©2014 Poultry Science Association, Inc.
Function of the digestive system1
Birger Svihus2
Norwegian University of Life Sciences, PO Box 5003, N-1432 Aas, Norway
Primary Audience: Academic Nutritionists, Industrial Nutritionists
SUMMARY
The tremendous amounts of feed handled by commercial poultry breeds require an optimally
functioning digestive tract. Functionality of the different segments of the digestive tract may
be affected by diet and feeding systems, however. Retention time, moisture content, and pH of
contents in the crop are, to a large extent, determined by feeding systems, where intermittent
feeding is necessary for a stimulation of crop use. Retention time and pH of the gizzard contents
are similarly affected by access to structural components, such as whole cereals or coarse fibers.
These materials will stimulate normal development of the gizzard, increase retention time, and
decrease pH. less is known about characteristics of an optimally functioning small intestine,
but stimulation of gizzard development will possibly improve functionality of the small intestine through a better feed flow regulation. Functionality of the digestive tract will possibly
have a large effect on response to dietary manipulations (e.g., enzyme and pre- or probiotics
addition), and therefore needs to be taken into consideration in experimental design and results
interpretation.
Key words: crop storage, gizzard function, cecum, passage rate
2014 J. Appl. Poult. Res. 23:306–314
http://dx.doi.org/10.3382/japr.2014-00937
INTRODUCTION
The digestive tract of the modern chicken has
had to adapt to tremendous changes due to intensive breeding for number of eggs for layers
and growth rate for broiler chickens. A 30-d-old
male broiler chicken, for example, consumes
around 10% of its live weight per day, and the
digestive tract will thus have to handle slightly
over 7 g of feed per hour. To put this in perspective, a 75-kg person would have to eat more
than 450 g per hour during the 16 awake hours
to have an equal food intake relative to BW, or
equivalent to 1 loaf of bread.
1
It is logical to assume that this high production rate, and thus high feed intake, makes the
digestive tract vulnerable to impaired functionality. The impaired functionality can be due to
insufficient development of the digestive tract,
or it can be due to external factors, such as microflora or insufficiencies in the feed. In severe
cases of impaired functionality it may be easy
to observe this dysfunction, for example where
Clostridium perfringens has resulted in necrosis
of the digestive tract wall, or where a total lack
of structural component has resulted in a dilated proventriculus and a nonfunctional gizzard.
However, in many cases, a suboptimal function-
Presented as a part of the Informal Nutrition Symposium “From Research Measurements to Application: Bridging the Gap”
at the Poultry Science Association’s annual meeting in San Diego, California, July 22–25, 2013.
2
Corresponding author: [email protected]
Svihus: INFORMAL NUTRITION SYMPOSIUM
ality may take place without such conspicuous
signs of malfunction. In nutritional sciences, a
very important task is to assess performance and
digestibility when different feeds and additives
are used. An impaired digestibility may be due
to the nature of the diets, or it may be due to a
dysfunctional digestive tract. Thus, it is important to understand what characterizes a functional digestive tract when birds shall be used
for dietary assessment. Also, it is important to be
aware that conditions of the experiment may affect functionality. For example, it is well known
that mash diets will result in a far lower feed
intake than when pelleted diets are used, as in
commercial practice. The lower feed intake will
result in a lower demand on the digestive tract,
and thus may give unrealistically high digestibility values.
In general, the digestive tract of poultry is
similar to other animal species. The feed material is ingested, moisturized, ground into small
particles, acidified, and attacked by endogenous
enzymes. The macronutrients are broken down
into monosaccharides, dipeptides and amino
acids, free fatty acids, and monoglycerides that
can be absorbed. However, bird-specific peculiarities exist, as described herein.
CROP FUNCTION
The food is not moisturized and ground in the
mouth, but is rather swallowed without any considerable processing (except in some species,
where the outer shell of some seeds is removed).
After swallowing, the feed can either enter the
crop or pass directly to the proventriculus or gizzard when this section of the digestive tract is
empty [1]. The storage capacity of the gizzard
is usually limited to a maximum of 5 to 10 g of
feed, and thus storage in the crop is required if
large quantities of feed are to be consumed. Although the extent to which feed entered the crop
varied greatly among individual birds, 50% of
the diet eaten in the morning after an overnight
fast and in the afternoon before darkness, on
average, entered the crop [2]. Observations of
commercial broilers on ad libitum feeding have
shown that they eat in a semicontinuous manner
[3], and that the crop is not used to its maximal
capacity under such conditions. In fact, the crop
is mainly thought to have a role as a storage organ for birds under situations of discontinuous
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feeding, and is not involved in feed intake regulation [2]. Ad libitum feeding will thus probably
discourage use of the crop. Although large variations among individual birds were observed,
data from our laboratory have confirmed that ad
libitum-fed broiler chickens do not use the crop
to any significant extent [4]. Instead of storing
feed in the crop, they eat small meals approximately every half an hour [5]. Even though more
data are needed, this indicates that ad libitumfed birds will adapt a habit of letting feed bypass
the crop. When birds are trained to intermittent
feeding, however, feed intake changes to mealtype feeding, which involves transient storage of
large quantities of feed in the crop. Boa-Amponsem et al. [6] also found negligible amounts of
feed materials in the crop of ad libitum-fed fastand slow-growing broilers, whereas intermittent
feeding resulted in significantly increased crop
contents. Barash et al. [7] showed that birds
adapted to 2 meals per day were able to consume approximately 40% of the daily intake of
ad libitum-fed birds during each meal. It has
been shown that broiler chickens use both the
crop and the proventriculus or gizzard as storage
organs for food when adapted to long periods of
food deprivation [8]. Barash et al. [9] observed a
significant increase in weight and feed-holding
capacity of both crop and gizzard when chicks
were fed meals 1 or 2 times per day instead of
ad libitum. Thus, Buyse et al. [8] and Svihus et
al. [10] still found considerable amounts of feed
in the crop of broiler chickens 5 and 4 h after last
feeding, respectively. In a recent unpublished
experiment, 33-d-old broiler chickens adapted
to intermittent feeding in average had around 40
g of feed DM in their crop 1 h after commencement of feeding, and the average amount was
still 10 g 5 h later.
This serves to explain the main role of the
crop, namely as a transient store for ingested
food. This is a necessity for birds, as the stomach region (the proventriculus and gizzard) does
not have a large storage capacity. The crop is
not thought to have any direct nutritional roles,
as it does not secrete enzyme and considerable
absorption has not been reported. However, a
considerable moisturization takes place there,
which may aid the grinding and enzymatic digestion further down the digestive tract. Also,
any exogenous enzymes and other components
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that are activated by moisturization will potentially be able to exert their effect in the crop. Results indicate that the contents of the crop are
gradually moistened; reaching 50% moisture
within approximately 60 min [4]. As the crop
is the only segment of the digestive tract where
water content may be a limiting factor for enzyme activity, the time needed for soaking may
be a critical factor in determining the efficacy
of an exogenous enzyme, provided that the crop
is indeed a major site of enzyme activity. In the
crop, large variations in pH have been observed.
In several experiments, pH has been found to be
above 6, whereas a pH between 4.5 and 5.9 has
been observed in other experiments. Feeds for
monogastrics are usually reported to have a pH
varying between 5.5 and 6.5 (e.g., [11]). Thus,
it is reasonable to assume that once feed enters
the crop, pH will be similar to that of the feed.
However, a prolonged retention time in the crop
is associated with a considerable fermentation
activity, which produces organic acids and reduces pH [12]. Thus, different retention times,
and therefore different extents of fermentation,
may explain pH variation among experiments.
In accordance with this, Bolton [13] observed
that the pH dropped as retention time increased,
but only for chick feed and not for layer feeds,
the latter having a higher initial pH and a much
higher buffering capacity, presumably due to
higher calcium carbonate content. Our unpublished results showed that crop contents collected from meal-fed broiler chickens 2 h after
feeding had an average pH of 4.8. Thus, it is
clear that functionality of the crop is to a large
extent dependent on feeding systems or feeding
behavior, which subsequently will influence dietary effects.
PROVENTRICULUS
AND GIZZARD FUNCTION
The proventriculus and gizzard are the true
stomach compartments of birds, where hydrochloric acid and pepsinogen are secreted by the
proventriculus and mixed with contents due to
muscular movements in the gizzard. However,
the gizzard has an important additional function
in grinding feed material, as this is not done in
the mouth. Thus, the gizzard contains strongly
myolinated muscles and has a koilin layer,
which will aid in the grinding process due to its
sand-paper-like surface. Grinding activity and
the regulation of this activity in the gizzard has
been described in detail by Duke [14], and will
only be briefly outlined herein. Also, a detailed
overview of function of the gizzard has recently
been published [15]. The grinding cycle begins
with contraction of the thin muscles, followed
by opening of the pylorus and a powerful peristaltic contraction in the duodenum. The pair of
thick muscles contracts immediately after commencement of the duodenal contraction, which
results in some gastric material being pushed
in an aborad direction into the duodenum and
some material being pushed in an orad direction
into the proventriculus. As the thick muscles
begin to relax, the proventriculus contracts and
returns content to the gizzard. This contraction
cycle takes place up to 4 times per minute and
grinds material due to rubbing against the koilin layer on the inside of the gizzard and against
other particles in the gizzard during contraction
of the large muscles, whereas the small muscles
move material toward the grinding zones between contractions of the large muscles. This
grinding cycle is why the proventriculus and
gizzard must be considered as one compartment
in regards to digestive function, where material
flows rather rapidly through the proventriculus,
but will potentially be refluxed back into the
proventriculus repeatedly during gizzard contractions. Jackson and Duke [2] reported that
feed material may bypass the gizzard when this
segment is empty. In an experiment where growing turkeys were fed a finely ground diet after a
10-h fast, the small intestine was filled with feed
within 25 min from commencement of feeding.
Svihus et al. [10] also reported that considerable
amounts of feed had passed the gizzard within
30 min of feeding.
Mean retention time in the proventriculus
and gizzard has been estimated to vary between
half an hour and an hour [16–18]. This seems
to be in accordance with results by Svihus et
al. [10], where 50% of the marker in feed eaten
during 10 min had passed the gizzard within 2
h. It has been reported that the volume of the
gizzard may increase substantially when structural components are added to the diet, sometimes increasing to more than double the original size [19, 20]. Although it has been reported
Svihus: INFORMAL NUTRITION SYMPOSIUM
that larger particles are selectively retained in
the gizzard [21], and that passage rate of a nonstructural marker, such as titanium oxide, is the
same independent of diet structure [10], it is obvious that mean retention time of feed particles
will increase substantially with increasing diet
structure. If retention time is close to 1 h when
a standard commercial diet with few structural
components is fed, mean retention time can be
assumed to approach 2 h if gizzard development
is stimulated by added structural components.
Interestingly, Rougière and Carré [22] found
that retention time of chromium-mordanted sunflower hulls in the gizzard was 4 times longer
than for titanium oxide. Also, retention time was
much higher for broiler chickens genetically selected for high digestibility. The former demonstrates the tremendous ability of the gizzard to
selectively retain large and tough particles while
letting small and soluble particles pass very rapidly.
The gastric juice secreted from the proventriculus has been reported to have a pH around 2
[23]. However, the amount, retention time, and
chemical characteristics of the feed in the gizzard or proventriculus area will result in a more
variable and usually higher pH. In a recent experiment at our laboratory, for example, the pH
of gizzard contents from broiler chickens varied
between 1.9 and 4.5, with an average value of
3.5. As summarized by Svihus [15], most of the
recent average values recorded for broiler chickens are reported to be between 3 and 4 for normal pelleted diets. Older data, however, reports
pH values between 2 and 3 [24–28], although a
similar low pH has been reported more recently
as well [5, 29, 30]. Due to the high calcium carbonate content in the diet, pH values for gizzard
contents are commonly between 4 and 5 for layer hens [31–33], although a pH around 3.5 has
also been reported for laying hens [34].
It has been shown repeatedly that when structural components, such as whole or coarsely
ground cereals, or fiber materials, such as hulls
or wood shavings, are added, the pH of the gizzard content decreases by a magnitude of 0.2 to
1.2 units [5, 30, 33, 35–40]. The logical explanation for this is the increased gizzard volume and
thus a longer retention time, which allows for
more hydrochloric acid secretion. As feed usually has a pH close to neutral, high feed intake can
309
be expected to result in an elevated gizzard pH
unless gastric juice secretion is able to increase
in accordance with intake. This is probably the
main reason why gizzard pH is reported to be
higher with pelleted diets when compared with
mash diets [38, 41, 42], although less structure
due to the grinding effect of pelleting will also
contribute to this effect [41, 43]. As reviewed extensively by Svihus [15], the increase in the size
of the gizzard when the diet contains structural
components in the form of coarse fibers or cereals improves digestive function both through an
increased retention time, a lower pH, and better
grinding. This, probably combined with a better
synchronization of feed flow, has been shown to
improve nutrient utilization.
SMALL INTESTINAL FUNCTION
The small intestine is the site for most digestion and practically all absorption of nutrients.
The first part of this segment is the duodenal
loop. Although this segment ends at the outlet of
the pancreatic and bile ducts, the acidic contents
from the gizzard are mixed with bile and pancreatic juices through gastroduodenal refluxes
during the very short retention here [23], estimated by Noy and Sklan [44] to be less than 5
min. Consequently, pH quickly rises to a level
above 6 [45] and the process of digestion starts.
Sklan et al. [46] reported that 95% of the fat
was digested in the duodenum. Although Duke
[23] claimed that no histologically distinct segment exists posterior to the duodenum, the adjacent segment that ends at the yolk sack residue
(Meckel’s diverticulum) is usually referred to as
the jejunum. This segment has a key role, as all
the major nutrients are to a large extent digested
and absorbed here. The prominent role is reflected in the fact that the empty weight of this segment is usually 20 to 50% higher than the ileum
[47, 48]. Despite the large size, retention time in
this segment is usually reported to be only 40 to
60 min, which is approximately half the retention time of the ileum [22, 49]. The shorter retention time despite a 25% larger holding capacity
[47] is a logical consequence of a larger amount
of material entering this segment compared with
the ileum. It has been demonstrated that absorption of digestion products from fat [44, 46, 50],
starch [51], and protein [44, 52] are to a large
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extent completed by the end of the jejunum.
The ileum is the last segment of the small intestine and ends at the ileo-ceco-colic junction.
Despite the fact that the length of this segment
is approximately the same as the jejunum [50],
weight is much lower, as discussed previously.
Although some digestion and absorption of fat,
protein, and starch may take place, this segment
is mainly thought to play a role as a site for water and mineral absorption. It has been shown,
however, that the ileum may play a significant
role for digestion and absorption of starch in
fast-growing broiler chickens. Zimonja and Svihus [53] found starch digestibility of pelleted
wheat diets to increase from 81 to 98% from ileum to excreta, and Svihus et al. [43] observed
starch digestibility to increase from 91 to 99%
from the anterior third to the posterior third of
the ileum. Likewise, Hurwitz et al. [50] found
some fat absorption to take place in the ileum.
Due to the fact that most the feed DM has been
absorbed, the passage through this segment is
much slower than through the jejunum, as discussed previously.
Changes in functionality of the small intestine are more difficult to assess. Weight of the
small intestine is sometimes recorded, but effects are often not seen and interpretation of
changes is often difficult. More interesting is
to assess changes in the intestinal function by
histological approaches, and numerous such
studies have been carried out, not the least to
study interactions between pro- and prebiotics
and intestinal function. However, as stated by
Yamauchi [54] in a review of the topic, a clear
understanding of the relationship between the
morphology and function of the intestine is, to
a large extent, lacking. Whereas it is often assumed that an increased villus height is an indication of improved function (e.g., [55]), it has
been demonstrated that ileal villi may enlarge as
a consequence of a dysfunctional jejunum (e.g.,
due to resection of this section) [54]; thus, an
increased villi height may also be a consequence
of an increased need for digestive capacity. Also,
although this is surprisingly rarely discussed,
the method used for selection of the intestinal
segment for measurement is not always clear.
To avoid systematic errors due to a conscious or
subconscious desire to find what is expected, the
assessment should be blinded (the person carry-
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ing out the histological assessment should not be
aware of the treatment), and a method to ensure
a random selection of area to measure should be
in place. This is seldom—if ever—reported in
methods description for these kinds of assessments.
FUNCTION OF THE CECA
The pair of ceca found in domesticated poultry species (except pigeons) is also a unique feature of the poultry digestive tract, and ceca of
various sizes and forms can be observed in most
avian species [56]. An extensive review of ceca
function has recently been published [57] and
will be the basis for this short overview.
The pair of ceca is located at the junction
of the ileum and colon as elongated blind sacs
directed along the ileum [25]. The ceca in galliformes are usually long and particularly well
developed with a constricted proximal portion,
measured by Clarke [58] to be 1 to 2 mm wide
in 3-wk-old chickens, which join the colon just
distal to the muscular ring separating the ileum
from the colon. Duke [59] and Duke et al. [60]
observed cecal emptying twice per day, on average, in turkeys, at dawn and midafternoon. Due
to the infrequent emptying, retention time in the
ceca will usually be long, as indicated by the fact
that cecal content was not significantly reduced
after 24 h of food deprivation [61, 62]. Apart
from during voiding of fecal and cecal material,
continuous antiperistaltic movements of the colon have been observed, and these antiperistaltic
movements will transport material from the anal
opening or the coprodeum into the ceca in a very
short time. It appears that the types of material
that enter the ceca are finely ground particles
or soluble, low-molecular weight, non-viscous
molecules of ileal and renal origin. One important function of the ceca is electrolyte and water
absorption, for which the ceca have been described as the quantitatively most important segment of the gut. Thomas [63], in his comprehensive review of water and electrolyte absorption
in the fowl, stated that net water absorption in
the gut does not occur until after the ileum, and
is mainly due to reabsorption of electrolytes and
water of intestinal and renal origin in the ceca. It
was estimated that 36% of the water and 75% of
the sodium of renal origin were absorbed from
Svihus: INFORMAL NUTRITION SYMPOSIUM
the lower digestive tract, with the ceca being the
most important organ. Although the quantitative
importance is uncertain, it is also possible that
the ceca can play a role in recycling of renal nitrogen.
The functionality of the ceca is to a very large
extent affected by diet, and the ceca enlarge as a
consequence of an increased amount of fermentable material in the diet. An extreme example
is the willow ptarmigan, where the ceca is 30%
longer in the winter as a consequence of a more
fiber-rich diet [64], but even in turkeys a 25%
longer ceca containing twice the amount of DM
has been observed after adaptation to a highfiber diet [60].
Based on this information, it is logical that
functionality of the digestive tract may have a
large effect on response to different dietary manipulations. Some examples of significant interactions between dietary responses and digestive
tract functionality will be further discussed.
FORM OF FEED AND DIGESTIVE
TRACT FUNCTIONALITY
One important factor is the form of the feed,
which to a large extent will determine feed intake. Pelleting of the diet will usually increase
feed intake of broiler chickens by 10 to 20% [41,
65], and thus will increase the demands on an
already high-performing digestive system. An
increase in digestibility when diets were given
as mash compared with pellets was observed
by Svihus and Hetland [66] and indicates that
pelleting may cause an overload of the digestive
system. Engberg et al. [41] found significantly
higher levels of digestive enzymes when diets
were given as mash compared with pellets, and
also showed that pelleted diets resulted in a much
more poorly developed gizzard than when mash
diets were given. Thus, as the gizzard probably
has an important role as a feed-flow regulator
[15], it is possible that the combined effect of a
high feed intake and a low gizzard-stimulating
effect increases the risk of a too-rapid passage
of material through the digestive tract. This fits
with conclusions made by Rougière and Carré
[22], who concluded that retention time in the
proventriculus or gizzard was a major limiting
factor for digestion in broiler chickens based on
passage studies. A high feed intake due to pellet-
311
ing may therefore have particularly detrimental
effects when no structural components exist in
the diet, resulting in a small and under-developed gizzard. Environmental conditions may
be important in this context, as birds will compensate for lack of structural components in the
diet, to some extent, by eating litter materials,
such as wood shavings, if available [31, 67]. As
pelleted diets are used commercially for broiler
chicken, this means that the use of mash diets
under experimental conditions may not reflect
the commercial reality in terms of digestibility
and digestive function.
RESPONSE TO ADDITIVES
AND DIGESTIVE TRACT
FUNCTIONALITY
Apart from the effect of feed intake, changes
in functionality of the digestive tract due to diet
structure and feeding system, for example, may
also affect results in numerous other ways. Two
prominent examples are effects of exogenous
enzymes and pre- or probiotics.
Exogenous enzymes added to the diet must
exert their effect during the short time from
when the feed is moistened in the anterior digestive tract to the point that feed residues have
passed the small intestine. In addition, the range
of pH encountered in the digestive tract must be
relevant for its activity and must not threaten its
stability. Furthermore, the enzyme must be able
to withstand the digestive processes to function,
not the least activity of host digestive proteases.
This complicated matrix of conditions will determine the scale and variation of activity of an
enzyme added to the diet and, thus, its biological
effects. Therefore, it is essential to understand
these digestive conditions and how they may
vary in order to predict the beneficial potential
of added enzymes. Most exogenous enzymes
have an optimum pH between 4 and 6 [68, 69],
but great variation may exist between different
sources of enzymes, which results in catalytic
activity at both lower and higher pH. Ding et
al. [70], for example, showed that the specific
xylanase studied maintained more than 50% of
its maximum activity at a pH of 3. The slightly
acidic pH optimum is one of the reasons for the
assumption that the crop and the gizzard are the
most important sites of activity for exogenous
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enzymes [71, 72]. In that case, it is obvious that
functionality of both the crop and the gizzard
may have a large effect on responses to enzyme
supplementation. Intermittent feeding will increase retention time and decrease pH of the
crop, and structural components will increase
retention time and decrease pH in the gizzard,
as discussed previously. In accordance with this,
Svihus et al. [4] reported that supplemental phytase was able to degrade 50% of the phytic acid
during 100 min of retention in the crop of broiler
chickens. Despite this, an experiment designed
to increase retention time in the crop and gizzard
failed to demonstrate any improved efficacy of
phytase [5].
Responses to prebiotics may particularly be
affected by the extent to which the feed is retained in the crop. An acidifier will, for example,
both potentially affect efficacy of exogenous enzymes and potentially affect microflora proliferation. Similarly, efficacy of probiotics may be
strongly affected by functionality of the anterior
digestive tract. An increased retention time in the
crop may cause a proliferation of the added microflora and may affect pH. Similarly, but with
opposite effects, a well-functioning gizzard may
reduce survivability of the probiotics through an
increased retention time and a decreased pH.
Functionality of the posterior digestive tract
may also be affected by functionality of the gizzard due to structural components, as discussed
previously. A dysfunctional gizzard may allow
too much and poorly degraded nutrients to be
passed through, and thus an increased level of
undigested nutrients may enter the ileum and
ceca. The result may be morphological and microbiological changes, although it is not clear to
what extent such changes may affect functionality negatively.
CONCLUSIONS AND APPLICATIONS
1. Functionality of the digestive tract in
birds is pivotal for optimal performance,
and diet composition, form, and feeding
system may have a large influence on digestive function.
2. The importance of a proper development
of the gizzard for the digestive function
and a maximized digestibility is now
very well accepted, but the applied im-
plication both for commercial diet formulation and under experimental conditions is still not fully appreciated.
3. Intermittent feeding is necessary to ensure that all birds in a flock are making
use of the crop as an intermediate storage organ.
4. Although the moisturization that takes
place during retention of material in the
crop may contribute to a higher digestibility, a significant effect of retention
for performance and digestion still needs
to be demonstrated.
5. Despite the crucial role of the small intestine for digestion and absorption and
the critical importance of maximal functionality due to a very short retention
time, the characteristics of an optimally
functioning small intestine are still not
completely clear.
6. Functional importance and criteria for
assessing optimal functionality of the
ceca are lacking to a large extent.
7. As functionality of the digestive tract
is affected to a large extent by both diet
characteristics and feeding management,
interpretation of studies designed to assess nutritional effects should always
take these factors into consideration.
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