Latitudinal trends in digestive flexibility: Testing the climatic variability hypothesis with data on the intestinal length of rodents

American Naturalist

Volumn 172, Issue 4, 2008, Pages

  Naya, Daniel E ^a   Bozinovic, Francisco ^a   Karasov, William H ^b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Digestive physiology; Macrophysiology; Meta analysis; Phenotypic plasticity

Indexed keywords

CLIMATE CHANGE; DIGESTION; LATITUDINAL GRADIENT; META-ANALYSIS; METABOLISM; NUTRIENT; PHENOTYPIC PLASTICITY; PROTEIN; RODENT;

ANIMAL; ANIMAL FOOD; ARTICLE; DIGESTION; ECOSYSTEM; GEOGRAPHY; HISTOLOGY; META ANALYSIS; PHYSIOLOGY; RODENT; SMALL INTESTINE;

ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; DIGESTION; ECOSYSTEM; GEOGRAPHY; INTESTINE, SMALL; RODENTIA;

ANIMALIA; MAMMALIA; RODENTIA;

EID: 53149143887     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/590957     Document Type: Article

References (97)

1. Addo-Bediako, A., S. L. Chown, and K. J. Gaston. 2000. Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B: Biological Sciences 267:739-745.
2. Batzli, G. O., A. D. Broussard, and R. J. Oliver. 1994. The integrated processing response in herbivorous small mammals. Pages 324-336 in D. J. Chivers and P. Langer, eds. The digestive system in mammals. Cambridge University Press, Cambridge.
3. Bozinovic, F., C. Veloso, and M. Rosenmann. 1988. Cambios del tracto digestivo de Abrothrix andinus (Cricetidae): efecto de la calidad de dieta y requerimientos de energía. Revista Chilena de Historia Natural 61:245-251.
4. Bozinovic, F., F. F. Novoa, and C. Veloso. 1990. Seasonal changes in energy expenditure and digestive tract of Abrothrix andinus (Cricetidae) in the Andes range. Physiological Zoology 63:1216-1231.
5. Brokowska, A. 1995. Seasonal changes in gut morphology of the striped field mouse (Apodemus agrarius). Canadian Journal of Zoology 73:1095-1099.
6. Brown, J. H., and C. R. Feldmeth. 1971. Evolution in constant and fluctuating environments: thermal tolerance of desert pupfish (Cyprinodon). Evolution 25:390-398.
7. Cant, J. P., B. W. McBride, and W. J. Croom Jr. 1996. The regulation of intestinal metabolism and its impact on whole animal energetics. Journal of Animal Science 74:2541-2553.
8. Chown, S. L., and S. W. Nicolson. 2004. Insect physiological ecology. Oxford University Press, New York.
9. Chown, S. L., K. J. Gaston, and D. Robinson. 2004. Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Functional Ecology 18:159-167.
10. Cork, S. J. 1994. Digestive constraints on dietary scope in small and moderately small mammals: how much do we really understand? Pages 337-369 in D. J. Chivers and P. Langer, eds. The digestive system in mammals. Cambridge University Press, Cambridge.
11. Corp, N., M. L. Gorman, and J. P. Speakman. 1997. Apparent absorption efficiency and gut morphometry of wood mice, Apodemus sylvaticus, from two distinct populations with different diets. Physiological Zoology 70:610-614.
12. Cruz, F. B., L. A. Fitzgerald, R. E. Espinoza, and J. A. Schulte II. 2005. The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards. Journal of Evolutionary Biology 18:1559-1574.
13. del Valle, J. C., C. Busch, and A. A. López Mañanes. 2006. Phenotypic plasticity in response to low-quality diet in the South American omnivorous rodent Akodon azarae (Rodentia: Sigmodontinae). Comparative Biochemistry and Physiology A 145:397-405.
14. Demment, M. W., and P. J. Van Soest. 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. American Naturalist 125:641-672.
15. Derting, T. L., and W. H. Austin. 1998. Changes in gut capacity with lactation and cold exposure in a species with low rates of energy use, the pine vole (Mircrotus pinetorum). Physiological Zoology 71:611-623.
16. Derting, T. L., and C. Hornung. 2003. Energy demand, diet quality, and central processing organs in wild white-footed mice (Peromyscus leucopus). Journal of Mammalogy 84:1381-1398.
17. Derting, T. L, and E. B. Noakes III. 1995. Seasonal changes in gut capacity in the white-footed mouse (Peromyscus leucopus) and meadow vole (Microtus pennsylvanicus). Canadian Journal of Zoology 73:243-252.
18. Dobzhansky, T. 1950. Evolution in the tropics. American Scientist 38:209-221.
19. Doughty, P., and D. N. Reznick. 2004. Patterns and analysis of adaptive phenotypic plasticity in animals. Pages 126-150 in T. J. DeWitt and S. M. Schneider, eds. Phenotypic plasticity. Oxford University Press, Oxford.
20. Dudley, S., and J. Schmitt. 1996. Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. American Naturalist 147:445-465.
21. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
22. France, R. 1992. The North American latitudinal gradient in species richness and geographical range of freshwater crayfish and amphipods. American Naturalist 139:342-354.
23. French, J. B., and W. P. Porter. 1994. Energy acquisition and allocation in Peromyscus maniculatus exposed to aldicarb and cool temperatures. Environmental Toxicology and Chemistry 13:927-933.
24. Garland, T., Jr., and R. Díaz-Uriarte. 1999. Polytomies and phylogenetically independent contrasts: an examination of the bounded degrees of freedom approach. Systematic Biology 48:547-558.
25. Gaston, K. J., and S. L. Chown. 1999. Why Rapoport's rule does not generalize. Oikos 84:309-312.
26. Gaston, K. J., T. M. Blackburn, and J. I. Spicer. 1998. Rapoport's rule: time for an epitaph? Trends in Ecology & Evolution 13:70-74.
27. Green, D. A., and J. S. Millar. 1987. Changes in gut dimensions and capacity of Peromyscus maniculatus relative to diet quality and energy needs. Canadian Journal of Zoology 65:2159-2162.
28. Gross, J. E., Z. Wang, and B. A. Wunder. 1985. Effects of food quality and energy needs: changes in gut morphology and capacity of Microtus ochrogaster. Journal of Mammalogy 66:661-667.
29. Guralnick, R. 2006. Do flatland- and mountain-dwelling species show different structuring of their experienced environment over latitude? a western vs. central-eastern North America rodent multispecies comparison. Diversity and Distribution 12:731-741.
30. Gurevitch, J., and L. V. Hedges. 2001. Meta-analyses: combining the results of independent experiments. Pages 347-369 in S. M. Scheiner and J. Gurevitch, eds. Analysis of ecological experiments. Oxford University Press, New York.
31. Hammond, K. A. 1993. Seasonal changes in gut size of the wild prairie vole (Microtus ochrogaster). Canadian Journal of Zoology 71:820-827.
32. Hammond, K. A., and D. M. Kristan. 2000. Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiological and Biochemical Zoology 73:547-556.
33. Hammond, K. A., and B. A. Wunder. 1991. The role of diet quality and energy need in the nutritional ecology of a small herbivore, Microtus ochrogaster. Physiological Zoology 64:541-567.
34. Hansson, L., and M. Jaarola. 1989. Body size related to cyclicity in microtines: dominance behaviour or digestive efficiency? Oikos 55:356-364.
35. Hernández, M., and E. S. Vrba. 2005. Rapoport effect and biomic specialization in African mammals: revisiting the climatic variability hypothesis. Journal of Biogeography 32:903-918.
36. Hoffman, A. A., and M. Watson. 1993. Geographical variation in the acclimation response of Drosophila to temperature extremes. American Naturalist 142(suppl.):S93-S113.
37. Huchon, D., O. Madsen, M. J. J. B. Sibbald, K. Ament, M. J. Stanhope, F. Catzeflis, W. W. de Jong, and E. J. P. Douzery. 2002. Rodent phylogeny and a timescale for the evolution of glires: evidence from an extensive taxon sampling using three nuclear genes. Molecular Biology and Evolution 19:1053-1065.
38. Huey, R. B. 1978. Latitudinal patterns of between-altitude faunal similarity: mountains might be "higher" in the tropics. American Naturalist 112:225-254.
39. Hume, I. D. 1989. Optimal digestive strategies in mammalian herbivores. Physiological Zoology 62:1145-1163.
40. James, A. C., R. B. R. Azevedo, and L. Patridge. 1997. Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146:881-890.
41. Janzen, D. H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101:233-249.
42. Justice, K. E., and F. A. Smith. 1992. A model of dietary fiber utilization by small mammalian herbivores, with empirical results for Neotoma. American Naturalist 139:398-416.
43. Karasov, W. H. 1990. Digestion in birds: chemical and physiological determinants and ecological implications. Pages 391-415 in M. L. Morrison, C. J. Ralph, J. Verner, and J. R. Jehl, eds. Avian foraging: theory, methodology, and applications. Cooper Ornithological Society, Lawrence, KS.
44. Karasov, W. H., and J. M. Diamond. 1983. Adaptive regulation of sugar and amino acid transport by vertebrate intestine. American Journal of Physiology 245:G443-G462.
45. Karasov, W. H., and I. D. Hume. 1997. Vertebrate gastrointestinal system. Pages 407-480 in W. H. Dantzler, ed. Handbook of physiology. Sec. 13. Comparative physiology. Oxford University Press, New York.
46. Karasov, W. H., and S. R. McWilliams. 2005. Digestive constraints in mammalian and avian ecology. Pages 87-112 in J. M. Starck and T. Wang, eds. Physiological and ecological adaptations to feeding in vertebrates. Science, Enfield, NH.
47. Kimura, T. M. 1988. Adaptations to temperate climates and evolution of overwintering strategies in the Drosophila melanogaster species group. Evolution 42:1288-1297.
48. Kristan, D. M., and K. A. Hammond. 2003. Physiological and morphological response to simultaneous cold exposure and parasite infection by wild-derived house mice. Functional Ecology 17:464-471.
49. Lagomarsino, I. V., and D. O. Conover. 1993. Variation in environmental and genotypic sex-determining mechanism across a latitudinal gradient in the fish, Menidia menidia. Evolution 47:487-494.
50. Lee, W. B., and D. C. Houston. 1993. The effect of diet quality on gut anatomy in British voles. Journal of Comparative Physiology B 163:337-339.
51. _. 1995. The rate of change of gut anatomy in voles in relation to diet quality. Journal of Zoology (London) 236:341-345.
52. Letcher, A. J., and P. H. Harvey. 1994. Variation in geographical range size among mammals of the Palearctic. American Naturalist 144:30-42.
53. Levins, R. 1969. Thermal acclimation and heat resistance in Drosophila species. American Naturalist 103:483-499.
54. Loeb, S. C., R. G. Schwab, and M. W. Demment. 1991. Responses of pocket gophers (Thomomys bottae) to changes in diet quality. Oecologia (Berlin) 86:542-551.
55. Lovegrove, B. G. 2003. The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. Journal of Comparative Physiology B 173:87-112.
56. Martin, Y., G. Gerlach, C. Schlotterer, and A. Meyer. 2000. Molecular phylogeny of European Muroid rodents based on complete cytochrome b sequences. Molecular Phylogenetics and Evolution 16:37-47.
57. Martins, E. P. 2004. COMPARE, version 4.6b. Computer Programs for the Statistical Analysis of Comparative Data, Indiana University, Bloomington.
58. McDevitt, R. M., and J. R. Speakman. 1994. Central limits to sustainable metabolic rate have no role in a cold acclimation of the short-tailed field vole (Microtus agrestis). Physiological Zoology 67:1117-1139.
59. McWilliams, S. R., and W. H. Karasov. 2001. Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comparative Biochemistry and Physiology A 128:579-593.
60. Naya, D. E., and F. Bozinovic. 2004. Digestive phenotypic flexibility in post-metamorphic amphibians: studies on a model organism. Biological Research 37:365-370.
61. Naya, D. E., W. H. Karasov, and F. Bozinovic. 2007. Phenotypic plasticity in laboratory mice and rats: a meta-analysis of current ideas on gut size flexibility. Evolutionary Ecology Research 9:1363-1374.
62. Norrie, M. B., and J. S. Millar. 1990. Food resources and reproduction in four microtine rodents. Canadian Journal of Zoology 68:641-650.
63. Nowak, R. M. 1999. Mammals of the world. Johns Hopkins University Press, Baltimore.
64. Pagel, M. D. 1992. A method for the analysis of comparative data. Journal of Theoretical Biology 156:431-442.
65. Pagel, M. D., R. M. May, and A. R. Collie. 1991. Ecological aspects of the geographical distribution and diversity of mammalian species. American Naturalist 137:791-815.
66. Pei, Y. X., D. H. Wang, and I. D. Hume. 2001a. Effects of dietary fiber on digesta passage, nutrient digestibility, and gastrointestinal tract morphology in the granivorous Mongolian gerbil (Meriones ochrogaster). Physiological and Biochemical Zoology 74:742-749.
67. _. 2001b. Selective digesta retention and coprophagy in Brandt's vole (Microtus brandti). Journal of Comparative Physiology B 171:457-464.
68. Penry, D. L., and P. A. Jumars. 1987. Modeling animal guts as chemical reactors. American Naturalist 129:69-96.
69. Piersma, T., and J. Drent. 2003. Phenotypic flexibility and the evolution of organismal design. Trends in Ecology & Evolution 18:228-233.
70. Piersma, T., and A. Lindstrom. 1997. Rapid reversible changes in organ size as a component of adaptive behaviour. Trends in Ecology & Evolution 12:134-138.
71. Pigliucci, M. 2001. Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore.
72. _. 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution 20:481-486.
73. Purvis, A., and T. Garland Jr. 1993. Polytomies in comparative analyses of continuous characters. Systematic Biology 42:569-575.
74. Rapoport, E. H. 1975. Aerografía: estrategias geográficas de las especies. Fondo de Cultura Económica, Ciudad de Mexico.
75. 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.
76. Rohde, K. 1996. Rapoport's rule is a local phenomenon and cannot explain latitudinal gradients in species diversity. Biodiversity Letters 3:10-13.
77. Rohde, K., M. Heap, and D. Heap. 1993. Rapoport's rule does not apply to marine teleost and cannot explain latitudinal gradients in species richness. American Naturalist 142:1-16.
78. Rosenberg, M. S., D. C. Adams, and J. Gurevitch. 2000. MetaWin statistical software for meta-analysis, version 2.1. Sinauer, Sunderland, MA.
79. Sabat, P., and F. Bozinovic. 2000. Digestive plasticity and the cost of acclimation to dietary chemistry in the omnivorous leaf-eared mouse Phyllotis darwini. Journal of Comparative Physiology B 170:411-417.
80. Scheiner, S. M. 1993. Genetics and evolution of phenotypic plasticity. Annual Reviews in Ecology and Systematics 24:35-68.
81. _. 2002. Selection experiments and the study of phenotypic plasticity. Journal of Evolutionary Biology 15:889-898.
82. Schmitt, J., S. A. Dudley, and M. Pigliucci. 1999. Manipulative approaches to testing adaptive plasticity: phytochrome-mediated shade-avoidance responses in plants. American Naturalist 154(suppl.):S43-S54.
83. Schwaibold, U., and N. Pillay. 2003. The gut morphology of the African ice rat, Otomys sloggetti robertsi, shows adaptations to cold environments and sex-specific seasonal variation. Journal of Comparative Physiology B 173:653-659.
84. Secor, S. M. 2001. Regulation of digestive performance: a proposed adaptive response. Comparative Biochemistry and Physiology A 128:565-577.
85. Sibly, R. M. 1981. Strategies of digestion and defecation. Pages 109-139 in C. R. Townsend and P. Calow, eds. Physiological ecology: an evolutionary approach to resource use. Blackwell Scientific, Oxford.
86. Snyder, G. K., and W. W. Weathers. 1975. Temperature adaptations in amphibians. American Naturalist 109:93-101.
87. Speakman, J. R. 2000. The cost of living: field metabolic rates of small mammals. Pages 178-294 in A. H. Fisher and D. G. Raffaelli, eds. Advances in ecological research. Academic Press, San Diego, CA.
88. Speakman, J. R., and E. Krol. 2005. Limits to sustained energy intake. IX. A review of hypotheses. Journal of Comparative Physiology B 175:375-394.
89. Spicer, J. I., and K. J. Gaston. 1999. Physiological diversity and its ecological implications. Blackwell Scientific, Oxford.
90. Starck, J. M. 1999. Structural flexibility of the gastro-intestinal tract of vertebrates: implications for evolutionary morphology. Zoologischer Anzeiger 238:87-101.
91. Stevens, G. C. 1989. The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist 133:240-256.
92. Thompson, J. 1991. Phenotypic plasticity as a component of evolutionary change. Trends in Ecology & Evolution 6:246-249.
93. van Berkum, F. H. 1988. Latitudinal patterns of the thermal sensitivity of sprint speed in lizards. American Naturalist 132:327-343.
94. Virgl, J. A., and F. Messier. 1992. Seasonal variation in body composition and morphology of adult muskrats in central Saskatchewan, Canada. Journal of Zoology (London) 228:461-477.
95. Woodall, P. F. 1989. The effects of increased dietary cellulose on the anatomy, physiology and behaviour of the captive water voles, Arvicola terrestris (L.) (Rodentia: Microtinae). Comparative Biochemistry and Physiology A 94:615-621.
96. Yamamot, A., and S. Ohba. 1983. Strategic difference in thermal adaptation between two Drosophila species, D. virilis and D. immigrans. Oecologia (Berlin) 52:333-339.
97. Young Owl, M., and G. O. Batzli. 1998. The integrated processing response of voles to fiber content of natural diets. Functional Ecology 12:4-13.