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VI. The Efficiency of Utilization of Digested Nutrients

VI. The Efficiency of Utilization of Digested Nutrients

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THE NUTRITIVE VALUE OF FORAGE CROPS



39



assimilation of the feed. Energy is also lost in the methane produced

from microbial digestion of carbohydrates within the rumen, and in the

waste products excreted in the urine. The metabolizable energy (ME) in

the forage:

ME = digestible energy - methane energy - urine energy



(14)



thus more usefully expresses the proportion of the energy in the feed

which is available for the metabolic and productive activities of the animal. To measure metabolizable energy precisely requires, in addition to

total collection of feces and urine, the measurement of methane production in a respiration chamber. For many purposes, however, an estimate

of methane production:

Methane (g.) = 2.4 I X



+ 9.80 (sheep; Swift ef al., 1948)



(15)



where X = grams of carbohydrate digested + 100, based on data from

respiration chamber experiments, is likely to be sufficiently accurate;

but wherever possible this should be checked, as Eq. (15) may not be

valid in novel feed situations -for instance, when milled dehydrated

forages are fed to ruminants (Blaxter and Graham, 1956). Furthermore,

Flatt ( 1 966) has shown that methane and urine production is not constant, but decreases as the level of feeding of a particular feed is increased. As noted earlier, digestibility decreases as level of feeding increases (e.g., Moe et al., 1965). These changes in digestibility and in

methane and urine production tend to compensate. As a result Flatt

( 1 966) found that the metabolizable energy content of a feed changes

relatively little with change in the level at which it is fed, but this conclusion is not in complete agreement with that of Blaxter (1962), who

concluded that metabolizable energy decreases with an increase in level

of feed intake. Such divergences are in fact to be expected, because

metabolizable energy is not thefixed characteristic of a feed that is sometimes implied. Urine energy, in particular, reflects the physiological status

of the animal, the animal with a high positive nitrogen balance (e.g., the

dairy cow, used by Flatt, 1966) giving a lower urine energy loss than one

with lower nitrogen balance (e.g., the mature sheep, used by Blaxter,

1962). Because of this the dairy cow may show less decrease in the

metabolizable energy of a feed than the mature sheep at feeding levels

above maintenance.

In general terms, Armstrong et af. ( 1964b) and Graham ( 1964) found

that the metabolizable energy of grass was about 81 percent of the digestible energy content, and could therefore be calculated from its energy

digestibility measured in vitro.



40



W. F. RAYMOND



3 . N e t Energy

The classical studies of Kellner and Armsby established that as feeds

become less digestible their content of metabolizable energy is less

efficiently used by the ruminant animal. The methods of expression of

useful energy used by the European workers (starch equivalent) and the

North American workers (net energy) were different, as were some of the

underlying concepts, but for some purposes the two systems can be

equated, 1 pound of starch equivalent being taken as equal to 1,071

kcal. of net energy.

These systems of feed evaluation accept that when the animal digests

and metabolizes food there is a production of heat within the body which

represents a net loss of energy that is an inevitable part of the utilization

of the food (an exception is when the animal is in a very cold environment, and can use this heat production to maintain body temperature

instead of needing to oxidize useful food for this purpose). In precise

terms, net energy (NE) is an incremental measure:

N E = (ME,



-



ME,)



-(HB



- HA)



(16)



where ME and H are the metabolizable energy and heat production from

the same feed fed at levels A and B. But for practical feed evaluation

it is treated:

Net energy = (metabolizable energy) - (heat production)

(17)

As feeds become less digestible an increasing amount of heat is produced

for each unit of metabolizable energy derived from the feed, so that the

net energy falls more rapidly than metabolizable energy or total digestible nutrients content (L. A. Moore et al., 1953):

N E = 1.393 x T D N



-



34.63 ( r = 0.977)



(18)



A similar result is achieved in the starch equivalent system by making a

correction, based on the crude fiber content of the feed, which is thus inversely related to the level of digestibility. This wastage of heat was considered to be due to the energy of digestion, and the increase in heat production with less digestible feeds was attributed to the increased energy

needed to eat and digest such feeds.

This somewhat imprecise concept, challenged by recent developments

in knowledge of ruminant digestion and metabolism, does still appear to

account for much of the difference in energy value between feeds.

B. THEROLEOF VOLATILE FATTY

ACIDSIN RUMINANT

METABOLISM

1 . The U s e of Volatile Fatty Acids as Energy Metabolites

It has long been known that among the main products of microbial



THE NUTRITIVE VALUE O F FORAGE CROPS



41



fermentation within the rumen are steam-volatile fatty acids, in particular

acetic, propionic, and butyric acids, with smaller amounts of isobutyric

and longer-chain acids. Early in the 1950’s it was shown that these acids

are absorbed from the ruminant digestive tract and provide a major source

of energy metabolites for the animal (reviewed by Annison and Lewis,

1959). Recent work has suggested that some 70 to 80 percent of the

energy supply of the ruminant on normal feeds is provided by volatile

fatty acids (A. C. I. Warner, 1964). These acids are produced by fermentation of a very wide range of feed substrates-sugars, cellulose, hemicellulose, proteins, etc. As I. W. McDonald ( I 968) has emphasized,

digestion within the rumen serves the remarkable function of converting

a most diverse range of chemical constituents in the feedstuffs eaten by

the ruminant into the relatively simple range of compounds that it absorbs and uses as metabolites.

The acid produced by fermentation of feed within the rumen comprises

mainly acetic, propionic, and butyric acids, but it was found that the proportions in which these are produced differs among classes of feeds: in

general, as feeds become less digestible the combined proportions of

propionic and butyric acids decreases, and that of acetic acid increases

(Rook and Balch, 196 1). This observation assumed particular significance

with the demonstration by Blaxter and his associates (Armstrong and

Blaxter, 1957; Blaxter, 1962) that these three acids appear to be used

by the ruminant with different efficiencies for different metabolic purposes. In a detailed series of calorimetric experiments these workers

showed that, when these acids were infused into the rumen in vivo, they

were used with equal efficiency for maintenance purposes (respiration,

circulation, etc.), but that acetic acid was much less efficiently used for

lipogenesis (body fat synthesis) than propionic and butyric acids.

These results indicated that the decrease in efficiency ofuse of metabolizable energy as feeds become less digestible might at least in part be the result of theassociated shift in rumen fermentation products from propionate

plus butyrate on highly digestible feeds to predominantly acetate on feeds

of low digestibility. The observation that the three acids were equally

efficiently used for animal maintenance purposes led Blaxter ( 1 962) to

propose a system of feed evaluation in which the efficiency of utilization

of metabolizable energy for maintenance (K,J is assumed to be constant,

and the same for all feeds, but the efficiency of utilization for lipogenesis

(fattening KJ)decreases as feed becomes less digestible, that is:

K , = constant



K j = 0.8lQ + 3.0



(19)



42



W. F. RAYMOND



where Q is the ME, expressed as a percentage of the gross energy in the

feed.

The concept that the efficiency with which the ruminant uses its digestible and metabolizable energy intake is largely determined by the pattern

of volatile fatty acid production within the rumen has had a most profound effect on ruminant research in the last decade. In many experiments in which feeds or rations have been compared, higher levels of

animal production have been recorded on the feed or ration giving the

higher proportion of propionate plus butyrate in the total rumen acidsand the conclusion has been drawn that the higher level of production

was the result of the higher proportion of these acids.

But this elegant explanation of differences between ruminant feeds

contains anomalies, and its generalized validity must now be questioned.

First, the original infusion experiments examined the efficiency of utilization of the different acids for lipogenesis in the mature sheep; they cannot

equally well explain the decrease in efficiency of bovine milk production

with decreasing level of feed digestibility, for as Rook and Balch (196 1)

indicated, acetic acid, the predominant acid produced in the rumen from

feeds of low digestibility, is more efficiently used for milk production

than is propionic acid. Neither is there any evidence that acetic acid is

less efficiently used than propionic or butyric acids for body protein

synthesis, which comprised only a small part of the body-energy gain of

the sheep used in the experiments reported by Blaxter; in fact Rook and

Balch ( 1 96 1) indicated that efficiencies may be in the reverse order.

Second, the conclusion that the ratio of propionic plus butyric acids to

acetic acid is closely related to feed digestibility does not hold for all

feeds: Terry and Tilley (1962) found very little relationship between

rumen acid pattern and forage digestibility, and showed that the molar

proportion of propionic acid in the rumen acids ( P ) was more closely

related to the soluble carbohydrate content (C) in a range of forages:

P



= 0.48C



+ 16.5



( r = 0.75)



(2 1)



As forages of the same digestibility can differ markedly in their content

of soluble carbohydrate, a system of feed evaluation, based on rumen

acid proportions, would indicate a more efficient utilization for lipogenesis of the metabolizable energy in a high-sugar than in a low-sugar

forage of the same digestibility. Yet Thomson (1964) found identical

energy gains when ryegrass samples of high or low sugar contents were

fed to lambs. There was also an indication that a higher proportion of the

energy gain by the lambs on the low-sugar grass (7 percent soluble

carbohydrate, 29 percent crude protein) was in the form of body protein



THE NUTRITIVE VALUE OF FORAGE CROPS



43



than on the high-sugar grass (19 percent and 16 percent), a result which

could be of economic significance. For, paradoxically, the one form of

animal production, lipogenesis, for which propionic and butyric acids

have been indicated as superior to acetic acid, is the one least required

by the meat industry and the consumer.

Third, while the measured differences in the proportions of volatile

fatty acids between rations have generally been in the predicted direction,

they have also nearly always been much too small to account for the observed differences in animal production. Blaxter and Wainman ( 1 964,

Fig. 4) showed a decrease of 1.091 in K f for each 1 percent increase in

the molar proportion of acetic acid in the rumen acids. In a comparison

of immature and mature ryegrass feeds, Armstrong ( 1 960) found the Kf

value of the immature feed to be 26 percent greater than of the mature

feed; the corresponding molar proportions of acetic acid in the rumen

acids, 61.0 and 65.4, would indicate a difference of only 5 percent in

KJ values. On the basis of these and other experiments, in which no overall relationship could be established between the molar proportions of

rumen acids in animals fed on different grass feeds and the efficiency of

lipogenesis, Armstrong (1964) concluded that mechanisms, in addition

to that based on rumen volatile fatty acids, must be sought for the observed differences in energy value between feeds.

Finally the concept of energy metabolism based on the rumen acids

indicated that the metabolizable energy of all feeds should be equally

efficiently used for maintenance, and that differences would occur only

in their use for productive purposes. However, Brouwer et al. (1961)

reported that the requirement of metabolizable energy for maintenance

of the 500-kg. cow increased from 11.3 Mcal. with an early-cut hay to

12.7 Mcal. for a mature hay. From a recalculation of earlier calorimetric

experiments, Armstrong ( 1964) concluded that the efficiency of utilization of metabolizable energy for maintenance (K,,J decreased with a decrease in feed digestibility (metabolizable energy concentration in the

feed, Q ) :



K,,, = 50.9 + 0.3759



(22)



From data on a wider range of feeds, Blaxter (1964) derived the

relationship:

K,,, = 54.8



+ 0.30Q



(23)



and Graham (1964) also concluded that metabolizable energy is less

efficiently used for maintenance as feeds become more fibrous, i.e., as

Q decreases.



44



W. F. RAYMOND



“It seems clear then that the earlier assumption that the metabolizable

energy of all feeds is used with equal efficiency for maintenance purposes

involved too wide an extrapolation of the results of experiments with

rumen infusions of pure volatile fatty acids. In effect it implied that a constant proportion of the M.E. of feeds of widely differing digestibilities is

absorbed from the rumen as volatile fatty acids. Armstrong ( 1 964) has

suggested that, with diminishing digestibility in a series of feeds, an increasing fraction of the M.E. is lost as heat of fermentation, and a lower

proportion absorbed as useful energy” (Raymond, 1966b).

It is also most likely that maintenance requirement itself will effectively increase as a result of the greater muscular energy involved in

chewing and movement of the larger quantity of more fibrous feed required to provide a given amount of metabolizable energy from a low than

from a high digestibility feed.

These mechanisms, viz. the decreased proportion of metabolizable

energy absorbed as volatile fatty acids and the increased energy of digestion as feeds become less digestible, could both also be expected to occur

in the utilization of metabolizable energy above maintenance. This increased wastage of energy might thus be expected to contribute to the

coefficient 0.8 1 in Eq. (20); the remainder of this coefficient may then be

accounted for by less efficient lipogenesis as a result of the increasing

proportion of acetic acid in the rumen acids when feeds of low digestibility

are fed.

This analysis of the original proposals of Blaxter (1962) offers some

explanation of the discrepancies noted. Thus both Kf and K , can be

expected to decrease with decreasing feed digestibility; the quite small

differences in rumen acid proportions often found could be adequate to

explain the residual differences in Kf between feeds of different digestibilities: the decreasing efficiency of the lactating animal with decreasing

feed digestibility would be due to the dominance of losses of energy in

digestion, despite the higher efficiency of use of acetic acid for milk

production (Rook and Balch, 1961). On this basis, the decreasing efficiency of utilization of metabolizable energy as feeds become less digestible would result mainly from the decrease in digestibility per se (as in the

original Kellner system) with a further decrease in efficiency for lipogenesis due to the less favorable rumen acid pattern, which is not implicit

in the Kellner system. This concept would place emphasis on level of

feed digestibility, rather than on rumen acid pattern, as the main determinant of the eficiency with which the digestible and metabolizable

energy in feeds are utilized by the ruminant.

Yet since 1964 the number of publications in which differences in



THE NUTRITIVE VALUE OF FORAGE CROPS



45



nutritive value between feeds have been attributed mainly to differences

in rumen acid patterns has increased, rather than decreased. It would be

invidious-and unhelpful - to summarize them here; but it does appear

that emphasis on this mechanism has diverted attention from differences

in feed digestibility and feed intake, which have often been neither controlled, nor measured, in these experiments.

This comment implies, not that the rumen acids are not important, but

that interpretations of animal production results based on rumen acid

patterns must be considered more critically. First, it is important, where

rumen acid proportions are measured, that this is done accurately. Many

experiments have relied on single samples of rumen fluid taken at a fixed

time after feeding; but the concentration and proportions of the volatile

fatty acids in rumen fluid can vary markedly throughout the day (Terry

and Tilley, 1964b), reflecting the pattern of feeding of a given forage

(I. H. Bath and Rook, 1963; Faichney, 1 9 6 8 ~or

) of a forage with concentrate ration (McCullough and Smart, 1968). The more irregular the

feeding, the wider the fluctuations in rumen acids and the greater the need

for an intensive sampling schedule.

2 . Rumen Condition and Rumen Acid Patterns

There is also need for further study of the causes of the particular

rumen acid patterns produced when different feeds are digested. Some

evidence suggests that these are the result of the conditions established

within the rumen by the particular feed and feeding regime adopted,

rather than of the digestibility of the feed per se. Thus there was a shift

from a higher to a lower acetate:propionate fermentation when the proportion of cereal in a mixed cereal-hay diet was increased, but I. H. Bath

and Rook ( I 965) showed that this shift could not be accounted for solely

by the increasing digestibility of the diet. I t is known that increasing the

proportion of cereal in the diet leads to a decrease in the pH of the rumen

content (P. K. Briggs et al., 1957; Topps et al., 1965). This led R. L.

Reid et al. (1 957), C . L. Davis et al. ( 1 964), and Raymond ( 1 966a) to

suggest that the rumen conditions associated with cereal feeding may

favor the microbial production of propionic and butyric acids and discourage the production of acetic acid. This could be the result of a shift

either in the bacterial population or in the nature of the end products of

fermentation. Much reported evidence is consistent with this hypothesis.

Thus C. L. Davis et al. (1964) found that sodium bicarbonate, fed with

concentrates plus limited alfalfa hay, increased pH and led to an increased acetate and decreased propionate proportion in the rumen acids.

Terry and Tilley (1963) reported a reduction in rumen pH and a de-



46



W. F. RAYMOND



crease in the acetate:propionate ratio when the level of feeding of S.24

ryegrass was increased. McCullough and Smart ( 1968) found that a corn

silage-flaked corn mixture, fed in four equal feeds, gave a fairly level

rumen pH throughout the day. When the grain and silage were fed separately, the rumen pH and rumen acetate level were both markedly depressed after the grain feeding, and did not increase until the silage was

fed. Faichney (1968b) found a wide fluctuation in rumen pH when

alfalfa pellets were fed in a single feed, with pH below 6.0 and an acetate:

propionate ratio below 3.5 during the period of maximum acid concentration in the rumen. When the same quantity of pellets was fed in eight

feeds, rumen pH remained above 6.0 and the acetate:propionate ratio

was in the range 5.3 to 5.7 throughout the 24 hours. Von Kaufmann and

Rohr (1967) have summarized the changes in rumen acid patterns with

changes in rumen pH, measured in their own experiments (Fig. 4) which

are in close accord with the foregoing observations.



RUMEN pH

FIG.4. Schema of the changes in the molar contents of volatile fatty acids and lactic acid

within the rumen at different levels of rumen pH: at low pH levels, either lactic or propionic acid may occur under different conditions. (From von Kaufmann and Rohr, 1967.)



At present these results indicate an association between rumen pH

and rumen acid patterns, rather than a direct causation, but they help

to explain the conclusion that rumen acid patterns can differ between

feeds of the same digestibility: for rumen pH is clearly not solely determined by level of feed digestibility, but depends also on feed composition and pattern of feeding. This has led C. L. Davis et al. (1964) and

McCullough and Smart ( 1 968) to suggest that it may be possible to predetermine the pattern of feeding of a given ration so as to shift the



THE NUTRITIVE VALUE OF FORAGE CROPS



47



rumen acid pattern in the required direction. This could be toward a propionate fermentation if body fat synthesis is required. Of much greater

significance could be the possible control of milk composition; thus low

levels of butterfat are often found in milk produced from rations containing low levels of fiber, and this has been shown to result from the low

production of acetate (a precursor in milk-fat synthesis) in the rumen of

cows fed on these rations (Balch et al., 1952). The above authors have

suggested that by feeding concentrates and limited roughage together

(McCullough and Smart, 19681, or by supplementing with sodium bicarbonate (C. L. Davis er d.,1964), mean rumen pH would be increased,

and that this might lead to an increased acetate production and increased

butterfat levels in milk. Conversely, too low a level of rumen propionate

appears to reduce the level of solids-not-fat in milk. Baumgardt (1967)

has suggested that the maximum overall efficiency of use of metabolites

for milk production occurs with an acetate:propionate molar ratio of

2.75:1, and this could indicate the target toward which feeding regimes

should aim; this ratio is very close to that indicated by von Kaufmann

and Rohr ( 1967) in Fig. 4.

In this perspective, the patterns of rumen volatile fatty acids produced

from different forages are clearly of interest and importance. Although,

as noted above, these patterns may not be mediated directly through

rumen pH, the association seems close enough to indicate that, as the pH

at which forage is digested in the rumen decreases, there is likely to be a

shift in the products of rumen fermentation from acetic acid to propionic

plus butyric acids. Thus forages of high soluble carbohydrate content

tend to give the lowest rumen pH and the highest propionate values

(Eq. 21). Application of nitrogen fertilizer can decrease the soluble

carbohydrate content of grass (McIlroy, 1967). When this grass is fed

it gives a higher rumen pH level and a higher proportion of acetate in the

rumen acids than similar but unfertilized grass (Thomson, 1964; A. M.

Bryant and Ulyatt, 1965; Grimes, 1967). R. L. Reid and Jung (1965)

found no effect on rumen acid patterns resulting from nitrogen fertilization of grass; in that experiment there was also no effect on the soluble

carbohydrate content of the grass.

In these and other experiments no clear relationship has been shown

between rumen acid pattern and level of forage digestibility. Thus Italian

ryegrass of high digestibility and high sugar content has given 62 percent

of acetate in the rumen acids; white clover of the same digestibility has

given 67 percent (Terry and Thomson, unpublished). These results

with white clover at the Grassland Research Institute differ, however,

from those in New Zealand, where higher levels of sugar content and



48



W. F. RAYMOND



lower proportions of lumen acetate have been found with white clover

(R. W. Bailey, 1964).

The recent emphasis on lumen acids has also led to investigations of

in vitro techniques of estimating rumen acid production, despite the

indication by A. C. I. Warner (1964) of the assumptions involved in extrapolating from in vitro to in vivo results. The more recent work reported

here reinforces this qualification. Thus Raymond and Terry ( 1 966) and

Griffiths (1967) have reported that the proportions of acids produced in an

in vitro system can be changed by altering the pH of the system: a reduction in pH produces, as might be predicted, a shift from acetate to

propionate or butyrate production. This means that the acid production

measured in an in vitro system may reflect the pH at which the system is

buffered, rather than the nature of the feed being tested. As rumen pH

in vivo can vary between 5.0 and 7.0, in vitro systems are most unlikely

to give estimates of rumen acid patterns free from operator bias. It

might be suggested that the in vitro system should be buffered at the pH

measured in vivo when the test feed is fed-but the rumen acids could

then be measured in vivo. However, the different activity in vitro than

in vivo (A. C . I. Warner, 1964) must indicate the need for further research

before in vitro systems can be considered for the assessment of rumen

acid patterns.

Increasing attention is also being given to techniques for measuring the

rates of production of the volatile fatty acids during microbial digestion

of feeds within the rumen in vivo. One technique is based on measurement of the rate of isotope dilution of the different acids labeled with

I4C (Bergman et al., 1965; C . L. Davis, 1967; Weller et al., 1967), and

this has also been used to study the absorption of the acids in different

parts of the digestive tract (Weston and Hogan, 1968). In an alternative

technique, samples of lumen contents are removed and incubated in

vitro, and the rate of acid production is measured over periods of less

than 40 minutes to maintain physiological relevance. The acid production

is either extrapolated back to zero time (A. C . I. Warner, 1964) or used

as a direct estimate of rate of acid production in vivo (Faichney, 1968a).

These techniques, applied to forages, must increase our basic understanding of the nutritive value of these feeds; Leng et al. ( 1 968) have

recently reported studies with grazing sheep, for which they used an

isotope dilution technique.



c. THEUTILIZATION



FORAGES

I . The Digestion of Protein within the Rumen

OF THE C R U D E PROTEIN IN



Many experiments have shown that the digestibility (Eq. 2) of the



THE NUTRITIVE VALUE OF FORAGE CROPS



49



crude protein (percent N X 6.25) in forages is very closely related to the

crude protein content (e.g., Minson and Kemp, 1961; O’Shea and

Maguire, 1967). As with other feed components, Eq. (2) measures the

“apparent” digestibility of the feed nitrogen: the “true” digestibility

is very close to 100% (Van Soest, 1967), and the decrease in “apparent”

digestibility results from the relatively constant excretion of endogenous

fecal nitrogen per unit of feed dry matter eaten.

The utilization of this “digestible protein” fraction has been the subject of much study; this has established that the rumen microbial population digests and modifies almost all the nitrogenous constituents eaten in

the ruminant diet, so that the nature of these nitrogenous constituents

may bear little relation to the form in which the nitrogen is absorbed from

the digestive tract.

The first stage in this reorganization of the feed protein is deamination, the ammonia produced forming one of the main nitrogen substrates

for the rumen microbes which proliferate within the rumen medium, to

bring about the digestion of the feed polysaccharides, characteristic of

ruminant digestion. Entrained organisms then pass with the undigested

feed residues from the rumen into the hind tract, where they are subjected to intense proteolytic action in the acid conditions in the

abomasum. Here a high proportion of the microbial protein is broken

down into amino acids, which are then absorbed and used as the main

source of amino acids by the ruminant animal (Hungate, 1966).

It is for this reason that the biological value of feed protein, in the

terms appropriate to the nonruminant, has little relevance for the ruminant. As I. W. McDonald ( I 968) has emphasized, the biological value

will be determined by the amino acid composition of the microbial protein digested in the hind tract, which need bear little relation to the

amino acid composition of the feed. The main consideration then is with

the factors that determine how efficiently the feed protein (nitrogen) is

converted into microbial protein.

Immediately after ingestion of food by the ruminant, there is a rise in

the ammonia level within the rumen as a result of microbial degradation

of nitrogenous compounds. However, the rate at which this ammonia is

released may be greater than the rate at which the total rumen population

can utilize it, and excess ammonia may then be absorbed through the rumen epithelium into the blood, there to be detoxified and excreted in the

urine (I. W. McDonald, 1968). The efficiency of feed protein utilization

thus depends on the relative rates of the two processes of ammonia release within the rumen and ammonia assimilation into bacterial protein,

and optimum feeding should ensure that the former is not greatly in

excess of the latter, so that ammonia absorption from the rumen is mini-



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VI. The Efficiency of Utilization of Digested Nutrients

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