Tissue carbon incorporation rates and diet-to-tissue discrimination in ectotherms: Tortoises are really slow

Physiological and Biochemical Zoology

Volumn 85, Issue 1, 2012, Pages 96-105

  Murray, Ian W ^a   Wolf, Blair O ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBON ISOTOPE; DIET; DISCRIMINANT ANALYSIS; ECTOTHERMY; ISOTOPIC ANALYSIS; METABOLISM; PLASMA; REPTILE; SHELL;

ANIMALIA; GOPHERUS AGASSIZII; SERPENTES; SQUAMATA; TESTUDINES; TESTUDINIDAE;

EID: 84855824384     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/663867     Document Type: Article

References (61)

1. Alibardi L. 2005. Proliferation in the epidermis of chelonians and growth of the horny scutes. J Morphol 265:52-69.
2. Alibardi L. 2006. Ultrastructural and immunohistochemical observations on the process of horny growth in chelonian shells. Acta Histochem 108:149-162.
3. Alibardi L. and M. Toni. 2006. Immunolocalization and characterization of beta-keratins in growing epidermis of chelonians. Tissue Cell 38:53-63.
4. Altland P.D. and K.C. Brace. 1962. Red cell life span in the turtle and toad. Am J Physiol 203:1188-1190.
5. Barnes C., C.J. Sweeting, S. Jennings, J.T. Barry, and N.V.C. Polunin. 2007. Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21:356-362.
6. Bearhop S., S. Waldron, S.C. Votier, and R.W. Furness. 2002. Factors that influence assimilation rates and fractionation ofnitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451-458.
7. Brown J.H., J.F. Gillooly, A.P. Allen, V.M. Savage, and G.B. West. 2004. Towards a metabolic theory of ecology. Ecology 85: 1771-1789.
8. Bucheister A. and R.J. Latour. 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445-461.
9. Burnham K. and D. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
10. Cagle F.R. 1946. The growth of the slider turtle, Pseudemys scripta elegans. Am Midl Nat 36:685-729.
11. 15N incorporation in house sparrows. Oecologia 144:226-232.
12. Carleton S.A. and C. Martínez del Rio. 2010. Growth and catabolism in isotopic incorporation: a new formulation and experimental data. Funct Ecol 24:805-812.
13. Carr A. 1952. Handbook of turtles. Cornell University Press, Ithaca, NY.
14. 13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443-453.
15. Cerling T., L. Ayliffe, M. Dearing, J. Ehleringer, B. Passey, D. Podlesak, A. Torregrossa, and A. West. 2007. Determining biological tissue turnover using stable isotopes: the reaction progress variable. Oecologia 151:175-189.
16. Cherel Y., K.A. Hobson, F. Bailleul, and R. Groscolas. 2005. Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881-2888.
17. Dalerum F. and A. Angerbjorn. 2005. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647-658.
18. DeNiro M.J. and S. Epstein. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495-506.
19. Fisk A., K. Sash, J. Maerz, W. Palmer, J. Carroll, and M. Mac-Neil. 2009. Metabolic turnover rates of carbon and nitrogen stable isotopes in captive juvenile snakes. Rapid Commun Mass Spectrom 23:319-326.
20. Gannes L.Z., D.M. O'Brien, and C. Martínez del Rio. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271-1276.
21. Germano D.J. 1992. Longevity and age-size relationships of desert tortoises. Copeia 1992:367-374.
22. Germano D.J. 1994. Growth and maturity of North American tortoises in response to regional climates. Can J Zool 72:918-931.
23. Haschemeyer A.E.V. and M.A.K. Smith. 1979. Protein synthesis in liver, muscle, and gill of mullet (Mugil cephalus L.) in vivo. Biol Bull 156:93-102.
24. Herzka S.Z. and G.J. Holt. 2000. Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Can J Fish Aquat Sci 57:137-147.
25. 15N. Can J Fish Aquat Sci 50:2071-2076.
26. Hobson K.A., R.T. Alisauskias, and R.G. Clark. 1993. Stablenitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388-394.
27. Hobson K.A. and R.G. Clark. 1992. Assessing avian diets using stable isotopes. I. Turnover of d13C in tissues. Condor 94: 181-188.
28. 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638-641.
29. Jackson C.G., Jr., J.A. Trotter, T.H. Trotter, and M.W. Trotter. 1976. Accelerated growth rate and early maturity in Gopherus agassizii (Reptilia, Testudines). Herpetologica 32:139-145.
30. Jackson C.G., Jr., T.H. Trotter, J.A. Trotter, and M.W. Trotter. 1978. Further observations of growth and sexual maturity in captive desert tortoises (Reptilia: Testudines). Herpetologica 34:225-227.
31. Jones S.M. and R.E. Ballinger. 1987. Comparative life histories of Holbrookia maculata and Sceloporus undulatus in western Nebraska. Ecology 68:1828-1838.
32. Krasilnikov E.N. 1971. Age-conditioned changes of blood cells in turtles and lizards. Arkh Anat Gistol Embriol 61:27-32.
33. Kurle C.M. 2009. Interpreting temporal variation in omnivore foraging ecology via stable isotope modeling. Funct Ecol 23: 733-744.
34. MacAvoy S.E., L.S. Arneson, and E. Bassett. 2006. Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals. Oecologia 150:190-201.
35. MacAvoy S.E., S.A. Macko, and L.S. Arneson. 2005. Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can J Zool 83:631-641.
36. Martínez del Rio C. and R. Anderson-Sprecher. 2008. Beyond the reaction progress variable: the meaning and significance of isotopic incorporation data. Oecologia 156:765-772.
37. Martínez del Rio C., N. Wolf, S. Carleton, and L.Z. Gannes. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91-111.
38. McCue M.D. 2007. Stable isotopes track spatio-temporal patterns of nutrient allocation in postprandial pit-vipers. Res Rev BioSci 1:17-26.
39. McCue M.D. 2008. Endogenous and environmental factors influence the dietary fractionation of 13C and 15N in hissing cockroaches Gromphadorhina portentosa. Physiol Biochem Zool 81:14-24.
40. McCue M.D. 2011. Tracking the oxidative and nonoxidative fates of isotopically labeled nutrients in animals. BioScience 61:217-230.
41. 13C-labeled carbohydrates, lipids, and proteins in vivo. Physiol Biochem Zool 84:506-513.
42. Michener R.H. and D.M. Schell. 1994. Stable isotope ratios as tracers in marine aquatic food webs. Pp. 137-157 in K. Lajtha and R.H. Michener, eds. Stable isotopes in ecology and environmental science. Blackwell Scientific, Oxford.
43. Nieto R. and G.E. Lobley. 1999. Integration of protein metabolism within the whole body and between organs. Pp. 69-99 in G.E. Lobley, A. White, and J.C. MacRae, eds. Protein metabolism and nutrition. Wageningen Pers, Wageningen.
44. Olive P.J.W., J.K. Pinnegar, N.V.C. Polunin, G. Richards, and R. Welch. 2003. Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608-617.
45. Pilgrim M.A. 2005. Linking microgeographic variation in pigmy rattlesnake (Sistrurus miliarius) life history and demography with diet composition: a stable isotope approach. PhD diss. University of Arkansas at Fayetteville.
46. Podlesak D.W. and S.R. McWilliams. 2007. Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed. Physiol Biochem Zool 79: 534-549.
47. Pough F.H., R.M. Andrews, J.E. Cadle, M.L. Crump, A.H. Savitzky, and K.D. Wells. 2004. Herpetology. 3rd ed. Pearson Prentice Hall, Upper Saddle River, NJ.
48. 15N incorporation in a rapidly growing ectotherm. Oecologia 155: 651-663.
49. Rodnan G.P., F.G. Ebaugh Jr., and M.R.S. Fox. 1957. The life span of the red blood cell and the red blood cell volume in the chicken, pigeon, and duck as estimated by the use of Na2Cr51O4 with observations on red cell turnover rate in the mammal, bird and reptile. Blood 12:355-366.
50. Schoeller D.A. 1999. Isotope fractionation: why aren't we what we eat? J Archaeol Sci 26:667-673.
51. Seminoff J.A., K.A. Bjorndal, and A.B. Bolten. 2007. Stable carbon and nitrogen isotope discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia 2007:534-542.
52. 15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Prog Ser 308:271-278.
53. 13C analysis of diet. Oecologia 57:32-37.
54. Tracy C.R. and C.R. Tracy. 1995. Estimating age of desert tortoises (Gopherus agassizii) from scute rings. Copeia 1995: 964-966.
55. Trueman C.N., R.A.R. McGill, and P.H. Guyard. 2005. The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals: an experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19:3239-3247.
56. Vinegar M.B. 1975. Life history phenomena in two populations of the lizard Sceloporus undulatus in southwestern New Mexico. Am Midl Nat 93:388-402.
57. Warne R.W., C.A. Gilman, and B.O. Wolf. 2010. Tissue carbon incorporation rates in lizards: implications for studies using stable isotopes in terrestrial ectotherms. Physiol Biochem Zool 83:608-617.
58. Webb S.C., R.E.M. Hedges, and S.J. Simpson. 1998. Diet quality influences the d13C and d15N of locusts and their biochemical components. J Exp Biol 201:2903-2911.
59. Williams C.T., C.L. Buck, J. Sears, and A.S. Kitaysky. 2007. Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11-18.
60. Wilson D.S., C.R. Tracy, and C.R. Tracy. 2003. Estimating age of turtles from growth rings: a critical evaluation of the technique. Herpetologica 59:178-194.
61. Zug G.R. 1993. Herpetology: an introductory biology of amphibians and reptiles. Academic Press, San Diego, CA.