State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta)

Journal of Experimental Biology

Volumn 214, Issue 1, 2011, Pages 88-97

  Schwanz, Lisa ^a,b   Warner, Daniel A ^a   McGaugh, Suzanne ^a   Di Terlizzi, Roberta ^a,c   Bronikowski, Anne ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Comet analysis; Immune function; Phenotypic plasticity; Reproductive value; Somatic investment

Indexed keywords

HETEROPHILE ANTIBODY; PHYTOHEMAGGLUTININ;

AGE; AGGLUTINATION TEST; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BLOOD CELL COUNT; DNA REPAIR; ENERGY METABOLISM; FEMALE; HEMATOCRIT; HIBERNATION; IMMUNOLOGY; MALE; PHYSIOLOGY; SEASON; SEXUAL DEVELOPMENT; TURTLE;

AGE FACTORS; AGGLUTINATION TESTS; ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, HETEROPHILE; BLOOD CELL COUNT; DNA REPAIR; ENERGY METABOLISM; FEMALE; HEMATOCRIT; HIBERNATION; MALE; PHYTOHEMAGGLUTININS; SEASONS; SEX CHARACTERISTICS; TURTLES;

ANIMALIA; CHRYSEMYS; CHRYSEMYS PICTA; REPTILIA; TESTUDINES;

EID: 78651323224     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046813     Document Type: Article

References (70)

1. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B. and Sorci, G. (2004a). Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7, 363-368.
2. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Gaillard, M., Prost, J., Faivre, B. and Sorci, G. (2004b). An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am. Nat. 164, 651-659.
3. Alonso-Alvarez, C., Bertrand, S., Faivre, B. and Sorci, G. (2007). Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct. Ecol. 21, 873-879.
4. Baillie, S. R. and Prendergast, B. J. (2008). Photoperiodic regulation of behavioral responses to bacterial and viral mimetics: a test of the winter immunoenhancement hypothesis. J. Biol. Rhythms 23, 81-90.
5. Beckman, K. B. and Ames, B. N. (1998). The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
6. Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008). The dynamics of health in wild field vole populations: a haematological perspective. J. Anim. Ecol. 77, 984-997.
7. Bertrand, S., Criscuolo, F., Faivre, B. and Sorci, G. (2006). Immune activation increases susceptibility to oxidative tissue damage in zebra finches. Funct. Ecol. 20, 1022-1027.
8. Bilbo, S. D., Dhabhar, F. S., Viswanathan, K., Saul, A., Yellon, S. M. and Nelson, R. J. (2002). Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc. Natl. Acad. Sci. USA 99, 4067-4072.
9. Bronikowski, A. M. (2008). The evolution of aging phenotypes in snakes: a review and synthesis with new data. Age 30, 169-176.
10. Campbell, T. W. and Ellis, C. K. (2007). Avian and Exotic Animal Hematology and Cytology Third edition. Ames, IA: Blackwell Publishing Professional.
11. Cohen, A. A., McGraw, K. J., Wiersma, P., Williams, J. B., Robinson, W. D., Robinson, T. R., Brawn, J. D. and Ricklefs, R. E. (2008). Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am. Nat. 172, 178-193.
12. Congdon, J. D. and Tinkle, D. W. (1982). Reproductive energetic of the painted turtles (Chrysemys picta). Herpetologica 38, 228-237.
13. Congdon, J. D., Nagle, R. D., Kinney, O. M. and van Loben Sels, R. C. (2001). Hypotheses of aging in a long-lived vertebrate, Blanding's turtle (Emydoidea blandingii). Exp. Gerontol. 36, 813-827.
14. Congdon, J. D. R., Nagle, R. D., Kinney, O. M., van Loben Sels, R. C., Quinter, T. and Tinkle, D. W. (2003). Testing hypothesis of aging in long-lived painted turtles (Chrysemys picta). Exp. Gerontol. 38, 765-772.
15. Davis, A. K., Maney, D. L. and Maerz, J. C. (2008). The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct. Ecol. 22, 760-772.
16. Demas, G. E. (2004). The energetic of immunity: a neuroendocrine link between energy balance and immune function. Horm. Behav. 45, 173-180.
17. Derting, T. L. and Virk, M. K. (2005). Positive effects of testosterone and immunochallenge on energy allocation to reproductive organs. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 175, 543-556.
18. Ernst, C. H. (1972). Temperature-activity relationship in the painted turtles, Chrysemys picta. Copeia 1972, 217-222.
19. Ernst, C. H. and Lovich, J. E. (2009). Turtles of the United States and Canada, Second Edition. Baltimore, MD: Johns Hopkins University Press.
20. Finkel, T. and Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
21. Freitak, D., Ots, I., Vanatoa, A. and Hörak, P. (2003). Immune response is energetically costly in white cabbage butterfly pupae. Proc. R. Soc. Lond. B. Biol. Sci. 270, S220-S222.
22. Gibbons, J. W. (1968). Reproductive potential, activity, and cycles in the painted turtle, Chrysemys picta. Ecology 49, 399-409.
23. Gist, D. H., Michaelson, J. A. and Jones, J. M. (1990). Autumn mating in the painted turtle, Chrysemys picta. Herpetologica, 46, 331-336.
24. Harman, D. (1956). Aging: A theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
25. Harman, D. (1981). The aging process. Proc. Natl. Acad. Sci. USA 78, 7124-7128.
26. Hausmann, M. F., Winkler, D. W., Huntington, C. E., Vleck, D., Sanneman, C. E., Hanley, D. and Vleck, C. M. (2005). Cell-mediated immunosenescence in birds. Oecologia 145, 270-275.
27. Jacobson, E. R. (2007). Infectious Diseases and Pathology of Reptiles. Boca Raton, FL: CRC Press.
28. Kirkwood, T. B. L. and Rose, M. R. (1991). Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 332, 15-24.
29. Lee, K. A. (2006). Linking immune defense and life history at the levels of the individual and the species. Integr. Comp. Biol. 46, 1000-1015.
30. Les, H. L., Paitz, R. T. and Bowden, R. M. (2009). Living at extremes: development at the edges of viable temperature under constant and fluctuating conditions. Physiol. Biochem. Zool. 82, 105-112.
31. Love, O. P., Salvante, K. G., Dale, J. and Williams, T. D. (2008). Sex-specific variability in the immune system across life-history stages. Am. Nat. 172, E99-E112.
32. Madsen, T., Ujvari, B., Nandakumar, K. S., Hasselquist, D. and Holmdahl, R. (2007). Do "infectious" prey select for high levels of natural antibodies in tropical pythons? Evol. Ecol. 21, 271-279.
33. Martin, L. B., Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. Lond. B. Biol. Sci. 270, 153-158.
34. Martin, L. B., Han, P., Lewittes, J., Kuhlman, J. R., Klasing, K. C. and Wikelski, M. (2006). Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 20, 290-299.
35. Martin, L. B., Weil, Z. M. and Nelson, R. J. (2008). Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363, 321-339.
36. Matson, K. D., Ricklefs, R. E. and Klasing, K. C. (2005). A hemolysishemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29, 275-286.
37. McNamara, J. M. and Houston, A. I. (1996). State-dependent life histories. Nature 380, 215-221.
38. Merchant, M. and Britton, A. (2006). Characterization of serum complement activity of saltwater (Crocodylus porosus) and freshwater (Crocodylus johnstoni) crocodiles. Comp. Biochem. Physiol. 143 A, 488-493.
39. Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254-260.
40. Metcalfe, N. B. and Alonso-Alvarez, C. (2010). Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24, 984-996.
41. Moll, E. O. (1973). Latitudinal and intersubspecific variation in reproduction of the painted turtle, Chrysemys picta. Herpetologica 29, 307-318.
42. Muñoz, F. J. and De La Fuente, M. (2004). Seasonal changes in lymphoid distribution of the turtle Mauremys caspica. Copeia 2004, 178-183.
43. Nelson, R. J. and Demas, G. E. (1996). Seasonal changes in immune function. Q. Rev. Biol. 71, 511-548.
44. Nilsson, J.-A., Granbom, M. and Råberg, L. (2007). Does the strength of an immune response reflect its energetic cost? J. Avian Biol. 38, 488-494.
45. Ots, I., Kerimov, A. B., Ivankina, E. V., Ilyina, T. A. and Hõrak, P. (2001). Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. Lond. B. Biol. Sci. 268, 1175-1181.
46. Paitz, R. T., Gould, A. C., Holgersson, M. C. N. and Bowden, R. M. (2009). Temperature, phenotype, and the evolution of temperature-dependent sex determination: how do natural incubations compare to laboratory incubations? J. Exp. Zool. 314, 86-93.
47. Palacios, M. G., Cunnick, J. E., Winkler, D. W. and Vleck, C. M. (2007). Immunosenescence in some but not all immune components in a free-living vertebrate, the tree swallow. Proc. R. Soc. Lond. B. Biol. Sci. 274, 951-957.
48. Palacios, M. G., Cunnick, J. E., Vleck, D. and Vleck, C. M. (2009). Ontogeny of innate and adaptive immune defesnse components in free-living tree swallows, Tachycineta bicolor. Dev. Comp. Immunol. 33, 456-463.
49. Patnaik, B. K. (1994). Ageing in reptiles. Gerontology 40, 200-220.
50. Pitol, D. L., Issa, J. P. M., Caetano, F. H. and Lunardi, L. O. (2008). Radiographic stuffy of the seasonal distribution of leucocytes in turtles Phrynops hilarii (Chelona Chelidae). Micron 39, 1381-1386.
51. Prendergast, B. J., Freeman, D. A., Zucker, I. and Nelson, R. J. (2002). Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1054-R1062.
52. Robert, K. and Bronikowski, A. M. (2010). Evolution of senescence: physiological evolution in natural populations of the garter snake with divergent life history ecotypes. Am. Nat. 175, 147-159.
53. Robert, K., Rossini, A. K. and Bronikowski, A. M. (2007). Testing the free radical theory of aging hypothesis: physiological differences in long lived and short lived Colubrid snakes. Aging Cell 6, 395-404.
54. Rosskopf, W. J. (1982). Normal hemogram and blood chemistry values for California desert tortoises. Vet. Med. Small Anim. Clin. 77, 85-87.
55. Saad, A. H. and El Ridi, R. (1988). Endogenous corticosteroids mediate seasonal cyclic changes in immunity in lizards. Immunobiology 177, 390-403.
56. Schall, J. J., Bennett, A. F. and Putnam, R. W. (1982). Lizards infected with malaria: physiological and behavioral consequences. Science 217, 1057-1059.
57. Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
58. Sparkman, A. M. and Palacios, M. G. (2009). A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans. J. Anim. Ecol. 78, 1242-1248.
59. Sparkman, A., Arnold, S. J. and Bronikowski, A. M. (2007). An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophiselegans. Proc. R. Soc. Lond. B. Biol. Sci. 274, 943-950.
60. Tice, R. R. (1995). The single cell gel/comet assay: a microgel electrophoretic technique for the detection of DNA damage and repair in individual cells. In Environmental Mutagenesis (ed. D. H. Phillips and S. Venitt), pp. 315-339. Oxford: Bios Scientific.
61. Tizard, I. R. (2004). Veterinary Immunology: an Introduction, 7th edn. Elsevier.
62. Ungvari, Z., Krasnikov, B. F., Csiszar, A., Labinskyy, N., Mukhopadhyay, P., Pacher, P., Cooper, A. J. L., Podlutskaya, N., Austad, S. M. and Podlutsky, A. (2008). Testing hypotheses of aging in long-lived mice of the genus Peromyscus: association between longevity and mitochondrial stress resistance, ROS detoxification pathways, and DNA repair efficiency. Age 30, 121-133.
63. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. and Wittzell, H. (1999). Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B. Biol. Sci. 266, 1-12.
64. Wilbur, H. M. (1975a). A growth model for the turtle Chrysemys picta. Copeia 1975, 337-343.
65. Wilbur, H. M. (1975b). The evolutionary and mathematical demography of the turtle Chrysemys picta. Ecology 56, 64-77.
66. Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398-411.
67. Williams, G. C. (1966). Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100, 687-690.
68. Zapata, A. G., Varas, A. and Torroba, M. (1992). Seasonal variations in the immune system of lower vertebrates. Immunol. Today 13, 142-147.
69. Zimmerman, L. M., Paitz, R. T., Vogel, L. A. and Bowden, R. M. (2010). Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta). J. Exp. Biol. 213, 1477-1483.
70. Zuk, M. and Stoehr, A. M. (2002). Immune defense and host life history. Am. Nat. 160, S9-S22.