Changes in Form and Function of the Gastrointestinal Tract During Starvation: From Pythons to Rats

  • Jehan-Hervé Lignot


During episodes of food deprivation, animals enhance survival by minimising energy costs incurred by the metabolically demanding maintenance and activity of their digestive system. The response occurs at physiological, biochemical and molecular levels and mainly concerns the intestinal wall. After a feeding episode, this response leads to a rapid decrease in gut length and mass, as well as enzyme activities, protein synthesis and the expression of many proteolytic-related genes. Intestinal atrophy affects the mucosa, and induces a general decrease in its surface area through the diminishing of the mucosal area (shortening of the intestinal folds), changes in the microvilli surface area and by reducing both the size (hypotrophy) and number of cells along the intestinal barrier (hypoplasia). In most of the species studied, these morphological responses are time dependent and do not alter nutrient transport capacity, at least at the beginning of the fasting period. Fasting is usually anticipated in hibernating mammals, migratory vertebrates and infrequent feeders such as pythons. When preparing itself for fasting, the digestive system mainly uses tools such as hyperphagia, intracellular recycling and the production of new cells that are downregulated at the end of the postprandial period. As food deprivation continues starving animals may respond differently. This has been illustrated in rats that had reached a proteolytic phase during which energy requirements were mostly derived from increased protein utilisation. In these animals, cell proliferation and cell migration were seen to increase while apoptosis at the tip of the intestinal villi ceased. This has been considered as an optimising process that may also exist in other species.


Brush Border Brush Border Membrane Intestinal Villus Postprandial Period Prolonged Fasting 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aldewachi HS, Wright NA, Appleton DR, Watson AJ (1975) The effect of starvation and refeeding on cell population kinetics in the rat small bowel mucosa. J Anat 119:105–121PubMedGoogle Scholar
  2. Altmann GG (1972) Influence of starvation and refeeding on mucosal size and epithelial renewal in the rat small intestine. Am J Anat 133:391–400PubMedGoogle Scholar
  3. Battley PF, Piersma T, Dietz MW, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc Biol Sci 267(1439):191–195PubMedGoogle Scholar
  4. Bauchinger U (2002) Phenotypic flexibility of organs during long-distance migration in garden warblers (Sylvia borin): implications for migratory and reproductive periods. PhD Thesis, Technische Universität München, München 166 pGoogle Scholar
  5. Bozinovic F (1993) Nutritional ecophysiology of the Andean mouse Abrothrix andinus: energy requirements, food quality and turnover time. Comp Biochem Physiol 104(3):601–604Google Scholar
  6. Brown HO, Levine ML, Lipkin M (1963) Inhibition of intestinal epithelial cell renewal and migration induced by starvation. Am J Physiol 205(5):868–872PubMedGoogle Scholar
  7. Cant JP, McBride BW, Croom WJ (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Am Soc 74:2541–2553Google Scholar
  8. Challet E, Le Maho Y, Robin JP, Malan A, Cherel Y (1995) Involvement of corticosterone in the fasting-induced rise in protein utilization and locomotor activity. Pharmacol Biochem Behav 50:405–412PubMedGoogle Scholar
  9. Christel CM, Secor SM, DeNardo DF (2007) Metabolic and digestive response to food ingestion in a binge-feeding lizard, the Gila monster (Heloderma suspectum). J Exp Biol 210:3430–3439PubMedGoogle Scholar
  10. Clarke R (1975) The time-course of changes in mucosal architecture and epithelial cell production and cell shedding in the small intestine of the rat fed and fasting. J Anat 120:321–327PubMedGoogle Scholar
  11. Cogger HG (1992) Reptiles and amphibians of Australia. Reed, SydneyGoogle Scholar
  12. Coltman DW, Bowen WD, Iverson SJ, Boness DJ (1998) The energetics of male reproduction in an aquatically mating pinniped, the harbour seal. Physiol Zool 71(4):387–399PubMedGoogle Scholar
  13. Costello EK, Gordon JI, Secor SM, Knight R (2010) Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J 4(11):1375–1385PubMedGoogle Scholar
  14. Cramp RL, Franklin CE (2003) Is re-feeding efficiency compromised by prolonged starvation during aestivation in the green striped burrowing frog, Cyclorana alboguttata? J Exp Zool A 300(2):126–132Google Scholar
  15. Cramp RL, Franklin CE (2005) Arousal and re-feeding rapidly restores digestive tract morphology following aestivation in green-striped burrowing frogs. Comp Biochem Physiol A 142(4):451–460Google Scholar
  16. Cramp RL, Kayes SM, Meyer EA, Franklin CE (2009) Ups and downs of intestinal function with prolonged fasting during aestivation in the burrowing frog, Cyclorana alboguttata. J Exp Biol 212(22):3656–3663PubMedGoogle Scholar
  17. Das S, Yadav RK, Nagchoudhuri J (2001) Effect of fasting on the intestinal absorption of d-glucose and D-xylose in rats in vivo. Indian J Physiol Pharmacol 45(4):451–456PubMedGoogle Scholar
  18. Dekinga A, Dietz MW, Koolhaas A, Piersma T (2001) Time course and reversibility of changes in the gizzards of red knots alternately eating hard and soft food. J Exp Biol 204(12):2167–2173PubMedGoogle Scholar
  19. Dietz MW, Piersma T, Dekinga A (1999) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J Exp Biol 202(20):2831–2837PubMedGoogle Scholar
  20. Dobinson HM, Richards AJ (1964) The effects of the severe winter of 1962/63 on birds in Britain. Br Birds 57:373–433Google Scholar
  21. Dunel-Erb S, Chevalier C, Laurent P, Bach A, Decrock F, Le Maho Y (2001) Restoration of the jejunal mucosa in rats refed after prolonged fasting. Comp Biochem Physiol 129A:933–947Google Scholar
  22. Fujise T, Iwakiri R, Wu B, Amemori S, Kakimoto T, Yokoyama F, Sakata Y, Tsunada S, Fujimoto K (2006) Apoptotic pathway in the rat intestinal mucosa is different between fasting and ischemia-reperfusion. Am J Physiol 291:G110–G116Google Scholar
  23. Galluser M, Belkhou R, Freund JN, Duluc I, Torp N, Danielsen M, Raul F (1991) Adaptation of intestinal hydrolases to starvation in rats: effect of thyroid function. J Comp Physiol 161B(4):357–361Google Scholar
  24. Gauthier-Clerc M, Le Maho Y, Clerquin Y, Drault S, Handrich Y (2000) Penguin fathers preserve food for their chicks. Nature 408:928–929PubMedGoogle Scholar
  25. Geiger S, Wagner C, Lignot JH, Le Maho Y, Robin JP (2009) Intestinal response to prolonged fasting and subsequent feeding in Mallard (Anas platyrhynchos). Wildfowl 59(2):167–175Google Scholar
  26. Geyra A, Uni Z, Sklan D (2001) The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick. Br J Nutr 86(1):53–56PubMedGoogle Scholar
  27. Glue DE (1973) Seasonal mortality in four small birds of prey. Ornis Scand 4:97–102Google Scholar
  28. Goldberg AL, Tischler M, De Martino G, Griffin G (1980) Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed Proc 39:31–36PubMedGoogle Scholar
  29. Goodlad RA, Plumb JA, Wright NA (1988) Epithelial cell proliferation and intestinal absorptive function during starvation and refeeding in the rat. Clin Sci (Lond) 74(3):301–306Google Scholar
  30. Goodman MN, Larsen PR, Kaplan MN, Aoki TT, Young VR, Ruderman NB (1980) Starvation in the rat. II. Effect of age and obesity on protein sparing and fuel metabolism. Am J Physiol 239:E277–E286PubMedGoogle Scholar
  31. Groscolas R, Robin J-P (2001) Long-term fasting and re-feeding in penguins. Comp Biochem Physiol 128A:645–655Google Scholar
  32. Grossmann J, Mohr S, Lapentina EG, Fiocchi C, Levine AD (1998) Sequential and rapid activation of select caspases during apoptosis of normal intestinal epithelial cells. Am J Physiol 274(6):G1117–G1124PubMedGoogle Scholar
  33. Habold C, Chevalier C, Dunel-Erb S, Foltzer-Jourdainne C, Le Maho Y, Lignot JH (2004) Effects of fasting and refeeding on jejunal morphology and cellular activity in rats in relation to depletion of body stores. Scand J Gastroenterol 39:531–539PubMedGoogle Scholar
  34. Habold C, Foltzer-Jourdainne C, Arbiol C, Le Maho Y, Lignot JH (2006) Intestinal apoptosis changes linked to metabolic status in fasted and refed rats. Pflugers Arch Eur J Physiol 451(6):749–759Google Scholar
  35. Habold C, Reichardt F, Foltzer-Jourdainne C, Lignot JH (2007) Morphological changes of the rat intestinal lining in relation to body stores depletion during fasting and after refeeding. Pflugers Arch Eur J Physiol 455(2):323–332Google Scholar
  36. Handrich Y, Nicolas L, Le Maho Y (1993) Winter starvation in captive common barn-owls: physiological states and reversible limits. Auk 110:458–469Google Scholar
  37. Helmstetter C, Reix N, T’Flachebba M, Pope RK, Secor SM, Le Maho Y, Lignot JH (2009a) The effects of feeding on cell morphology and proliferation of the gastrointestinal tract of juvenile Burmese pythons (Python molurus). Zool Sci 26(9):632–638PubMedGoogle Scholar
  38. Helmstetter C, Pope RK, T’Flachebba M, Secor SM, Lignot JH (2009b) Functional changes with feeding of the gastro-intestinal epithelia of Burmese pythons (Python molurus). Can J Zool 87(12):1255–1267Google Scholar
  39. Hopper AF, Wannemacher RW Jr, McGovern PA (1968) Cell population changes in the intestinal epithelium of the rat following starvation and protein-depletion. Proc Soc Exp Biol Med 128(3):695–698PubMedGoogle Scholar
  40. Hourdry J, Dauca M (1977) Cytological and cytochemical changes in the intestinal epithelium during anuran metamorphosis. Int Rev Cytol (Suppl) 5:337–385Google Scholar
  41. Hudson NJ, Franklin CE (2002) Maintaining muscle mass during extended disuse: aestivating frogs as a model species. J Exp Biol 205:2297–2303PubMedGoogle Scholar
  42. Hudson NJ, Franklin CE (2003) Preservation of three-dimensional capillary structure in frog muscle during aestivation. J Anat 202:471–474PubMedGoogle Scholar
  43. Hudson NJ, Bennett MB, Franklin CE (2004) Effect of aestivation on long bone mechanical properties in the green-striped burrowing frog, Cyclorana alboguttata. J Exp Biol 207:475–482PubMedGoogle Scholar
  44. Hudson NJ, Lavidis NA, Choy PT, Franklin CE (2005) Effect of prolong inactivity on skeletal motor nerve terminals during aestivation in the burrowing frog, Cyclorana alboguttata. J Comp Physiol 191A:373–379Google Scholar
  45. Hume ID, Biebach H (1996) Digestive tract function in the long distance migratory garden warbler, Sylvia borin. J Comp Physiol 166B:388–395Google Scholar
  46. Ihara T, Tsujikawa T, Fujiyama Y, Ueyama H, Ohkubo I, Bamba T (2000) Enhancement of brush border membrane peptidase activity in rat jejunum induced by starvation. Pflugers Arch 440(1):75–83PubMedGoogle Scholar
  47. Ishizuya-Oka A, Shimozawa A (1992) Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivo in vitro. J Morphol 213:185–195PubMedGoogle Scholar
  48. Ito J, Uchida H, Yokote T, Ohtake K, Kobayashi J (2010) Fasting-induced intestinal apoptosis is mediated by inducible nitric oxide synthase and interferon-γ in rat. Am J Physiol 298(6):G916–G926Google Scholar
  49. Iwakiri R, Gotoh Y, Noda T, Sugihara H, Fujimoto K, Fuseler J, Aw TY (2001) Programmed cell death in rat intestine: effect of feeding and fasting. Scand J Gastroenterol 36:39–47PubMedGoogle Scholar
  50. Kakimoto T, Fujise T, Shiraishi R, Kuroki T, Park JM, Ootani A, Sakata Y, Tsunada S, Iwakiri R, Fujimoto K (2008) Indigestible material attenuated changes in apoptosis in the fasted rat jejunal mucosa. Exp Biol Med (Maywood) 233(3):310–316Google Scholar
  51. Karasov WH (1997) Vertebrate gastrointestinal system. In: Dantzler WH (ed) Handbook of physiology, section 13. University Press, OxfordGoogle Scholar
  52. Karasov WH, Pinshow B (1998) Changes in lean mass and in organs of nutrients assimilation in a long-distance Passerine migrant at a springtime stopover site. Physiol Zool 71:435–448PubMedGoogle Scholar
  53. Karasov WH, Pinshow B, Starck JM, Afik D (2004) Anatomical and histological changes in the alimentary tract of migrating blackcaps (Sylvia atricapilla): a comparison among fed, fasted, food-restricted, and refed birds. Physiol Biochem Zool 77(1):149–160PubMedGoogle Scholar
  54. Klein N, Frölich F, Krief S (2008) Geophagy: soil consumption enhances the bioactivities of plants eaten by chimpanzees. Naturwissenschaften 95:325–331PubMedGoogle Scholar
  55. Koldovsky O (1981) Developmental, dietary and hormonal control of intestinal disaccharidases in mammals (including man). In: Randle PF, Steiner DF, Whelan WJ (eds) Carbohydrate metabolism and its disorders. Academic Press, LondonGoogle Scholar
  56. Koubi HE, Robin JP, Dewasmes G, Le Maho Y, Frutoso J, Minaire Y (1991) Fasting-induced rise in locomotor activity in rats coincides with increased protein utilization. Physiol Behav 50:337–343PubMedGoogle Scholar
  57. Krishnamani R, Mahaney WC (2000) Geophagy among primates: adaptive significance and ecological consequences. Anim Behav 59:899–915PubMedGoogle Scholar
  58. Le Maho Y, Vu Van Kha H, Koubi H, Dewasmes G, Girard J, Ferri P, Cagnard M (1981) Body composition, energy expenditure and plasma metabolites in long-term fasting geese. Am J Physiol 241:342–354Google Scholar
  59. Lignot JH, Helmstetter C, Secor SM (2005) Postprandial morphological response of the intestinal epithelium of the Burmese python, python molurus. Comp Biochem Physiol 141A:280–291Google Scholar
  60. Loveridge JP, Withers PC (1981) Metabolism and water balance of active and cocooned African bullfrogs Pyxicephalus adspersus. Physiol Zool 54:203–214Google Scholar
  61. Luciano L, Groos S, Sridhar Rao K, Gupta PD, Reale E (1997) Early morphological events during apoptotic process in enterocytes. Rec Adv Microsc Cells Tissues Organs 4:391–395Google Scholar
  62. Luppa H (1977) Histology of the digestive tract. In: Gans CE, Parsons TS (eds) Biology of the reptilia, vol 6. Academic Press, New YorkGoogle Scholar
  63. Marti CD, Wagner PW (1985) Winter mortality in common barn-owls and its effect on population density and reproduction. Condor 87:111–115Google Scholar
  64. McAvoy JW, Dixon KE (1977) Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis. J Exp Zool 202:128–138Google Scholar
  65. McClanahan LL, Shoemaker VH, Ruibal R (1976) Structure and function of the cocoon of a ceratophryd frog. Copeia 179–185Google Scholar
  66. McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol Mol Integr Physiol 144A(4):381–394Google Scholar
  67. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol 156A:1–18Google Scholar
  68. McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol Mol Integr Physiol 128A(3):579–593Google Scholar
  69. Mithieux G, Bady I, Gautier A, Croset M, Rajas F, Zitoun C (2004) Induction of control genes in intestinal gluconeogenesis is sequential during fasting and maximal in diabetes. Am J Physiol 286(3):E370–E375Google Scholar
  70. Ogihara H, Suzuki T, Nagamachi Y, Inui K, Takata K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochem J 31(3):169–174PubMedGoogle Scholar
  71. Owen M, Cook WA (1977) Variations in body weight, wing length and condition of mallard Anas platyrhynchos platyrhynchos and their relationship to environmental changes. J Zool (London) 183:377–395Google Scholar
  72. Parsons TS, Cameron JE (1977) Internal relief of the digestive tract. In: Gans C, Parsons TS (eds) Biology of the reptilia, vol 6. Academic Press, New YorkGoogle Scholar
  73. Pawlina IM, Boag DA, Robinson FE (1993) Population structure and changes in body mass and composition of mallards (Anas platyrhynchos) wintering in Edmonton, Alberta. Canadian J Zool 71:2275–2281Google Scholar
  74. Piersma T (1998) Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight? J Avian Biol 29:511–520Google Scholar
  75. Piersma T, Lindström A (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12(4):134–138PubMedGoogle Scholar
  76. Potten CS, Allen TD (1977) Ultrastructure of cell loss in intestinal mucosa. J Ultrastruct Res 60:272–277PubMedGoogle Scholar
  77. Reeder WG (1964) The digestive system. In: Moore JA (ed) Physiology of the amphibia. Academic Press, New YorkGoogle Scholar
  78. Reichardt F, Chaumande B, Habold C, Robin J-P, Ehret-Sabatier L, Le Maho Y, Liewig N, Angel F, Lignot J-H (2011) Kaolinite ingestion facilitates restoration of body energy reserves during refeeding after prolonged fasting. Fund Clin Pharmacol. doi:10.1111/j.1472-8206.2011.00989.x. [Epub ahead of print]Google Scholar
  79. Rigaud D, Hassid J, Meulemans A, Poupard AT, Boulier A (2000) A paradoxical increase in resting energy expenditure in malnourished patients near death: the king penguin syndrome. Am J Clin Nutr 72:355–360PubMedGoogle Scholar
  80. Robin J-P, Frain M, Sardet C, Groscolas R, Le Maho Y (1988) Protein and lipid utilization during long-term fasting in emperor penguins. Am J Physiol 254:R61–R68PubMedGoogle Scholar
  81. Robin J-P, Boucontet L, Chillet P, Groscolas R (1998) Behavioral changes in fasting emperor penguins: evidence for a “refeeding signal” linked to a metabolic shift. Am J Physiol Regul Integr Comp Physiol 274:R746–R753Google Scholar
  82. Schreiber AM, Cai L, Brown DD (2005) Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci U S A 102(10):3720–3725PubMedGoogle Scholar
  83. Secor SM (2001) Regulation of digestive performance: a proposed adaptive response. Comp Biochem Physiol Mol Integr Physiol 128A(3):565–577Google Scholar
  84. Secor SM (2003) Gastric function and its contribution to the postprandial metabolic response of the Burmese python Python molurus. J Exp Biol 206:1621–1630PubMedGoogle Scholar
  85. Secor SM (2005) Physiological responses to feeding, fasting, and estivation for anurans. J Exp Biol 208:2595–2608PubMedGoogle Scholar
  86. Secor SM, Diamond J (1995) Adaptive responses to feeding in Burmese pythons: pay before pumping. J Exp Biol 198:1313–1325PubMedGoogle Scholar
  87. Secor SM, Diamond J (1999) Maintenance of digestive performance in the turtles Chelydra serpentina, Sternotherus odoratus, and Trachemys scripta. Copeia 1999:75–84Google Scholar
  88. Secor SM, Diamond J (2000) Evolution of regulatory responses to feeding in snakes. Physiol Biochem Zool 73:123–141PubMedGoogle Scholar
  89. Secor SM, Lignot JH (2010) Morphological plasticity of vertebrate aestivation. Prog Mol Subcell Biol 49:183–208PubMedGoogle Scholar
  90. Secor SM, Whang EE, Lane JS, Ashley SW, Diamond J (2000) Luminal and systemic signals trigger intestinal adaptation in the juvenile python. Am J Physiol 279:G1177–G1187Google Scholar
  91. Shamoto K, Yamauchi K (2000) Recovery responses of chick intestinal villus morphology to different refeeding procedures. Poult Sci 79(5):718–723PubMedGoogle Scholar
  92. Shi Y-B, Ishizuya-Oka A (1996) Biphasic intestinal development in amphibians: Embryogenesis and remodeling during metamorphosis. Curr Top Dev Biol 32:205–235PubMedGoogle Scholar
  93. Sohma M (1983) Ultrastructure of the absorptive cells in the small intestine of the rat during starvation. Anat Embryol (Berl) 168(3):331–339Google Scholar
  94. Starck JM, Beese K (2001) Structural flexibility of the intestine of Burmese python in response to feeding. J Exp Biol 204:325–335PubMedGoogle Scholar
  95. Starck JM, Beese K (2002) Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting. J Exp Biol 205:1377–1388PubMedGoogle Scholar
  96. Starck JM, Rahmaan GHA (2003) Phenotypic flexibility of structure and function of the digestive system of Japanese quail. J Exp Biol 206(11):1887–1897PubMedGoogle Scholar
  97. Starck JM, Cruz-Neto AP, Abe AS (2007) Physiological and morphological responses to feeding in broad-nosed caiman (Caiman latirostris). J Exp Biol 210:2033–2045PubMedGoogle Scholar
  98. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system, 2nd edn. Cambridge University Press, New YorkGoogle Scholar
  99. Stewart KS, Fleming LW (1973) Relationship between plasma and erythrocyte magnesium and potassium concentrations in fasting obese subjects. Metabolism 22:535–547PubMedGoogle Scholar
  100. Suter W, Van Eerden MR (1992) Simultaneous mass starvation of wintering diving ducks in Switzerland and The Netherlands: a wrong decision in the right strategy? Ardea 80:229–242Google Scholar
  101. Symonds BL (2007) Getting the jump on skeletal muscle disuse atrophy: preservation of contractile performance in aestivating Cyclorana alboguttata (Günther 1867). J Exp Biol 210:825–835PubMedGoogle Scholar
  102. Tarachai P, Yamauchi K (2000) Effects of luminal nutrient absorption, intraluminal physical stimulation, and intravenous parenteral alimentation on the recovery responses of duodenal villus morphology following feed withdrawal in chickens. Poult Sci 79(11):1578–1585PubMedGoogle Scholar
  103. Thouzeau C, Froget G, Monteil H, Le Maho Y, Harf-Monteil C (2003) Evidence of stress in bacteria associated with long-term preservation of food in the stomach of incubating king penguins (Aptenodytes patagonicus). Polar Biol 26:115–123Google Scholar
  104. Uni Z, Noy Y, Sklan D (1995) Posthatch changes in morphology and function of the small intestines in heavy- and light-strain chicks. Poult Sci 74:1622–1629PubMedGoogle Scholar
  105. Uni Z, Ganot S, Sklan D (1998) Posthatch development of mucosal function in the broiler small intestine. Poult Sci 77(1):75–82PubMedGoogle Scholar
  106. van Beurden EK (1980) Energy metabolism of dormant Australian water-holding frogs (Cyclorana platycephalus). Copeia 1980:787–799Google Scholar
  107. van Gils JA, Battley PF, Piersma T, Drent R (2005) Reinterpretation of gizzard sizes of red knots world-wide emphasises overriding importance of prey quality at migratory stopover sites. Proc Biol Sci 272(1581):2609–2618PubMedGoogle Scholar
  108. Vermeer DE, Frate DA (1979) Geophagia in rural Mississippi—environmental and cultural contexts and nutritional implications. Am J Clin Nutr 32:2129–2135PubMedGoogle Scholar
  109. Wurth SMA, Musacchia XJ (1964) Renewal of intestinal epithelium in the freshwater turtle, Chrysemys picta. Anat Rec 148(3):427–439PubMedGoogle Scholar
  110. Yamauchi K, Iida S, Isshiki Y (1992) Post-hatching developmental changes in the ultrastructure of the duodenal absorptive epithelial cells in 1, 10 and 60-d-old chickens, with special reference to mitochondria. Br Poult Sci 33(3):475–488PubMedGoogle Scholar
  111. Yamauchi K, Kamisoyama H, Isshiki Y (1996) Effects of fasting and refeeding on structures of the intestinal villi and epithelial cells in White Leghorn hens. Br Poult Sci 37:909–921PubMedGoogle Scholar
  112. Yamaushi K, Isshiki Y (1991) Scanning electron microscopic observations on the intestinal villi in growing White Leghorn and broiler chickens from 1 to 30 days of age. Br Poult Sci 32(1):67–78Google Scholar
  113. Yokota H, Mori H, Furuse M (1992) Changes in body composition of germ-free and conventional chickens during starvation. Comp Biochem Physiol Comp Physiol 103(3):565–568PubMedGoogle Scholar
  114. Yoshizato K (1989) Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int Rev Cytol 119:97–149PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.UMR 5119 ECOSYM, Université de Montpellier II, CNRS, IFREMER, Adaptation Ecophysiologique et Ontogénie (AOE)Montpellier Cedex 05France

Personalised recommendations