Is Intestinal Absorption Capacity Rate-Limiting for Performance in Poultry?12

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Is INTESTINAL ABSORPTION CAPACITY RATE-LIMITING FOR PERFORMANCE IN POULTRY. 3192 W J. CROOM3,J. BRAKE, B. A. COLES, G. B. HAVENSTEIN and V. L. CHRISTENSEN Depamnent Poultry Science, North Carolina State University, Raleigh, NC 27695-7608 Phone: (919) 515-8788 F M : (919) 515-2625 E-mail: jim-croom @ncsu.edu B. W. MCBRIDE Depariment of Animal and Poultry Science, Universityof Guelph, Guelph, ON N l G 2W1, Canada E. D. PEEBLES Department of Poultry Science, Mississippi State University,Mississippi State, MS 39762 I. L. T A W R Depament of Medicine, Medical Universityof South Carolina, Charleston, SC 29425

Primarv Audience: Industrv and Academic Nutritionists, Geneticists

1 Presented

at the 1998 Poultry Science Association Informal Poultry Nutrition Symposium: "Impactof Early Nutrition on Poultry." 2 The use of trade names in this publication does not imply endorsement by the North Carolina agriculturalResearch Service of the products named or criticism of similar ones not mentioned. 3 To whom correspondence should be addressed

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IMPORTANCE OF EARLY DESCRIPTION OF PROBLEM THE There is a perception among poultry GASTROINTESTINAL GROWTH

nutritionists that the absorption of nutrients is a potential rate-limiting factor in survival, growth, and feed conversion in hatchhgs as well as in growing birds, and this has been proposed to be an important emerging issue in the poultry and livestock industries (see reviews [l,21). For poultry, this perception has been fostered by the emergence of ideas concerning the development and function of the digestive tract that have been developed over the last two decades. They are: 1) growth during the early posthatch period places a priority on the development of "supply organs," such as the digestive tract, in order to assure later growth of ''demand tissues," such as muscle [3,4]; 2) genetic selection for growth and reproduction has altered the digestive tract of poultry to such a degree that digestive processes are not fully developed at hatch [5,6,7]; and 3) the gastrointestinaltract accounts for a large share of the bird's total energy needs, and genetic selection for production traits may not have resulted in concomitant selection for perfectly correlated enhanced gastrointestinal tract function and energetic efficiency [8, 9, 101. Collectively, these concepts imply that an insufficient capacity of the intestinal tract for nutrient absorption could negatively affect performance and survival [3, 8, 111. Similarly, potential energetic inefficiencies in the gut tissues could limit phenotypic expression in birds with superior genotypes [2]. Although our assumption, based on current data, is that absorptive capacity is rate-limiting, alternative interpretations of existing information support the premise that the gut has achieved perfect balance with post-absorptive tissue metabolism [12,13]. Recent work has been directed at achieving a better understanding of factors that affect nutrient absorption and the development of potential therapeutic techniques to remedy possible limitations in nutrient absorption. This paper will briefly review the rationale related to current perceptions about intestinal development and function as a rate-limiting process for poultry production and discuss new technologies that are available to address these problems.

Previous studies have shown that at posthatch, the gastrointestinal tract of the hatchling chick or goose accounts for a larger percentage of whole body weight [3, 41 than in adult birds. This percentage steadily decreases with age. Similar findings have been reported for the domestic turkey [9,10] (Figure 1). This developmental pattern is believed to reflect a survival strategy in which great importance is placed on the development of nutrient supply functions early in life in order that post-absorptive growth functions can be maximized later in the life cycle [14]. During early life, the bird can afford to partition only a limited quantity of nutrients and energy for tissue growth, which must be distributed among different organ systems. Because supply organs are responsible for making energy available for post-absorptive growth processes and because growth ceases when the energy supply from the supply organs is less than the maintenance supply of the demand organs, the bird places a high priority on early intestinal growth and development. It has been suggested that final growth in the bird is directly proportional to an early high specific growth rate of supply organs [4]. Dror et al. [111 have concluded that development of the duodenum and jejunum may be limiting for growth in young birds of heavy breeds. This agrees with earlier work by Pinchasov et al. [15], who concluded that "the GI" is more limiting in heavy- than in light-breed chicks."

MODERN GENETIC SELECTION HAS ALTERED THE INTESTINAL TRACT Genetic selection for production parameters has altered both the form and the function of the intestinal tract in poultry. Dror et al. [ll] found that the relative weight of the duodenum and jejunum was greater in a light breed of chickens than in a breed selected for increased body weight. Similar differences were noted by Nir et al. [16] between light-breed and heavy-breed chicks. Nitsan et al. [8] reported that cockerels from a line selected for high 8-wk body weight had smaller intestinal tracts relative to body weight at hatch than did a

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non-selected parent line. This difference disappeared after Day 8 posthatch. Cherry et ai. [17] reported that broiler chickens selected for high body weights tended to have smaller gastrointestinal tracts relative to body weight than those selected for low body weight or White Leghorns. Comparisons of the digestive tracts of wild turkeys and those of genetically selected modern turkeys give insight into the magnitude of the changes that result from modern genetic selection. Studies comparing the digestive tracts of wild and modern domestic turkey hatchlings demonstrate that wild turkeys have a longer (intestinal lengthbit body weight) and less dense (weight/unit length) intestinal tract than domestic lines of turkeys that had been selected for 16-wk body weight or 180-day egg production [18] (Figure 2). Additionally, the intestinal mucosa constitutes a smaller percentage of wet and dry intestinal weights of wild turkeys at hatch [19] (Figure 3). Similar values for intestinal mucosal percentages have been reported by Jackson and Diamond [20] for the wild Red Jungle Fowl (Gaiius gaiius). It is likely that these differences reflect an adaptation to domestication and genetic selection. Wdd turkeys need to maintain a longer intestinal tract in order to supply a template for quick upregulation of absorptive processes when nutrient supplies

are abundant; however, they cannot afford to maintain a large quantity of energetically expensive absorptive epithelium. In contrast, domestic turkeys can afford to develop a shorter, more dense intestinal tract with a higher percentage of absorptive mucosa because they are provided with a constant supply of nutrients. Similar findings were reported by Coles [21] in a comparison of wild turkeys with Hybrid and Egg line turkeys. Not only intestinal size but digestive enzyme activity has changed with genetic selection for production parameters. N u et ai. [16] reported that the total activity of pancreatic amylase and chymotrypsin were significantly increased in light-breed chicks as compared to heavy-breed chicks in response to overfeeding.They postulated that this could be a limiting factor in the ability of heavybreed chicks to digest excessive amounts of food. Nitsan et ai. [8] and N u et ai. [5] have suggested that secretion of digestive enzymes could be a limiting factor in food intake, digestion, and subsequent growth in broiler chicks. O'Sullivan et ai. [22] reported that turkey poults from lines selected for high 56-day body weights had higher pancreatic enzyme levels than lighter lines when compared at a common age. However, when comparisons were made at a c o m o n body weight (8025 g), these differences disappeared, suggesting that feed

Symposium Article 245

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LINE FIGURE 2. Intestinal density (weight of intestinal tissue/unit length of intestine) at hatching in wild turkeys and domestic turkeys selected for growth and egg production. Intestinal density of wild turkeys was significantly less (Pc.05) 1191.

intake was mediating these digestive enzyme levels. Pinchasov and Noy [23] found that turkey poults have a slightly limited capacity to digest starch during the first 2 to 4 days posthatch, but develop an adequate capacity thereafter. Similarly, Sell et ai. [24]found that 2-day-old poults have appreciable intestinal maltase- and isomaltase-specific activities. Coles [21] demonstrated that the wild turkey has higher disaccharidase-specific activities in the s m a l l intestine at hatch than Hybrid line turkeys.

These studies suggest that genetic selection has affected digestive and absorptive function, especially in newly hatched chicks or poults, and that these effects may have important implications for poultry production systems. As growth rate increases and market age decreases, the percentage of time the animal spends as a neonate increases. This places increased importance on early digestive and absorptive events that occur immediately posthatch. It also points toward the possible need for dietary interventionand management practices at an early age in order to ensure maximal performance.

THEIMPORTANCE OF THE ENERGETIC COSTS OF INTESTINAL ABSORPTION LINE

FIGURE 3. Intestinal absorptive mucosa as a percentage of total intestinal tissue weight (dry matter basis) at hatching in wild turkeys and domestic turkeys selected for growth and egg production. Mucosa percentage was significantly less (Pc .05) for wild turkeys [19].

The gastrointestinal tract can account for as much as 20% of the total energy needs of cattle [25]. Park [Z]reported that the gastrointestinal tracts of chickens can account for as much as 15-25% of whole bird energy requirements. A recent review by Cant et ai. [27, in which the energy requirements of the gastrointestinal tract were modeled, suggests that if an animal used any more than this to support gastrointestinal function, the overall

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utilization of energy for growth would be greatly decreased. Hence, it appears that this range is a biological constant for higher vertebrates. A detailed analysis of the energy requirements of intestinal tissues of 2-wk-old turkey poults reveals that 5 0 6 0 % of the intestinal tissue requirements are expended in the onecelled layer of absorptive mucosa [9]. Of the energy expended by the mucosa, 30% can be accounted for by the Na+/K+ ATPase, located on the basolateral membrane of the enterocytes. This enzyme maintains the Na+ gradient necessary for support of the intestinal transport of glucose, amino acids, and other nutrients [B]. Park [26] has reported a similar value for the percentage of energy used by the Na+/K+ ATPase in chicks. It is obvious from these figures that gastrointestinal function and nutrient absorption are important regardless of the energetic costs these processes impose upon the animal. Mitchell and Smith [29] were the first to associate a decrease in small intestine length, wet weight, and absorptive mucosal mass, resulting from genetic selection in chickens for enhanced growth, with increased overall energetic efficiency. They postulated that the decrease in intestinal absorptivemucosal mass resulted in more efficient functioning of the small intestine since the intestinal mucosa accounts for a major portion of the energy expenditure in the gut. Diamond [30]found a two-fold redundancy in the intestinal absorptive capacity for glucose and dietary glucose intake in the rat, rabbit, cat, chicken, and mouse. Obst and Diamond [31], however, speculated that the modern chicken may not have the intestinal glucose absorptive capacity to meet its metabolic needs (Figure 4).

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FIGURE 4. Comparison of glucose intake, glucose absorption, and basal metabolic rate (BMR) in Cornish-White Rock chickens from hatch to 11 wk of age [31.I

Jackson and Diamond [20] found that there was no redundancy in the ability of the Red Jungle Fowl to ingest glucose and its ability to absorb glucose. These authors have suggested that jungle fowl, because they evolved in an environment where nutrient availability was sporadic, cannot afford to maintain a constant high level of absorptive capacity. They speculated that in times of high nutrient availability, they are capable of quick upregulation of absorptive function in their intestinal tract. This is not the only biological model in which intestinal glucose absorption appears to be rate-limiting for postabsorptive processes. Weiss et al. [32] have recently demonstrated that both intestinal disaccharidaseactivity and intestinal glucose absorption are rate-limiting for lactation in the growing rat. In contrast, Nir et al. [12] found that chicks force-fed feed exceeding the amount consumed voluntarily, developed a remarkable capacity to digest and absorb food. Similarly, Jorgensen et al. [l3] concluded that genetic selection favoring broilers with efficient feed conversion ratio (FCR)inherently excludes birds eating more than their digestive capacity. Although Mitchell and Smith [29] alluded to changes in the "efficiency of absorption" due to genetic selection in chickens, it was Bird et al. [33] who first attempted to quantitatively define the efficiency of absorption in terms of energetic costs. These authors proposed a method of evaluating the energetic efficiency of glucose absorption in mice by constructing a scalar in which glucose uptake from the gut was expressed in comparison to total ATP expenditures by intestinal tissue (see review by Croom et al. [2] for a detailed discussion of this concept). This scalar was defined as the apparent energetic efficiency (APEE) of glucose absorption. This method has been used to demonstrate changes in glucose absorption associated with age and 331 as well as for a peptide enhancement [B, partially trisomic genotype [34]. This scalar has been used to describe the energetic efficiency of intestinal glucose absorption in mice [33,34,35,36]and turkey poults [lo]. Croom and his associates were the fitst to evaluate the APEE of glucose absorption in animals selected for enhanced growth, feed efficiency (mice and turkey poults), or body composition (mice). Fan et al. [lo] observed that turkey poults selected for enhanced

Symposium Article 247

CROOM et al. growth did not demonstrate any changes in the APEE of glucose transport (Figure 5). These findings pose an interesting paradox. Even though the poults selected for growth do not have an enhanced APEE for jejunal glucose uptake, the poults themselves have a better FCR and a greater body weight. Similar observations have been made in mice selected for growth [35l. Croom et al. [2] suggested two possible interpretations for these observations: 1) selection for increased efficiency of glucose absorption is concomitant with genetic selection for increased growth or feed efficiency; or 2) there is an uncoupling of genetic selection for the efficiency of growth and that of intestinal function. An enhancement of the energetic efficiency of glucose uptake or total glucose absorption should result in enhanced performance. These questions are exceedmgly complex and are not easily resolved. Fortunately, recent advances in the development of technologiesto increase intestinal absorption may allow resolution of these economically important questions.

tose and glycine absorption from the intestines. Although these initial studies were conducted in rats, subsequent studies have shown that EGF enhances glucose, galactose, proline, glutamine, and water uptake from the small and large intestines of mice, rabbits, and turkeys [38,39,40,41,42,43]. PYY is a member of the pancreatic polypeptide family of brain/gut peptides. It has a primary structure of 36 amino acids and is believed to be the primary humoral agent involved in the "ileal brake syndrome" as reviewed by Taylor [MI. This syndrome appears to be an intestinal regulatory mechanism by which the body corrects nutrient malabsorption. Administration of PYY has been reported to decrease not only pancreatic secretion but also gastric and intestinal motility. Bird et al. [28] were the first to report that PYY increases glucose absorption in mice injected subcutaneously with 300 pgkg of body weight for 3 days. Of special interest was the observation that the increase in glucose absorption associated with PYY administration was not accompanied by an increase in APEE of glucose uptake (Figure 6). This suggests that PYY administration can affect the rate and efficiency of glucose absorption and may increase the efficiency of metabolizable energy utilization. Especially intriguing are reports showing that gastrointestinal peptides can enhance intestinal nutrient absorption at hatching or birth when administered in ovo or in utero. Buchmilleret al. [45j reported that term rabbit fetuses administered E G F in utero via miniosmotic pumps had greater intestinal lactase and maltase activity as well as greater transport of glucose and proline. Similarly,

GASTROINTESTINAL PEPTIDE ENHANCEMENT OF NUTRIENT ABSORPTION Recent studies have demonstrated that the gastrointestinal peptides, epidermal growth factor (EGF), and peptide YY (PYY) enhance carbohydrate, amino acid, and fat absorptionfrom the intestinal tract (see review by Bird et al. [B]). Schwartz and Storozuk [37l were the first to demonstrate that either systemic or intraluminal injections of EGF, a gastrointestinal growth factor with a primary structure of 56 amino acids, enhances galac-

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FIGURE 5. Apparent energetic efficiency (APEE) of glucose uptake at 16 wk of age in a random bred control line (RBC2) and fast growth line (F) of turkeys [lo].

FIGURE 6. Apparent energetic efficiency (APEE) of glucose uptake in 2-month-old mice administered PW subcutaneouslyfor 3 days [28].

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Goetzman et al. [46] reported enhanced intestinal enzyme content and increased glucose and glutamine transport in premature, neonate simians administered EGF in utero via miniosmotic pumps. Peebles et al. [47, 481 have shown that enhancement in absorptive function by both EGF and PYY do not involve changes in yolk uptake from the yolk sac and stalk (Figure 7). Furthermore, they have noted that in ovo administration in broiler hatching eggs with PYY results in heavier hatchlings [41. Coles et al. [40] demonstrated that administration of EGF or PYY in ovo at Day 25 of incubation to Nicholas turkey eggs increased the rate of glucose absorption by poults at hatch by 200-250% (Figure 8). No intestinal tissue oxygen consumption measurements were reported in this study. Park [XI, however, found that jejunal enterocytes isolated from young and adult chickens significantly decreased O2 uptake after exposure to EGF in vitro. Additionally, the intracellular pH of

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enterocytes from adult buds was transiently reduced. Coles et al. [41] administered either physiological saline (control) or PYY to broiler eggs at Day 18 of incubation. Growth andFCR were determined at 7,21, and 42 days of age. Feed intake was recorded weekly. Broilers from FYY-treated eggs had greater growth and improved FCR during the first week posthatch (Figures 9 and 10). The authors speculated that the lack of effect on growth and FCR after Week 1 was due to the turnover of intestinal epithelial cells affected by PYY in ovo. Chick enterocytes turn over in approximately 48 hr [49].It is likely that the failure to observe an effect on growth and FCR after 7 days was related to the replacement of enterocytesaffected by PYYwith newlydifferentiated enterocytes not having enhanced insertion of SGLTl transporters from the intracellular pool into the luminal membrane. Consequently, PYY may have to be administered after hatching to ensure continuation of increases in growth and improved feed efficiency. Coles et al. [50] have recently tested the effects of combining in ovo and posthatch administration of PYY to broiler eggs and chicks on posthatch growth and FCR. The FCR for Weeks 2 to 3 improved for PYY-treated birds and average weight of PYY-treated birds exceeded that of controls by Week 6 [so]. Recently,K o h e t al. [51] reported that in ovo administration of recombinant human insulin-like growth factor-1 to broiler chicken eggs during the fust 4 days of incubation resulted in dramatic changes in growth and FCR as the result of increased posthatch skeletal muscle growth. It is interesting to note that Gdlermo et al. [52] found increases in PYY gene expression to be associated with increases in growth hormone and insulin-like growth factor-1in growth-hormonetransgenic mice. Similarly, Bird et al. [53]found that repeated exogenous administration of recombinant bovine somatotropin to sheep increased the rate of glucose and proline absorption from the duodenum. The increases in growth and FCR observed by K o c d s et al. [51] may thus be due in part to a secondary effect of increased endogenous PYY on the intestines of the embryo and chick.

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hypothesis that intensive genetic selection ABSORPTION for growth in poultry has "uncoupled intestinal ENHANCEMENT IN POULTRY: nutrient delivery from increased postabsorption nutrient demand. This may have HYPEOR HELP? resulted from alterations in genetic correla-

To date, the case for intestinal nutrient absorption being rate-limiting in poultry production is based on limited, direct experimentation using intestinal absorption - enhancing peptides and a large body of data suggesting that intestinal structure and function of modern meat-type poultry may not be adequate for maximum growth rate. However, when taken as a whole, these studies support the

tions between intestinal absorption and postabsorptive synthetic process. The lack of correlation may apply not only to the rate and amount of nutrients absorbed from the digestive tract but also to the energetic cost of nutrient absorption. This is especially true of the production data presented above, which suggests that the concept may have sound practical merit.

CONCLUSIONS AND APPLICATIONS 1. Like any new technology, the application of absorption enhancement to practical production systems cannot be implemented until a number of key variables associated with its use can be more clearlydefined. These include the influence of genotype, age, and physiological state on the dose and time of administration for maximizing intestinal absorption. 2. Additionally, the dose-response characteristics and duration of action of proabsorptive agents such as PYY need to be more fully understood, and the cost vs. return must be evaluated. 3. The understanding of variables such as these will help production specialists define if and when absorption enhancement will be beneficial.

REFERENCES AND NOTES 1. Croom, WJ., Jr. kR Bird, B.L Black, and B.W. McBridc, 1993.Mani ulation of gastrointestinal nutrient delivery in livestock. Dairy Sci. 762112-2124.

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and some enzymes in broiler chicks after hatching. Br. Poultry Sci. 32515-523.

2. Croom, WJ., Jr., B. McBride, kR Bird, Y.K. Fan, J. W e , M. Fmetschel, and 1.L Taylor,1998. Regulation of intestinal glucose absorption: A new issue in animal science. Canadian J. h i m . Sci. 78:l-13.

9. Fan, Y.K., J. Croom, V.L Christensen, B.L Black, AR Bird, LR Daniel, B.W. McBride, and El. Eken, 1997. Jejunal glucose u take and oxygen consumption in turke poults selecte%for rapid growth. Poultry Sci. 76:l A 1 7 4 5

3. Kalanbaf,M.N., EA Dumington, and P.B. Siegd, 1988.Allomorphic rela tionships from hatching to 56 d in oarental lines and Pi crosses of chickens selected% ge;erations for high 0; low body weight. Growth Dev. Aging 52:ll-22.

lO.Fan,Y.K.,WJ.Croom,Jr.,V.LCMstensen,kR Bird, LR Daniel, B.W. McBride, and EJ.Eisen, 1998. A rent energetic efficiencyof glucose uptake in youn a a turke selected for rapid growth. Canadian Anim. %i. Z301-306.

La4

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11. Dror, Y., I. Nir,and 2 Nitsan, 1977. The relative h of internal organs in light and heavy breeds. Br. oultry Sci. 18493-496.

4. C., 1981. Postnatal gmwth and or n developGrowth 4 E 2 W 4 1 . ment in the goose (-&.

r

5. Nir, I., Z. Nitsan, and M. Mahpgruq 1993.Comparative growth and development of the digestive organs and of some enzymes in broiler and egg type chicks after hatching. Br. Poultry Sci. 3452S532.

12. Nir, I,N. Shapira, Z Nitsan, and Y. Dror, 1974. Force-feeding effects on growth, carcass,and blood composition in the young chick. Br. J. Nutr. 32229-239.

6. Sell, J.L,CR Angel, FJ. Piquer, EG. MPUrarino, and H A AI-Batshan, 1991. Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poultry Sci. 701200-1205.

7. Krogdahl, k and J.LSell, 1989. Influences of age on lipase, amylase, and protease activities in pancreatic tissue and intestinal contents of young turkeys. Poultry Sci. 68:1561-1S68. 8. Nitsan, Z., G. Ben-Avisham, Z. %ref, and I. Nir, 1991. Growth and development of the digestive organs

13. Jorgensen, H., P. Sorensen, and B.O. Eggurn, 1990. Protein and energy metabolism in broiler chickens selected for either b weight gain or feed efficiency. Br. Poultry Sci. 3151324. . 14. L.ilja, C., 1983. A comparative study of postnatal n development in some species of birds.

15.Pinchnsov, Y.,I. Nk,and Z. Nitsan, 1985. Metabolic and anatomical a& tations of heavy bodied chicks to intermittent feeding. I.kood intake, growth rate, organ weight, and body composition. Poultry Sci. M2098-2109.

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CROOM et al. 16. Nir, I., Z. Nitspn, Y. Dror, and N. Shapira, 1978. Influence of overfeeding on growth, obesity, and intestinal tract in young chicks of light and heavy breeds. Br. J. Nutr. 3927-35.

33. Bird, A.R, WJ. Croom, Jr.,Y.K. Fan, LR Daniel, B.L Black, B.W. McBride, EJ.Eisen,LS. Bull, and 1.L Taylor, 1994. Jejunal glucose abso tion is enhanced by epidermal growth factor in mice. J.%utr. 1x231-240.

17. Cherry, J.A., I. Nir, D.E Jones, EA. Dnmhgton, Z. Nitsan, and P.B. Siegel, 1987. Growth associated traits

34. Cefalu, J.A., WJ. Croom, Jr., EJ. Eisen, EE Jones, and LR Daniel, 1998. Jejunal function and plasma amino and concentrations in the segmental trisomic Ts65Dn mouse. Growth, Aging, and Dev. 6247-59.

in parental and Fi populationsof chickensunder different feeding. Poultry Sci. feeding programs. 2. Bd 66:l-9. 18. Nestor, K.E, D.O. Noble, NJ. Zhu, a n d Y. Moritsu, 1996. Direct and correlated responses to long term selection for increased bodyweight and egg production in turkey. Poultry Sci. 75118&1191. 19. WJ. Croom, 1999. Unpublished observations. 20. Jackson, S. and J. Diamond, 1995. Ontogenetic development of t function growth and metabolism in a wild bird, t h e % ed Jungle Fowl. Amer. J. Physiol. 269R116sR1173. 21. Coles, B.A., 1994.A comparativestudyof intestinal development in domestic and wild turkey lines. M.S. Thesis, North Carolina State University, Raleigh, N C 22. O'SuIlivan, N.P., EA. Dnnninglon, AS. Larsen, and P.B. Siegel, 1992. Correlated responses m lines of chickens divergentlyselected for fifty-suc day body weight. 3. Digestive enzymes. Poultry Sci. 71:610-617. 23. Pinchasov, Y. and Y. Noy, 1994. Early postnatal am= the gastrointestinal tract of turkey poults gallODavo. Comp. Biochem. Physiol. 107A:221-226. 24. Sell, J.L, 0. KoldovsLy, and B.L Reid, 1989. Intestinal disaccharidases of young turkeys: Temporal development and influence of diet composition. Poultry Sci. 68265-2n.

25. McBridc, B.W. and J.M. Kelly, 1990. Energy ccst of absorption and metabolism in the ruminant gastrointestinal tract and liver: A review. J. h i m . Sci. 68:29973010.

35. Fan, Y.L, WJ. Croom, Jr., LR Daniel, A.R Bird,

EL Black, EJ. Eisen,and B.W. McBride, 19%. Selection for growth does not affect apparent energetic efficiency of jejunal glucose uptake in mice. J. Nutr. 1262851-2860.

36.Fan,Y.K., WJ. Croom, Jr., LR Daniel, A.R Bird, B.L Black, EJ. Elsen,and B.W. McBride, 1996. Selection for body composition does not affect energetic efficiency of jejunal glucose uptake in mice. J. Nutr. 1262861-2866. 37. S c h w e M.2 and RB. Storozuk, 1988. Influence of epidermal growth factor on intestinal function in the rat: Comparison of system infusion versus luminal perfusion. Am. J. Surg. 15518-22.

38. Opleta-Madsen, IC, J. Hardin, and D.G. Gall, 1991. Epidermal growth factor upregulates intestinal electrolyte and nutrient transport. Amer. J. Physiol. 260: G807. 39. Opleta-MaaSen, K., J. Hardio, and D.G. Gall, 1991. E idermal growth factor and postnatal development or intestinal transport and membrane structure. Pediatric Res. 30342. 40. Coles, B.A., J. Croom, L.R. Daniel, V.L. Christensen, and J. Brake, 1997. In peptide YY (PYY) administration improves feed conversion ratios in week-old broiler chickens. Poultry Sci. 76(Suppl):71.

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41. Coles, B.A., WJ. C m m , Jr., LR Daniel, V.L. Chrisftmen, J. Brake, C.P. Phelps, A. Gore, and 1.L Taylor, 1998. In pyp peptide YY (PYY) administration improves p w t h and feed conversion ratios in week-old broiler chicks. Poultry Sci. (in press). 42. Oka, Y., F.K. Ghishan, H.L Greene, and D.N.

26. Park, H., 1993. Nutritional and physiological regulation Na+, K+, ATPase in the avian gastrointestinal tract. Ph.D. Thesis, University of Guelph, Guelph, ON, Canada.

trone on the functional maturation of rat intestine. Z'Erinology 1 1 2 : ~ ~ .

27. Cant, J.P., B.W. McBride, and WJ. Croom, Jr., 1996. The regulation of intestinal metabolism and its im act on whole animal energetics.J. Anim. Sci. 74:25412533.

43. Bruns, D.E, A.V. Krishnan, D. Feldman, RW. Gray, S.Christakos, G.N. Hlrscb, and M.E Bruns, 1989. E p i d e r m a p h factor ,increases intestinal callindinDgt and 1, dihydmtamm D receptors in neonatal rats. Endocrinology 125:438-485.

28. Bird, A R , WJ. Croom, Jr., Y.K. Fan, B.L Black, B.W. McBride, and 1.L Taylor, 1996. Peptide re of intestinal glucose absorption. J. Anim. Sci. 2540.

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29. Mitchell, M.A. and MW. Smith, 1991. The effects of genetic selection for increased growth on mucosal and muscle weights in the different regions of the small intestine of the domestic fowl domestlcus). Comp. Biochem. Physiol. 99k2.51-258.

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30. Diamond, J., 1991.Evolutionary design of intestinal nutrient abso tion Enough but not too much. News Physiol. Sci. 6 9 2 3 6 . .

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ACKNOWLEDGEMENT The assistance of Ms. Jackie Seale in reparation of this manuscript is gratefully acknmledgedq