The role of the crop in poultry production

Abstract

The importance of the crop is often underestimated in poultry production. In addition to storing ingested feed, it also can impact nutrient digestion by digesta softening and the initial activity of feed (endogenous and exogenous) and microbial enzymes. The crop represents the first major defence against poultry pathogens and zoonotic organisms with well established adaptive and innate immune function, and a lactobacilli dominated microbiota capable of reducing the passage of these organisms further along the digestive tract. However, the potential to improve bird productivity and health, as well as affect meat and egg safety, are influenced by the nature of the diet, and in particular feed entry and extended presence in the crop. This is required to promote lactobacilli fermentation, the production of lactic acid and other volatile fatty acids, and the lowering of crop pH. Management practices such as meal feeding and the use of lighting programs with extended dark periods encourage crop utilisation. Further, the use of feed additives such as prebiotics and probiotics may enhance crop function, which in turn contributes to well-being of the entire digestive tract. A healthy and functional crop, along with other segments of digestive tract, has increased importance in an era of reduced antibiotic use in poultry feeds.

Full text

The role of the crop in poultry production
H.L. CLASSEN
1
*, J. APAJALAHTI
2
, B. SVIHUS
3
and M. CHOCT
4
1
Department of Animal and Poultry Science University of Saskatchewan,
Saskatoon, SK, Canada S7N 5A8;
2
Alimetrics Ltd., Koskelontie 19B, FIN-02920,
Espoo, Finland;
3
Department of Animal and Aquacultural Sciences, Norwegian
University of Life Sciences, PO Box 5003, N-1432, Aas, Norway;
4
Poultry
Cooperative Research Centre, PO Box U242, University of New England, Armidale,
NSW 2351, Australia
*Corresponding author: hank.classen@usask.ca
The importance of the crop is often underestimated in poultry production. In
addition to storing ingested feed, it also can impact nutrient digestion by digesta
softening and the initial activity of feed (endogenous and exogenous) and microbial
enzymes. The crop represents the first major defence against poultry pathogens and
zoonotic organisms with well established adaptive and innate immune function, and
a lactobacilli dominated microbiota capable of reducing the passage of these
organisms further along the digestive tract. However, the potential to improve
bird productivity and health, as well as affect meat and egg safety, are
influenced by the nature of the diet, and in particular feed entry and extended
presence in the crop. This is required to promote lactobacilli fermentation, the
production of lactic acid and other volatile fatty acids, and the lowering of crop
pH. Management practices such as meal feeding and the use of lighting programs
with extended dark periods encourage crop utilisation. Further, the use of feed
additives such as prebiotics and probiotics may enhance crop function, which in
turn contributes to well-being of the entire digestive tract. A healthy and functional
crop, along with other segments of digestive tract, has increased importance in an
era of reduced antibiotic use in poultry feeds.
Keywords: crop; lighting; meal feeding; lactobacilli; salmonella; food safety
Introduction
The digestive tract of vertebrate animals is complex and has evolved to serve its primary
function of supplying nutrients to the host animal, while at the same time serving as a
barrier to infection and harm from compounds within the digestive tract. As can be
expected, functions of gastrointestinal tract (gut) segments are interdependent to provide
for efficient digestion and other gut functions (Scanes and Pierzchala-Koziec, 2014).
Evolution of the gut took place in a natural environment, where omnivorous chickens
accessed a wide range of foods and were not always able to find the level of nutrients
doi:10.1017/S004393391600026X
© World's Poultry Science Association 2016
World's Poultry Science Journal, Vol. 72, September 2016
Received for publication January 19, 2016
Accepted for publication March 30, 2016 1

necessary for maximum growth and reproduction. The importance for gut segments
would also change to match the nature of the feedstuffs being consumed. For
example, the gizzard, and caeca and caecal fermentation would increase in importance
in the presence of fibrous, poorly digestible materials that might be found in winter. It is
well understood today that gut segments change to reflect diet changes and that
communication mechanisms are in place between gut segments to optimize nutrient
retention.
With increasing use of high quality ingredients in poultry feeding, the importance of all
segments of the gut and their interrelationships has often been forgotten or neglected with
emphasis instead being directed to delivery of digestible nutrients. However, more
recently the importance of segments such as the proventriculus/gizzard and caeca has
received renewed attention. A well-developed gizzard has been demonstrated to have
relevance in digestion and gut health, and the caeca play a critical role in determining gut
health and colonisation by zoonotic organisms. For reviews of these gut segments see
Svihus (2011) and Svihus et al. (2013a). The crop has also been the subject of a wide
range of research, but its importance in broiler feeding remains either poorly understood
or neglected in research and poultry feeding. Based on the interdependence of gut
segments and the relatively neglected crop, the objectives of this paper are to examine
the digestive process that occurs in the crop, define its role in improving broiler nutrition
and health, and then speculate on how it can be manipulated to benefit broiler production.
Crop anatomy
The crop is a thin walled diverticulum of the oesophagus and retains the basic structural
pattern of the digestive tract (Hodges, 1974). Extending from the lumen are non-
keratinised stratified squamous epithelium of the mucous membrane, lamina propria
(connective tissue), muscularis mucosae, sub-mucosa (a layer of loose connective
tissue), muscularis externa and the serosa. The structure of the crop is well
innervated and vascularised implying potential for interaction with other gut segments,
and possibly a variety of roles related to digestion and gut health. Mucous glands are
found in the oesophagus and also at the interface between the oesophagus and crop, but
are not found in the crop diverticulum (Fuller and Brooker, 1974). Similarly, structural
differences have been noted between the oesophageal area of the crop (slightly
convoluted surface with a high density of bacteria) and the apex of the diverticulum
(flatter surface, numerous sloughing epithelial cells, and fewer bacteria) (Bayer et al.,
1975). The non-secretory nature of the crop suggests a limited capacity for digestion, but
moisture and enzymes derived from consumption (water, feed), saliva and
microorganisms play a role in initiating the digestive process. Demonstrated bacterial
adhesion to starch granules is just one example of how digestion can occur in the crop
(Bayer et al., 1975). The importance of the crop in diet digestion will be affected by the
proportion of the feed that enters the crop and the amount of time it spends there.
Although the nature of the crop epithelium indicates less absorptive capacity than
areas such as the small intestine, absorption by diffusion of organic acids such as
lactic acid and DL-2-hydroxy-4(methylthio) butanoic acid has been suggested (Cutler
et al., 2005; Richards et al., 2005). The possibility of transporter mediated absorption has
not been evaluated in chickens, but since it occurs in other examples of stratified
squamous epithelium (Connor et al., 2010), this possibility can't be ruled out in the
avian crop. Again, residency time of feed and absorbable molecules in the crop impact
this potential.
Role of the crop: H.L. Classen et al.
2 World's Poultry Science Journal, Vol. 72, September 2016

Feed residency in the crop
The degree to which feed enters and the time it is resident in the crop is variable and
highly dependent on the nature of bird feeding behaviour, feed presentation (e.g., meal
vs. ad libitum) and bird management (e.g., periods of darkness). Estimates of crop
retention time in birds given ad libitum access to feed and 24 hours of light per day
are 7.4 and 24.6 minutes for broiler and White Leghorn chicks, respectively (Shires et al.,
1987). In this setting, it appears that feed is primarily directed to and accumulates in the
gastric stomach and small intestine. The observation that broiler chickens eat very
frequently, approximately every 30 minutes when having ad libitum access to feed,
corroborates this (Svihus et al., 2013b). Therefore, not only will crop residency be
short, but it is also likely that most feed will not enter the crop (Chaplin et al., 1992;
Savory, 1985). An extreme contrast to this situation is broiler breeders fed on an every-
other-day feeding schedule during the rearing period, where the crop does not empty until
20 hours after feeding (de Beer et al., 2008). Similarly, the time feed spends in the crop
can be affected by lighting programs with extended periods of darkness. In turkeys given
a 14L:10D lighting program, digesta remained in the crop for 9 hours after the end of the
photophase (Cutler et al., 2005). Turkeys and chickens are diurnal and eat during the day
if not limited by day length or other environmental factors such as high temperature.
Feeding behaviour during the photophase has a daily pattern with the nature of the
pattern dependent on the length of the dark period (Schwean-Lardner et al., 2014).
Feed intake may or may not be high immediately after lights come on, and increases
again prior to lights going off (Buyse et al., 1993; Schwean-Lardner et al., 2014). Early
morning feeding can be rationalised by hunger associated with the extended period of
time during darkness, but when not seen may be attributed to the capacity of the crop to
store feed for an extended period of time and therefore a lack of hunger (Scanes et al.,
1987). The late day increase in feed intake is anticipatory and takes time for birds to learn
after first being exposed to a dark period. The rationale is that birds increase feed intake
so that their nutritional needs are met for at least a portion of the dark period. Buyse et al.
(1993) found that the crop contained only small quantities of ingesta during the
photoperiod in a 14L:10D lighting program, in apparent agreement with Shires et al.
(1987). However, the ingesta content of the crop increased dramatically (10.5-fold) at the
beginning of the scotophase as a result of late day feeding. The crop content decreased
gradually during the scotoperiod and of note feed transit time was longer during the
night; this was also found by others (Cutler et al., 2005; Duve et al., 2011; Scanes et al.,
1987). These authors speculated that the storage of feed in the crop, its gradual release
and the increased food transit time at night resulted in the majority of the bird's nocturnal
energy needs being met. Anticipatory feeding appears to be affected by the length of the
scotoperiod. In a comparison of 16L:8D and 13L:4D:3L:4D lighting programs, Duve et
al. (2011) found that birds on the latter lighting program failed to display anticipatory
feeding before either of the dark periods and suggested that its absence was caused by a
lack of need to feed, rather than not predicting the dark period. This research plus other
work (Schwean-Lardner et al., 2013) suggest that dark periods of greater than four hours
are necessary to induce anticipatory feeding behaviour. In conclusion, use of the crop as a
feed storage device is minimal when highly nutritious feed is readily available and there
are no constraints on feeding behaviour. However, birds utilize crop storage in response
to hunger (e.g. food deprivation) or regular periods of darkness (Savory, 1985).
The control of crop filling and emptying is complex, but the gizzard plays a central role
(Chaplin et al., 1992; Jackson and Duke, 1995) as it regulates passage of feed to the
remainder of the digestive tract. Signalling includes neurological (vagus nerve; Denbow,
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 3

1989) and hormonal (e.g. ghrelin; Kaiya et al., 2009; glucagon-like peptide-1, Tachibana
et al., 2003) mechanisms.
Bacterial populations and role in digestive tract health and pathogen
colonisation
Lactobacilli dominate the bacterial community of the crop, but coliforms, streptococci
and bifidobacteria have also been found (Abbas Hilmi et al., 2007; Fuller, 1973; Fuller
and Brooker, 1974; Fuller and Turvey, 1971; Guan et al., 2003; Peinado et al., 2013; Petr
and Rada, 2001). At least some lactobacilli are capable of binding to the crop epithelium
to form biofilm layers that are relatively uniquely found on non-secretory stratified
squamous epithelium (Edelman et al., 2002; Fuller and Turvey, 1971; Lebeer et al.,
2011). The nature of the adherence is not fully understood, but S-layer proteins may be
responsible (Hagen et al., 2005). Hagen et al. (2005) speculate that the diversity of S-
layer proteins among Lactobacillus gallinarum strains may provide an opportunity for
different strains to live together without direct competition for attachment sites on the
crop epithelium. Adherence is vital for colonisation to prevent washout in intestinal
compartments with continuous digesta passage. However, if only a small proportion
of feed enters the crop, the low flow-through in the diverticulum may enable
reproduction of bacteria that are not capable of resisting washout by adherence.
Indeed, the crop could act as a natural fed-batch fermenter (like the caecum), seeding
the intestine with metabolically active bacteria. The exact nature of the crop microbiota
continues to increase in clarity as newer techniques of identification become available
(Cousin et al., 2012; Hammons et al., 2010).
Bacterial colonisation of the crop is initiated either just prior to or after hatch (Barnes et
al., 1980). Colonisation is variable in young chicks immediately after hatch, and the
speed and nature of crop bacterial colonisation is influenced by a variety of factors in the
diet. Grains are naturally rich in lactic acid producing bacteria and unless toasted at
extreme temperatures bacteria recover after rehydration (Apajalahti, unpublished). This is
an important part of the bird's life as they also are most susceptible to colonisation by
non-desirable pathogenic and zoonotic organisms at that time (Gast and Beard, 1989;
Smith and Tucker, 1980). Factors affecting speed of lactobacilli colonisation include
dietary introduction of competitive Lactobacillus strains, prebiotics and organic acids
affecting their competitiveness, medication (Rada and Marounek, 1996), and the nutrient
content of the feedstuffs themselves (Rubio et al., 1998). It is worth noting that
lactobacilli are fastidious bacteria with equally complex nutrient requirements as the
host itself; they need to have access to simple sugars, amino acids and vitamins for
growth. Lactobacilli can be eliminated by anti-bacterial agents such as penicillin and
monensin, and when this occurs, the number of coliforms increases (Apajalahti and
Kettunen, 2006; Rada and Marounek, 1996). Of note, Escherichia coli are capable of
binding to crop squamous cells. Their colonisation can be inhibited by adhering strains of
lactobacilli (ST1 Lactobacillus crispatus) because of shared adhesion sites (classic
competitive exclusion), but not by those that are weakly adhesive (L. crispatus strain
134mi) (Edelman et al., 2003). Similarly, lactobacilli are capable of inhibiting Salmonella
colonisation of the gut (Gusils et al., 1999). This ability to prevent colonisation can be
attributed to a number of mechanisms including competing for adherence sites,
stimulation of the immune system, antibacterial agents and lactic acid production
(direct inhibitory effect of lactate or indirect effect of lowered pH). These studies (and
many others) support the concept that a stable and dominant position of lactobacilli in the
Role of the crop: H.L. Classen et al.
4 World's Poultry Science Journal, Vol. 72, September 2016

crop is essential for gut health and the development and maintenance of a balanced crop
microbiota (Fuller 1973; 1977).
The absence of feed, such as during withdrawal prior to slaughter or moulting
procedures, results in a shift in the bacterial community and predisposition of the
crop to Salmonella and Campylobacter spp. colonisation. Feed withdrawal increases
the potential for pathogen presence as a result of decreased lactobacilli colonisation
and consequent weakened barrier of entry for pathogens. Among other changes,
decreased lactobacilli numbers result in decreased production of lactic and acetic acid
(the ratio of which is a species specific feature; Hammes and Vogel, 1995), and increased
pH (Durant et al., 1999; Hinton et al., 2000a). The presence of Salmonella and
Campylobacter spp. in the crop of broilers at slaughter represents a human disease
risk because of the higher potential of carcass contamination at slaughter from the
crop than caecal rupture (Corrier et al., 1999; Hargis et al., 1995; van Gerwe et al.,
2010). This emphasizes the need to reduce Salmonella spp. colonisation during grow-out
and maintaining this status during the feed withdrawal period. Inclusion of organic acids
or fermentable growth substrates for lactobacilli in water can reduce the Salmonella and
Campylobacter spp. contamination of crops and broiler carcasses (Byrd et al., 2001
(lactic acid); Chaveerach et al., 2004 (acidified drinking water); Hinton et al., 2000b
(glucose); 2002 (sucrose)).
Feed withdrawal during moulting in laying hens also markedly increases the survival of
Salmonella spp. in the crop (Humphrey et al., 1993) and may provide an environment
that increases the expression of genes necessary for intestinal invasion (Durant et al.,
1999). In comparison to feed withdrawal, providing low calcium, low calcium and zinc,
or low energy by-product diets have been shown to reduce S. Enteritidis infection, and
maintain lactobacilli in the crop and a lower crop pH (Ricke et al., 2004; 2013; Seo et al.,
2001).
The presence of pathogens harboured in the crop and additional organisms that pass
through to the lower gut suggest the need for expression of both adaptive and innate
immune responses in the crop. Research has confirmed this logic with the demonstration
of well-developed lymph nodules in the upper alimentary tract in the form of oesophageal
tonsils (Arai et al., 1988). A further demonstration of immune competency in the crop is
the development of lymphoid aggregates in crop walls following challenge with S.
enterica ser. Enteritidis (Seo et al., 2003; Vaughn et al., 2008a; 2008b) and the
presence of secretory immunoglobulins (IgA) that specifically bind to S. enterica ser.
Enteritidis antigens (Seo et al., 2002; 2003). The high expression of β-defensin
gallinacin-6 (Gal-6) in the oesophagus and crop, and the demonstration of its
antimicrobial activity against food-borne pathogens, demonstrates that the crop can
play a role in chicken innate host defence (Hong et al., 2012; van Dijk et al., 2007).
Another innate immune function is indicated by Thaxton et al. (2006) who found an
increase in crop nitrate content after gavaging turkeys with S. Typhimurium. The authors
suggest that the results are indicative of the activation of inducible nitric oxide synthase
in resident macrophages. Taken together, these findings suggest an influence of the crop
in local and total digestive tract health and pathogen colonisation.
The crop forms part of the acidic barrier formed by the crop and gizzard, which reduces
passage of bacteria including pathogenic Clostridium spp. and representatives of zoonotic
genera such as Salmonella and Campylobacter spp. to the distal gut (Sekelja et al., 2012).
The modulation of crop bacteria may affect caecal microbiota, as demonstrated by
experiments using dietary butyric acid in an unprotected and partially protected form
to study S. enterica ser. Enteritidis colonisation in the crop and caeca (Fernández-Rubio
et al., 2009). Both sources of butyric acid reduced crop and caecal colonisation, but the
unprotected butyric acid was more effective in the crop and less effective in the caeca as
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 5

expected. Unprotected butyric acid in the diet is taken up by the small intestinal
epithelium and hardly reaches the caeca. However, the still important effect of the
diet amended with unprotected butyric acid in the caeca suggests that controlling
colonisation in the crop benefits the entire digestive tract.
Crop pH and fermentation
The acidity of the chicken crop can vary with values ranging from well below pH 5 to
greater than pH 6 (Bowen and Waldroup, 1969; Hinton et al., 2000a; Józefiak et al.,
2006; Rynsburger, 2009; Svihus et al., 2013b). The pH varies with the degree of crop
fermentation primarily by lactobacilli and by the production of lactic acid together with
weaker acetic acid (Cutler et al., 2005; Józefiak et al., 2006). In turn, fermentation is
influenced by factors such as the presence of substrate (feed or prebiotic) and again
colonisation by lactobacilli (Barnes et al., 1980; Fonseca et al., 2010). The pH of the
crop can also be impacted by other non-fermented components of the diet. Feed
ingredients have been found to have differing acid binding (buffering) capacity that
can affect crop pH with mineral ingredients having the highest capacity followed by
protein ingredients and then energy sources (Lawlor et al., 2005). Considering the high
calcium levels in laying hen diets, one would expect that crop pH values would be high.
Although this has been reported to be the case (Bolton, 1965), an examination of pH
values for hens fed on an ad libitum basis from 17 research trials averaged pH 4.91 with
a range of 4.29 to 6.00 (Durant et al., 1999, 2000; Gordon and Roland, 1997; Kubena et
al., 2005; Moore et al., 2004; Nahashon et al., 1994; Ricke et al., 2004). Of interest, the
values for hens being moulted by feed withdrawal averaged pH 5.91 with a range of 5.42
to 6.96. These values suggest that considerable fermentation occurs in the crop of laying
hens and in turn the reduction in pH can affect its microbial community.
As noted above, extended dark periods result in anticipatory eating and crop storage
(Cutler et al., 2005). In turkeys provided with a 14:10D lighting program, feed gradually
emptied from the crop for 9 hours after the beginning of darkness and during that time
pH decreased from 5.9 to 5.0; at the same time levels of lactic acid and other short chain
fatty acids were increasing. This demonstrates that the presence of feed in the crop for an
extended time enhances fermentation. In a second experiment, Cutler et al. (2005) found
that the number of S. enterica ser. Typhimurium in crop digesta decreased from 7.1 to 4.9
(log10)/gram of crop digesta over an eight hour period starting after the end of the
photophase. This research confirms the beneficial effect of fermentation on crop pH
and subsequently bacterial colonisation.
The low pH has direct inhibition effects against a variety of pathogenic and zoonotic
organisms and also enhances the impact of butyric acid when it is used in water or broiler
feed. The effectiveness against these organisms increases at lower pH because butyric
acid in its undissociated form can cross bacterial membranes and acidify the bacterial cell
cytoplasm. Therefore, unprotected free sodium butyrate should be more effective against
bacteria when converted to protonated butyric acid at the acidic pH of the upper portion
of the digestive tract (Van Immerseel et al., 2006).
Pendulous crop
Loss of tone in muscle can result in pendulous crop. The condition is more prevalent in
turkeys, but can be found in broiler chickens and occasionally occurs at relatively high
levels (Ebling et al., 2015). Despite the usually low incidence, research on pendulous
Role of the crop: H.L. Classen et al.
6 World's Poultry Science Journal, Vol. 72, September 2016

crop may provide clues on management and nutrition required to produce a ‘healthy’
crop. The etiology of pendulous crop is not clear, but incidence has been linked to
genetic, environmental and nutritional influences (Asmundson and Hinshaw, 1937;
Wheeler et al., 1960). In a comparison of feeding glucose monohydrate or starch to
turkeys, a high incidence of pendulous crop was found for the birds fed glucose
monohydrate and none were found for birds fed starch. In addition, abnormal
fermentation was found as a result of yeast and fungi colonisation of the pendulous
crop birds. Evidence from turkey lighting research (Vermette et al., 2016) has found a
higher incidence of pendulous crop in hens given 23 in contrast to those receiving 14, 17
and 20 hours per day. It may be that crop feed storage is required to maintain a scheduled
flow of feed through the crop and maintenance of a desired lactobacilli biofilm on crop
epithelium, thereby preventing abnormal colonisation by other microbiota.
Potential effects on bird performance
Exposing birds to darkness and meal feeding both promote crop storage of feed, and can
improve feed efficiency (Schwean-Lardner et al., 2012; Su et al., 1999; Svihus et al.,
2010; 2013b). The improvement in feed efficiency in these cases has been attributed to
factors such as altered metabolism during darkness (Apeldoorn et al., 1999), a more
concave growth curve (Buyse et al., 1996b), and improved nutrient retention (Buyse et
al., 1996a; Svihus et al., 2013b). An argument can be made that increased food softening
and acid exposure, the initiation of the digestive process due to endogenous and
exogenous enzymes, and slower digesta transit (at least during darkness) as a result of
feed presence in the crop may result in improved nutrient digestibility and feed efficiency.
Svihus et al. (2013b) speculated that improved gizzard digestion as indicated by reduced
gizzard pH contributed to the improvement in feed efficiency seen with intermittent
feeding. Of interest, in a comparison of graded levels daylength (14, 17, 20, 23
hours), gizzard size increased and jejunum and ileum weights decreased with shorter
days, which result in improved feed efficiency (Classen, Schwean-Lardner and Fancher,
unpublished).
As mentioned above, lactobacilli require simple sugars and amino acids in their
growth. Why then does the utilisation of dietary substrates and nutrients by the crop
lactobacilli not reduce the feed conversion efficiency of the host? The effect of this
apparent competition for nutrients between the host and the upper intestinal microbiota
(in the crop and small intestine) on bird performance depends on i) the extent to which
the host can benefit from the produced microbes and their metabolic products, ii) other
nutritional and health benefits provided by the growing intestinal lactobacilli, and iii) the
proportion of feed entering the crop and becoming utilised by its microbes. Lactobacilli
have anaerobic metabolism, and therefore are able to extract only little energy from
carbohydrates such as glucose. In their metabolism, homofermentative species produce
mainly lactic acid, but heterofermentative species also to a varying extent produce acetic
acid and ethanol (Hammes and Vogel, 1995). The acids and ethanol are central metabolic
intermediates and excellent substrates for the host and, provided that they are readily
taken up from the digestive tract, cellular dehydrogenases convert them into
intermediates that enter the citric acid cycle and subsequent ATP-producing electron
transport chain. If lactobacilli converted 100% of glucose to lactate, acetate, or
ethanol and the metabolites would be completely absorbed, the energy deficit for the
bird would be only 5% (calculation based on ATP yield from glycolysis, citric acid cycle
and aerobic respiration).
In a crop with lower pH as a result of fermentation, conditions are optimised for some
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 7

enzymes, both endogenous and exogenous (Zeller et al., 2016). In particular, it is well
established that phytate hydrolysis in the crop can be extensive (Lan et al., 2010;
Onyango et al., 2005; Svihus et al., 2010; Zeller et al., 2015; 2016). Increased crop
hydrolysis does not necessarily lead to differences in terminal ileum phytate
disappearance (Zeller et al., 2015). However, reducing phytate's ability to bind
minerals and protein at this early stage of the digestive process should reduce its
negative effects on nutrient digestibility (Yu et al., 2012). Of interest is the finding
that β-glucanase supplementation of broiler diets containing oats or barley increased
the lactic acid concentration and lowered the pH in the crop (Józefiak et al., 2006).
This demonstrates that exogenous enzymes are active in the crop and as a consequence
influence conditions in the lower gut that beneficially affect production characteristics. In
the latter research, enzyme use improved performance criteria, but it is not possible to
relate this improvement to effects in the crop. Unfortunately, the lighting program used
was not identified so it is also not possible to know whether increased crop storage would
enhance the β-glucanase effect. The potential for enzyme activity in the crop will be
affected by the match between the crop environment and enzyme activity requirements,
as well the time of substrate exposure.
Developing and maintaining a healthy crop
The crop, though often relegated to being just a storage organ, can play a role in broiler
health and nutrient retention, as well as colonisation by zoonotic organisms. Positive
effects of the crop on broiler health, nutrient retention, as well as colonisation by zoonotic
organisms appear to relate to regular utilisation of the crop for feed storage. Because of
the susceptibility to colonisation by undesirable organisms in newly hatched birds, early
promotion of crop lactobacilli colonisation is highly desirable.
Providing birds with darkness is an easy method of stimulating crop utilisation.
However, the use of continuous or near-continuous light is predominant in the early
part of a broiler's life with introduction of more substantial periods of darkness no earlier
than four days and most often seven or more days of age. The degree of crop utilisation
during this period is not known, but it is common to judge crop fill on the day after
placement, with a recommendation that ~90% of birds will have feed in their crop. This
degree of fill may relate to it being the first meal, and as feeding behaviour acclimatizes
to continuous light the degree of crop storage may be decreased. It is possible that earlier
provision of darkness would increase crop storage of feed. Intermittent lighting post-
hatch has been recommended for broilers to synchronize flocks and provide young chicks
with rest (Malleau et al., 2007). Similarly, day-of-placement introduction of darkness (4 x
4L:2D) is also recommended for laying hen pullets (Lohmann Tierzucht, 2016).
During the rearing period of broilers, turkeys and laying hens, a longer dark period
could be initiated to encourage anticipatory feeding prior to the scotophase. A longer
dark phase would appear to be appropriate because of the evidence that four hours of
darkness is required to develop anticipatory feeding behaviour. Alternately, a longer dark
period could be combined with intermittent lighting during the ‘photophase’. Simulating
dawn and dusk would be recommended for both intermittent and diurnal phases of the
broiler life cycle to provide a stronger signal of the upcoming dark period.
Near slaughter age, it is not uncommon for broilers to be returned to near continuous
light to increase ease of bird handling and preparation for feed withdrawal. This may
reduce crop lactobacilli numbers and make the crop more susceptible to Salmonella and
Campylobacter spp. colonisation, a situation that will worsen during feed withdrawal.
Maintaining a longer dark period until marketing and then planned feeding prior to
Role of the crop: H.L. Classen et al.
8 World's Poultry Science Journal, Vol. 72, September 2016

broiler harvesting may reduce this problem by maintaining a healthy crop, and provide
feed longer in the crop (with fermentation and low pH) during withdrawal. Concerns
regarding digesta contamination at slaughter because of feed in the crop may not be
warranted if the feed withdrawal process is properly managed.
Feed withdrawal stimulates enhanced crop use, and this can readily be accomplished
by planned meal timing or simply allowing feeders to empty on one or more occasions
during a day (Svihus, 2015). This type of feeding could also be used to enhance crop use
in broilers exposed to a diurnal lighting program (one light and one dark period per day).
Meal feeding during the mid portion of the photophase would ensure crop use for a
longer portion of the total day period, and complement crop use after lights come on and
during anticipatory feeding before lights go off.
Enhancing the maturation of the crop microbiota after hatch may provide a less
susceptible environment to pathogenic load, and appropriate probiotics (Beasley et al.,
2004; Abbas Hilmi et al., 2007), and carbohydrates and other nutrients targeted for
lactobacilli may be useful to accomplish that goal (Lebeer et al., 2011). Although in
ovo application of probiotics would seem appropriate to ensure earliest possible bacterial
colonisation (Edens et al., 1997), the authors are unaware of successful applications.
Conclusions
The crop is often not considered in making broiler nutrition or management decisions.
However, there is evidence that a functional crop can play a role in bird performance and
health, and the safety of poultry meat and eggs. For this to happen, the early
establishment of lactobacilli in the crop and providing substrate for fermentation by
ensuring regular crop feed storage are essential. Commercial probiotics in the
marketplace today have not been optimised for the specific requirements of the crop
habitat and the substrates of the undigested feed slurry. Indeed, cocktails of multiple, site
specific bacterial strains would be needed to extend beneficial effects throughout the
intestinal tract. It seems logical that combinations of nutritional and management
techniques are required to achieve a functional crop, including use of probiotics,
prebiotics, organic acids, exogenous enzymes, meal feeding and lighting programs.
This paper has focused exclusively on the crop, but in the larger picture, all segments
of the gut should be considered when planning for successful broiler production.
Therefore, in addition to decisions on the crop, nutrition that stimulates gizzard size
and activity, diets that provide ingredients digested at rates that provide for efficient
production and maintenance of the small intestine, and dietary constituents that fuel
healthy caecal fermentation may be an important method of improving broiler
performance and health in an antibiotic free era.
References
ABBAS HILMI, H.T., SURAKKA, A., APAJALAHTI, J. and SARIS, P.E.J. (2007) Identification of the
most abundant Lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Applied and
Environmental Microbiology 73: 7867-7873.
APAJALAHTI, J. and KETTUNEN, A. (2006) Rational development of novel microbial modulators, in:
BARUG, D., DE JONG, J., KIES, A.K. & VERSTEGEN, M.W.A. (Eds) Antimicrobial Growth Promoters.
Where Do We Go From Here? pp. 165-181 (Wageningen Academic Publishers, Wageningen).
APELDOORN, E.J., SCHRAMA, J.W., MASHALY, M.M. and PARMENTIER, H.K. (1999) Effect of
melatonin and lighting schedule on energy metabolism in broiler chickens. Poultry Science 78: 223-229.
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 9

ARAI, N., HASHIMOTO, Y., KITAGAWA, H., KON, Y. and KUDO, N. (1988) Immunohistochemical
study on the distribution of lymphoid tissues in the upper alimentary and respiratory tracts of chickens. The
Japanese Journal of Veterinary Science 50: 183-192.
ASMUNDSON, V.S. and HINSHAW, W.R. (1937) On the inheritance of pendulous crop in turkeys
(Meleagris gallopavo). Poultry Science 17: 276-285.
BARNES, E.M., IMPEY, C.S. and COOPER, D.M. (1980) Manipulation of the crop and intestinal flora of
the newly hatched chick. The American Journal of Clinical Nutrition 33: 2426-2433.
BAYER, R.C., CHAWAN, C.B. and BIRD, F.H. (1975) Scanning electron microscopy of the chicken crop –
The avian rumen? Poultry Science 54: 703-707.
BEASLEY, S.S., TAKALA, T.M., REUNANEN, J., APAJALAHTI, J. and SARIS, P.E.J. (2004)
Characterisation and electrotransformation of Lactobacillus crispatus isolated from chicken crop and
intestine. Poultry Science 83: 45-48.
BOLTON, W. (1965) Digestion in the crop of the fowl. British Poultry Science 6: 97-102.
BOWEN, T.E. and WALDROUP, P.W. (1969) The influence of propylene glycol on pH of the gastrointestinal
tract and the incidence of leg abnormalities in broiler chicks. Poultry Science 48: 608-613.
BUYSE, J., ADELSOHN, D.S., DECUYPERE, E. and SCANES, C.G. (1993) Diurnal-nocturnal changes in
food intake, gut storage of ingesta, food transit time and metabolism in growing broiler chickens: a model for
temporal control of energy balance. British Poultry Science 34: 699-709.
BUYSE, J., KÜHN, E.R. and DECUYPERE, E. (1996a) The use of intermittent lighting in broiler raising. 1.
Effect on broiler performance and efficiency of nitrogen retention. Poultry Science 75: 589-594.
BUYSE, J., SIMONS, P.C.M., BOSHOUWERS, F.M.G. and DECUYPERE, E. (1996b) Effect of
intermittent lighting, light intensity and source on the performance and welfare of broilers. World's
Poultry Science Journal 52: 121-130.
BYRD, J.A., HARGIS, B.M., CALDWELL, D.J., BAILEY, R.H., HERRON, K.L., MCREYNOLDS, J.L.,
BREWER, R.L., ANDERSON, R.C., BISCHOFF, K.M., CALLAWAY, T.R. and KUBENA, L.F. (2001)
Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella
and Campylobacter contamination in broilers. Poultry Science 80: 278-283.
CHAPLIN, S.B., RAVEN, J. and DUKE, G.E. (1992) The influence of the stomach on crop function and
feeding behaviour in domestic turkeys. Physiology & Behavior 52: 261-266.
CHAVEERACH, P., KEUZENKAMP, D.A., LIPMAN, L.J.A. and VAN KNAPEN, F. (2004) Effect of
organic acids in the drinking water for young broilers on Campylobacter infection, volatile fatty acid
production, gut microflora and histological cell changes. Poultry Science 83: 330-334.
CONNOR, E.E., LI, R.W., BALDWIN, R.L. VI and LI, C. (2010) Gene expression in the digestive tissues of
ruminants and their relationships with feeding and digestive processes. Animal 4: 993-1007.
CORRIER, D.E., BYRD, J.A., HARGIS, B.M., HUME, M.E., BAILEY, R.H. and STANKER, L.H.
(1999) Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed
withdrawal. Poultry Science 78: 45-49.
COUSIN, S., GULAT-OKALLA, M., MOTREFF, L., GOUYETTE, C., BOUCHIER, C., CLERMONT,
D. and BIZET, C. (2012) Lactobacillus gigeriorum sp. nov., isolated from chicken crop. International
Journal of Systematic and Evolutionary Microbiology 62: 330-334.
CUTLER, S.A., RASMUSSEN, M.A., HENSLEY, M.J., WILHELMS, K.W., GRIFFITH, R.W. and
SCANES, C.G. (2005) Effects of Lactobacilli and lactose on Salmonella typhimurium colonisation and
microbial fermentation in the crop of the young turkey. British Poultry Science 46: 708-716.
DE BEER, M., MCMURTRY, J.P., BROCHT, D.M. and COON, C.N. (2008) An examination of the role of
feeding regimens in regulating metabolism during the broiler breeder grower period. 2. Plasma hormones and
metabolites. Poultry Science 87: 264-275.
DENBOW, D.M. (1989) Peripheral and central control of food intake. Poultry Science 68: 938-947.
DURANT, J.A., CORRIER, D.E., BYRD, J.A., STANKER, L.H. and RICKE, C. (1999) Feed deprivation
affects crop environment and modulates Salmonella enteritidis colonisation and invasion of leghorn hens.
Applied and Environmental Microbiology 65: 1919-1923.
DURANT, J.A., CORRIER, D.E., STANKER, L.H. and RICKE, S.C. (2000) Expression of the hilA
Salmonella typhimurium gene in a poultry Salm. enteritidis isolate in response to lactate and nutrients.
Journal of Applied Microbiology 89: 63-69.
DUVE, L.R., STEENFELDT, S., THODBERG, K. and NIELSEN, B.L. (2011) Splitting the scotoperiod:
effects on feeding behaviour, intestinal fill and digestive transit time in broiler chickens. British Poultry
Science 52: 1-10.
EBLING, P.D., PONTALTI, G.C., VILLANUEVA, A.P. and RIBEIRO, A.M.L. (2015) Pendulous crop in
broilers. Brazilian Journal of Poultry Science 17: 395-398.
EDELMAN, S., LESKELÄ, S., RON, E., APAJALAHTI, J. and KORHONEN, T.K. (2003) In vitro
adhesion of an avian pathogenic Escherichia coli 078 strain to surfaces of the chicken intestinal tract and
ileal mucus. Veterinary Microbiology 91: 41-56.
Role of the crop: H.L. Classen et al.
10 World's Poultry Science Journal, Vol. 72, September 2016

EDELMAN, S., WESTERLUND-WIKSTRÖM, B., LESKELÄ, S., KETTUNEN, H., RAUTONEN, N.,
APAJALAHTI, J. and KORHONEN, T.K. (2002) In vitro adhesion specificity of indigenous Lactobacilli
with the avian intestinal tract. Applied and Environmental Microbiology 68: 5155-5159.
EDENS, F.W., PARKHURST, C.R., CASAS, I.A. and DOBROGOSZ, W.J. (1997) Principles of ex ovo
competitive exclusion and in ovo administration of Lactobacillus reuteri.Poultry Science 76: 179-196.
FERNÁNDEZ-RUBIO, C., ORDÓÑEZ, C., ABAD-GONZÁLEZ, J., GARCIA-GALLEGO, A.,
HONRUBIA, M.P., MALLO, J.J. and BALAÑA-FOUCE, R. (2009) Butyric acid-based feed additives
help protect broiler chickens from Salmonella Enteritidis infection. Poultry Science 88: 943-948.
FONSECA, B.B., BELETTI, M.E., DA SILVA, M.S., DA SILVA, P.L., DUARTE, I.N. and ROSSI, D.A.
(2010) Microbiota of the cecum, ileum morphometry, pH of the crop and performance of broiler chickens
supplemented with probiotics. Revista Brasileira de Zootecnia 39: 1756-1760.
FULLER, R. (1973) Ecological studies on the Lactobacillus flora associated with the crop epithelium of the
fowl. Journal of Applied Microbiology 36: 131-139.
FULLER, R. (1977) The importance of Lactobacilli in maintaining normal microbial balance in the crop.
British Poultry Science 1: 85-94.
FULLER, R. and BROOKER, B.E. (1974) Lactobacilli which attach to the crop epithelium of the fowl.
American Journal of Clinical Nutrition 27: 1305-1312.
FULLER, R. and TURVEY, A. (1971) Bacteria associated with the intestinal wall of the fowl (Gallus
domesticus). Journal of Applied Bacteriology 34: 617-622.
GAST, R.K. and BEARD, C.W. (1989) Age-related changes in the persistence and pathogenicity of
Salmonella typhimurium in chicks. Poultry Science 68: 1454-1460.
GORDON, R.W. and ROLAND, D.A. Sr (1997) The influence of environmental temperature on in vivo
limestone solubilisation, feed passage rate, and gastrointestinal pH in laying hens. Poultry Science 76: 683-
688.
GUAN, L.L., HAGEN, K.E., TANNOCK, G.W., KORVER, D.R, FASENKO, G.M. and ALLISON, G.E.
(2003) Detection and identification of Lactobacillus species in crops of broilers of different ages by using
PCR-denaturing gradient gel electrophoresis and amplified ribosomal DNA restriction analysis. Applied and
Environmental Microbiology 69: 6750-6757.
GUSILS, C., GONZÁLEZ, S.N. and OLIVER, G. (1999) Some probiotic properties of chicken Lactobacilli.
Canadian Journal of Microbiology 45: 981-987.
HAGEN, K.E., GUAN, L.L., TANNOCK, G.W., KORVER, D.R. and ALLISON, G.E. (2005) Detection,
characterisation, and in vitro and in vivo expression of genes encoding S-proteins in Lactobacillus gallinarum
strains isolated from chicken crops. Applied and Environmental Microbiology 71: 6633-6643.
HAMMES, W.P. and VOGEL, R.F. (1995) The genus Lactobacillus: in WOOD, B.J.B. & HOLZAPFEL, W.
H. (Eds) The Genera of Lactic Acid Bacteria, pp. 19-54 (Chapman & Hall, Glasgow, Scotland).
HAMMONS, S., OH, P.L., MARTÍNEZ, I., CLARK, K., SCHLEGEL, V.L., SITORIUS, E.,
SCHEIDELER, S.E. and WALTER, J. (2010) A small variation in diet influences the Lactobacillus
strain composition in the crop of broiler chickens. Systematic and Applied Microbiology 33: 275-281.
HARGIS, B.M., CALDWELL, D.J., BREWER, R.L., CORRIER, D.E. and DELOACH, J.R. (1995)
Evaluation of the chicken crop as a source of Salmonella contamination for broiler carcasses. Poultry
Science 74: 1548-1552.
HINTON, A. Jr, BUHR, R.J. and INGRAM, K.D. (2000a) Physical, chemical and microbiological changes in
the crop of broiler chickens subjected to incremental feed withdrawal. Poultry Science 79: 212-218.
HINTON, A. Jr, BUHR, R.J. and INGRAM, K.D. (2000b) Reduction of Salmonella in the crop of broiler
chickens subjected to feed withdrawal. Poultry Science 79: 1566-1570.
HINTON, A. Jr, BUHR, R.J. and INGRAM, K.D. (2002) Carbohydrate-based cocktails that decrease the
population of Salmonella and Campylobacter in the crop of broiler chickens subjected to feed withdrawal.
Poultry Science 81: 780-784.
HODGES, R.D. (1974) The Histology of the Fowl. Academic Press, London.
HONG, Y.H., SONG, W., LEE, S.H. and LILLEHOJ, H.S. (2012) Differential gene expression profiles of β-
defensins in the crop, intestine, and spleen using a necrotic enteritis model in 2 commercial broiler chicken
lines. Poultry Science 91: 1081-1088.
HUMPHREY, T.J., BASKERVILLE, A., WHITEHEAD, A., ROWE, B. and HENLEY, A. (1993)
Influence of feeding patterns on the artificial infection of laying hens with Salmonella enteritidis phage
type 4. Veterinary Record 132: 407-409.
JACKSON, S. and DUKE, G.E. (1995) Intestine fullness influences feeding behaviour and crop filling in the
domestic turkey. Physiology & Behavior 58: 1027-1034.
JÓZEFIAK, D., RUTKOWSKI, A., JENSEN, B.B. and ENBERG, R.M. (2006) The effect of β-glucanase
supplementation of barley- and oat-based diets on growth performance and fermentation in broiler
gastrointestinal tract. British Poultry Science 47: 57-64.
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 11

KAIYA, H., FURUSE, M., MIYAZOTO, M. and KANGAWA, K. (2009) Current knowledge of the roles of
ghrelin in regulating food intake and energy balance in birds. General and Comparative Endocrinology 163:
33-39.
KUBENA, L.F., BYRD, J.A., MOORE, R.W., RICKE, S.C. and NISBET, D.J. (2005) Effects of drinking
water treatment on susceptibility of laying hens to Salmonella enteritidis during forced molt. Poultry Science
84: 204-211.
LAN, G.Q., ABDULLAH, N., JALALUDIN, S. and HO, Y.W. (2010) In vitro and in vivo enzymatic
dephosphorylation of phytase in maize-soya bean meal diets for broiler chickens by phytase of
Mitsuokella jalaludinii.Animal Feed Science and Technology 158: 155-164.
LAWLOR, P.G., LYNCH, P.B., CAFFREY, P.J., O'REILLY, J.J. and O'CONNELL, M.K. (2005)
Measurements of the acid-binding capacity of ingredients used in pig diets. Irish Veterinary Journal 58:
447-452.
LEBEER, S., VERHOEVEN, T.L.A., CLAES, I.J.J., DE HERTOGH, G., VERMEIRE, S., BUYSE, J.,
VAN IMMERSEEL, F., VANDERLEYDEN, J. and DE KEERSMAECKER, S.C.J. (2011) FISH
analysis of Lactobacillus biofilms in the gastrointestinal tract of different hosts. Letters in Applied
Microbiology 52: 220-226.
LOHMANN TIERZUCHT (2016). Lohmann LSL-Lite Management Guide. Cuxhaven, Germany, http://www.
hylinena.com/UserDocs/products/Lohmann_LSL-Lite.pdf (accessed May 15, 2016).
MALLEAU, A.E., DUNCAN, I.J.H., WIDOWSKI, T.M. and ATKINSON, J.L. (2007) The importance of
rest in young domestic fowl. Applied Animal Behaviour Science 106: 52-79.
MOORE, R.W., PARK, S.Y., KUBENA, L.F., BYRD, J.A., MCREYNOLDS, J.L., BURNHAM, M.R.,
HUME, M.E., BIRKHOLD, S.G., NISBET, D.J. and RICKE, S.C. (2004) Comparison of zinc acetate and
propionate addition on gastrointestinal tract fermentation and susceptibility of laying hens to Salmonella
enteritidis during forced molt. Poultry Science 83: 1276-1286.
NAHASHON, S.N., NAKAUE, H.S. and MIROSH, L.W. (1994) Phytase activity, phosphorus and calcium
retention, and performance of Single Comb White Leghorn layers fed diets containing two levels of available
phosphorus and supplemented with direct-fed microbials. Poultry Science 73: 1552-1562.
ONYANGO, E.M., BEDFORD, M.R. and ADEOLA, O. (2005) Phytase activity along the digestive tract of
the broiler chick: A comparative study of an Escherichia coli-derived and Peniophora lycii phytase.
Canadian Journal of Animal Science 85: 61-68.
PEINADO, M.J., ECHÁVARRI, A., RUIZ, R., SUÁREZ-PEREIRA, E. and MELLET, C.O. (2013)
Effects of inulin and di-D-fructose dianhydride-enriched caramels on intestinal microbiota composition
and performance of broiler chickens. Animal 7: 1779-1788.
PETR, J. and RADA, V. (2001) Bifidobacteria are obligate inhabitants of the crop of adult laying hens.
Journal of Veterinary Medicine Series B 48: 227-233.
RADA, V. and MAROUNEK, M. (1996) Effect of monensin on crop microflora of broiler chickens. Annales
De Zootechnie 45: 283-288.
RICHARDS, J.D., ATWELL, C.A., VÁZQUEZ-AÑÓN, M. and DIBNER, J.J. (2005) Comparative in vitro
and in vivo absorption of 2-hydroxy-4(methylthio) butanoic acid and methionine in the broiler chicken.
Poultry Science 84: 1397-1405.
RICKE, S.C., DUNKLEY, C.S. and DURANT, J.A. (2013) A review of development of novel strategies for
controlling Salmonella Enteritidis colonisation in laying hens. Poultry Science 92: 502-525.
RICKE, S.C., PARK, S.Y., MOORE, R.W., KWON, Y.M., WOODWARD, C.L., BYRD, J.A., NISBET,
D.J. and KUBENA, L.F. (2004) Feeding low calcium and zinc molt diets sustains gastrointestinal
fermentation and limits Salmonella enterica serovar Enteritidis colonisation in laying hens. Journal of
Food Safety 24: 291-308.
RUBIO, L.A., BRENES, A., SETIÉN, I., DE LA ASUNCIÓN, G., DURÁN, N. and CUTULI, M.T. (1998)
Lactobacilli counts in crop, ileum and caecum of growing broiler chickens fed on practical diets containing
whole or dehulled sweet lupin (Lupinus angustifolius) seed meal. British Poultry Science 39: 354-359.
RYNSBURGER, J.M. (2009) Physiological and nutritional factors affecting protein digestion in broiler
chickens. M.Sc. thesis, University of Saskatchewan.
SAVORY, C.J. (1985) An investigation into the role of the crop in control of feeding in Japanese quail and
domestic fowls. Physiology & Behavior 35: 917-928.
SCANES, C.G., CAMPBELL, R. and GRIMINGER, P. (1987) Control of energy balance during egg
production in the laying hen. Journal of Nutrition 117: 605-611.
SCANES, C.G. and PIERZCHALA-KOZIEC, K. (2014) Biology of the gastro-intestinal tract in poultry.
Avian Biology Research 7: 193-222.
SCHWEAN-LARDNER, K., FANCHER, B.I. and CLASSEN, H.L. (2012) Impact of daylength on the
productivity of two commercial broiler strains. British Poultry Science 53: 7-18.
SCHWEAN-LARDNER, K., FANCHER, B.I., GOMIS, S., VAN KESSEL, A., DALAL, S. and
CLASSEN, H.L. (2013) Effect of day length on cause of mortality, leg health, and ocular health in
broilers. Poultry Science 92: 1-11.
Role of the crop: H.L. Classen et al.
12 World's Poultry Science Journal, Vol. 72, September 2016

SCHWEAN-LARDNER, K., FANCHER, B.I., LAARVELD, B. and CLASSEN, H.L. (2014) Effect of day
length on flock behavioural patterns and melatonin rhythms in broilers. British Poultry Science 55: 21-30.
SEKELJA, M., RUD, I., KNUTSEN, S.H., DENSTADLI, V., NÆS, T. and RUDI, K. (2012) Abrupt
temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Applied
and Environmental Microbiology 78: 2941-2948.
SEO, K., HOLT, P.S., BRAKETT, R.E., GAST, R.K. and STONE, H.D. (2002) Mucosal humoral immunity
to experimental Salmonella enteritidis infection in the chicken crop. Avian Diseases 46: 1015-1020.
SEO, K., HOLT, P.S. and GAST, R.K. (2001) Comparison of Salmonella Enteritidis infection in hens molted
via long-term feed withdrawal versus full-fed wheat middling. Journal of Food Protection 12: 1971-1921.
SEO, K., HOLT, P.S., VAUGHN, L.E., GAST, R.K. and STONE, H.D. (2003) Detection of Salmonella
enteritidis-specific immunoglobulin A antibodies in crop samples from chickens infected with Salmonella
enteritidis.Poultry Science 82: 67-70.
SHIRES, A., THOMPSON, J.R., TURNER, B.V., KENNEDY, P.M. and GOH, Y.K. (1987) Rate of
passage of corn-canola meal and corn-soybean meal diets through the gastrointestinal tract of broiler and
White Leghorn chickens. Poultry Science 66: 289-298.
SMITH, H.W. and TUCKER, J.F. (1980) The virulence of Salmonella strains for chickens: Their excretion by
infected chickens. Journal of Hygiene (Cambridge) 4: 479-488.
SU, G., SØRENSEN, P. and KESTIN, S.C. (1999) Meal feeding is more effective than early feed restriction at
reducing the prevalence of leg weakness in broiler chickens. Poultry Science 78: 949-955.
SVIHUS, B. (2011) The gizzard: function, influence of diet structure and effects on nutrient availability. World's
Poultry Science Journal 67: 207-224.
SVIHUS, B. (2015) Optimising gut function in broilers through crop and gizzard manipulation. Proc. Arkansas
Nutrition Conference, Rogers, AR, US September 9-11 (11pages); accessed at http://www.
thepoultryfederation.com/annual-events/nutrition-conference/download-2015-proceedings on January 3,
2016.
SVIHUS, B., CHOCT, M. and CLASSEN, H.L. (2013a) Function and nutritional roles of the avian caeca: a
review. World's Poultry Science Journal 69: 249-264.
SVIHUS, B., LUND, V.B., BORJGEN, B., BEDFORD, M.R. and BAKKEN, M. (2013b) Effect of
intermittent feeding, structural components and phytase in performance and behaviour of broiler chickens.
British Poultry Science 54: 222-230.
SVIHUS, B., SACRANIE, A., DENSTADLI, V. and CHOCT, M. (2010) Nutrient utilisation and
functionality of the anterior digestive tract caused by intermittent feeding and inclusion of whole wheat
in diets for broiler chickens. Poultry Science 89: 2617-2625.
TACHIBANA, T., MATSUMOTO, M., FURUSE, M., HASEGAWA, S., YOSHIZAWA, F. and
SUGAHARA, K. (2003) Central, but not peripheral, glucagon-like peptide-1 inhibits crop emptying in
chicks. Comparative Biochemistry and Physiology - Part A 134: 777-781.
THAXTON, J.P., CUTLER, S.A., GRIFFITH, R. and SCANES, C.G. (2006) Changes in tissue nitrite
concentration in the crop of the turkey poult in response to Salmonella typhimurium challenge. Poultry
Science 85: 1015-1019.
VAN DIJK, A. VELDHUIZEN, E.J.A., KALKHOVE, S.I.C., TJEERDSMA-VAN BOKHOVEN, J.L.M.,
ROMIJN, R.A. and HAAGSMAN, H.P. (2007) The β-defensin gallinacin-6 is expressed in the chicken
digestive tract and has antimicrobial activity against food-borne pathogens. Antimicrobial Agents and
Chemotherapy 51: 912-922.
VAN GERWE, T., BOUMA, A., WAGENAAR, J.P., JACOBS-REITSMA, W.F. and STEGEMAN, A.
(2010) Comparison of Campylobacter levels in crops and ceca of broilers at slaughter. Avian Diseases 54:
1072-1074.
VAN IMMERSEEL, F., RUSSELL, J.B., FLYTHE, M.D., GANTOIS, I., TIMBERMONT, L.,
PASMANS, F., HAESEBROUCK, F. and DUCATELLE, R. (2006) The use of organic acids to
combat Salmonella in poultry: a mechanistic explanation of efficacy. Avian Pathology 35: 182-188.
VAUGHN, L.E., HOLT, P.S. and GAST, R.K. (2008a) Cellular assessment of crop lymphoid tissue from
specific-pathogen-free White Leghorn chickens after Salmonella enteritidis challenge. Avian Diseases 52:
657-664.
VAUGHN, L.E., HOLT, P.S., MOORE, R.W., GAST, R.K. and ANDERSON, K.E. (2008b) Crop immune
response post-Salmonella enteritidis challenge in eight commercial egg-layer strains and specific-pathogen-
free White Leghorn chickens. Avian Diseases 52: 79-87.
VERMETTE, C., SCHWEAN-LARDNER, K., GOMIS, S., CROWE, T. and CLASSEN, H.L. (2016) The
impact of graded levels of daylength on turkey productivity to eighteen weeks of age. Poultry Science 95:
985-996.
WHEELER, H.O., REID, B.L., FERGUSON, T.M. and COUCH, J.R. (1960) Differences in susceptibility
of Broad Breasted Bronze and Beltsville Small White turkeys to dietary-induced pendulous crop. Poultry
Science 39: 263-267.
Role of the crop: H.L. Classen et al.
World's Poultry Science Journal, Vol. 72, September 2016 13

YU, S., COWIESON, A., GILBERT, C., PLUMSTEAD, P. and DALSGAARD, S. (2012) Interactions of
phytate and myo-inositol phosphate esters (IP
1-5
) including IP
5
isomers with dietary protein and iron and
inhibition of pepsin. Journal of Animal Science 90: 1824-1832.
ZELLER, E., SCHOLLENBERGER, M, KÜHN, I. and RODEHUTSCORD, M. (2015) Hydrolysis of
phytate and formation of inositol phosphate isomers without or with supplemented phytases in different
segments of the digestive tract of broilers. Journal of Nutritional Science 4: e1 doi:10.1017/jns.2014.62.
ZELLER, E., SCHOLLENBERGER, M, KÜHN, I. and RODEHUTSCORD, M. (2016) Dietary effects on
inositol phosphate breakdown in the crop of broilers. Archives of Animal Nutrition 70: 57-71.
Role of the crop: H.L. Classen et al.
14 World's Poultry Science Journal, Vol. 72, September 2016