Comparative Development of the Small Intestine in the Turkey Poult and Pekin Duckling 1
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1 Comparative Development of the Small Intestine in the Turkey Poult and Pekin Duckling 1 T. J. Applegate,*,2 D. M. Karcher,* and M. S. Lilburn *Department of Animal Sciences Purdue University, West Lafayette, Indiana 47907; and Department of Animal Sciences, The Ohio State University, Wooster, Ohio ABSTRACT Turkey poults and Pekin ducklings hatch from eggs of similar weights and have the same incubation periods and body weights at hatch. The male Pekin duckling, however, can attain a market weight of 3.2 kg in approximately 6 wk, whereas at the same age, male turkeys only weigh approximately 2.1 kg. For this study, fertile turkey eggs (n = 400, mean weight: 87.2 g, range: 85 to 89.9 g) and Pekin duck eggs (n = 565, mean weight: 88.6 g, range: 85 to 92.0 g) were weighed and incubated. Embryos and hatchlings were sampled during the last week of incubation, at hatch, and through 7 d of age. Yolk-free BW of poults were 2.7 g heavier than ducklings at hatch. Yolk-free BW of ducklings, however, were INTRODUCTION Turkey poults and Pekin ducklings have similar incubation periods and hatch from eggs of similar weights with similar body weights at hatch. The commercial male Pekin duckling, however, can attain a market weight of 3.2 kg in 6 wk or less (Applegate et al., 1999c), whereas the male turkey will only weigh 2.3 kg at 6 wk of age (Ferket, 2003). Even though the small intestine in poults undergoes considerable development during incubation, it is still functionally immature at hatch in terms of digestive and absorptive capabilities (Sell et al., 1991). Although there has been little reported on intestinal development of ducklings during embryonic development, the small intestine exhibits accelerated growth relative to the whole body posthatch (Baranyiova et al., 1983; Gille et al., 1999). Functional maturation of the small intestine involves morphological and physiological changes and is a major con Poultry Science Association, Inc. Received for publication August 27, Accepted for publication November 5, Purdue University Agricultural Research Program Journal Article no To whom correspondence should be addressed: applegt@ purdue.edu. (Key words: duck, poult, small intestine, villus) greater than poults at 1 d of age (P 0.06), and by 7 d of age ducklings were 140 g heavier (P 0.01). Yolk sac weight was similar at 21 and 25 d of incubation, yet was significantly lower in ducks at hatch, 1, and 2 d of age (P 0.05). In the duckling, jejunum and ileum weights (3.7 heavier), length (1.6 longer), and density (g/cm; 2.3 more dense) were consistently heavier than in the turkey from hatch through 7 d (P 0.01). Histological sections of the distal jejunum revealed more rapid villus growth in the duck from 0 to 3 d of age. The combination of increased intestinal growth (weight and length) and maturation (villus length) allowed ducks to achieve an additional 143 g of BW gain during the critical hatch through 7dofgrowth Poultry Science 84: straint to optimal early growth in many avian species (Konarzewski et al., 1989). Physiological maturation (i.e., digestive and absorptive functionality) of the digestive tract occurs largely through increased production of pancreatic and intestinal mucosal enzymes (Nitsan et al., 1991a,b; Sell et al., 1991) and changes in nutrient transporters (Holdsworth and Hastings-Wilson, 1967; Shehata et al., 1984; Obst and Diamond, 1992). The physical development of the gastrointestinal tract (i.e., the increase in surface area of the small intestine), however, may be a more limiting influence on early growth (Nitsan et al., 1991a; Sell et al., 1991). Early posthatch growth of ducklings far exceeds that of turkey poults even though egg weight, length of the incubation period, and BW at hatching are similar. Comparisons of intestinal growth and development between species might provide some insight into the physiological factors underlying the differences in posthatch growth. It was hypothesized that anatomical development of the small intestine is more rapid in the Pekin ducklings than in the turkey poult, thus allowing for enhanced nutrient use and increased growth during the first week after hatching. Results previously published by Applegate and Lilburn on the turkey poult (1999a,b) and Applegate et al. (1999c) on the duckling are reported in this paper and were used to evaluate the stated hypothesis. 426
2 DUCK AND TURKEY INTESTINAL DEVELOPMENT 427 TABLE 1. Duck and turkey egg weight and egg component comparisons Egg 1 Yolk 2 Albumen Species (g) (g) (%) (g) (%) Duck ± ± ± ± ± 0.56 Turkey ± ± ± ± ± 0.64 Effect of species Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 565; turkey: 85- to 90-g eggs from 34- and 44-wkold hens, n = 400 (±SEM). 2 Duck yolk and albumen means represent 25 eggs; turkey yolk and albumen means represent 10 eggs (±SEM). MATERIALS AND METHODS Fertile commercial turkey eggs (n = 400, average weight = 87.2 g) from 34- and 44-wk-old hens and Pekin duck eggs (n = 565, average weight = 88.6 g) from 32- and 44-wk-old hens were collected and incubated separately. The embryos or hatchlings from each species (n = 5 from each hen age) were sampled on the following days relative to hatching: 7, 3, 0 (hatch), 1, 2, 3, 5, and 7 for determination of the residual yolk sac weight and yolkfree BW. A practical corn-soybean meal based diet that met or exceeded NRC (1994) nutrient recommendations for each species was fed during the posthatch period. Birds were housed in electrically heated brooder cages and had ad libitum access to feed and water. At 0, 1, 2, 3,5,and7dofage, the small intestine was excised beginning at the proximal end of the duodenum and extending to the ileocecal junction. The duodenal loop and lower small intestine (jejunum and ileum) were separated, flushed with 0.9% saline, blotted dry, and weighed. The length of each segment was also recorded. At 0, 1, and 3 d of age, a 2-cm portion of the distal jejunum (proximal to Meckel s diverticulum) was excised from each respective species (duckling and poult, n = 10), flushed with 0.9% saline, and fixed in 10% neutral buffered formalin. A 0.5- mm section was then processed and embedded in Polyfin paraffin. 3 Paraffin sections (5 or 6 µm) were subsequently stained with hematoxylin and eosin. The villus measurements from the distal jejunum sections (n = 10 per species/d) were made from images obtained from an Olympus IX70 inverted microscope, 4 processed with a Vay Tek deconvolution imaging system. 5 The actual measurements were made using Image- Pro Plus software. 6 Villus height (villus tip to crypt junction) and crypt depth (depth of the invagination between adjacent villi) were determined on 20 villi per bird. As the age-by-species interaction was significant (P 0.05) for all characteristics measured (except yolk sac weight), the statistical analysis of the differences between species within each sampling day was determined by ANOVA. 7 3 Polysciences Inc., Warrington, PA. 4 Olympus America Inc., Melville, NY. 5 Vay Tek, Fairfield, IA. 6 Media Cybernetics, Inc., Silver Spring, MD. 7 SAS Institute, Cary, NC. All procedures and protocols were approved by Purdue University and the Ohio State University Animal Care and Use Committees. RESULTS Duck and turkey egg weights were very similar, but the actual egg components varied with the turkeys having a smaller yolk and more albumen than the ducks (Table 1). The probability of species differences was highly significant for yolk weight (P = ) and for albumen weight (P = 0.03). Yolk-free BW of poults were 2.7 g heavier than ducklings at hatch, but this was reversed at 1 d of age when the mean yolk-free BW of ducklings was 3.4 g greater than that of poults (P < 0.05, Table 2). This difference became progressively greater through the first week posthatch, and at 7 d ducklings were 140 g heavier (P = 0.01). Yolk sac weight was similar at 21 and 25 d of incubation, yet was significantly less in ducklings at 0, 1, and2dofage(p < 0.05, Table 3). Species comparisons of duodenum length, weight, and density are presented in Figure 1. The differences in duodenal weight were significant (P < 0.05) only at 0, 2, and 7 d of age with poults having a heavier duodenum at 0 and 2 d. Although the duodenum of a duckling weighs less for the first 2 d of age, the duodenum weights of ducklings quickly surpass the duodenal weights of the poults by 7 d of age (P < 0.05). The duodenum length was consistently greater in ducklings from 0 through 7 d of age (P < 0.05). The poults consistently had a higher duodenum density throughout the first week (P < 0.05) when compared with the ducklings. The duodenal weights of ducklings and poults were also compared on a relative basis. The poults were significantly different from the ducklings from 0 through7dofage(p < , Table 4) except for 1 d of age. In the duckling, jejunum and ileum weight, length, and density were consistently heavier than the poult from 0 through 7 d of age (P < 0.05, Figure 2) when the lower small intestine of the duckling was 3.7 heavier, 1.6 longer, and 2.3 more dense (g/cm). The jejunum-ileum weights when compared relative to BW showed the ducklings had heavier jejunum-ileums from 0 to 7 d of age (P < , Table 5). Histological sections of the distal jejunum (Table 6) revealed that the ducklings had significantly longer villi
3 428 APPLEGATE ET AL. TABLE 2. Duckling and poult BW (devoid of the yolk sac) comparisons 1 Species Duck 35.2 ± ± ± ± ± ± ± ± 3.8 Turkey 30.6 ± ± ± ± ± ± ± ± 6.0 (g) Effect of species Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85 to 90 g eggs from 34- and 44-wk-old hens, n=10(±sem). TABLE 3. Duckling and poult yolk sac weight comparisons 1 Species Duck ± ± ± ± ± Turkey ± ± ± ± ± ± 0.09 (g) Effect of species Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85- to 90-g eggs from 34- and 44-wk-old hens, n=10(±sem). 2 Duckling yolk sac weight was negligible. TABLE 4. Duckling and poult relative duodenum weight comparisons 1 Species (g/100 g of BW) Duck 0.66 ± ± ± ± ± ± 0.04 Turkey 0.79 ± ± ± ± ± ± 0.06 Effect of species Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85- to 90-g eggs from 34- and 44-wk-old hens, n=10(±sem). and deeper crypts (P < ) although there was no significant difference in yolk-free BW at hatch. By 3 d relative to hatch, the duckling had longer villi height and deeper crypts. Therefore, ducklings have more rapid villus growth from 0 to 3 d of age. The large differences in villus height and crypt depth is shown in Figure 3. DISCUSSION As a turkey or duck hen ages, the composition of eggs changes with an increase in yolk size and a decrease in the amount of albumen (Applegate and Lilburn, 1996, 1998a,b; Applegate et al., 1998). Within these reports, Applegate and Lilburn noted an appreciably greater transfer of dry matter and lipid out of the yolk sac, resulting in heavier BW at hatching, independent of changes in egg weight. Even if BW differences are not measurable among hatchlings from different ages of hens, they may still have a reduced capacity for metabolic homeostasis (Applegate and Lilburn, 1999a; Applegate et al., 1999). After hatching, structural growth of the small intestine, however, cannot be directly attributed to age of the hen alone (Applegate and Lilburn, 1999a,b; Applegate et al., 1999). The comparison between species reported herein contained data from studies with turkeys that were in their 2nd (prepeak egg production) and 11th weeks of production (34 and 44 wk of age) vs. those from studies with ducks that were in their 6th (prepeak egg production) and 18th weeks of production (32 and 44 wk of age). The commercial Pekin duck provides for a unique subject for studying the effects of hen production age on embryonic and hatchling growth because egg weight can be maintained within a given range with a quantitative feed restriction. Quantitative feed restriction prevents the laying of excessively large eggs and enhances the hatching uniformity of a flock. The turkey eggs used in this study were preselected from a larger population of eggs to obtain those within given egg size ranges. Holub et al. (1994) stated that duck eggs have more gross energy per gram of egg mass prior to incubation than chickens and can more efficiently transfer that gross energy to the embryo during incubation. Within the current studies, the duck eggs contained 4.1% more yolk
4 DUCK AND TURKEY INTESTINAL DEVELOPMENT 429 FIGURE 1. Duckling (line) and poult (dashed line) duodenum weight, length, and density (g/cm) comparisons. Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85- to 90-g eggs from 34- and 44-wk-old hens, n = 10. *Difference between species is significant (P 0.05). Error bars indicate standard error of the mean. (32.10 vs %), thereby suggesting the same statement could be made relative to the duck containing more gross energy than that of the turkey. Yolk sac weights, however, were not different at 21 or 25 d of incubation but were lighter in ducklings beginning on the day of hatch. This result is contrary to the findings of Knizetova et al. (1988), who reported that the proportion of yolk sac (3 to 7%) of BW at hatching is higher in the duckling than that of the poult. The report by Knizetova et al. (1988), however, FIGURE 2. Duckling (line) and poult (dashed line) jejunum-ileum weight, length, and density (g/cm) comparisons. Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85- to 90-g eggs from 34- and 44-wk-old hens, n = 10. *Difference between species is significant (P 0.05). Error bars indicate standard error of the mean. used 75- and 95-g eggs in comparisons with previously published literature in contrast to the 85- to 92-g eggs in the current study. Any differences in residual yolk sac weights on the day of hatch in the current study would be a result of use of the yolk and were reflected in differences in yolk-free BW. By 3 d of age, the ducklings drastically increased their yolk-free BW (120% increase from 0 d of age), whereas poults only had a marginal increase (36% increase from 0 d of age). TABLE 5. Duckling and poult relative jejunum-ileum weight comparisons 1 Species (g/100 g of BW) Duck 2.62 ± ± ± ± ± ± 0.07 Turkey 1.56 ± ± ± ± ± ± 0.11 Effect of species Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; Turkey: 85 to 90 g eggs from 34- and 44-wkold hens, n = 10(±SEM).
5 430 APPLEGATE ET AL. TABLE 6. Duckling and poult distal jejunum villus height (villus tip to crypt), and crypt depth (depth of the invagination between adjacent villi) comparisons 1 Variable and species Villus height Duck ± ± ± 12.0 Turkey ± ± ± 16.2 of species effect Crypt depth Duck 55.9 ± ± ± 2.6 Turkey 26.5 ± ± ± 1.8 of species effect Duck: 85- to 92-g eggs from 32- and 44-wk-old hens, n = 25; turkey: 85- to 90-g eggs from 34- and 48-wkold hens, n = 10(±SEM). (µm) The accelerated growth of the gastrointestinal tract of poultry following hatching indicates organs and tissues that fulfill a supply function for achieving early body development is of great importance to meet the energetic demands of a body but also limits the body size that can be reached at that point in time (Mitchell and Smith, 1991; Sell et al., 1991; Starck, 1998). Uni et al. (1995) stated the increased volume of villi with age is greater in the jejunum and ileum than in the duodenum. Applegate et al. (1999) supported this statement by indicating the villi in poults from older hens may be more developmentally advanced in poults at hatch, but posthatch growth of the intestine is not affected by hen age. In this experiment, major differences were observed between the 2 species for weight, length, and density of the duodenum and jejunum-ileum. Although ducklings surpassed poults in all 3 of these aspects for the jejunumileum, ducklings never surpassed the poults in duodenum density but did in duodenum length and, finally, by 7 d of age in duodenum weight. The possible effect of egg size was removed by making comparisons of the duodenum and jejunum-ileum weights relative to BW. On a relative basis, ducklings never surpassed poults in duodenal weight but easily surpassed poults in weight of the jejunum-ileum. Therefore, ducklings may have increased length of villi and accelerated growth of those villi within the jejunum-ileum. Starck (1998) tentatively concluded that the growth of the gastrointestinal tract is determined by the number of intestinal crypts and the size of absorptive surface (villi). The observed massive differences in villus height and crypt depth between the ducklings and poults may explain the differences observed in yolk sac weight and yolk-free BW. In the distal jejunum, ducklings had approximately 5 deeper crypts and 2.4 higher villi as compared with poults. Katanbaf et al. (1988) implied the accelerated growth of the gastrointestinal tract after hatching served the function of a supply organ. Others have asserted that rapid intestinal growth is a prerequisite for sustained body growth rates in ducklings (King et al., 2000) and other bird species (Lilja, 1983). Body size and growth rate at any point during development are determined by organ structures and functions (Mitchell and Smith, 1991). Therefore, the overall development of the animal can be greatly enhanced or delayed depending on the development and amount of energy placed into supply organs within the first few days of growth. Presumably, the great differences observed in intestinal development allow ducklings to gain an additional 143 g of BW during this 7- d period of physiological and metabolic transitions. Other plausible mechanisms contributing to these dramatic differences in growth, however, should not be overlooked, including: diet consumption capacity, digestive enzyme capacity, and nutrient transporter numbers. In summary, there are no differences observed between the species in yolk-free BW at hatch, yet there is a drastic change in yolk-free BW, resulting in heavier ducklings compared with poults by 3 d of age. Thus, the small intestine of a Pekin duckling develops more rapidly after hatching (concomitant with large differences in BW) as compared with the small intestine of a turkey poult. Much of this difference was reflected in the weight, length, and villus height measurements of the jejunum and ileum. FIGURE 3. Duckling and poult distal jejunum villi comparison at 3 d of age. Sections were 5 µm thick and were stained with hematoxylin and eosin. Magnification = 100.
6 DUCK AND TURKEY INTESTINAL DEVELOPMENT 431 ACKNOWLEDGMENTS The authors thank Maple Leaf Farms (Milford, IN) and Cooper Farms (Ft. Recovery, OH) for their generous donations of fertile eggs used in these experiments. REFERENCES Applegate, T. J., and M. S. Lilburn Independent effects of hen age and egg size on incubation and poult characteristics in commercial turkeys. Poult. Sci. 75: Applegate, T. J., and M. S. Lilburn. 1998a. Effect of hen age, body weight, and age of photostimulation. 1. Egg, incubation, and poult characteristics of commercial turkeys. Poult. Sci. 77: Applegate, T. J., and M. S. Lilburn. 1998b. Effect of hen age, body weight, and age of photostimulation. 2. Embryonic characteristics of commercial turkeys. Poult. Sci. 77: Applegate, T. J., D. Harper, and M. S. Lilburn Effect of hen production age on egg composition and embryo development in commercial Pekin ducks. Poult. Sci. 77: Applegate, T. J., and M. S. Lilburn. 1999a. Effect of turkey (Meleagridis gallopavo) breeder hen age and egg size on poult development. 1. Intestinal growth and glucose tolerance of the turkey poult. Comp. Biochem. Physiol. 124B: Applegate, T. J., and M. S. Lilburn. 1999b. Effect of turkey (Meleagridis gallopavo) breeder hen age and egg size on poult development. 2. Intestinal villus growth, enterocyte migration and proliferation of the turkey poult. Comp. Biochem. Physiol. 124: Applegate, T. J., E. Ladwig, L. Weissert, and M. S. Lilburn Effect of hen age on intestinal development and glucose tolerance of the Pekin duckling. Poult. Sci. 78: Baranyiova, E., A. Holub, and E. Ponizilova Changes in the mass and chemical composition of the gastrointestinal tract and liver of ducks in the first two months after hatching. Acta Vet. Brunensis 52: Ferket, P.R Growth of toms improves substantially. Watt Poult. USA (7): Gille, U., F.-V. Salomon, and J. Ronnert Growth of the digestive organs in ducks with considerations on their growth in birds in general. Br. Poult. Sci. 40: Holub, A., E. Ponizilova, and E. Baranyiova Energy losses in fowl and duck eggs during incubation. Acta Vet. Brunensis 63: Holdsworth, C. D., and T. Hastings-Wilson Development of active sugar and amino acid transport in the yolk sac and intestine of the chicken. Am. J. Physiol. 212: Katanbaf, M. N., E. A. Dunnington, and P. B. Siegel Allomorphic relationships from hatching to 56 days in parental lines and F1 crosses of chickens selected 27 generations for high or low body weight. Growth Dev. Aging. 52: King, D. E., E. K. Asem, and O. Adeola Ontogenetic development of intestinal digestive functions in white Pekin ducks. J. Nutr. 130: Knizetova, H., B. Knize, and J. Cerveny Size of yolk sac in waterfowl and changes during 24 hours after hatching. Pages in Waterfowl Production: Proceedings of the International Symposium on Waterfowl Production, the Satellite Conference for the XVIII World s Poultry Congress. International Academic Publishers, New York. Konarzewski, M., J. Kozlowski, and M. Ziolko Optimal allocation of energy to growth of the alimentary tract in birds. Funct. Ecol. 3: Lilja, C A comparative study of postnatal growth and organ development in some species of birds. Growth 47: Mitchell, M. A., and M. W. Smith The effects of genetic selection for increased growth rate on mucosal and muscle weights in the different regions of the small intestine of the domestic fowl (Gallus domesticus). Comp. Biochem. Physiol. 99: National Research Council Nutrient Requirements for Poultry. 9th. rev. ed. National Academy Press, Washington, DC. Nitsan, Z., G. Ben-Avraham, Z. Zoref, and I. Nir. 1991a. Growth and development of the digestive organs and some enzymes in broiler chicks after hatching. Br. Poult. Sci. 32: Nitsan, Z., E. A. Dunnington, and P. B. Seigel. 1991b. Organ growth and digestive enzyme levels to fifteen days of age in lines of chickens differing in body weight. Poult. Sci. 70: Obst, B. S., and J. Diamond Ontogenesis of intestinal nutrient transporters in domestic chickens (Gallus gallus) and its relation to growth. Auk 109: Sell, J. L., C. R. Angel, F. J. Piquer, E. G. Mallarino, and H. A. Al-Batshan Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poult. Sci. 70: Shehata, A. T., J. Lerner, and D. S. Miller Development of nutrient transporter systems in chick jejunum. Am. J. Physiol. 246:G101 G107. Starck, J. M Structural variants and invariants in avian embryonic and postnatal development. Pages in Avian Growth and Development: Evolution Within the Altricial- Precocial Spectrum. J. M. Starck and R. E. Ricklefs, ed. Oxford, New York. Uni, Z., Y. Noy, and D. Sklan Posthatch changes in morphology and function of the small intestines in heavy- and light-strain chicks. Poult. Sci. 74:
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