The first internal changes to be correlated with feelings of hunger were the so- called hunger contractions of the stomach. However, vagotomy, which abolishes these contractions, does not seriously interfere with the regulation of food intake in poultry or pigs. In the chicken hunger contractions occur in the crop and in the proventriculus and gizzard, whereas with ruminants there is a decrease in the frequency of contractions during periods without food.
Distension of a balloon in the stomach depresses intake, but does not completely abolish feeding, while intra-gastric administration of the amount of food normally taken in a meal also depresses, but does not totally inhibit, feeding showing that stomach distension is not the only controller of intake.
Clearly, the presence of food in the stomach and/or its passage through and absorption from the intestines are important factors in inducing satiety, but not the sole factors.
Dilution of food with non-nutrients, or ‘dietary bulk’, reduces the con- centration of nutrients in the food so that more food is eaten before nutrient- induced satiety occurs. However, the volume accumulating in the stomach, and later passed to the intestines, may be limited by the capacity of these viscera and a physical, distension-induced satiety may result. This is particularly true in ruminant animals with foods high in fibrous constituents that have to stay in the rumen for many hours. Chapter 11 discusses this aspect in more detail.
Poultry
Stimulation of the crop by filling it with water, saline or a balloon, or cooling the crop, all depress food intake (Richardson, 1970). Such treatments involve considerable disturbance and there would have been less stress if the crop were loaded via a surgically implanted cannula. Introduction of 12 or 20 ml of a paste of food into the crop via a cannula depressed food intake (Shurlock and Forbes, 1981b). To determine whether bulk or nutrients were involved in this response, glucose solutions were given into the crop. Amounts > 1.5 g in 10 ml of water significantly depressed food intake during the 1 h after injection, while at least 3.8 g was necessary to depress intake over a 3-h period. The effect of additional amounts of glucose was greatest with loads of up to 4 g, and with greater weights there was little additional effect on food intake, suggesting that the receptor(s) involved are maximally stimulated by 4 g. Even so, intake was only depressed by one-half of that of the control during the 1 h after injection and by one-third during the 3 h after.
Feedbacks from the Gastrointestinal Tract 43
Although the results of this experiment might indicate the presence of receptors sensitive to glucose in the crop, or lower down the digestive tract or post-absorptively, they do not rule out the possibility of distension receptors, because more concentrated solutions take up more water and therefore occupy more space; osmoreceptors might also be present. Shurlock and Forbes (1981b) therefore compared the effects on feeding of glucose and the non- absorbable substances, sorbitol and potassium chloride, all at an osmolality of 3 osm. During the 3 h after injection into the crop, the food intakes were depressed to an equal extent by all three solutes. It was concluded that glucose introduced into the crop was probably not, therefore, influencing intake by stimulating post-absorptive receptors, but by an osmotic or distension effect.
Mechanoreceptors are to be found in the muscular stomach of the chicken, and both the crop and the gizzard are well innervated by branches of the vagus nerve. The crop is, however, a diverticulum, and food often bypasses it; thus it cannot be the main controller of meal size. Following surgical removal of the crop, daily intake is normal once the immediate effects of surgery and the adaptation period are over (Savory, 1985). Cropectomy is followed by decreased meal size and increased feeding frequency, although eventual oesophageal dilation often leads to a gradual return to normal meal frequency.
Introduction of food slurry into the intestines of growing turkeys increased the proportion of boli entering the crop during an evening meal by decreasing the proportion of boli travelling directly to the gizzard (Jackson and Duke, 1995). A slowing of stomach emptying by the presence of digesta in the intestines is a general feature of the control of the digestive tract, making it difficult to pinpoint the site of effects of artificial or natural changes.
Pigs
Indirect evidence of a physical limit to intake in the pig has been obtained from observations of the effects of dietary dilution. Pigs attempt to compensate for dilution of the food by increasing their intake when its energy concentration is reduced. Although there appear to be no reports in the literature of balloon inflation in the porcine stomach, loading young pigs with hypertonic saline or water equal in volume to the volume of milk taken voluntarily after a 3-h fast depressed intake. As pigs grow older they can compensate better for diet dilution (see Chapter 11).
Pekas (1983) loaded the stomachs of young pigs daily through a cannula, which led to a reduction in voluntary intake that almost exactly compensated for the weight of food introduced. When loading was carried out on 4 days/week, compensation was incomplete on these days so that total intake increased.
However, a reduction of voluntary intake on the other three days of each week led to weekly intakes, growth rates and carcass compositions indistinguishable from those of controls. Long-term (or at least medium-term) control mechanisms are involved, therefore.
The rate at which the stomach discharges its contents into the duodenum has an important influence on the signals generated by that part of the intestine
and is partly controlled by the quantity and quality of duodenal contents.
Infusion of fats and products of lipolysis into the stomach was compensated almost exactly by reduced food intake, suggesting that the rate of stomach emptying plays a major part in determining meal size. Glucose infusions into the stomach similarly depress intake, but this effect can be ascribed to intestinal osmotic or caloric effects of the glucose that delay stomach emptying and prolong gastric distension.
Ruminants
As already mentioned in Chapter 1, a considerable body of evidence had been built up by about 1960 to support the concept that the food intake of ruminants was restricted primarily by ruminal capacity; this was reviewed by Balch and Campling (1962). It is clear that there are also effects of the VFAs produced by fermentation, and of the osmolality of ruminal contents, and it is proposed in Chapter 10 that these various factors are integrated in an additive manner. Dietary effects on intake mediated by the rumen are covered in Chapters 11 and 12.
Physical aspects
It is generally considered that the voluntary intake of forages is limited by the capacity of the digestive tract, particularly the rumen, to store and allow passage of digesta (see review by Allen, 1996). This is based on observed relationships between intake and digestibility, rate of digestion, fibre content and other indicators of the residence time of material in the rumen. In addition, placing bulky objects such as water-filled balloons in the rumen results in reductions in forage intake, and mechanoreceptors have been demonstrated in the ruminal wall whose firing rate is increased by stretch, with afferent neurones in the vagal nerves carrying information to the gastric centre of the medulla oblongatain the CNS, as described by Leek (1986).
CORRELATIONS BETWEEN RUMINAL CAPACITY AND INTAKE Not only is intake affected by the rates of digestion and passage, but also by the capacity of the digestive tract, principally the rumen. Positive correlations have been found between level of intake and the weight of the empty reticulo-rumen, but cause and effect are difficult to establish. There are positive correlations between the weight of voluntary intake of forage just before slaughter and the weight of ruminal contents at slaughter in cattle (Tayler, 1959), but the causality cannot be established with certainty.
Increases in the volume of other abdominal organs, such as abdominal fat or the pregnant uterus, can apparently cause compression of the rumen and a reduction in food intake. Tayler (1959) found a negative correlation between the weight of abdominal fat and the intake of herbage in cattle. In late pregnancy there is an increase in the girth of the abdomen, but this is not always great enough to accommodate the growth of the uterus. Although the rate of passage
Feedbacks from the Gastrointestinal Tract 45
of particles of forage food through the digestive tract is increased during pregnancy, under some circumstances this is not enough to prevent a limitation of voluntary intake (see Chapter 16).
For animals of any given size, the fatter they are the heavier they are, so intake is often inversely correlated with body weight. On the other hand, there is a positive relationship between intake and body weight in growing animals, and between mature animals of different skeletal sizes but of equal fatness.
ADDITION OF MATERIAL TO THE RUMEN Addition of food material directly into the rumen through a fistula reduces subsequent intake (Hodgson, 1971a) but, of course, supplies nutrients as well as bulk. Removal of digesta from the rumen is followed by increased intake, but this removes a source of nutrients as well as physical bulk, so that physical and metabolic factors are again confounded in such situations.
In the early 1960s, Campling and Balch conducted a series of experiments using a more critical approach. One of their methods was to insert balloons via a fistula into the rumen of non-pregnant, non-lactating mature cows; the balloons were then filled with water and the effect on intake during a 4-h period of access to food was noted. When 50–100 l of water-filled balloons were introduced for 10–14 days, there was a 0.54 kg/day decrease in dry matter intake (DMI) for each 10 l of water (Campling and Balch, 1961). If the water was added directly into the rumen of cattle there was no effect on intake, even when large quantities were involved (45 l). With sheep, addition of 8 l of water directly into the rumen had no effect on forage intake, while inclusion of only 2 l in a balloon depressed intake by 27% (Davies, 1962). There is often a negative relationship between the water content of grass or silage and voluntary intake; water trapped in stems and leaves acts more like water in balloons than free water.
It is likely that physical aspects were unduly emphasized as a result of the approach adopted in the work of Balch and Campling, because the 20-h fast that preceded each feeding period would leave the animals in considerable nutrient deficit, causing them to need to eat a much larger amount than would otherwise be eaten during such a small part of the day. Also, the use of ruminal DM as a measure of fill is inappropriate, as volume is related more closely to total weight, i.e. wet weight, of the ruminal contents.
More recent studies using balloons in the rumen of lactating cows fed grass silage (Anil et al., 1993) showed that there was a 70 g DM decrease in intake for every additional litre of water put in the balloon over a 3-h period, and that this response was approximately linear over the range 0–25 l – similar to the 54 g DM/l decrease noted by Campling and Balch (1961) with non-lactating cows fed on hay. This approach has been extended to include gradual increases in the volume of balloons in the rumen of cattle by Mowatt (1963), who found little evidence of a compensatory increase in ruminal capacity.
However, some recovery of DM intake towards pre-treatment levels was seen in sheep with balloons maintained in the rumen when fed on a pelleted diet, but not when fed on straw (Egan, 1972).
A single, large balloon in the rumen might interfere with the normal flow of materials and, at worst, block the reticulum and prevent onward flow of digesta.
An alternative is to use many small balls, and tennis balls have been used for this purpose (Schettiniet al., 1999). Steers fed a low-quality forage diet had 50 or 100 balls placed in the rumen, with a specific gravity (SG) of either 1.1 or 1.3, for 18-day periods, of which the first 10 days were for adaptation. There were significant effects on intake of both number of balls and of SG, even though increasing the SG did not increase the volume (see Fig. 3.1).
As both SGs used were higher than the SG of ruminal fluid, it is assumed that all the balls eventually sank to the bottom of the posterior ventral sac of the rumen, where they would directly stimulate the mechanoreceptors in that region, as well as exerting a stretching effect on the ruminal wall more dorsally, where receptors are more numerous. The effects of volume and SG were approximately additive, supporting the additivity hypothesis proposed in Chapter 10. Note, however, that the authors conclude by saying: ‘The large change in ruminal mass and volume as a function of the experimental treatments in our study … resulted in a relatively small change in the voluntary intake of a hay diet. This suggests that factors other than distension of the gut have a large influence on voluntary intake of low-quality forage diets by ruminants.’
The effect on food intake of balls or balloons in the rumen would be predicted to be greater with a more fibrous diet than with a more concentrated one, given the belief that physical factors are more important in the control of forage intake as compared with concentrates. When lactating cows were fed on diets containing either 250 or 350 g NDF/kg (low- and high-fibre, respectively), and plastic containers of water (each of 500 ml) were inserted into the rumen to occupy 25% of pre-trial rumen volume for each cow, food intake was significantly decreased by the addition of ruminal inert bulk when the high-fibre diet was fed, but had no effect with the low-fibre diet (Dado and Allen, 1995).
Feedbacks from the Gastrointestinal Tract 47
Fig. 3.1. Effects of adding 50 or 100 tennis balls, SG 1.1 or 1.3, to the rumen on daily intake of low-quality hay. Shaded bars, weight of balls (kg); open bars, volume of balls (l); solid bars, intake (kg DM/day); C, control (from Schettini et al., 1999).
With the former food, the objects displaced an equal volume of ruminal contents, suggesting that this food ‘filled’ the rumen; food intake was depressed.
Overall, therefore, as far as the voluntary intake of long forages is concerned, ruminal distension with balloons and similar objects has consistent and predictable effects, but ones that are not as large as might be expected from the volume displaced.
As an alternative experimental technique for demonstrating effects of ruminal fill on intake, Welch (1967) introduced into the rumen via a fistula 150 g of polypropylene fibres, each 30 cm in length, which were too long to exit the rumen. Intake of hay was depressed to 33% of control values and remained low.
With shorter fibres (3.5 or 7 cm), regurgitation was possible so that the fibres were broken down by re-chewing and fragments were found in faeces; intake was initially depressed, but recovered during the few weeks after administration of the fibres. Such manipulations are apparently not unpleasant, as sheep voluntarily consume polypropylene fibres when offered a fibre-free diet.
Muscular activity of the reticulo-rumen causes particles of digesta to rub against the papillae, stimulating the epithelial receptors, but the role of these receptors in the control of feeding is unclear. Baumont et al. (1990) placed blocks of expanded polystyrene in the rumen that floated on top of ruminal fluid so that they would stimulate tactile responses as well as increasing the bulk of ruminal contents. Hay intake was significantly reduced by 2 l of cubes, but there was no effect on the frequency of reticulo-ruminal contractions during eating.
However, the frequency of contractions during rumination was increased and more periods of rumination occurred. The polystyrene blocks became rounded during their stay in the rumen, showing that they must have been rubbing on the ruminal papillae, but their bulk meant that they were also likely to have been stimulating the distension receptors.
Baumont et al. (1990) provided tactile stimulation of the dorsal ruminal papillae without distension by means of a stiff brush via the fistula. This induced pseudo-rumination and extra-reticular contractions in sheep given a non-stimulating liquid diet to a similar extent as did a small amount of hay or 1 l of polystyrene cubes. On the other hand, insufflating the rumen with air for 5 min or adding 2 l of a buffer solution – which would cause distension but not stimulate tactile receptors – did not induce pseudo-rumination and had no effect on contractions. These results suggest that the use of a balloon in the rumen might not mimic all of the effects of forage, especially if the balloon gets dragged down into the rumen away from the sensitive areas of the reticulum and the cranial dorsal sac of the rumen.
DIGESTION AND PASSAGE OF FOOD There is an overwhelming amount of literature on positive relationships between extent and/or rate of digestion of forages and voluntary intake by ruminants. In interpreting these data it is necessary to remember that the evidence from such relationships, that intake is limited physically, is circumstantial.
The more digestible the food, the less indigestible material remains to occupy space in the rumen. By the mid-1960s it was becoming clear that this positive relationship did not continue to hold true with foods of very high
digestibility, and Baumgardt (1970) reviewed the evidence that intake is controlled to balance energy requirements when the food is highly digestible and of small particle size. With highly digestible long forages, however, intake continues to be positively related to digestibility, even at the very highest level of digestibility (see review by Minson, 1982).
Ruminants eating forages have to trade off the advantage of holding the food in the rumen for a long time to allow extensive digestion against the advantage of moving digesta along the tract to allow for further food intake.
While relationships are found between the digestibility of the diet and voluntary intake (see Chapter 11), the total extent of digestion by the whole alimentary tract is not sufficient to give an adequate understanding of the physical limit to intake, as it depends not only on the physical form of the food, but also on its potential to be digested. Digestibility is the product of the retention time in the rumen and the degradation characteristics of the food concerned. The longer a portion of food stays in the rumen, the closer it will come to being digested to the maximum extent possible, i.e. its potential digestibility, but factors such as level of feeding and ruminal capacity cause variations in residence time and therefore in actual digestibility. Increasing the rate of passage of food particles by grinding forages results in increased levels of voluntary intake, while the extent of food digestion is reduced due to the decreased time spent by each particle in the digestive tract.
The degree to which food particles are digested in the rumen could be as important as whole-tract digestibility. Several studies have found that the intakes of different hays were closely related to the rate of disappearance of hay from Dacron bags in the rumen (potential ruminal degradability). Intakes have often shown a much closer relationship with this than with digestibility or rate of degradation, making ruminal degradability a useful predictor of intake. For example, a very close fit was obtained for browse plants fed to goats, when the independent variables included the digestion rate constant (c from the equation p = a + b(1–ect), see Chapter 11), the soluble fraction of the food and the insoluble but fermentable fraction of the food. As Dacron bag studies are tedious, the measurement of the rate and amount of gas production of samples of foods incubated in vitrowith ruminal contents as a measure of degradation is a very promising method for predicting intake of forages (Getachew et al., 1998).
Rates and extents of breakdown of forage particles depend in part on the animal – the time and vigour devoted to chewing, for example – but are to a great degree dependent on the physical and chemical characteristics of the plant material being eaten. The subject of relationships between plant structure and breakdown in the rumen is well covered by Wilson and Kennedy (1996).
They make the vital point that genetic modification of herbage plants to make their tissues more readily digested by ruminants is certain to reduce the strength of stems and leaves during growth, leading to increased likelihood of lodging, i.e. collapsing in heavy wind and/or rain. Thick cuticles, inimical to digestion, are very protective during drought conditions; plant toxins reduce attacks by pests; endogenous antimicrobials deter infections of the living plant but may also reduce microbial attack in the rumen.
Feedbacks from the Gastrointestinal Tract 49