Function of the digestive system 1

2014 Poultry Science Association, Inc. Function of the digestive system 1 2 Birger Svihus 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. 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- 1 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: birger.svihus@nmbu.no

Svihus: INFORMAL NUTRITION SYMPOSIUM 307 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 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

308 JAPR: Symposium 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 309 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 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

310 JAPR: Symposium 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 carrying 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 311 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 pelleting 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

312 JAPR: Symposium 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 implication 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. REFERENCES AND NOTES 1. Chaplin, S. B., J. Raven, and G. E. Duke. 1992. The influence of the stomach on crop function and feeding-behavior in domestic turkeys. Physiol. Behav. 52:261 266. 2. Jackson, S., and G. E. Duke. 1995. Intestine fullness influences feeding behaviour and crop filling in the domestic turkey. Physiol. Behav. 58:1027 1034. 3. Nielsen, B. L. 2004. Behavioural aspects of feeding constraints: Do broilers follow their gut feelings? Appl. Anim. Behav. Sci. 86:251 260. 4. Svihus, B., A. Sacranie, V. Denstadli, and M. Choct. 2010. Nutrient utilization and functionality of the anterior digestive tract caused by intermittent feeding and inclusion of whole wheat in diets for broiler chickens. Poult. Sci. 89:2617 2625. 5. Svihus, B., V. B. Lund, B. Borjgen, M. R. Bedford, and M. Bakken. 2013. Effect of intermittent feeding, structural components and phytase on performance and behaviour of broiler chickens. Br. Poult. Sci. 54:222 230. 6. Boa-Amponsem, K., E. A. Dunnington, and P. B. Siegel. 1991. Genotype, feeding regimen, and diet interactions in meat chickens. 2. Feeding behaviour. Poult. Sci. 70:689 696. 7. Barash, I., Z. Nitsan, and I. Nir. 1992. Metabolic and behavioural adaptation of light-bodied chicks to meal feeding. Br. Poult. Sci. 33:271 278.

Svihus: INFORMAL NUTRITION SYMPOSIUM 313 8. Buyse, J., D. S. Adelsohn, E. Decuypere, and C. G. Scanes. 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 intake. Br. Poult. Sci. 34:699 709. 9. Barash, I., Z. Nitsan, and I. Nir. 1993. Adaptation of light-bodied chicks to meal feeding: Gastrointestinal-tract and pancreatic-enzymes. Br. Poult. Sci. 34:35 42. 10. Svihus, B., H. Hetland, M. Choct, and F. Sundby. 2002. Passage rate through the anterior digestive tract of broiler chickens fed on diets with ground or whole wheat. Br. Poult. Sci. 43:662 668. 11. Ao, T., A. H. Cantor, A. J. Pescatore, and J. L. Pierce. 2008. In vitro evaluation of feed-grade enzyme activity at ph levels simulating various parts of the avian digestive tract. Anim. Feed Sci. Technol. 140:462 468. 12. Abbas Hilmi, H. T., A. Surakka, J. Apajalahti, and P. E. J. Saris. 2007. Identification of the most abundant Lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Appl. Environ. Microbiol. 73:7867 7873. 13. Bolton, W. 1965. Digestion in the crop of the fowl. Br. Poult. Sci. 6:97 102. 14. Duke, G. E. 1992. Recent studies on regulation of gastric motility in turkeys. Poult. Sci. 71:1 8. 15. Svihus, B. 2011. The gizzard: Function, influence of diet structure and effects on nutrient availability. World s Poult. Sci. J. 67:207 223. 16. Shires, A., J. R. Thompson, B. V. Turner, P. M. Kennedy, and Y. K. Goh. 1987. Rate of passage of canola meal and corn-soybean meal diets through the gastrointestinal tract of broiler and white leghorn chickens. Poult. Sci. 66:289 298. 17. van der Klis, J. D., M. W. A. Verstegen, and W. de Wit. 1990. Absorption of minerals and retention time of dry matter in the gastrointestinal tract of broilers. Poult. Sci. 69:2185 2194. 18. Dänicke, S., W. Vahjen, O. Simon, and H. Jeroch. 1999. Effects of dietary fat type and xylanase supplementation to rye-based broiler diets on selected bacterial groups adhering to the intestinal epithelium, on transit time of feed, and on nutrient digestibility. Poult. Sci. 78:1292 1299. 19. Amerah, A. M., V. Ravindran, R. G. Lentle, and D. G. Thomas. 2008. Influence of feed particle size on the performance, energy utilization, digestive tract development, and digesta parameters of broiler starters fed wheat- and cornbased diets. Poult. Sci. 87:2320 2328. 20. Amerah, A. M., V. Ravindran, and R. G. Lentle. 2009. Influence of insoluble fiber and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. Br. Poult. Sci. 50:366 375. 21. Hetland, H., B. Svihus, and Å. Krogdahl. 2003. Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. Br. Poult. Sci. 44:275 282. 22. Rougière, N., and B. Carré. 2010. Comparison of gastrointestinal transit times between chickens from D+ and D- genetic lines selected for divergent digestion efficiency. Animal 4:1861 1872. 23. Duke, G. E. 1986. Alimentary canal: Anatomy, regulation of feeding, and motility. Pages 269 288 in Avian Physiology. P. D. Sturkie, ed. Springer-Verlag, New York, NY. 24. Farner, D. S. 1960. Digestion and the digestive system. Pages 411 467 in Biology and Comparative Physiology of Birds. A. J. Marshall, ed. Academic Press, New York, NY. 25. McLelland, J. 1989. Anatomy of the avian cecum. J. Exp. Zool. Suppl. 3:2 9. 26. Riley, W. W., Jr., and R. E. Austic. 1984. Influence of dietary electrolytes on digestive tract ph and acid-base status of chicks. Poult. Sci. 63:2247 2251. 27. Mahagna, M., I. Nir, M. Larbier, and Z. Nitsan. 1995. Effect of age and exogenous amylase and protease on development of the digestive tract, pancreatic enzyme activities and digestibility of nutrients in young meat-type chicks. Reprod. Nutr. Dev. 35:201 212. 28. Mahagna, M., and I. Nir. 1996. Comparative development of digestive organs, intestinal disaccharidases and some blood metabolites in broiler and layer-type chicks after hatching. Br. Poult. Sci. 37:359 371. 29. Hetland, H., B. Svihus, and V. Olaisen. 2002. Effect of feeding whole cereals on performance, starch digestibility and duodenal particle size distribution in broiler chickens. Br. Poult. Sci. 43:416 423. 30. Sacranie, A., B. Svihus, V. Denstadli, B. Moen, P. A. Iji, and M. Choct. 2012. The effect of insoluble fiber and intermittent feeding on gizzard development, gut motility, and performance of broiler chickens. Poult. Sci. 91:693 700. 31. Hetland, H., and B. Svihus. 2007. Inclusion of dust bathing materials affects nutrient digestion and gut physiology of layers. J. Appl. Poult. Res. 16:22 26. 32. Steenfeldt, S., J. B. Kjaer, and R. M. Engberg. 2007. Effect of feeding silages or carrots as supplements to laying hens on production performance, nutrient digestibility, gut structure, gut microflora and feather pecking behaviour. Br. Poult. Sci. 48:454 468. 33. Senkoylu, N., H. E. Samli, H. Akyurek, A. A. Okur, and M. Kanter. 2009. Effects of whole wheat with or without xylanase supplementation on performance of layers and digestive organ development. Ital. J. Anim. Sci. 8:155 163. 34. Gordon, R. W., and D. A. Roland. 1997. The influence of environmental temperature on in vivo limestone solubilization, feed passage rate, and gastrointestinal ph in laying hens. Poult. Sci. 76:683 688. 35. Gabriel, I., S. Mallet, and M. Leconte. 2003. Differences in the digestive tract characteristics of broiler chickens fed on complete pelleted diet or on whole wheat added to pelleted protein concentrate. Br. Poult. Sci. 44:283 290. 36. Engberg, R. M., M. S. Hedemann, S. Steenfeldt, and B. B. Jensen. 2004. Influence of whole wheat and xylanase on broiler performance and microbial composition and activity in the digestive tract. Poult. Sci. 83:925 938. 37. Bjerrum, L., K. Pedersen, and R. M. Engberg. 2005. The influence of whole wheat feeding on salmonella infection and gut flora composition in broilers. Avian Dis. 49:9 15. 38. Huang, D. S., D. F. Li, J. J. Xing, Y. X. Ma, Z. J. Li, and S. Q. Lv. 2006. Effects of feed particle size and feed form on survival of Salmonella typhimurium in the alimentary tract and cecal S. typhimurium reduction in growing broilers. Poult. Sci. 85:831 836. 39. González-Alvarado, J. M., E. Jimenez-Moreno, D. G. Valencia, R. Lazaro, and G. G. Mateos. 2008. Effects of fiber source and heat processing of the cereal on the development and ph of the gastrointestinal tract of broilers fed diets based on corn or rice. Poult. Sci. 87:1779 1795.

314 JAPR: Symposium 40. Jiménez-Moreno, E., J. M. Gonzalez-Alvarado, R. Lazaro, and G. G. Mateos. 2009. Effects of type of cereal, heat processing of the cereal, and fiber inclusion in the diet on gizzard ph and nutrient utilization in broilers at different ages. Poult. Sci. 88:1925 1933. 41. Engberg, R. M., M. S. Hedemann, and B. B. Jensen. 2002. The influence of grinding and pelleting of feed on the microbial composition and activity in the digestive tract of broiler chickens. Br. Poult. Sci. 43:569 579. 42. Frikha, M., H. M. Safaa, M. P. Serrano, X. Arbe, and G. G. Mateos. 2009. Influence of the main cereal and feed form of the diet on performance and digestive tract traits of brown-egg laying pullets. Poult. Sci. 88:994 1002. 43. Svihus, B., E. Juvik, H. Hetland, and Å. Krogdahl. 2004. Causes for improvement in nutritive value of broiler chicken diets with whole wheat instead of ground wheat. Br. Poult. Sci. 45:55 60. 44. Noy, Y., and D. Sklan. 1995. Digestion and absorption in the young chick. Poult. Sci. 74:366 373. 45. Svihus, B. 2011. Effect of digestive tract conditions, feed processing and ingredients on response to NSP enzymes. Pages 129 159 in Enzymes in Farm Animal Nutrition, 2nd ed. M. R. Bedford and G. Partridge, ed. CABI International, Wallingford, UK. 46. Sklan, D., S. Hurwitz, P. Budowski, and I. Ascarelli. 1975. Fat digestion and absorption in chicks fed raw or heated soybean meal. J. Nutr. 105:57 63. 47. Hetland, H., and B. Svihus. 2001. Effect of oat hulls on performance, gut capacity and feed passage time in broiler chickens. Br. Poult. Sci. 42:354 361. 48. Rodgers, N. J., M. Choct, H. Hetland, F. Sundby, and B. Svihus. 2012. Extent and method of grinding of sorghum prior to inclusion in complete pelleted broiler chicken diets affects broiler gut development and performance. Anim. Feed Sci. Technol. 171:60 67. 49. Weurding, R. E., A. Veldman, W. A. G. Veen, P. J. van der Aar, and M. W. A. Verstegen. 2001. Starch digestion rate in the small intestine of broiler chickens differs among feedstuffs. J. Nutr. 131:2329 2335. 50. Hurwitz, S., A. Bar, M. Katz, D. Sklan, and P. Budowski. 1973. Absorption and secretion of fatty acids and bile acids in the intestine of the laying fowl. J. Nutr. 103:543 547. 51. Riesenfeld, G., D. Sklan, A. Bar, U. Eisner, and S. Hurwitz. 1980. Glucose absorption and starch digestion in the intestine of the chicken. J. Nutr. 110:117 121. 52. Sklan, D., and S. Hurwitz. 1980. Protein digestion and absorption in young chicks and turkeys. J. Nutr. 110:139 144. 53. Zimonja, O., and B. Svihus. 2009. Effects of processing of wheat or oat starch on technical pellet quality and nutritional value for broilers. Anim. Feed Sci. Technol. 149:287 297. 54. Yamauchi, K. 2007. Review of a histological intestinal approach to assessing the intestinal function in chickens and pigs. Anim. Sci. J. 78:356 370. 55. Awad, W. A., K. Ghareeb, and J. Böhm. 2011. Evaluation of the chicory inulin efficacy on ameliorating the intestinal morphology and modulating the intestinal electrophysiological properties in broiler chickens. J. Anim. Physiol. Anim. Nutr. (Berl.) 95:65 72. 56. Clench, M. H., and J. R. Mathias. 1995. The avian cecum: A review. Wilson Bull. 107:93 121. 57. Svihus, B., M. Choct, and H. L. Classen. 2013. Function and nutritional roles of the avian caeca: A review. World s Poult. Sci. J. 69:249 263. 58. Clarke, P. L. 1978. The structure of the ileo-caecocolic junction of the domestic fowl (Gallus gallus L). Br. Poult. Sci. 19:595 600. 59. Duke, G. E. 1989. Relationship of cecal and colonic motility to diet, habitat, and cecal anatomy in several avian species. J. Exp. Zool. Suppl. 3:38 47. 60. Duke, G. E., E. Eccleston, S. Kirkwood, C. F. Louis, and H. P. Bedbury. 1984. Cellulose digestion by domestic turkeys fed low or high fiber diets. J. Nutr. 114:95 102. 61. Hinton, A., Jr., R. J. Buhr, and K. D. Ingram. 2000. Physical, chemical, and microbiological changes in the ceca of broiler chickens subjected to incremental feed withdrawal. Poult. Sci. 79:483 488. 62. Warriss, P. D., L. J. Wilkins, S. N. Brown, A. J. Phillips, and V. Allen. 2004. Defaecation and weight of the gastrointestinal tract contents after feed and water withdrawal in broilers. Br. Poult. Sci. 45:61 66. 63. Thomas, D. H. 1982. Salt and water excretion by birds: The lower intestine as an integrator of renal and intestinal excretion. Comp. Biochem. Physiol. 71:527 535. 64. Pulliainen, E., and P. Tunkkari. 1983. Seasonal variation in the gut length of willow grouse (Lagopus lagopus) in Finnish Lapland. Ann. Zool. Fenn. 20:53 56. 65. Svihus, B., K. H. Kløvstad, V. Perez, O. Zimonja, S. Sahlström, R. B. Schüller, W. K. Jeksrud, and E. Prestløkken. 2004. Physical and nutritional effects of pelleting of broiler chicken diets made from wheat ground to different coarsenesses by the use of roller mill and hammer mill. Anim. Feed Sci. Technol. 117:281 293. 66. Svihus, B., and H. Hetland. 2001. Ileal starch digestibility in growing broiler chickens fed on a wheat-based diet is improved by mash feeding, dilution with cellulose or whole wheat inclusion. Br. Poult. Sci. 42:633 637. 67. Hetland, H., B. Svihus, and M. Choct. 2005. Role of insoluble fiber on gizzard activity in layers. J. Appl. Poult. Res. 14:38 46. 68. de Vries, R. P., and J. Visser. 2001. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 65:497 522. 69. Simon, O., and F. Igbasan. 2002. In vitro properties of phytases from various microbial origins. Int. J. Food Sci. Technol. 37:813 822. 70. Ding, M., Y. Teng, Q. Yin, J. Zhao, and F. Zhao. 2008. The N-terminal cellulose-binding domain of EGXA increases thermal stability of xylanase and changes its specific activities on different substrates. Acta Biochim. Biophys. Sin. (Shanghai) 40:949 954. 71. Liebert, F., C. Wecke, and F. J. Schôner. 1993. Phytase activity in different gut contents of chickens as dependent on level of phosphorus and phytase supplementation. Pages 201 205 in Enzymes in Animal Nutrition. C. Wenk and M. Boessinger, ed. Proceedings of the 1st Feed Enzyme Symposium, Kartause Ittingen, Switzerland. 72. Lan, G. Q., N. Abdullah, S. Jalaludin, and Y. W. Ho. 2010. In vitro and in vivo enzymatic dephosphorylation of phytate in maize-soya bean meal diets for broiler chickens by phytase of Mitsuokella jalaludinii. Anim. Feed Sci. Technol. 158:155 164.