Factors Affecting the Mean Retention Time of Particles in the Forestomach of Ruminants and Camelids

20 Factors Affecting the Mean Retention Time of Particles in the Forestomach of Ruminants and Camelids M. Lechner-Doll, M. Kaske, and W. v. Engelhardt Department of Physiology School of Veterinary Medicine Hannover, Germany I. Introduction 455 II. Mean Retention Time of Digesta in the Forestomach 456 A. Some Methodological Aspects of the Estimation of Digesta Mean Retention Time 456 B. Influence of Feed Intake 458 C. Selective Retention of Feed Particles 458 D. Species Differences 459 III. Effects of Particle Size and Particle Density on Mean Retention Time in the Forestomach 463 A. Particle Size 463 B. Breakdown of Particles 465 C. Particle Density 467 D. Distribution of Particles in the Reticulorumen 470 E. The Quantitative Contributions of Particle Size and Particle Density to the Mean Retention Time 471 F. Separation of Particles in the Reticulorumen 472 IV. Present Understanding 474 References 475

I. Introduction The advantage forestomach fermenters have over potential monogastric competitors is their superior ability to utilize plant cell walls. The evolu­ tionary success of the ruminant family was initiated about 8 million years ago (Janis 1976) when a savannah-type of vegetation arose during a period of relative aridity. The microbial degradation of cell wall constituents is a relatively slow process. To achieve effective cellulose digestion, ruminants and camelids Physiological Aspects of Digestion and Metabolism in Ruminants: Proceedings of the Seventh International Symposium on Ruminant Physiology Copyright© 1991 by Academic Press, Inc. All rights of reproduction in any form reserved.

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evolved large fermentation chambers in their stomachs, and they retain feed particles substantially longer than fluid in these chambers. This strategy has two consequences: (1) a long mean retention time (MRT) of feed particles in the reticulorumen (RR) will improve the utilization of cell-wall constituents; however, (2) a long MRT may restrict feed intake, because intake of roughage is limited mostly by the capacity of the foresto­ mach (Waldo 1986). Many attempts have been made to predict forage intake in ruminants (Waldo et al. 1972; Neal et al. 1984; Hodgson 1985; Caird and Homes 1986; Cochran et al. 1986; Murphy et al. 1986; Quigley et al. 1986b; Waldo 1986; Erdman et al. 1987; Ewing and Johnson 1987; Mertens 1987; Pond et al. 1988) and to find ways of increasing the intake of roughage (Santini et al. 1983; Quigley et al. 1986a Williams et al. 1989). The objective of this paper is to discuss factors that determine MRT of fluid and particles in the forestomach of ruminants and camelids. The term forestomach in the following text refers to the reticulorumen of the ruminant species and to the forestomach compartments 1 and 2 of camelids. ;

II. Mean Retention Time of Digesta in the Forestomach MRT of fluid and of digesta particles in the forestomach is generally related to the forestomach capacity, the level of intake, and the digesti­ bility of the diet ingested. Furthermore, MRT of digesta particles in the forestomach of ruminants fed a roughage-based diet may differ consider­ ably between the various ruminant species according to whether they are concentrate selectors, intermediate feeders, or grazers (Hofmann and Ste­ wart 1972).

A. Some Methodological Aspects of the Estimation of Digesta Mean Retention Time 1. Estimation of digesta mean retention time using markers The use of fluid markers in rate-of-passage studies (polyethylene glycol, chromium-EDTA, cobalt-EDTA) is well established; comparable results are obtained with different markers (Uden et al. 1980; Warner 1981). The estimation of particle MRT is more difficult. Particle markers may trans­ fer to the fluid phase or to other particles, making an accurate estimation of feed-particle MRT impossible (Uden et al. 1980; Ehle et al. 1984; Poncet and Al Abd 1984; Erdman and Smith 1985; Faichney 1986; Kennedy and Murphy 1988). Furthermore, some particle markers (e.g., chromium) may alter the physical properties of the particles labeled, especially their den­ sity. The density of particles tends to increase during the labeling proce-

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dure (Ehle et al. 1984; Lindberg 1985, 1988), which may result in a higher passage rate (Evans et al. 1973; Lindberg 1985; Kaske and Engelhardt 1990); that is, the MRT of the labeled particle fraction may be different from the MRT of natural, unlabeled feed particles. Results of studies using labeled particles to estimate MRT of feed particles should therefore be treated with caution. However, the method is valuable to quantify relative changes of particle MRT and relative differences between animal species (Warner 1981). More accurate results can be obtained by the direct determination of particle pool sizes in the forestomach using indigestible lignin as a refer­ ence substance (Faichney 1986; Kennedy and Murphy 1988). This method requires emptying of the forestomach or the use of an appropriate doublemarker method for the determination of pool sizes; another requirement is the continuous feeding of a diet of known composition (Faichney et al. 1990). 2. Mathematical approaches for the estimation of marker mean retention times in the forestomach MRT of markers in the entire gastrointestinal tract can be readily calcu­ lated by integration of the fecal marker excretion curve (Coombe and Kay 1965; Thielemans et al. 1978; Faichney 1975, 1986). The results of at­ tempts to estimate the MRT of particles in the forestomach from the pattern of fecal excretion of particle markers (Grovum and Williams 1973) are questionable, mainly because of inadequacies in the mathematical approaches used to describe patterns of marker excretion (Faichney and Boston 1983; Faichney 1986; Kennedy and Murphy 1988; Pond et al. 1988; Murphy et al. 1989). It is easy to determine the MRT of the fluid fraction of the digesta in the forestomach from the dilution curve of a water-soluble marker, as the curve fits a simple monoexponential function (Faichney 1975). For the solids fraction, however, the difficulty of obtaining representative samples of the particulate matter in forestomach contents limits the accuracy of particle-marker dilution curves. Furthermore, the dilution curve for marked particles does not normally fit a simple exponential function (O'Connor et al. 1984; Faichney 1986; Faichney et al. 1990). A minimum of two different particle pools has to be distinguished (see below); this leads to deviation of the particle markers' concentration curve from the simple one-pool kinetic of fluid markers in the forestomach. In practice, for most cases where MRT of particles in the forestomach is of interest, the measurement of fluid and particle MRT in the entire gastrointestinal tract and the estimation of fluid MRT in the forestomach is likely to be sufficient. Forestomach MRT of particles can then be estimated by difference, assuming a similar MRT of fluid and particle markers distal to the forestomach (Lechner-Doll et al. 1990).

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Β. Influence of Feed Intake Most investigators have found that MRT of particles and of fluid decreases when level of feed intake increases (Thornton and Minson 1972; Grovum and Williams 1977; Mudgal et al. 1982; Faichney 1983; White et al. 1984; Ledoux et al. 1985; Aitchison et al. 1986; Faichney and Gherardi 1986; Merchen et al. 1986; Shaver et al. 1986; Waghorn et al. 1986; Funk et al. 1987; Deswysen and Ellis 1988; Lindberg 1988; Uden, 1988). However, doubling the intake leads to only a 2 0 - 4 0 % decrease of particle MRT in the forestomach; and some investigators have not found any significant effect of the intake level on MRT (Ulyatt et al. 1984; Van Vuuren 1984). The inconsistency of these findings may be partly explained by variable, unknown changes of the forestomach volume in response to variations of the intake level. Increasing forestomach volumes were observed with increasing intake (Grovum and Williams 1977; Mudgal et al. 1982; Ulyatt et al. 1984; Aitchison et al. 1986; Shaver et al. 1986; Lindberg 1988). Such an increased forestomach volume may partly compensate for the effect of the higher intake level on MRT. Higher passage rates at the higher intake levels are the result of larger amounts of digesta leaving the RR during each motility cycle,- the number of motility cycles is not markedly affected (Ulyatt et al. 1984; Deswysen et al. 1987). Because of the shorter MRT of digesta, microbial fiber diges­ tion in the RR will be reduced; this may be partly compensated for by higher microbial activity in the hindgut. However, total digestibility of dry matter is often decreased by about 2 to 7% at higher intake levels (Colucci et al. 1982; Staples et al. 1984; McCollum and Galyean 1985a,b; Aitchison et al. 1986; Faichney and Gherardi 1986; Firkins et al. 1986; Fadlalla and Kay 1987; Shaver et al. 1986, 1988).

C. Selective Retention of Feed Particles Feed particles are selectively retained in the forestomach of ruminants and camelids. A comparison of the retention times of fluid and labeled small particles in the forestomach of cattle, sheep, goats, and camels is shown in Figure 1. Fluid MRT in the forestomach (approximately 10 hr) was similar in all the four species, studied on a thornbush savannah pasture of North­ ern Kenya. The labeled particles, on the other hand, were retained sub­ stantially longer than the fluid and longer in the cattle (28 hr) and camels (25 hr) than in the sheep and goats (both 20 hr). The ratio particle MRT: fluid MRT (Fig. 1) was consequently greater in the cattle and camels than in the sheep and goats. In the cattle and camels, the labeled particles were retained about 3 times longer than fluid, but in the sheep and goats, only 1.6 times longer. This implies that particles were more selectively retained in the forestomach of cattle and camels compared to sheep and goats.

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• I Fluid

EES Particles (2 mm)

40^

a D Ε ο -+-> w

30 Η

20 Α

JZ

(Τ 2

MRT port. MRT fluid

"I

0 - 1 — ™2.8 Cattle

1.6 Sheep

ι

1.7 Goats

3.2 Camels

Figure 1. Mean retention times (MRT) of fluid and of feed particles in the forestomach of cattle, sheep, goats, and camels foraging on a thornbush savannah pasture in Northern Kenya. MRT were measured in animals with forestomach fistulae using Co-EDTA or CrEDTA as fluid markers and Ce-labeled particles ground to pass a 2-mm screen as the particle marker; error bars: SEM. From Lechner-Doll et al. (1990).

The effectiveness of the selection mechanism by which feed particles are retained longer than fluid does not change markedly when MRT varies due to variations of the intake level or to feed quality (Grovum and Williams 1977; Fadlalla et al 1987; Lindberg 1988; Lechner-Doll et al 1990). Factors determining and affecting the selectivity of particle reten­ tion will be discussed below.

D. Species Differences 1. Feeding habits Ruminants are classified according to morphological criteria and feeding habits into browsing concentrate selectors, intermediate feeders, and grazers (Hofmann and Stewart 1972). Concentrate selectors like roe deer or dik-dik select a diet of plants with a relatively high digestibility (Kay et al 1980; Maloiy et al 1988). Their forestomachs have comparatively simple anatomical structures (Hofmann 1988; Langer 1988). Forestomach volumes are relatively small, and forestomach contents account for only 7 to 8% of body weight (Giesecke and van Gylswyk 1975; Hoppe et al 1977; Clemens and Maloiy 1983; Hofmann 1988; Langer 1988; Maloiy et al 1988). Most of the smaller ruminant species are concentrate selectors,their high-energy demand can best be met by a high-quality, easily digesti-

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ble feed with a low fiber content. The concentrate selectors do not need a long MRT of digesta particles in their forestomach for the microbial degradation of cell-wall constituents. Although concentrate selectors are mostly small and include the very small ruminant species, some large ruminants such as the giraffe and the moose are also included in this group. The large group of intermediate feeders (e.g., goat, elk, sika and red deer, Grant's gazelle, and impala) have developed a feeding strategy between the extremes of concentrate selectors and grazers (Coppock et al. 1986a,b, Hofmann 1988; Howe et al. 1988). Within a limited range, they are able to change their feeding habits. According to the feeding situation, they may behave more like concentrate selectors or more like grazers. The grazers (e.g., cattle, bison, buffalo, and most of domestic sheep) are phylogenetically the younger ruminant species. Grazers are well adapted to utilize poor-quality fibrous feed, having developed large, wellsubdivided fermentation chambers (Hofmann 1988; Langer 1988). Fore­ stomach contents in grazers may account for approximately 15 to 20% of body weight (Giesecke and van Gylswyk 1975; Hoppe 1984; Huston et al. 1986). RR fluid volumes of up to 32% of body weight have been reported for indigenous sheep on a poor-quality fibrous diet (Weyreter et al. 1987). Because of the large capacity of their forestomachs and their efficient selective retention of particles, grazers are able to retain feed particles in their forestomachs for a longer time, exposing them longer to fermenta­ tion and rumination. Grazers are thus better able to utilize fibrous feed than are concentrate selectors. 2. Adaptation to changes of forage composition The influence of feed quality on rumen kinetics is demonstrated by the results of an experiment where (1) feed quality in a grazing area changed through the year, and (2) the responses of four different species with different feeding habits were compared. The study area was the thornbush savannah of Northern Kenya. The forestomach volume and digesta flow parameters were determined in cattle, sheep, goats, and camels during the green and the dry seasons (Lechner-Doll et al. 1990). During the green season, good-quality forage was plentiful. During the dry season, feed was limited, and grasses in particular had a low digestibility. In all four species, MRT of small particles was significantly longer in the dry season than in the green season (Fig. 2). The increase of particle MRT during dry season was significantly higher in cattle and sheep (plus 27% and plus 46%, respectively) than in goats and camels (23% and 18%, respectively). These differences appear to reflect the different feeding hab­ its of the animals. Cattle, and to some extent sheep, feed predominantly on monocotyledons. Monocotyledons undergo more drastic seasonal changes in quality than do the dicotyledons preferred by goats and camels (Rutagwenda 1989). The cattle spent more than 97% of their feeding time grazing on monocotyledons in both the green and the dry season, while the

2 0 Retention Time of Particles in the Forestomach • I Green season

461 E 3 Dry season

50

Cattle

Sheep

Goats

Camels

Figure 2. Mean retention times (MRT) of labeled particles in the forestomach of cattle, sheep, goats, and camels foraging in a thornbush savannah in Northern Kenya during the green and dry seasons. Particle MRT were estimated in animals fitted with forestomach fistulae. Ce-labeled particles ground to pass a 2-mm screen were used as the particle marker; error bars: SEM. From Lechner-Doll et al (1990).

sheep spent 50% of their feeding time grazing on monocotyledons in the dry, and 35% in the green season. Goats and camels, on the other hand, preferred dicotyledons of better quality in both seasons. Goats spent only 8% of their feeding time grazing on monocotyledons in the dry season, and camels less than 3%. The cattle and sheep consequently were confronted with more severe seasonal changes in the digestibility of their diet than were the goats and camels. Increasing the MRT of particles would be an effective strategy for im­ proving the utilization of low-quality feed in the dry season. Such a strategy would be especially important for cattle and sheep. Camels and goats, on the other hand, with their ability to browse, are able to select plants of a better quality during the dry season (Coppock et al. 1986a,b; Schwartz 1988; Rutagwenda et al. 1990). For browsers, therefore, an in­ crease of MRT of particles during the dry season is not so important as it is for grazers. The increase of MRT of particles in the foregoing experiment was ac­ companied by an increase in forestomach volume. Parallel to the increase in particle MRT, the forestomach fluid volume increased in all four spe­ cies during the dry season (Fig. 3). During the green season, cattle, sheep, goats, and camels had a proportionally similar volume of fluid in their forestomach, about 10% of body weight. The volume increase during the dry season was relatively greater in the cattle and sheep (39% and 55% of the green season value, respectively) than in the goats and camels (both 28% of the green season value).

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• 1 Green season

E 3 Dry season

25 τ

—

Φ

Cattle

Sheep

Goats

Camels

Figure 3. Fluid volume of the forestomach of cattle, sheep, goats, and of camels foraging on a thornbush savannah pasture in Northern Kenya during the green and dry seasons. Fluid volumes were estimated in animals fitted with forestomach fistulae using Cr-EDTA or Co-EDTA as fluid markers; error bars: SEM. From Lechner-Doll et al. (1990).

Although the intake level was not measured in these experiments, the remarkable parallelism between changes of forestomach fluid volume and MRT of particles in response to seasonal changes of feed quality indicated that the longer MRT in the dry season was not primarily the effect of a lower feed intake. These results are consistent with findings of McCollum and Galyean (1985b); with increasing maturity of the pasture, voluntary forage intake of steers grazing blue grama rangeland declined only slightly. As an effect of the reduced forage digestibility, higher levels of RR fill were found, with longer retention time of particulate and fluid digesta in the RR. 3. Camels Camels have a unique ability to adapt to extreme feeding conditions,- in this respect, they differ from the ruminants. According to morphological criteria, camels (Camelus dromedarius) have been classified as bulk and roughage eaters (Langer 1988). However, the studies of their feeding habits (Coppock et al. 1986a Schwartz 1988; Rutagwenda et al. 1990) have shown that camels have a superior ability to select the more nutritive plants from a heterogeneous pasture. On the basis of feeding behavior, camels foraging on a thornbush savannah pasture have to be classified as selective browsers. Indeed, as browsers, camels are even superior to goats. More than 97% of the plants selected by camels were dicotyledons, with ;

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grasses accounting for less than 3% (Rutagwenda et al. 1990). Thus camels efficiently avoided ingesting slowly digestible monocotyledons when grazing on a thornbush savannah pasture, even during the dry season. Responses of the forestomach fluid volume and MRT of particles to changes of feed quality between seasons were in the same range for camels and for goats (Figs. 2 and 3). MRT of feed particles was shorter than in cattle under these conditions. In another experiment, camels were fed exclusively a low-quality, highfiber diet, without any possibility of selecting higher quality plants. Un­ der these conditions, the camels were able to retain feed particles in their forestomach for very long periods (Heller et al. 1986). On this low-quality diet, MRT of large feed particles in the forestomach was 74 hr, and the forestomach fluid volume reached 17% of body weight, values which are typical for grazers (Giesecke and van Gylswyk 1975; Hoppe et al. 1977; Clemens and Maloiy 1983; Hofmann 1988; Langer 1988). Thus, in contrast to most ruminant species, camels are not restricted to one feeding strategy with its limitations. Camels can, if necessary, utilize and survive on a very low-quality, fiber-rich diet as grazers can, but if they have the chance to select dicotyledonous plants from the environment, they browse very efficiently on the more nutritive parts of these plants.

III. Effects of Particle Size and Particle Density on Mean Retention Time in the Forestomach A. Particle Size 1. Critical particle size From particle size measurements of digesta using wet- or dry-sieving techniques, it was concluded that the probability of a particle leaving the forestomach decreases exponentially with its size (Poppi et al. 1980; Kennedy and Poppi 1984; Weston and Cantle 1984; Poppi et al. 1985; Shaver et al. 1988). Although there are differences in the fractional out­ flow rates of particles between sheep, cattle, and camels, in all these species small particles have a far higher probability of leaving the foresto­ mach than larger particles (Lechner-Doll and Engelhardt 1989). On the basis of size, the particles in the forestomach digesta can be considered as being made up of two pools, one consisting of particles too large to leave the forestomach, the other consisting of particles small enough to leave. This concept, which evolved from measurements of the size of particles at different levels in the digestive tract (e.g., Waghorn et al. 1986), from theoretical considerations (e.g., Hungate 1966) and from attempts to de­ velop dynamic mathematical models of rumen digestion (e.g., Murphy et al. 1986), implies the existence of a critical size to which particles must be reduced before they are small enough to leave the RR. That size is the

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critical particle size (CPS), which represents the threshold between the two pools. In practice, the CPS is specified empirically in terms of the pore size (aperture) of a sieve that will allow passage of digesta particles small enough to travel out through the reticulo-omasal orifice (ROO), but re­ tains larger digesta particles. For sheep and cattle digesta, the sieve aper­ ture is 1-2 mm and for camel digesta, about 3 mm (Reid et al. 1977-, Poppi et al. 1980, 1985; Kennedy 1984; Lechner-Doll and Engelhardt 1989). The CPS seems to be a fairly stable value not much affected by feed, feed intake, or feed quality (Ulyatt et al. 1986; Waghorn et al. 1986). The fact that the size of particles passing through a sieve may be larger than the pore (aperture) size of the sieve appears to have sometimes been ignored in calculating the CPS. Estimations of particle size, applying sieving techniques, are somewhat arbitrary and depend on the length and the shape of particles (Kennedy and Murphy 1988). Vaage et al. (1984) reported that elongated digesta particles are retained by sieves with qua­ dratic apertures mainly according to their length. Theoretical consider­ ations of the Overbalancing Principle showed that elongated particles should be retained on a square mesh sieve if particle length exceeds twice the diagonal of the sieve aperture (a-2V2, where a = the length of the side of the aperture) (Vaage et al. 1984). This hypothesis was confirmed by measurements of digesta particle lengths retained on various sieves using a wet-sieving technique (Vaage et al. 1984; Lechner-Doll and Engelhardt 1989). The sieve size of 1.18 mm, most often used to distinguish between the pool of large and small particles in the forestomach, would therefore retain particles longer than 3.34 mm. But even taking these particle sizes into account, particles leaving the RR would be much smaller than the size of the ROO. 2. The reticulo-omasal orifice The internal diameter of the ROO when fully open is five- to tenfold larger than the CPS (Bueno 1972- Bueno and Ruckebusch 1974; Welch 1982; McBride et al. 1983). This would suggest that the CPS may not be deter­ mined by the ROO and, further, that it might be possible for particles larger than the CPS to pass out of the RR. To investigate the relationship between particle size and particle pas­ sage, an experiment was carried out to observe the behavior of plastic particles of differing lengths, immersed in a buffer in the RR (Kaske et al. 1991). The RR of the eight sheep were emptied, 10 g each of plastic particles with lengths of 1, 5, 10, and 20 mm and a density of 1.03 g - m l were introduced, and the RR were then refilled with a buffer solution. To counteract sedimentation of the particles, C 0 was bubbled continuously through spargers at the bottom of the rumen, keeping most of the particles in suspension. Because of the low ratio of solids to fluid, particle interac­ tions would be expected to be small; forestomach motility and outflow rates were not different from those of sheep with digesta-filled RR. Within

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4 hours, 32, 25, 13, and 2% of the particles introduced with lengths of 1, 5, 10, and 20 mm, respectively, had left the RR. The animals did not rumi­ nate, so the particles that left were unchanged in size or shape. The outflow rate of the 1-mm particles was only 2.5 times higher than that of the 10-mm particles. On the other hand, the rate of outflow of 10-mm particles was 6.5 times that of the 20-mm particles. Thus the CPS of the plastic particles would, under these experimental conditions, appear to lie between 10 and 20 mm. A sieve with an aperture between 3.5 and 7 mm would be required to retain particles above the critical size, which is substantially larger than the 1-2 mm aperture calculated by Reid et al. (1977), Poppi et al. (1985), and Ulyatt et al. (1986) for normal digesta particles. These results demonstrate that the ROO in the conscious sheep is capable of passing particles several times larger than the CPS.

B. Breakdown of Particles If particle size is the key determinant of particle passage, as the CPS concept implies, then the breakdown of large particles should play a major role in the control of particle passage. The physical breakdown of fibrous feed results primarily from mastica­ tion during eating, a process that seems to be more efficient in sheep than in cattle (Chai et al. 1984), and from rumination. Rechewing during rumi­ nation is more important for the continued comminution of large particles (Reid et al. 1979; Poppi et al. 1981; Lee and Pearce 1984; Mosely and Jones 1984; Weston and Kennedy 1984; Dixon and Milligan 1985; Ulyatt et al. 1986; McLeod and Minson 1988a,b Nelson 1988; Waghorn et al. 1989). Microbial activity contributes to only a small extent to the direct breakdown of roughage particles (Murphy and Nicoletti 1984; Kennedy 1985; Ulyatt et al. 1986). Indirectly, however, microbial fermentation makes a substantial contribution to particle breakdown by increasing the fragility of fibrous particles, thus improving the efficiency of their breakdown during rumination (Chai et al. 1984; 1988; McLeod and Min­ son, 1988a). Microbial detrition may play a more important role in particle breakdown in cattle fed a concentrate diet (Ehle et al. 1982) than in roughage-fed animals. Faichney (1986) calculated breakdown rates and resulting MRT of parti­ cles for sheep fed alfalfa. He measured particle-pool sizes with undigestible lignin as the particle phase marker. In accordance with the CPS hypothesis, a sieve size of 1.18 mm was used to distinguish between the pool of large particles and the pool of small particles (Fig. 4). The MRT in the large-particle pool was 12.0 hr. The breakdown rate of large particles can be estimated using the reciprocal value of the MRT in the largeparticle pool; i.e., 8.3% of the large particles present in the RR were comminuted per hour. MRT in the pool of small particles was 18.4 hr about 50% longer than the MRT in the large-particle pool. The calculated ;

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B r e a k d o w n rate:

Small

particles in the reticulorumen

Outflow rate:

Figure 4. Mean retention times (MRT) of particles in the large (retained on a 1.18-mm screen) and small (passing a 1.18-mm screen) particle pool, breakdown rate of large particles, and outflow rate of small particles in sheep fed alfalfa. Calculated from Faichney et al. ( 1986).

outflow rate of small particles was only 5.4%-hr" . Thus, the lower out­ flow rate of small particles rather than the faster breakdown rate of the large particles limits passage of particulate matter. The fact that small particles are retained longer in the forestomach than might be expected, if the CPS hypothesis is correct, suggests that particle size is not the only, perhaps not even the main determinant of particle passage. In many studies where animals were fed with long, chopped or ground roughage, only a slight or even no decrease of particle MRT was found for the ground diets (Jaster and Murphy 1983; Weston and Kennedy 1984; Bergner and Klenke 1985; Kerley et al. 1985a,b Kinser et al. 1985; Faichney and Gherardi 1986; Firkins et al. 1986; Martz and Belyea 1986; Welch 1986; Fadlalla et al. 1987; Hunt et al. 1987; Cherney et al. 1988; Shaver et al. 1988; Stokes et al. 1988). Indeed, in some studies, where the ground diet was fed at the same level as a chopped diet, there was a considerable increase in MRT of particles and fluid in the forestomach of the animals on the ground diet, such that the dry matter (DM) pool was almost doubled (Faichney 1983, 1985, 1986). Kennedy and Murphy (1988) concluded that an increase of the DM concentration of the forestomach contents might have enhanced the entrapment of particles in the denser fibrous matrix of sheep fed a ground and pelleted diet. Faichney (1986) called this trapping of particles in forestomach contents the filter-bed effect. The filter-bed effect seems to contribute substantially to the selec­ tive retention of large and small particles, and it may be the reason why even the smallest particles flow from the RR more slowly than fluid 1

;

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(Faichney 1986). Differences in the selectivity of small-particle retention between ruminant species (Fig. 1) may be due to differences in the fibrous matrix in the forestomach, causing a variable filter-bed effect. The filter-bed effect seems to be most important when the DM content in the RR is high.

C. Particle Density 1. Methods of density determination It has been known for more than 30 years that, in addition to particle size, particle density influences the MRT of particles in the gastrointestinal tract (Balch and Kelly 1951; King and Moore 1957). However, because of methodological difficulties in measuring the density of digesta particles, the extent to which particle density influences MRT remains poorly de­ fined. Digesta particle density has most commonly been estimated from flo­ tation or sedimentation of particles in solutions of different, known densi­ ties (Evans et al 1973; Durkwa 1983; Hooper and Welch 1985a,b,c Nocek and Kohn 1987). Essentially this method measures the density of the structural components. However, rather than absolute density, it is the functional density of the particles that is relevant in the RR (Ehle and Stern 1986; Welch 1986; Nocek and Kohn 1987; Kennedy and Murphy 1988; Sutherland 1988). The functional density (FD) of digesta particles in the RR may be defined as the sum of all factors contributing to its effective buoyancy, including the structural components of the particle, its popula­ tion of microorganisms, the size and shape of the particle, the fluid and the gas inside the particle, as well as attached gas bubbles. The gas associated with the particle is a critical factor: air-filled internal spaces of freshly ingested particles and the gas produced during fermentation can markedly influence the FD and thereby the movements of particles in the RR. It follows that measurement of FD should be carried out with as little disturbance as possible to the particle and its environment. An alternative approach, more clearly related to FD, is based on the flotation-sedimentation velocities of digesta particles in original rumen contents (Sutherland 1988). In this, a digesta sample is taken from the RR with minimal disturbance and rapidly transferred to a plastic bag, which is then immersed, loosely closed, in a water bath (40°C) for 2 min. During the holding period the less dense, more buoyant particles rise and the more dense, less buoyant particles sink according to their FD. The digesta are then divided horizontally by folding the bag over a stiff horizontal wire. The upper portion, containing the more buoyant particles, the lower por­ tion, containing the less buoyant particles, are transferred to separate containers. Both portions can then be examined physically, chemically, or microbiologically. This procedure is quick; it is carried out in a rela­ tively natural milieu (rather than in the alien environment of standard ;

468

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W.v. E n g e l h a r d t

solutions); microbial activity is maintained; interactions of particles and the suspending fluid are preserved; while undiluted samples of di­ gesta, enriched with buoyant or sedimenting particles, are produced for analysis. 2. Effect of Particle Density on Mean Retention Time The relationships between particle density and digesta passage have been studied using inert rubber or plastic particles (e.g., Balch and Kelly 1951; Welch 1982; DesBordes and Welch 1984; Murphy et al. 1989) or labeled indigestible plant cell walls (Lindberg 1985, 1988). These materials avoid the methodological difficulties involved in determining the density of digesta particles, and the complexities introduced by changes occurring in the FD of particles during their incubation in the RR. Available data demonstrating the influence of particle density on MRT in the RR of cattle and sheep are shown in Fig. 5. Within the normal density range of digesta particles, 0.8 to 1.5 g - m l (Evans et al. 1973), there is a clear negative relationship between particle density and MRT. Particles with a low density are retained considerably longer in the RR than particles with a high density (52-91 hr and 19-44 hr, respectively). The data of most investigators suggest a linear relationship -1

100

0.8

0.9

1.0

1.1

1.2

1.3

Density of particles [g*ml""^] Sheep: ALindberg ( 1 9 8 5 ) , • Cattle: • A

Katoh et al. ( 1 9 8 8 ) , Ο Kaske and Engelhardt ( 1 9 9 0 )

Campling and Freer ( 1 9 6 2 ) , ·

Ehle et al. ( 1 9 8 4 ) ,

•Ehle(l984),

Ehle and Stern ( 1 9 8 6 )

Figure 5- Mean retention times (MRT) of small inert particles of different densities in the reticulorumen of cattle and sheep.

469

20 Retention Time of Particles in the Forestomach

between density and MRT of particles in the forestomach (Evans et al. 1973; Lindberg 1985; Kaske and Engelhardt 1990). Some caution should be used when drawing conclusions from studies with inert particles. It is possible that their behavior may differ from the behavior of normal digesta particles. Inert particles lack factors that normally contribute to FD, and they probably most resemble indigestible structural material left after all fermentable material has been removed. To that extent they may be useful in studies of rumen clearance. 3. Changes of particle density The density of normal digesta particles in contrast to that of inert parti­ cles, changes during their stay in the forestomach. Freshly eaten roughage particles entering the RR, generally have a FD of about 0.8 g - m l because of the gas in their internal spaces. Thereafter their density increases as they continue to reside in the RR. Effects of microbial digestion on the density of forage particles were studied by Nocek and Kohn (1987). Lu­ cerne and timothy hays, chopped or ground and sieved to various sizes, were incubated in polyester bags (pore size, 59 μπι) suspended in the RR for periods of 1 to 100 hr. Particle density of the original material and of the residues in the bags after incubation were determined by progressive immersion of particles in solutions of known density. There was a rapid increase in density of timothy particles within 1 hr, from 0.9 g-ml" up to approximately 1.1 g - m l . A relatively slow increase followed, with maxi­ mal values of about 1.3 g - m l being reached after incubation times of 76 to 100 hr. Alfalfa particles initially were more dense than timothy parti­ cles, and the changes in the first hour were less marked; thereafter, the density of alfalfa particles increased, generally more slowly than timothy particles, reaching a maximum between 1.2 and 1.3 g - m l . The more coarsely prepared forage particles tended to have higher densities (Nocek and Kohn 1987). A comparable pattern of increasing particle density with time was found when ground hay was soaked in water, sterilized rumen fluid, or buffer solutions (Hooper and Welch 1985a,b,c). These findings of Nocek and Kohn (1987) and of Hooper and Welch (1985a,b,c) suggest that several factors can potentially contribute to changes in particle density. Thus, while the increase in particle density with particle MRT seems well-established, the mechanism of that increase remains to be fully elucidated. Sutherland (1988) investigated the relationship between particle size and FD in digesta taken from sheep fed chopped lucerne hay. The digesta samples were fractionated according to their flotation-sedimentation be­ havior and then wet-sieved. Table 1 shows the relationship between size and FD found in dorsal rumen digesta 3 - 6 hr after feeding. The large particles were mostly buoyant, while the small particles mostly sedimented. The FD of the small particles (those passing a 1-mm sieve) was -1

1

-1

-1

-1

470 Table 1

Μ. L e c h n e r - D o l l , Μ . K a s k e , a n d W . v . E n g e l h a r d t

Proportion of Buoyant and Sedimenting Digesta Particles of Different Sizes from the Reticulorumen of Sheep Fed Lucerne (% of dry matter) 0

Behavior

4

2

Buoyant Indeterminate Sedimenting

90 3 8

86 4 11

Sieve Size (mm) 1 .5 53 5 42

20 3 77

.25

Fines

7 2 91

21 10 68

Samples were taken from the dorsal rumen 3 - 6 hr after feeding, separated according their flotationsedimentation behavior, and sieved using a wet-sieving technique (calculated from Sutherland 1988). a

thus higher than the FD of most of the larger particles. This relationship between particle size and FD implies that particle breakdown leads not only to a reduction in size but it also results in an increase of mean particle density.

D. Distribution of Particles in the Reticulorumen Evans et al. (1973) reported that particles were not evenly distributed in the RR of cattle in respect to their size and their density. In the dorsal rumen, more particles of a low density were found, and many of the particles were large. In the ventral rumen, more particles with a higher density were present, and most of these particles in the ventral rumen were small. This was confirmed by Sutherland (1988) for sheep fed lucerne. Large particles (retained on a 1-mm sieve) accounted for 28, 15, and 15% of the dry matter in the dorsal rumen, in the ventral rumen, and in the reticu­ lum, respectively. Table 2 shows the corresponding proportions of buoyant, indeterminate, and sedimenting particles. Particle size distribu­ tions in the ventral rumen and the reticulum were not different. However, more particles of a higher density were found in the reticulum than in the ventral rumen (Table 2).

Table 2 Proportion of Buoyant and Sedimenting Particles in the Dorsal Rumen, in the Ventral Rumen, and in the Ventral Reticulum of Sheep Fed Lucerne (% of dry matter) 0

Behavior

Dorsal Rumen

Ventral Rumen

Ventral Reticulum

Buoyant Indeterminate Sedimenting

38 5 58

26 16 58

14 6 80

a

From Sutherland (1988).

471

2 0 R e t e n t i o n T i m e o f P a r t i c l e s in t h e F o r e s t o m a c h

E. The Quantitative Contributions of Particle Size and Particle Density to the Mean Retention Time To estimate the quantitative contributions of particle size and particle density to MRT, an experiment was carried out in which inert plastic particles of two lengths and four densities were given to sheep with the morning feed (Kaske and Engelhardt 1990). These plastic particles were comminuted by rumination almost as if they were normal feed particles, and breakdown due to rumination was not markedly influenced by their densities (Kaske et al. 1990). Results are shown in Fig. 6. Both sizes of particles showed a general inverse relation between MRT and den­ sity. However, there was little difference between the MRT for parti­ cles of 0.92 g - m l and 1.03 g - m l for both sizes (66.5 hr for 1-mm, 85.9 hr for the 10-mm particles). This may indicate that a density of 1.03 g - m l is insufficient to achieve effective sedimentation in RR con­ tents. For all four densities, the MRT of the 10-mm particles was of the order of 24 hr longer than that of the 1-mm particles, suggesting that size was responsible for an additional retention of the larger particles of about 24 hr. All large particles with a low density (0.92 and 1.03 g-ml ) were found in the feces comminuted to a size below 4 mm (equivalent to a sieve size of 1.4 mm); that is, all had been ruminated before they left the forestomach. -1

-1

-1

-1

Large particles (10 mm)

E3 Small particles (1 mm)

100

Particle density [g*ml ' ] Figure 6. Mean retention times (MRT) of plastic particles in the reticulorumen of sheep fed hay ad libitum. Plastic particles of 10-mm and 1-mm length and densities of 0.92, 1.03, 1.22, and 1.44 g-ml" (10 g of each) were given with the morning feed; error bars: SEM From Kaske and Engelhardt (1990). 1

472

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W . v . E n g e l h a r d t

By contrast, some of the long particles with a higher density (1.44 g-ml ) and a MRT of about 50 hr, were found in the feces unaltered in length, indicating that they had escaped the RR without being ruminated. These results show clearly that both size and density affect MRT. The relative contribution of the two factors was then estimated by regression analysis using the data shown in Fig. 6. For our calculations, we assumed an exponential relation between MRT and particle size (Poppi et al. 1980; Kennedy and Poppi 1984; Weston and Cantle 1984; Poppi et al. 1985; Lechner-Doll and Engelhardt 1989) and a linear relationship between MRT and particle density (Evans et al. 1973; Lindberg 1985; Kaske and Engelhardt 1990). We found 87% of the total variation in MRT could be explained by the two factors, particle size and particle density. Obviously there was no major role for other factors. Particle size accounted for 28% of the total variation in MRT, while particle density accounted for 59% of the variation. Particle density was therefore the major determinant of MRT in this experiment. The influence FD of a particle has on the probability of its being rumi­ nated is still unclear. Murphy et al. (1989) calculated an inverse relation between particle density and the rate of rumination, while Kaske et al. (1991) found that the probability of a particle's being ruminated during its stay in the RR was independent of particle density. -1

F. Separation of Particles in the Reticulorumen Whether a particle can leave the RR or not depends mainly on its probabil­ ity of being present in the ventral reticulum during the opening of the ROO (Reid 1985, 1986; Waghorn et al. 1986). There is a greater concentra­ tion of particles of higher density present in the ventral reticulum than in the dorsal or ventral rumen (Sutherland 1988; Table 2); we can assume that this is the reason for the preferential outflow of higher density particles. The key question remains to be answered: What is the mechanism responsible for raising the concentration of small, dense particles in the ventral reticulum? 1. The fibrous raft circulating in the rumen (Waghorn and Reid 1977; Wyburn 1980) may selectively entrap particles with a lower density. The effect of this would be to increase the concentration of particles of higher density among the population of particles free to pass to the reticulum. 2. The flow of small particles from the ventral rumen to the reticulum could be selective. Preferential passage of particles with a higher density would lead to an accumulation of such particles in the reticulum.

473

2 0 R e t e n t i o n T i m e o f P a r t i c l e s in t h e F o r e s t o m a c h

3. The motility of the reticulum may differentially propel its contents. Thus it could rapidly move lighter particles in its dorsal region back into the rumen, so that particles with a higher density remain in the ventral region (Reid 1985; Waghorn et al. 1986). All three possible separation mechanisms are based on the flotationsedimentation behavior of the digesta particles and on the motility of the forestomach. Entrapment of small particles in the fibrous raft in the rumen will obviously reduce the movement of such particles to the reticu­ lum as well as increase their MRT. However, there are no indications that the filter-bed effect results in particles with a low density being selectively retained. When plastic particles of a low density (1.03 g-ml" ) were placed in the dorsal rumen, the ventral rumen, or the reticulum of four normally fed sheep, the site of placement had no significant effect on the outflow of the plastic particles from the forestomach (M. Kaske, unpublished); simi­ lar results have been found in cattle (Welch 1982). These observations suggest that neither selective trapping of particles in the fibrous raft nor selective retention of particles of low density in the ventral rumen is responsible for the accumulation of particles of higher density in the reticulum. It follows that small particles do not selectively reach the reticulum because of their density. If the flow of feed particles to the reticulum is not selective, it is likely that the separation mechanism is located in the reticulum itself. This hypothesis received support from observations made in sheep in which particles of different sizes and densities were placed in the reticulum, and their subsequent distribution in the RR was determined (Kaske 1987). In four sheep, the RR was emptied, 10 g each of plastic particles of three lengths (1, 5, or 10 mm) and three densities (1.03, 1.22, 1.44 g-ml" ) were placed in the reticulum, and the RR was refilled with buffer solution. After 30 min, particles were harvested separately from the reticulum and the ventral rumen. Figure 7 shows the percentage of particles of different densities found in the reticulum and the ventral rumen after 30 min. Particle size appeared to have no influence on the distribution of the particles. However, there was a marked effect of density; the majority of high-density particles was found in the reticulum, while the majority of the low-density particles was found in the ventral rumen. These results show that separation between particles of different densi­ ties can indeed occur in the reticulum. Particles with a low density are preferentially moved back into the rumen, while particles with a higher density remain in the reticulum, and therefore have a higher probabil­ ity of leaving the forestomach. This mechanism would also account for the selective retention of particles with a low density in the fore­ stomach. 1

1

474

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W . v . E n g e l h a r d t

CD Low density

(1.03

Ε

„

1ο οf ~

Ε

ε §

CT

Medium density

(1.22 ονηΓ ) 1

Η High density (1.44 ginC ) 1

100

80 Η 60

Ε

1

0)

8& ί> C φ

40 20

Reticulum

Ventral rumen

Figure 7- ΕParticle distribution (% of particles introduced) in the reticulorumen filled with buffer solution. Plastic particles with densities of 1.03,1.22, and 1.44 g-ml~ were introduced into the reticulum and recovered after 30 min from the ventral rumen and from the reticulum error bars: SD. Pooled data for particles with lengths of 1, 5, and 10 from Kaske (1987). Ω. 1

* I

;

IV. Present Understanding Particles are selectively retained in the forestomach of ruminants and camelids. Digesta particles are retained considerably longer in the foresto­ mach than fluid. The level of intake and the quality of feed ingested did influence the MRT in most of the studies. On the other hand, the selectiv­ ity of particle retention seems not to be markedly affected by intake and feed. To explain the selective retention, physical properties of the particles and particle interactions have to be considered. The particles leaving the forestomach are almost exclusively small. On the other hand, the breakdown of large particles is faster than is the outflow of small particles, implying that small particles are effectively retained in the forestomach. The filter-bed effect (Faichney 1986) may partly explain the long reten­ tion of small particles in the forestomach. The entrapment of the small particles within the fibrous raft seems to be particularly important in large ruminants, as in cattle, in camels, and in animals fed a diet that increases the dry matter content in the RR (Kennedy and Murphy 1988). The probability that feed particles will leave the forestomach is mainly determined by particle density and particle size. Particle density is more important than size for the selective retention of particles in sheep. Most larger feed particles have a low density and are therefore retained for a

2 0 R e t e n t i o n T i m e o f P a r t i c l e s in t h e F o r e s t o m a c h

475

Figure 8. Scheme of the separation mechanism based on the flotation-sedimentation behavior of digesta particles and the reticular contractions.

longer period in the contents of the forestomach. During breakdown and microbial digestion, particle density increases. As a result, the small parti­ cles tend to have a higher density, and they are preferentially found in the reticulum. Smaller particles thus have a better chance of leaving the forestomach. We suppose that the separation mechanism between particles of differ­ ent densities is based mainly on the contractions of the reticulum at the beginning of each motility cycle. During the reticular contractions, particles with a low density are pushed in a dorsal and caudal direction. Small particles with a higher density, on the other hand, have a greater tendency to remain in the ventral reticulum (Fig. 8). In this way, the heavier particles, most of which are also small, have a higher probability of entry into the omasum when the ROO opens during the second reticular contrac­ tion.

Acknowledgments This work was supported by the German Research Foundation (DFG En 65/11) and the H. Wilhelm Schaumann Foundation for the improvement of agricultural sciences. We are greatly indebted to Drs. C. S. W. Reid and G. J. Faichney for their suggestions about preparing the manuscript.

References Aitchison, E. M., Gill, M., and Osbourn, D. F. (1986). The effect of supplementation with maize starch and level of intake of perennial ryegrass [Lolium perenne cv. Endura) hay on the removal of digesta from the rumen of sheep. Br. J. Nutr. 56,477-486. Balch, C. C., and Kelly, A. (1951). Factors affecting the utilization of food by dairy cows. 3. Specific gravity of digesta from the reticulo-rumen of cows. Br. J. Nutr. 4 , 3 9 5 - 3 9 7 . Bergner, H., and Klenke, E. F. (1985). Mittlere Verweildauer (mean retention time) von

476

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W . v . E n g e l h a r d t

Cr-EDTA and Ru-Phenantrolin im Verdauungstrakt von Schafen und Bullen bei Fütterung von Strohpellets. Arch. Anim. Nutr. 35, 649-660. Bueno, L. (1972). Action du sphincter reticulo-omasal sur le transit alimentaire chez les bovins. Ann. Rech. Vet. 3, 83-91. Bueno, L., and Ruckebusch, Y. (1974). The cyclic motility of the omasum and its control in sheep. /. Physiol. 238, 295-312. 51

103

Caird, L., and Holmes, W. (1986). The prediction of voluntary intake of grazing dairy cows. /. Agric. Sei. [Camb.) 107, 43-54. Chai, K., Kennedy, P. M., and Milligan, L. P. (1984). Reduction in particle size during rumination in cattle. Can. J. Anim. Sei. 64 (Suppl.), 339-340. Chai, K., Milligan, L. P., and Mathison, G. W. (1988). Effect of muzzling on rumination in sheep. Can. J. Anim. Sei. 68, 387-397. Campling, R. C , and Freer, M. (1962). The effect of specific gravity and size on the mean retention time of inert particles in the alimentary tract of the cow. Br. J. Nutr. 16, 507-518. Cherney, J. H., Cherney, D. J. R., and Mertens, D. R. (1988). Fiber composition and digestion kinetics in grass stem internodes as influenced by particle size. /. Dairy Sei. 71, 2 1 1 2 2122. Clemens, E. T. and Maloiy, G. M. O. (1983). Digestive physiology of East African wild ruminants. Comp. Biochem. Physiol. A 76,319-333. Cochran, R. C , Adams, D. C , Galyean, M. L., and Wallace, J. D. (1986). Estimating particle turnover in the rumen of meal-fed beef steers: Procedural evaluations. /. Anim. Sei. 63, 1469-1475. Colucci, P. E., Chase, L. E., and Van Soest, P. J. (1982). Feed intake, apparent diet digestibility, and rate of particulate passage in dairy cattle. /. Dairy Sei. 65, 1445-1456. Coombe, J. B., and Kay, R. Ν. B. (1965). Passage of digesta through the intestines of the sheep—Retention times in the small and large intestines. Br. J. Nutr. 19,325-338. Coppock, D. L., Swift, D. M., and Ellis, J. E. (1986a). Seasonal nutritional characteristics of livestock diets in a nomadic pastoral ecosystem. /. Appl. Ecol. 23, 585-595. Coppock, D. L., Ellis, J. E., and Swift, D. M. (1986b). Livestock feeding ecology and resource utilization in a nomadic pastoral ecosystem. /. Appl. Ecol. 23, 573-583. DesBordes, C. K., and Welch, J. G. (1984). Influence of specific gravity on rumination and passage of indigestible particles. /. Anim. Sei. 59,471-475. Deswysen, A. G., Ellis, W. C , and Pond, K. R. (1987). Interrelationships among voluntary intake, eating and ruminating behavior and ruminal motility of heifers fed corn silage. /. Anim. Sei. 64, 835-841. Deswysen, A. G., and Ellis, W. C. (1988). Site and extent of neutral-detergent-fiber digestion, efficiency of ruminal digesta flux, and fecal output as related to variations in voluntary intake and chewing behavior in heifers. /. Anim. Sei. 66, 2678-2686. Dixon, R. M., and Milligan, L. P. (1985). Removal of digesta components from the rumen of steers determined by sieving techniques and fluid, particulate and microbial markers. Br. f. Nutr. 5 3 , 3 4 7 - 3 6 2 . Durkwa, L. (1983). "Length and Specific Gravity of Particles Passed From the Rumen and Changes in Ingesta Specific Gravity." Thesis, University of Vermont, Burlington, Vermont. Ehle, F. R., Murphy, M. R., and Clark, J. H. (1982). In situ particle size reduction and the effect of particle size on degradation of crude protein and dry matter in the rumen of dairy steers. /. Dairy Sei. 65,963-971. Ehle, F. R. (1984). Influence of particle size on determination of fibrous feed components. /. Dairy Sei. 67, 1482-1488. Ehle, F. R., Bas, F., Barno, B., Martin, R., and Leone, F. (1984). Particulate rumen turnover rate measurement as influenced by density of passage markers. /. Dairy Sei. 67, 2 9 1 0 2913. ;

2 0 R e t e n t i o n T i m e o f P a r t i c l e s in t h e

Forestomach

477

Ehle, F. R., and Stern, M. D. (1986]. Influence of particle size and density on particulate passage through alimentary tract of Holstein heifers. /. Dairy Sei. 69, 564-568. Erdman, R. Α., and Smith, L. W. (1985). Ytterbium binding among particle size fractions of forage cell walls. /. Dairy Sei. 68,3071-3075. Erdman, R. Α., Vandersall, J. H., Russek-Cohen, E., and Switalski, G. (1987). Simultaneous measurement of rates of ruminal digestion and passage of feeds for prediction of ruminal nitrogen and dry matter digestion in lactating dairy cows. /. Anim. Sei. 64, 565-577. Evans, E. W., Pearce, G. R., Burnett, J., and Pillinger, S. L. (1973). Changes in some physical characteristics of the digesta in the reticulorumen of cows fed once daily. Br. f. Nutr. 29, 357-376. Ewing, D. L., and Johnson, D. E. (1987). Corn particle starch digestion, passage and size reduction in beef steers: A dynamic model. /. Anim. Sei. 64, 1194-1204. Fadlalla, B., and Kay, R. Ν. B. (1987). Digestion and retention time of stained food in sheep. /. Agric. Sei. (Camb.) 109, 545-549. Fadlalla, B., Kay, R. N. B., and Gooddall, E. D. (1987). Effects of particle size on digestion of hay by sheep. /. Agric. Sei. [Camb.) 109, 551-561. Faichney, G. J. (1975). The use of markers to partition digestion within the gastrointestinal tract of ruminants. In "Digestion and Metabolism in the Ruminant." (I. W. McDonald and A. C. I. Warner, eds.), pp. 277-291. University of New England Publishing Unit, Armidale, Australia. Faichney, G. J. (1983). The effect of physical form of lucerne hay on the passage of markers through the rumen of sheep. Proc. Nutr. Soc. Aust. 8, 186. Faichney, G. J., and Boston, R. C. (1983). Interpretation of the fecal excretion patterns of solute and particle markers introduced into the rumen of sheep. /. Agric. Sei. [Camb.) 101, 575-581. Faichney, G. J. (1985). The mean retention time of particles in the rumen of sheep given chopped and ground lucerne hay. In "Ruminant Physiology—Concepts and Conse­ quences." (S. K. Baker, J. M. Gawthorne, J. B. Mackintosh, and D. B. Purser, eds.), pp. 126. School of Agriculture, University West Australia, Perth, Australia. Faichney, G. J. (1986). The kinetics of particulate matter in the rumen. In "Control of Digestion and Metabolism in Ruminants." (L. P. Milligan, W. L. Grovum, and A. Dobson, eds.), pp. 173-195. Reston Publishing, Reston, Va. Faichney, G. J., and Gherardi, S. G. (1986). Relationships between organic matter digesti­ bility, dry-matter intake and solute mean retention times in sheep given a ground and pelleted diet. /. Agric. Sei. {Camb.) 106, 219-222. Faichney, G. J., Poncet, C , and Boston, R. C. (1990). Passage of internal and external markers of particulate matter through the rumen of sheep, submitted for publication. Firkins, J. L., Berger, L. L., Merchen, N. R., Fahey, G. C , and Nelson, D. R. (1986). Effects of feed intake and protein degradability on ruminal characteristics and site of digestion in steers. /. Dairy Sei. 69, 2111-2123. Funk, Μ. Α., Galyean, M. L. Branine, M. E. and Krysl, L. J. (1987). Steers grazing blue grama rangeland throughout the growing season. I. Dietary composition, intake, digesta kinetics and ruminal fermentation. /. Anim. Sei. 65, 1342-1353. Giesecke, D., and van Gylswyk, N. O. (1975). A study of feeding types and certain rumen functions in six species of South African ruminants. /. Agric. Sei. (Camb.) 85, 75-83. Grovum, W. L., and Williams, V. f. (1973). Rate of passage of digesta in sheep. 4. Passage of markers through the alimentary tract and the biological relevance of rate-constants de­ rived from changes in concentration of markers in faeces. Br. J. Nutr. 30, 231-242. Grovum, W. L., and Williams, V. f. (1977). Rate of passage of digesta in sheep. 6. The effect of level of food intake on mathematical predictions of the kinetics of digesta in the reticu­ lorumen and intestines. Br. J. Nutr. 38, 425-435. Heller, R., Lechner, Μ., Weyreter, Η., and Engelhardt, W. ν. (1986). Forestomach fluid volume and retention of fluid and particles in the gastrointestinal tract of the camel (Camelus dromedarius). J. Vet. Med. A 88,396-399. ;

;

478

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W . v . E n g e l h a r d t

Hodgson, J. (1985). The control of herbage intake in the grazing ruminant. Proc. Nutr. Soc. 44, 339-346. Hofmann, R. R., and Stewart, D. R. M. (1972). Grazer or browser: A classification based on stomach structure and feeding habits of East African ruminants. Mammalia 36,226-240. Hofmann, R. R. (1988). Morphophysiological evolutionary adaptations of the ruminant digestive system. In "Aspects of Digestive Physiology in Ruminants." (A. Dobson, and M. J. Dobson, eds.), pp. 1-20. Comstock Publishing Associates, Ithaca, N.Y. Hooper, A. P., and Welch, f. G. (1985a). Functional specific gravity of ground hay samples in ionic solutions. /. Dairy Sei. 68, 848-856. Hooper, A. P., and Welch, J. G. (1985b). Effects of particle size and forage composition on functional specific gravity. /. Dairy Sei. 68, 1181-1188. Hooper, A. P., and Welch, J. G. (1985c). Change of functional specific gracity of forages in various solutions. /. Dairy Sei. 68, 1652-1658. Hoppe, P. P., Qvortrup, S. Α., and Woodford, Μ. H. (1977). Rumen fermentation and food selection in East African sheep, goats, Thomson's gazelle, Grant's gazelle and impala. /. Agric. Sei. [Camb.) 89, 129-135. Hoppe, P. P. (1984). Strategies of digestion in African herbivores. In "Herbivore Nutrition in the Tropics and Subtropics." (F. Gilchrist and R. Mackie, eds.), pp. 222-243. The Science Press, Johannesburg, Union of South Africa. Howe, J. C , Barry, Τ. N., and Popay, A. I. (1988). Voluntary intake and digestion of gorse [Ulex europaeus) by goats and sheep. /. Agric. Sei. (Camb.) I l l , 107-114. Hungate, R. E. (1966). "The Rumen and Its Microbes." Academic Press, N.Y. Hunt, C. W., Paterson, J. Α., Williams, J. E., and Forwood, J. R. (1987). Effect of particle length and NaOH treatment of wheat straw on digestive kinetics in cattle. Nutr. Rep. Int. 35, 901-908. Huston, J. E., Rector, B. S., Ellis, W. C , and Allen, M. L. (1986). Dynamics of digestion in cattle, sheep, goats and deer. /. Anim. Sei. 62, 208-215. Janis, C. (1976). The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 30, 757-774. Jaster, E. H and Murphy, M. R. (1983). Effects of varying particle size of forage on digestion and chewing behavior of dairy heifers. /. Dairy Sei. 66, 802-810. Kaske, M. (1987). "Die Retention von Partikeln unterschiedlicher Dichte and Größe im Retikulorumen von Schafen." Dissertation School of Veterinary Medicine, Hannover, F.R.G. Kaske, M., and Engelhardt, W. V. (1990). The effect of size and density on mean retention time of particles in the gastrointestinal tract of sheep. Br. f. Nutr., 163,457-465. Kaske, M., Hatiboglu, S., and Engelhardt, W. v. (1991). The influence of density and size of particles on rumination and passage from the reticulorumen of sheep, submitted for publication. Katoh, K., Sato, F., Yamazaki, Α., Sasaki, Y., and Tsuda, T. (1988). Passage of indigestible particles of various specific gravities in sheep and goats. Br. J. Nutr. 60,683-687. Kay, R. Ν. B., Engelhardt, W. v., and White, R. G. (1980). The digestive physiology of wild ruminants. In "Digestive Physiology and Metabolism in Ruminants." (Y. Ruckebusch, and P. Thivend, eds.), pp. 743-761. MTP Press, Lancaster, England. Kennedy, P. M., and Poppi, D. P. (1984). Critical particle size in sheep and cattle. In "Tech­ niques in Particle Size Analysis of Feed and Digesta in Ruminants." (P. M. Kennedy, ed.), pp. 170. Can. Soc. Anim. Sei. occ. publ. 1, Kennedy, P. M. (1984). Summary and conclusions from discussion. In "Techniques in Parti­ cle Size Analysis of Feed and Digesta in Ruminants." (P. M. Kennedy, ed.), Can. Soc. Anim. Sei. occ. publ. 1, 184-186. Edmonton, Alberta, Canada. Kennedy, P. M. (1985). Influences of cold exposure on digestion of organic matter, rates of passage of digesta in the gastrointestinal tract, and feeding and rumination behaviour in sheep given four forage diets in the chopped, ground, and pelleted form. Br. J. Nutr. 5 3 , 159-173. v

2 0 R e t e n t i o n T i m e o f P a r t i c l e s in t h e

Forestomach

479

Kennedy, P. M., and Murphy, M. R. (1988). The nutritional implications of differential passage of particles through the ruminant alimentary tract. Nutr. Res. Rev. 1, 189-208. Kerley, M. S., Kinser, A. R., Firkins, J. L., Fahey, G. C., and Berger, L. L. (1985a). Effects of roughage particle size on site of nutrient digestion and digesta flow through the gastroin­ testinal tract of sheep fed corncob-concentrate diets. /. Anim. Sei. 61, 504-513. Kerley, M. S., Firkins, J. L., Fahey, G. C., and Berger, L. L. (1985b). Roughage content and particle size: Their effects on size reduction and fiber composition of particles passing through the gastrointestinal tract of sheep fed corncob-concentrate diets. /. Dairy Sei. 68, 1363-1375. King, K. W., and Moore, W. E. C. (1957). Density and size as factors affecting passage rate of ingesta in the bovine and human digestive tracts. /. Dairy Sei. 40, 528-536. Kinser, A. R., Kerley, M. S., Fahey, G. C., and Berger, L. L. (1985). Effect of roughage particle size on ruminal, digestive and metabolic characteristics of early-weaned lambs fed pel­ leted corncob-concentrate diets. /. Anim. Sei. 61, 514-524. Langer, P. (1988). 'The mammalian herbivore stomach." Gustav Fischer, Stuttgart, F.R.G. Lechner-Doll, M., and Engelhardt, W. v. (1989). Particle size and passage from the foresto­ mach in camels compared to cattle and sheep fed a similar diet. /. Anim. Physiol. Anim. Nutr. 61, 120-128.

Lechner-Doll, M., Rutagwenda, T., Schwartz, H. J., Schultka, W., and Engelhardt, W. v. (1990). Seasonal changes of ingesta flow in indigenous livestock on a thornbush savannah in Northern Kenya, /. Agric. Sei. (Camb.), in press. Ledoux, D. R., Williams, J. E., Stroud, Τ. E., Garner, G. B., and Paterson, J. A. (1985). Influence of forage level on passage rate, digestibility and performance of cattle. /. Anim. Sei. 61, 1559-1566. Lee, J. Α., and Pearce, G. R. (1984). The effectiveness of chewing during eating on particle size reduction of roughages by cattle. Aust. f. Agric. Res. 35, 609-618. Lindberg, J. E. (1985). Retention time of chromium-labelled feed particles and of water in the gut of sheep given hay and concentrate at maintenance. Br. J. Nutr. 53, 559-567. Lindberg, J. E. (1988). Retention times of small feed particles and of water in the gut of dairy goats fed at different levels of intake. /. Anim. Physiol. Anim. Nutr. 59, 1 7 3 181. Maloiy, G. M. O., Rugangazi, Β. M., and Clemens, Ε. T. (1988). Physiology of the dik-dik antelope. Comp. Biochem.

Physiol. 91 A, 1-8.

Martz, F. Α., and Belyea, R. L. (1986). Role of particle size and forage quality in digestion and passage by cattle and sheep. /. Dairy Sei. 69, 1996-2008. McBride, B. W., Milligan, L. P., and Turner, Β. V. (1983). Endoscopic observation of the reticulo-omasal orifice of cattle. /. Agric. Sei. (Camb.) 101, 749-750. McCollum, F. T., and Galyean, M. L. (1985a). Influence of cottonseed meal supplementation on voluntary intake, rumen fermentation and rate of passage of prairie hay in beef steers. /. Anim.

Sei. 60, 5 7 0 - 5 7 6 .

McCollum, F. T., and Galyean, M. L. (1985b). Cattle grazing blue grama rangeland. II. Seasonal forage intake and digesta kinetics. /. Range Manage. 38, 543-546. McLeod, Μ. N., and Minson, D. J. (1988a). Large particle breakdown by cattle eating ryegrass and alfalfa. /. Anim. Sei. 66, 992-999. McLeod, Μ. N., and Minson, D. J. (1988b). Breakdown of large particles in forage by simulated digestion and detrition. /. Anim. Sei. 66,1000-1004. Merchen, N. R., Firkins, J. L., and Berger, L. L. (1986). Effect of intake and forage level on ruminal turnover rates, bacterial protein synthesis and duodenal amino acid flows in sheep. /. Anim. Sei. 62, 216-225. Mertens, D. R. (1987). Predicting intake and digestibility using mathematical models of ruminal function. /. Anim. Sei. 64, 1548-1558. Mosely, G., and Jones, J. R. (1984). The physical digestion of perennial ryegrass [Lolium perenne)

381-390.

and white clover [Trifolium

repens) in the foregut of sheep. Br. ]. Nutr. 5 2 ,

480

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W.v. E n g e l h a r d t

Mudgal, V. D., Dixon, R. M., Kennedy, P. M., and Milligan, L. P. (1982). Effect of two intake levels on retention time of liquid, particle and microbial markers in the rumen of sheep. /. Anim. Sei. 54, 1051-1055. Murphy, M. R., and Nicoletti, J. M. (1984). Potential reduction of forage and rumen digesta particle size by microbial action. /. Dairy Sei. 67, 1221-1226. Murphy, M. R., Baldwin, R. L., and Ulyatt, M. J. (1986). An update of a dynamic model of ruminant digestion. /. Anim. Sei. 62, 1412-1422. Murphy, M. R., Kennedy, P. M., and Welch, J. G. (1989). Passage and rumination of inert particles varying in size and specific gravity as determined from analysis of faecal appear­ ance using multicompartment models. Br. J. Nutr. 62, 481-492. Neal, H. D. S. C., Thomas, C., and Cobby, J. M. (1984). Comparison of equations for predicting voluntary intake by dairy cows. /. Agric. Sei. [Camb.) 103, 1-10. Nelson, M. L. (1988). Factors affecting the particle size distribution of grazed forage due to ingestive mastication by steers and wethers. /. Anim. Sei. 66, 1256-1266. Nocek, J. E., and Kohn, R. A. (1987). Initial particle form and size on change in functional specific gravity of alfalfa and timothy hay. /. Dairy Sei. 70, 1850-1863. O'Connor, J. D., Robinson, P. H., Sniffen, C. J., and Allen, M. S. (1984). A gastrointestinal tract simulation model of digesta flow in ruminants. In "Techniques in Particle Size Analysis of Feed and Digesta in Ruminants." (P. M. Kennedy, ed.), Can. Soc. Anim. Sei. occ. publ. 1, 102-122. Edmonton, Alberta, Canada. Poncet, C , and Al Abd, A. (1984). Particulate and fluid passage studies in sheep fed a hay-based diet. Can. f. Anim. Sei. 64, (suppl.), 77-79. Pond, K. R., Ellis, W. C , Matis, J. H., Ferreiro, Η. M., and Sutton, J. D. (1988). Compartment models for estimating attributes of digesta flow in cattle. Br. J. Nutr. 60, 571-595. Poppi, D. P., Norton, B. W., Minson, D. J., and Hendricksen, R. E. (1980). The validity of the critical size theory for particles leaving the rumen. /. Agric. Sei. [Camb.) 94, 275-280. Poppi, D. P., Minson, D. J., and Ternouth, J. H. (1981). Studies of cattle and sheep eating leaf and stem fractions of grasses. III. The retention time in the rumen of large feed particles. Aust. f. Agric. Res. 32, 123-137. Poppi, D. P., Hendricksen, R. E., and Minson, D. J. (1985). The relative resistance to escape of leaf and stem particles from the rumen of cattle and sheep. /. Agric. Sei. (Camb.) 105,9-14. Quigley, J. D., James, R. E., and McGilliard, M. L. (1986a). Dry matter intake in dairy heifers. 1. Factors affecting intake of heifers under intensive management. /. Dairy Sei. 6 9 , 2 8 5 5 2862. Quigley, J. D., James, R. E., and McGilliard, M. L. (1986b). Dry matter intake in dairy heifers. 2. Equations to predict intake of heifers under intensive management. /. Dairy Sei. 69, 2863-2867. Reid, C. S. W., Ulyatt, M. J., and Monro, J. A. (1977). The physical breakdown of feed during digestion in the rumen. Proc. N.Z. Soc. Anim. Prod. 37, 173-175. Reid, C. S. W., John, Α., Ulyatt, M. J., Waghorn, G. C , and Milligan, L. P. (1979). Chewing and the physical breakdown of feed in sheep. Ann. Rech. Vet. 10, 205-207. Reid, C. S. W. (1985). The progress of solid feed residues through the rumino-reticulum: The ins and outs of particles. In "Ruminant Physiology—Concepts and Consequences." (S. K. Baker, J. M. Gawthorne, J. B. Mackintosh, and D. B. Purser, eds.), pp. 79-84. School of Agriculture University of Western Australia, Perth, Australia. Reid, C. S. W. (1986). Digestive physiology; the challenges today and tomorrow. In "Control of Digestion and Metabolism in Ruminants." (L. P. Milligan, W. L. Grovum, A. Dobson, eds.), pp. 540-557. Reston Publishing, Reston, Va. Rutagwenda, T. (1989). "Adaptation of Indigenous Sheep and Goats to Seasonal Changes of Forage on a Semiarid Thornbush Savannah in Northern Kenya." Dissertation, School of Veterinary Medicine Hannover, F.R.G. Rutagwenda, T., Lechner-Doll, M., Schwartz, H. J., Schultka, W., and Engelhardt, W. v. (1990). Dietary preference and degradability of forage on a semiarid thornbush savannah by indigenous ruminants, camels and donkeys. Anim. Feed Sei. Technol. in press.

20 Retention Time of Particles in the Forestomach

481

Santini, F. J., Hardie, A. R., and Jorgensen, Ν. Α. (1983). Proposed use of adjusted intake based on forage particle length for calculation of roughage indexes. /. Dairy Sei. 66, 811-820. Schwartz, H. J. (1988). Verbesserte Nutzung natürlicher Weiden in den Trockenzonen Afri­ kas durch Besatz mit gemischten Herden. In "Beispiele Deutscher Agrarforschung in den Tropen und Subtropen." (J. H. Weniger, ed.), pp. 33-44.1.C.T., Berlin, F.R.G. Shaver, R. D., Nytes, A. J., Satter, L. D., and Jorgensen, Ν. A. (1986). Influence of amount of feed intake and forage physical form on digestion and passage of prebloom alfalfa hay in dairy cows. /. Dairy Sei. 69, 1545-1559. Shaver, R. D., Satter, L. D., and Jorgensen, Ν. Α. (1988). Impact of forage fiber content on digestion and digesta passage in lactating dairy cows. /. Dairy Sei. 71, 1556-1565. Staples, C. R., Fernando, R. L., Fahey, G. C., Berger, L. L., and Jaster, Ε. H. (1984). Effects of intake of a mixed diet by dairy steers on digestion events. /. Dairy Sei. 67, 995-1006. Stokes, S. R., Goetsch, A. L., and Landis, K. L. (1988). Feed intake and digestion by beef steers consuming and receiving ruminal insertions of prairie hay differing in level and particle size. /. Anim. Sei. 66, 1267-1274. Sutherland, Τ. M. (1988). Particle separation in the forestomach of sheep. In "Aspects of Digestive Physiology in Ruminants." (A. Dobson, and M. J. Dobson, eds.), pp. 43-73. Comstock Publishing Associates, Ithaca, N.Y. Thielemans, M. F., Francois, E., Bodart, C., and Thewis, A. (1978). Mesure du transit gastroin­ testinal chez le pore a l'aide des radiolanthanides. Comparaison avec le mouton. Ann. Biol. Anim. Biochim. Biophys. 18, 237-247. Thornton, R. F., and Minson, D. J. (1972). The relationship between voluntary intake and mean apparent retention time in the rumen. Aust. f. Agric. Res. 23, 871-877. Uden, P., Colucci, E., and Van Soest, P. J. (1980). Investigation of chromium, cerium and cobalt as markers in digesta rate of passage studies. /. Sei. Food Agric. 31, 625-632. Uden, P. (1988). The effect of grinding and pelleting hay on digestibility, fermentation rate, digesta passage and rumen and fecal particle size in cows. Anim. Feed Sei. Technol. 19, 145-158. Ulyatt, M. J., Waghorn, G. C., John, Α., Reid, C. S. W., and Monro, J. (1984). Effect of intake and feeding frequency on feeding behaviour and quantitative aspects of digestion in sheep fed chaffed lucerne hay. /. Agric. Sei. (Camb.) 102, 645-657. Ulyatt, M. J., Dellow, D. W., John, Α., Reid, C. S. W., and Waghorn, G. C. (1986). Contribution of chewing during eating and rumination to the clearance of digesta from the ruminoreticulum. In "Control of Digestion and Metabolism in Ruminants." (L. P. Milligan, W. L. Grovum, and A. Dobson, eds.), pp. 498-515. Reston Publishing, Reston, Va. Vaage, A. S., Shelford, J. Α., and Moseley, G. (1984). Theoretical basis for the measurement of particle length when sieving elongated particles. In "Techniques in Particle Size Analysis of Feed and Digesta in Ruminants." (P. M. Kennedy, ed.), pp. 76-82. Can. Soc. Anim. Sei. occ. publ. 1, Edmonton, Alberta, Canada. Van Vuuren, A. M. (1984). Effect of level of hay intake, method of marker administration, and stage of lactation on rate of passage through the reticulorumen. Can. J. Anim. Sei. 64, (suppl.), 80-81. Waghorn, G. C , and Reid, C.S.W.(1977). Rumen motility in sheep and cattle as affected by feeds and feeding. Proc. N.Z. Soc. Anim. Prod. 37, 176-181. Waghorn, G. C , Reid, C. S. W., Ulyatt, M. J., and John, A. (1986). Feed comminution, particle composition and distribution between the four compartments of the stomach in sheep fed chaffed lucerne hay at two feeding frequencies and intake levels. /. Agric. Sei. (Camb.) 106, 287-296. Waghorn, G. C , Shelton, I. D., and Thomas, V. J. (1989). Particle breakdown and rumen digestion of fresh ryegrass (Lolium perenne L.) and lucerne (Medicago sativa L.) fed to cows during a restricted feeding period. Br. J. Nutr. 61, 409-423. Waldo, D. R., Smith, L. W., and Cox, E. L. (1972). Model of cellulose disappearance from the rumen. /. Dairy Sei. 55, 125-129.

482

Μ. L e c h n e r - D o l l , Μ. K a s k e , a n d W . v . E n g e l h a r d t

Waldo, D. R. (1986). Effect of forage quality on intake and forage-concentrate interactions. J. Dairy Sei. 69,617-631. Warner, A. C. I. (1981). Rate of passage of digesta through the gut of mammals and birds. Nutr. Abstr. Rev. 51, 789-820. Welch, f. G. (1982). Rumination, particle size, and passage from the rumen. /. Anim. Sei. 54, 885-894. Welch, J. G. (1986). Physical parameters of fiber affecting passage from the rumen. /. Dairy Sei. 69, 2750-2754. Weston, R. H., and Kennedy, P. M. (1984). Various aspects of reticulorumen digestive func­ tion in relation to diet and digesta particle size. In "Techniques in Particle Size Analysis of Feed and Digesta in Ruminants." (P. M. Kennedy, ed.). Can. Soc. Anim. Sei. occ. publ. 1, 1-17 Edmonton, Alberta, Canada. Weston, R. H., and Cantle, J. A. (1984). The movement of undigested plant particle fractions through the stomach of roughage-fed young sheep. Can. f. Anim. Sei. 64, (suppl.), 322-323. Weyreter, H., Heller, R., Dellow, D. W., Lechner-Doll, M., and Engelhardt, W. v. (1987). Rumen fluid volume and retention time of digesta in an indigenous and a conventional breed of sheep fed a low quality, fibrous diet. /. Anim. Physiol. Anim. Nutr. 58, 89-100. White, R. G., Holleman, D. F., Schwartz, C. C , Regelin, W. L., and Franzman, A. W. (1984). Control of rumen turnover in northern ruminants. Can. J. Anim. Sei. 64, (suppl.), 3 4 9 350. Williams, C. B., Oltenacu, P. Α., and Sniff en, C. J. (1989). Application of neutral detergent fiber in modeling feed intake, lactation response, and body weight changes in dairy cattle. /. Dairy Sei. 72, 652-663. Wyburn, R. S. (1980). The mixing and propulsion of the stomach contents of ruminants. In "Digestive Physiology and Metabolism in Ruminants." (Y. Ruckebusch and P. Thivend, eds.), pp. 3 5 - 5 1 . MTP Press, Lancaster, England.