Morphometrics of the avian small intestine compared with that of nonflying mammals: A phylogenetic approach

Physiological and Biochemical Zoology

Volumn 81, Issue 5, 2008, Pages 526-550

  Lavin, Shana R ^a   Karasov, William H ^a   Ives, Anthony R ^a   Middleton, Kevin M ^b,c   Garland Jr , Theodore ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOENERGETICS; BIRD; BODY MASS; CLADISTICS; COMPARATIVE STUDY; DIET; DIGESTIVE SYSTEM; MAMMAL; METABOLISM; MORPHOMETRY; PHYLOGENY; TESTING METHOD;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIRD; COMPARATIVE STUDY; COMPUTER PROGRAM; GENETICS; HISTOLOGY; MAMMAL; MORPHOMETRICS; PHYLOGENY; REGRESSION ANALYSIS; SMALL INTESTINE; SPECIES DIFFERENCE;

ANIMALS; BIRDS; BODY WEIGHTS AND MEASURES; INTESTINE, SMALL; MAMMALS; MODELS, BIOLOGICAL; PHYLOGENY; REGRESSION ANALYSIS; SOFTWARE; SPECIES SPECIFICITY;

ANIMALIA; AVES; MAMMALIA;

EID: 46149108174     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/590395     Document Type: Article

References (118)

1. Afik D., B.W. Darken, and W.H. Karasov. 1997a. Is diet-shifting facilitated by modulation of intestinal nutrient uptake? test of an adaptational hypothesis in yellow-rumped warblers. Physiol Zool 70:213-221.
2. Afik D., S.R. McWilliams, and W.H. Karasov. 1997b. A test for passive absorption of glucose in yellow-rumped warblers and its ecological significance. Physiol Zool 70:370-377.
3. Ankney C.D. 1977. Feeding and digestive organ size in lesser snow geese. Auk 94:275-282.
4. Barnes G.G. and V.G. Thomas. 1987. Digestive organ morphology, diet, and guild structure of North American Anatidae. Can J Zool 65:1812-1817.
5. Barry R.E., Jr. 1976. Mucosal surface areas and villous morphology of the small intestines of small mammals: functional interpretations. J Mammal 57:273-289.
6. Biviano A.B., C. Martinez del Rio, and D.L. Phillips. 1993. Ontogenesis of intestine morphology and intestinal disaccharidases in chickens (Gallus gallus) fed contrasting purified diets. J Comp Physiol B 163:508-518.
7. Blomberg S.P., T. Garland Jr., and A.R. Ives. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745.
8. Burnham K.P. and D.R. Anderson. 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd ed. Springer, New York.
9. Caviedes-Vidal E. and W.H. Karasov. 1996. Glucose and amino acid absorption in house sparrow intestine and its dietary modulation. Am J Physiol 271:R561-R568.
10. Caviedes-Vidal E., T. McWhorter, S.R. Lavin, J.G. Chediack, C.R. Tracy, and W.H. Karasov. 2007. The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci USA 104:19132-19137.
11. Chang M.H. and W.H. Karasov. 2004. How the house sparrow absorbs glucose. J Exp Biol 340:3109-3121.
12. Chivers D.M. and C.M. Hladik. 1980. Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 116:337-386.
13. Chown S.L., E. Marais, J.S. Terblanche, C.J. Klok, J.R.B. Lighton, and T.M. Blackburn. 2007. Scaling of insect metabolic rate is inconsistent with the nutrient supply network model. Funct Ecol 21:282-290.
14. DeGolier T.F., S. Mahoney, and G.E. Duke. 1999. Relationships of avian cecal lengths to food habits, taxonomic position, and intestinal lengths. Condor 101:622-634.
15. Diamond J.R. 1991. Evolutionary design of intestinal nutrient absorption: enough but not too much. News Physiol Sci 6:92-96.
16. Duncan R.P., D.M. Forsyth, and J. Hone. 2007. Testing the metabolic theory of ecology: allometric scaling exponents in mammals. Ecology 88:324-333.
17. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125:1-15.
18. _. 2004. Inferring Phylogenies. Sinauer, Sunderland, MA. Ferraris R.P. and J.M. Diamond. 1989. Specific regulation of intestinal nutrient transporters by their dietary substrates. Annu Rev Physiol 51:125-141.
19. Fine K.D., C.A. Santa Ana, J.L. Porter, and J.S. Fordtran. 1993. Effect of D-glucose on intestinal permeability and its passive absorption in human small intestine in vivo. Gastroenterology 105:1117-1125.
20. Fisher R.B. and D.S. Parsons. 1950. The gradient of mucosal surface area in the small intestine of the rat. J Anat 84:272-282.
21. Freckleton R.P., P.H. Harvey, and M. Pagel. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712-726.
22. Garland T., Jr. 1998. Testing the predictions of symmorphosis: conceptual and methodological issues. Pp. 40-47 in E.R. Weibel, L. Bolis, and C.R. Taylor, eds. Principles of Animal Design: The Optimization and Symmorphosis Debate. Cambridge University Press, New York.
23. Garland T., Jr., and S.C. Adolph. 1991. Physiological differentiation of vertebrate populations. Annu Rev Ecol Syst 22:193-228.
24. _. 1994. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797-828.
25. Garland T., Jr., A.F. Bennett, and E.L. Rezende. 2005. Phylogenetic approaches in comparative physiology. J Exp Biol 208:3015-3035.
26. Garland T., Jr., and R. Díaz-Uriarte. 1999. Polytomies and phylogenetically independent contrasts: an examination of the bounded degrees of freedom approach. Syst Biol 48:547-558.
27. Garland T., Jr., A.W. Dickerman, C.M. Janis, and J.A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265-292.
28. Garland T., Jr., and A.R. Ives. 2000. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346-364.
29. Grafen A. 1989. The phylogenetic regression. Philos Trans R Soc B 326:119-157.
30. Guillemette M. 1994. Digestive-rate constraint in wintering common eiders (Somateria mollissima): implications for flying capabilities. Auk 111:900-909.
31. Hansen T.F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341-1351.
32. Harris M.S., J.G. Kennedy, K.A. Siegesmund, and D.E. Yorde. 1988. Relationship between distension and absorption in rat intestine. Gastroenterology 94:1164-1171.
33. Heard G.S. and E.F. Annison. 1986. Gastrointestinal absorption of vitamin B6 in the chicken (Gallus domesticus). J Nutr 116:107-120.
34. Herrera C.M. 1984. Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65:609-617.
35. Ives A.R., P.E. Midford, and T. Garland Jr. 2007. Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252-270.
36. Johnson J.B. and K.S. Omland. 2004. Model selection in ecology and evolution. Trends Ecol Evol 19:101-108.
37. Karasov W.H. 1990. Digestion in birds: chemical and physiological determinants and ecological implications. Stud Avian Biol 13:391-415.
38. _. 1992. Test of the adaptive modulation hypothesis for dietary control of intestinal nutrient transport. Am J Physiol 263:R496-R502.
39. Karasov W.H., D. Afik, and B.W. Darken. 1996. Do northern bobwhite quail modulate intestinal nutrient absorption in response to dietary change? a test of an adaptational hypothesis. Comp Biochem Physiol A 113:233-238.
40. Karasov W.H. and S.J. Cork. 1994. Glucose absorption by a nectarivorous bird: the passive pathway is paramount. Am J Physiol 267:G18-G26.
41. Karasov W.H. and I.D. Hume. 1997. The vertebrate gastrointestinal system. Pp. 409-480 in W.H. Dantzler, ed. Handbook of Physiology. Sec. 13. Comparative Physiology. Vol. 1. Oxford University Press, New York.
42. Karasov W.H. and S.R. McWilliams. 2005. Digestive constraints in mammalian and avian ecology. Pp. 87-112 in J.M. Starck and T. Wang, eds. Physiological and Ecological Adaptations to Feeding in Vertebrates. Science, Enfield, NH.
43. Kisielinski K., S. Willis, A. Prescher, B. Klosterhalfen, and V. Schumpelick. 2002. A simple new method to calculate small intestine absorptive surface in the rat. Clin Exp Med 2:131-135.
44. Klasing K.C. 1998. Comparative Avian Nutrition. CAB International, Davis, CA.
45. Klurfeld D.M. 1999. Nutritional regulation of gastrointestinal growth. Front Biosci 4:D299-D302.
46. Lane J.S., E.E. Whang, D.A. Rigberg, O.J. Hines, D. Kwan, M.J. Zinner, D.W. McFadden, J. Diamond, and S.W. Ashley. 1999. Paracellular glucose transport plays a minor role in the unanesthetized dog. Am J Physiol 276:G789-G794.
47. Lavin S.R. 2007. Small Intestine Morphometrics and Paracellular Absorption in Birds and Mammals. PhD diss. University of Wisconsin, Madison.
48. Lavin S.R. and W.H. Karasov. 2008. Allometry of paracellular absorption in birds. Physiol Biochem Zool 81:551-560.
49. Lavin S.R., T.J. McWorter, and W.H. Karasov. 2007. Mechanistic bases for differences in passive absorption. J Exp Biol 210:2754-2764.
50. Leopold A.S. 1953. Intestinal morphology of gallinaceous birds in relation to food habits. J Wildl Manag 17:197-203.
51. Levey D.J. and M.L. Cipollini. 1996. Is most glucose absorbed passively in northern bobwhite? Comp Biochem Physiol A 113:225-231.
52. Levey D.J. and W.H. Karasov. 1992. Digestive modulation in a seasonal frugivore, the American robin (Turdus migratorius). Am J Physiol 262:G711-G718.
53. Levin R.J. 1984. Absorption from the alimentary tract. Pp. 1-22 in B.M. Freeman, ed. Physiology and Biochemistry of the Domestic Fowl. Academic Press, London.
54. Ludden T.M., S.L. Beal, and L.B. Sheiner. 1994. Comparison of the Akaike Information Criterion, the Schwarz criterion and the F test as guides to model selection. J Pharmacokinet Pharmacodynam 22:431-445.
55. Makanya A.N., J.N. Maina, T.M. Mayhew, S.A. Tschanz, and P.H. Burri. 1997. A stereological comparison of villous and microvillous surfaces in small intestines of frugivorous and entomophagous bats: species, inter-individual and cranio-caudal differences. J Exp Biol 200:2415-2423.
56. Martinez del Rio C. 1990. Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol Zool 63:987-1011.
57. Mayhew T.M. and C. Middleton. 1985. Crypts, villi and microvilli in the small intestine of the rat: a stereological study of their variability within and between animals. J Anat 141:1-17.
58. McClelland J. 1979. Digestive system. Pp. 69-181 in A.S. King and J. McLelland, eds. Form and Function in Birds. Vol. 1. Academic Press, London.
59. McMahon T.A. and J.T. Bonner. 1983. On Size and Life. Scientific American, New York.
60. McWhorter T.J., B.H. Bakken, W.H. Karasov, and C. Martinez del Rio. 2006. Hummingbirds rely on both paracellular and carrier-mediated intestinal glucose absorption to fuel high metabolism. Biol Lett 2:131-134.
61. Morse D.H. 1975. Ecological aspects of adaptive radiation in birds. Biol Rev 50:167-214.
62. Moss R. 1989. Gut size and the digestion of fibrous diets in tatranoid birds. J Exp Zool 3(suppl.):61-65.
63. Nagy K.A. 2001. Food requirements of wild animals: predictive equations for free-living mammals, reptiles, and birds. Nutr Abstr Rev Ser B 71:21R-31R.
64. _. 2005. Field metabolic rate and body size. J Exp Biol 208:1625.
65. Norberg U.M. 1995. How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol 9:48-54.
66. Nudds R.L. and D.M. Bryant. 2002. Consequences of load carrying by birds during short flights and is found to be behavioral and not energetic. Am J Physiol 283:R249-R256.
67. Pagel M.D. 1992. A method for the analysis of comparative data. J Theor Biol 156:431-442.
68. Pappenheimer J.R. 1993. On the coupling of membrane digestion with intestinal absorption of sugars and amino acids. Am J Physiol 265:G409-G417.
69. Parra R. 1978. Comparison of foregut and hindgut fermentation in herbivores. Pp. 205-229 in G.G. Montgomery, ed. The Ecology of Arboreal Folivores. Smithsonian Institution, Washington, DC.
70. Pulliainen E., P. Helle, and P. Tunkkari. 1981. Adaptive radiation of the digestive system, heart, and wings of Turdis pilaris, Bombycilla garrulous, Sturnus vulgaris, Pyrrhula pyrrhula, Pinicola enucleator, and Loxia pytopsittacus. Ornis Fenn 58:21-28.
71. Purvis A. and T. Garland Jr. 1993. Polytomies in comparative analyses of continuous characters. Syst Biol 42:569-575.
72. Rezende E.L., F. Bozinovic, and T. Garland Jr. 2004. Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution 58:1361-1374.
73. Richardson K.C. and R.D. Wooller. 1990. Adaptations of the alimentary tract of some Australian lorikeets to a diet of pollen and nectar. Aust J Zool 38:581-586.
74. Ricklefs R.E. 1996. Morphometry of the digestive tracts of some passerine birds. Condor 98:279-292.
75. Riesenfeld G., D. Sklan, A. Barr, U. Eisner, and S. Hurwitz. 1980. Glucose absorption and starch digestion in the intestine of the chicken. J Nutr 110:117-121.
76. Rohlf F.J. 2006. A comment on phylogenetic correction. Evolution 60:1509-1515.
77. Schmidt-Nielsen K. 1984. Scaling: Why Is Animal Size So Important? Cambridge University Press, Cambridge.
78. Schwartz R.M., J.K. Furne, and M.D. Levitt. 1995. Paracellular intestinal transport of six-carbon sugars is negligible in the rat. Gastroenterology 109:1206-1213.
79. Smith M.W., M.A. Mitchell, and M.A. Peacock. 1990. Effects of genetic selection on growth rate and intestinal structure in the domestic fowl (Gallus domesticus). Comp Biochem Physiol A 97:57-63.
80. Snipes R.L. 1997. Intestinal absorptive surface in mammals of different sizes. Adv Anat Embryol Cell Biol 138:III-VIII, 1-90.
81. Southgate D.A.T. 1995. Digestion and metabolism of sugars. Am J Clin Nutr 62:203S-210S.
82. Tracy C.R., T.J. McWhorter, C. Korine, M. Wojciechowski, B. Pinshow, and W.H. Karasov. 2007. Absorption of sugars in the Egyptian fruit bat (Rousettus aegyptiacus): a paradox explained. J Exp Biol 210:1726-1734.
83. Uhing M.R. and R.E. Kimura. 1995. Active transport of 3-O-methyl-glucose by the small intestine in chronically catheterized rats. J Clin Invest 95:2799-2805.
84. Van Der Klis J.G., 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.
85. Walsberg G.E. 1975. Digestive adaptations of Phainopepla nitens associated with the eating of mistletoe berries. Condor 77:169-174.
86. White C.R. 2003. Allometric analysis beyond heterogeneous regression slopes: use of the Johnson-Neyman technique in comparative biology. Physiol Biochem Zool 76:135-140.
87. Ziswiler V. and D.S. Farner. 1972. Digestion and the digestive system. Pp. 343-430 in D.S. Farner and J.R. King, eds. Avian Biology. Vol. II. Academic Press, New York.
88. Boyle W.A. and C.J. Conway. 2007. Why migrate? a test of the evolutionary precursor hypothesis. Am Nat 169:344-359.
89. Butler M.A. and A.A. King. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am Nat 164:683-695.
90. Butler M.A., T.W. Schoener, and J.B. Losos. 2000. The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution 54:259-272.
91. Cooper D.M. and R. Thompson. 1977. Note on estimation of parameters of autoregressive-moving average process. Biometrika 64:625-628.
92. Efron B. and R.J. Tibshirani. 1993. An Introduction to the Bootstrap. Chapman & Hall, New York.
93. Felsenstein J. 1988. Phylogenies and quantitative characters. Annu Rev Ecol Syst 19:445-471.
94. Freckleton R.P. and P.H. Harvey. 2006. Detecting non-Brownian trait evolution in adaptive radiations. PLoS Biol 4:2104-2111.
95. Freckleton R.P., M. Pagel, and P.H. Harvey. 2003. Comparative methods for adaptive radiations. Pp. 391-407 in T.M. Blackburn and K.J. Gaston, eds. Macroecology: Concepts and Consequences. Blackwell Science, Oxford.
96. Gage M.J.G. and R.P. Freckleton. 2003. Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc B 270:625-632.
97. Garland T., Jr., P.H. Harvey, and A.R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18-32.
98. Grafen A. 1992. The uniqueness of the phylogenetic regression. J Theor Biol 156:405-423.
99. Hansen T.F. and E.P. Martins. 1996. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50:1404-1417.
100. Hansen T.F. and S.H. Orzack. 2005. Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59:2063-2072.
101. Harville D.A. 1974. Bayesian inference for variance components using only error contrasts. Biometrika 61:383-385.
102. Housworth E.A. and E.P. Martins. 2001. Random sampling of constrained phylogenies: conducting phylogenetic analyses when the phylogeny is partially known. Syst Biol 50:628-639.
103. Housworth E.A., E.P. Martins, and M. Lynch. 2004. The phylogenetic mixed model. Am Nat 163:84-96.
104. Huelsenbeck J.P. and B. Rannala. 2003. Detecting correlation between characters in a comparative analysis with uncertain phylogeny. Evolution 57:1237-1247.
105. Judge G.G., W.E. Griffiths, R.C. Hill, H. Lutkepohl, and T.-C. Lee. 1985. The Theory and Practice of Econometrics. Wiley, New York.
106. Martins E.P. and T.F. Hansen. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646-667, erratum 153:448.
107. MathWorks. 1996. MATLAB, version 7.0. MathWorks, Natick, MA.
108. McKechnie A.E., R.P. Freckleton, and W. Jetz. 2006. Phenotypic plasticity in the scaling of avian basal metabolic rate. Proc R Soc B 273:931-937.
109. Muñoz-Garcia A. and J.B. Williams. 2005. Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny. Physiol Biochem Zool 78:1039-1056.
110. O'Meara B.C., C. Ane, M.J. Sanderson, and P.C. Wainwright. 2006. Testing for different rates of continuous trait evolution using likelihood. Evolution 60:922-933.
111. Pagel M. 1997. Inferring evolutionary processes from phylogenies. Zool Scr 26:331-348.
112. _. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
113. Paradis E. and J. Claude. 2002. Analysis of comparative data using generalized estimating equations. J Theor Biol 218:175-185.
114. Paradis E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
115. Patterson H.D. and R. Thompson. 1971. Recovery of interblock information when block sizes are unequal. Biometrika 58:545-564.
116. Rohlf F.J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143-2160.
117. Sessions S.K. and A. Larson. 1987. Developmental correlates of genome size in plethodontid salamanders and their implications for genome evolution. Evolution 41:1239-1251.
118. Smyth G.K. and A.P. Verbyla. 1996. A conditional likelihood approach to residual maximum likelihood estimation in generalized linear models. J R Stat Soc B 58:565-572.