of the forages used in our study. Rumination was responsible for the breakdown of a further 50% of the LP in the forages (Figure 1). Digestion is known to weaken forage structure so that breakdown during rumination is facilitated (Evans et al., 1973), but digestion is not considered to have a direct effect on LP breakdown in vivo. This study has demonstrated that mastication is not able to account for 17% of the observed breakdown of LP. It is suggested that this 17% loss of LP can be attributed to breakdown by digestion and detrition. This conclusion relies on several assumptions relating to the measurement of breakdown of LP during rumination. The first assumption is that the quantity of partially digested LP regurgitated can be converted, using the lignin ratio technique, back to the quantity of forage LP that gave rise to the regurgitated LP. The proportion of the regurgitated LP lost by digestion is calculated from the rise in the lignin concentration of the LP between entering the rumen and regurgitation. This approach relies on the assumption that, for the LP regurgitated, their lignin concentration before digestion is the same as
6 BREAKDOWN IN VIVO OF LARGE FORAGE PARTICLES 997 TABLE 4. LARGE PARTICLE (LP) BREAKDOWN IN FOUR FORAGES BY DIGESTION PLUS DETRITION Measurement Leaf Stem Leaf Stem SE e Intake of LP, g/d d 5,464 a 5,014 a 5,257 a 3,534 a 594 LP loss by Primary mastication, g/d d 1,859 a 1,256 a 1,392 a 591 a 349 Rumination, g/d e 2,656 a 2,416 a 2,460 a 2,009 a 512 Excreted in feces, g/d (corrected for digestion) 180 a 339 b 552 c 353 b 36 Total LP broken down by mastication or excreted, g/d 4,695 a 4,011 ab 4,404 a 2,953 b 384 LP broken down by digestion and detrition, g/d 769 a 1,003 a 853 a 581 a 147 Proportion of forage LP broken down by digestion plus detrition, % 14.1 a 20.0 a 16.2a 16.4a 4.4 a'bmeans in the same row without a common superscript differ (P <.05). Cstandard error of mean; four observations per mean. dfrom Table 2. efrom Table 3. the observed lignin concentration of the LP entering the rumen. This assumption can never be checked; but if there is an error, it would lead to an underestimation of the original lignin concentration of the regurgitated particles, because the LP most likely to survive to the stage of being regurgitated would be those with the highest lignin content. If this error occurred, digestion of regurgitated LP would be overestimated, leading to an overestimation of the loss of LP by rumination and, hence, to an underestimation of the contribution of digestion and detrition to LP breakdown. Another potential source of bias is the loss of lignin from LP in the rumen. If this had occurred, it would lead to an underestimation of the loss of LP by secondary mastication and to an overestimation of the importance of digestion and detrition. The third assumption relates to the extent of LP breakdown during rumination. This was determined as the difference in proportion of the total particles that were LP in both the regurgitated (up) and swallowed (down) material. There appears to be no problem in obtaining a representative sample of the material TABLE 5. SUMMARY OF PROPORTION OF LARGE FORAGE PARTICLES BROKEN DOWN BY DIFFERENT MECHANISMS Leaf Stem Leaf Stem Mean SE a Primary mastication, % Rumination, % Digestion and detrition, % Excreted in feces, % astandard error of mean; four observations per mean.
7 998 McLEOD AND MINSON Digestion ( plus Detrltlon 17% Eaten Primary 25% Mastication Secondary Mastication 50% Feces 8% Figure 1. Diagram showing the mean pathway of large particle breakdown of four contrasting forages by cattle. coming up because this was all collected, mixed and sampled for each regurgitation. However, with the material returning to the rumen, there were problems. A lot of the regurgitated material is immediately swallowed, and it is difficult to insert the diverter tube with sufficient speed to ensure that all this "taft" is collected. In this work, of the material regurgitated an average of % was collected in the down phase. Most of the material that escaped collection would have been the tail material. This has been shown to contain a higher proportion of LP than the following remasticated down material (Kennedy, 1985). Thus, the material actually collected would have tended to contain a lower proportion of LP than would have been found if all the tail material had been included. If this error had occurred, then the extent of breakdown of LP by secondary mastication shown in Table 3 would be an overestimation and the breakdown of LP by digestion and detrition would be underestimated. The maximum extent of this underestimation would be 5.7% of LP in the feed if all the material that failed to be collected was from the tail fraction and if the LP proportions in tail and down material published by Kennedy (1985) applied in this study. Digestion and detrition accounted for 17% of the breakdown of LP, but it would be wrong to conclude that this is the only important effect of digestion. Half the LP were broken down during secondary mastication, and all of these LP would have been softened to various extents by digestion. Thus, digestion contributed either directly or indirectly to the break- down of 67% of the LP in the forages studied, and this factor should be considered when developing laboratory methods to predict voluntary intake. This study has shown that the mode of LP breakdown is similar for all forages and, more importantly, that it is not related to voluntary intake. The lack of relation suggests that further work on the physiological mechanisms of LP breakdown are not likely to lead to principles that can be used in the design of laboratory techniques to estimate voluntary intake of forage. It appears that differences in intake are associated probably with the vascular material present in the forages, with the resistance of vascular material to breakdown by physical and microbial action and the combined effects of these two factors. The present work has established the relative importance of the factors that must now be incorporated in any laboratory technique to predict voluntary intake on a functional basis. It was concluded that the extent of LP breakdown by digestion and detrition was 17%, but this effect may be larger due to errors in the techniques adopted. Further work both in vivo and in vitro is required to confirm the present conclusions and the separate contributions of digestion and detrition to LP breakdown. Literature Cited Balch, C. C. and R. C. Campling Regulation of voluntary food intake in ruminants. Nutr. Abst. Rev. 32:609. Crampton, E. W Interrelations between digestible nutrient and energy content, voluntary dry matter intake and the overall feeding values of forages. J. Anita. Sci. 16:546. Evans, E. W., G. R. Pearce, J. Burnett and S. L. PiUinger Changes in some physical characteristics of the digesta in the reticulorumen of cows fed once daily. Br. J. Nutr. 29:357. Freer, M., R. C. Campling and C. C. Balch Factors affecting the voluntary intake of food by cows. 4. The behaviour and reticular motility of cows receiving diets of hay, oat straw and oat straw with urea. Br. J. Nutr. 16:279. Gill, J., R. C. Campling and D. R. Westgarth A study of chewing during eating in the cow. Br. J. Nutr. 20:13. Hendricksen, R. E., D. P. Poppi and D. J. Minson The voluntary intake, digestibility and retention time by cattle and sheep of stem and leaf fractions of a tropical legume (Lablab purpureus). Aust. J. Agric. Res. 32:389. Johnson, A. D. and J. G. Simons Direct reading emission spectroscopic analysis of plant tissue using a briquetting technique. Commun. Soil Sci.
8 BREAKDOWN IN VIVO OF LARGE FORAGE PARTICLES 999 Plant Anal. 3:1. Kennedy, P. M Effect of rumination on reduction of particle size of rumen digesta by cattle. Aust. J. Agric. Res. 36:819. Laredo, M. A. and D. J. Minson The voluntary intake, digestibility and retention time by sheep of leaf and stem fractions of five grasses. Aust. J. Agric. Res. 24:875. Lee, J. A. and G. R. Pearce The effectiveness of chewing during eating on particle size reduction of roughages by cattle. Aust. J. Agtic. Res. 35:609. Minson, D. J The effect of pelleting and wafering on the feeding values of roughages: A review. J. Br. Grassl. Soc. 18:39. Minson, D. J. and J. L. Cowper Equipment for automatically feeding forage to cattle at hourly intervals and removing uneaten feed. J. Anita. Sci. 44:814. Murphy, M. R. and J. M. Nicoletti Potential reduction of forage and rumen digesta particle size by microbial action. J. Dairy Sci. 67:1221. Poppi, D. P., R. E. Hendricksen and D. J. Minson The relative resistance to escape of leaf and stem particles from the tureen of cattle and sheep. J. Agric. Sci. (Camb.) 105:9. Poppi, D. P., D. J. Minson and J. H. Ternonth Studies of cattle and sheep eating leaf and stem fractions of grasses. IlL The retention time in the rumen of large feed particles. Aust. J. Agric. Res. 32:123. Poppi, D. P., B. W. Norton, D. J. Minson and R. E. Hendricksen The validity of the critical size theory for particles leaving the rumen. J. Agric. Sci. (Camb.) 94:275. Reid, C.S.W., A. John, M. J. Ulyatt, G. C. Waghorn and L. P. MiUigan Chewing and the physical breakdown of feed in sheep. Ann. Rech. Vet. 10:205. Steel, R.G.D. and J. H. Torrie Principles and Procedures of Statistics: A Biometrical Approach (2rid Ed.). McGraw-Hill Book Co., New York. Ulyatt, M. J Plant fibre and the regulation of digestion in the ruminant. In: G. Wallace and L. Bell (Ed.) Fibre in Human and Animal Nutrition. pp Royal Society of New Zealand, Bull. 20. The Royal Society of New Zealand, Wellington, New Zealand. Ulyatt, M. J., D. W. Dellow, A.'John, C.S.W. Reid and G. C. Waghorn Contribution of chewing during eating and rumination to the clearance of digesta from the ruminoreticulum. In: L. P. MiUigan, W. L. Grovum and A. Dobson (Ed.) Control of Digestion and Metabolism in Ruminants, pp Prentice-Hall, Englewood Cliffs, NJ. Van Soest, P. J Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fibre an lignin. J. Assoc. Off. Agric. Chem. 46:829. Van Soest, P. J. and R. H. Wine Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J. Assoc. Off. Anal. Chem. 50:50,
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