Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta)

Journal of Experimental Biology

Volumn 213, Issue 9, 2010, Pages 1477-1483

  Zimmerman, Laura M ^a   Paitz, Ryan T ^a   Vogel, Laura A ^a   Bowden, Rachel M ^a  

^a ILLINOIS STATE UNIVERSITY   (United States)

Author keywords

Ectotherm; Immunocompetence; Seasonal

Indexed keywords

ADAPTIVE IMMUNITY; ANIMAL; ARTICLE; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; MALE; SEASON; TURTLE;

ADAPTIVE IMMUNITY; ANIMALS; FEMALE; IMMUNITY, INNATE; MALE; SEASONS; TURTLES;

GNATHOSTOMATA (VERTEBRATE); REPTILIA; TESTUDINES; TRACHEMYS SCRIPTA; TRACHEMYS SCRIPTA ELEGANS; VERTEBRATA;

EID: 77951613117     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.037770     Document Type: Article

References (75)

1. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9, 467-484.
2. Baumgarth, N., Tung, J. W. and Herzenberg, L. A. (2005). Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Sem. Immunopathol. 26, 347-362.
3. Behnke, J. M. and Barnard, C. J. (1990). Coevolution of parasites and hosts: hostparasite arms races and their consequences. In Parasites: Immunity and Pathology (ed. J. M. Behnke), pp. 1-22. Bristol, PA: Taylor and Francis.
4. Benatuil, L., Kaye, J., Cretin, N., Godwin, J. G., Cariappa, A., Pillai, S. and Iacomini, J. (2008). Ig knock-in mice producing anti-carbohydrate antibodies: breakthrough of B cells producing low affinity anti-self antibodies. J. Immunol. 180, 3839-3848.
5. Bentley, G. E. (2001). Unraveling the enigma: The role of melatonin in seasonal processes in birds. Microsc. Res. Tech. 53, 63-71.
6. Blount, J. D., Houston, D. C., Møller, A. P. and Wright, J. (2003). Do individual branches of immune defense correlate? A comparative case study of scavenging and non-scavenging birds. OIKOS 102, 340-350.
7. Bouman, A., Heineman, M. J. and Faas, M. M. (2005). Sex hormones and the immune response in humans. Hum. Reprod. Update 11, 411-423.
8. Bourgeon, S. and Raclot, T. (2006). Corticosterone selectively decreases humoral immunity in female eiders during incubation. J. Exp. Biol. 209, 4957-4965.
9. Buehler, D. M., Piersma, T., Matson, K. and Tieleman, B. I. (2008). Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime. Amer. Nat. 172, 783-796.
10. Candore, G., Lorenzo, G. D., Mansueto, P., Melluso, M., Frada, G., Vecchi, M. L., Pellitteri, M. E., Drago, A., Salvo, A. D. and Caruso, C. (1997). Prevalence of organ-specific and non organ-specific autoantibodies in healthy centenarians. Mech. Aging Dev. 94, 183-190.
11. Coico, R., Sunshine, G. and Benjamini, E. (2003). Immunology, A Short Course. New York: Wiley-Liss Publications.
12. Dowell, S. F. (2001). Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerg. Infect. Diseases 9, 369-373.
13. El Ridi, R., Badir, N. and El Rouby, S. (1981). Effect of seasonal variations on the immune system of the snake, Psammophis schokari. J. Exp. Zool. 216, 357-365.
14. El Ridi, R., Wahby, A. F., Saad, A. H. and Soliman, M. A. W. (1987). Concanavalin A responsiveness and interleukin 2 production in the snake Spalersophis diadema. Immunobiology, 174, 177-189.
15. Ernst, C. H., Lovich, J. E. and Barbour, R. W. (1994). Turtles of the United States and Canada. Washington, D.C.: Smithsonian Institution Press.
16. Fairbrother, A., Smits, J. and Grasman, K. A. (2004). Avian Immunotoxicology. J. Toxicol. Environ. Health B 7, 105-137.
17. Farag, M. A. and El Ridi, R. (1984). Mixed leucocyte reaction (MLR) in the snake Psammophis sibilans. Immunology 55, 173-181.
18. Forsman, A. M., Vogel, L. A., Sakaluk, S. K., Grindstaff, J. L. and Thompson, C. F. (2008). Immune-challenged house wren broods differ in the relative strengths of their responses among different axes of the immune system. J. Evol. Biol. 21, 873-878.
19. Frasca, D., Landin, A. M., Riley, R. L. and Blomberg, B. B. (2008). Mechanisms for decreased function of B cells in aged mice and humans. J. Immunol. 180, 2741-2746.
20. Gibbons, J. W. (1990). The slider turtle. In Life History and Ecology of the Slider Turtle (ed. J. W. Gibbons), pp. 3-18. Washington, D.C.: Smithsonian Institution Press.
21. Gibbons, J. W., Semlitsch, R. D., Greene, J. L. and Schubauer, J. P. (1981). Variation in age and size at maturity of the slider turtle (Pseudemys scripta). Am. Nat. 117, 841-845.
22. Gomez, C. R., Nomellini, V., Faunce, D. E. and Kovacs, E. J. (2008). Innate immunity and aging. Exp. Gerontol. 43, 718-728.
23. Grey, H. (1963). Phylogeny of the immune response: Studies on some physical, chemical, and serologic characteristics of antibody produced in the turtle. J. Immunol. 91, 819-825.
24. Gulland, F. M. D. (1995). Impact of infectious diseases on wild animal populations: a review. In Ecology of Infectious Diseases in Natural Populations (ed. B. T. Grenfell and A. P. Dobson), pp. 20-51. New York, NY: Cambridge University Press.
25. Haussmann, 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.
26. Holgersson, M. C. N. (2009). Turtles and Salmonella: Consequences of coexistence. M.S. thesis, Illinois State University, Normal, IL.
27. Hrubec, T. C., Robertson, J. L., Smith, S. A. and Tinker, M. K. (1996). The effect of temperature and water quality on antibody response to Aeromonas salmonicida in sunshine bass (Morone chrysops × Morone saxatilis). Vet. Immunol. Immunopathol. 50, 157-166.
28. Hussein, M. F., Badir, N., El Ridi, R. and Akef, M. (1978). Effect of seasonal variation on lymphoid tissues of the lizards, Mabuya Quinquetaeniata licht and Uromastyx aegyptia forsk. Dev. Comp. Immunol. 2, 469-478.
29. Hussein, M. F., Badir, N., El Ridi, R. and El Deeb, S. (1979). Effect of seasonal variation on immune system of the lizard, Scincus scincus. J. Exp. Zool. 209, 91-96.
30. Ingram, G. A. and Molyneux, D. H. (1983). The humoral immune response of the spiny-tailed agamid lizard (Agama Caudospinosum) to injection with Leishmania agamae promastigotes. Vet. Immunol. Immunopathol. 4, 479-491.
31. Jackson, J. A. and Tinsley, R. C. (2002). Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis (Monogenea). Parasitol. Res. 88, 632-638.
32. Kanakambika, P. and Muthukkaruppan, V. R. (1972). The immune response to sheep erythrocytes in the lizard Calotes versicolor. J. Immunol. 109, 415-420.
33. Kaufmann, S. H. E., Sher, A. and Ahmed, R. (2002). Immunology of Infectious Diseases. Washington D.C.: ASM Press.
34. Klein, S. L. (2000). Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav. Process. 51, 149-166.
35. Kruman, I. I. (1992). Comparative analysis of cell replacement in hibernators. Comp. Biochem. Physiol. 101A, 11-18.
36. Lavoie, E. T. (2006). Avian immunosenescence. Age 27, 281-285.
37. Lavoie, E. T., Sorrell, E. M., Perez, D. R. and Ottinger, M. A. (2007). Immunosenescence and age-related susceptibility to influenza virus in Japanese quail. Dev. Comp. Immunol. 31, 407-414.
38. Le Morvan, C., Troutaud, D. and Deschaux, P. (1998). Differential effects of temperature on specific and nonspecific immune defenses in fish. J. Exp. Biol. 201, 165-168.
39. Lee, K. A. (2006). Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 46, 1000-1015.
40. Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-89.
41. Longenecker, B. M. and Mosmann, T. R. (1980). "Natural" antibodies to chicken MHC antigens are present in mice, rats, humans, alligators, and allogeneic chickens. Immunogenetics 11, 293-302.
42. Lutterschmidt, D. I., Lutterschmidt, W. I. and Hutchison, V. H. (2003). Melatonin and thermoregulation in ectothermic vertebrates: a review. Can. J. Zool. 81, 1-13.
43. 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.
44. Maniero, G. D. and Carey, C. (1997). Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. J. Comp. Physiol. B 167, 256-263.
45. Marchalonis, J. J., Ealey, E. H. M. and Diener, E. (1969). Immune response of the tuatara, Sphenodon punctatum. Aust. J. Exp. Biol. Med. Sci. 47, 367-380.
46. Martin, L. B., Han, P., Lewittes, J., Huhlman, J. R., Klasings, K. C. and Wikelski, M. (2006). Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 20, 290-299.
47. 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.
48. McEwen, B. S., Biron, C. A., Brunson, K. W., Bulloch, K., Chambers, W. H., Dhabhar, F. S., Boldfarb, R. H., Kitson, R. P., Miller, A. H., Spencer, R. L. et al. (1997). The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res. Rev. 23, 79-133.
49. McGlauchlen, K. S. and Vogel, L. A. (2003). Ineffective humoral immunity in the elderly. Microb. Infect. 5, 1279-1284.
50. Medzhitov, R. and Janeway, C. Jr (2000). Innate immunity. N. Engl. J. Med. 343, 338-344.
51. Merchant, M. and Britton, A. (2006). Characterization of serum complement activity of saltwater (Crocodylus porosus) and freshwater (Crocodylus johnstoni) crocodiles. Comp. Biochem. Physiol. A 143, 488-493.
52. Merchant, M., Roche, C., Elsey, R. M. and Prudhomme, J. (2003). Antibacterial properties of serum from the American alligator (Alligator mississippiensis). Comp. Biochem. Physiol. B 136, 505-513.
53. Mikkelsen, H., Lindenstrom, T. and Nielsen, M. E. (2006). Effects of temperature on production and specificity of antibodies in rainbow trout (Oncorhynchus mykiss). J. World Aquac. Soc. 37, 518-522.
54. Mondal, S. and Rai, U. (2001). In vitro effect of temperature on phagocytic and cytotoxic activities of splenic phagocytes of the wall lizard, Hemidactylus flaviviridis. Comp. Biochem. Physiol. A 129, 391-398.
55. Muñoz, F. J. and De la Fuente, M. (2001). The effect of the seasonal cycle on the splenic leukocyte functions in the turtle Mauremys caspica. Physiol. Biochem. Zool. 74, 660-667.
56. Muñoz, F. J., Galván, A., Lerma, M. and De la Fuente, M. (2000). Seasonal changes in peripheral blood leukocyte functions of the turtle Mauremys caspica and their relationship with corticosterone, 17-β-estradiol and testosterone serum levels. Vet. Immunol. Immunopathol. 77, 27-42.
57. Muñoz, F. J., Estrada-Parra, S., Romero-Rojas, A., Work, T. M., Gonzalez-Ballesteros, E. and Estrada-Garcia, I. (2009). Identification of CD3+ T lymphocytes in the green turtle Chelonia mydas. Vet. Immunol. Immunopathol. 131, 211-217.
58. Nelson, R. J. (2004). Seasonal immune function and sickness responses. Trends Immunol. 25, 187-192. (Pubitemid 38368166)
59. Nelson, R. J. and Demas, G. E. (1996). Seasonal patterns of stress, disease, and sickness responses. Curr. Dir. Psychol. Sci. 13, 198-202.
60. Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26.
61. Ochsenbein, A. F. and Zinkernagel, R. M. (2000). Natural antibodies and complement link innate and acquired immunity. Immunol. Today 21, 624-630.
62. Origgi, F. C., Klein, P. A., Mathes, K., Blahak, S., Marschang, R. E., Tucker, S. J. and Jacobson, E. R. (2001). Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in Mediterranean tortoises (spur-thighed tortoise [Testudo graeca] and Hermann's tortoise [Testuto hermanni]). J. Clin Microbiol. 39, 3156-3163.
63. 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.
64. Pye, G. W., Brown, D. R., Nogueira, M. F., Vliet, K. A., Schoeb, T. R. and Bennett, R. A. (2001). Experimental inoculation of broad-nosed caimans (Caiman latirostris) and Siamese crocodiles (Crocodyllus siamensis) with Mycoplasma alligatoris. J. Zoo. Wildl. Med. 32, 196-201.
65. Raffel, T. R., Rohr, J. R., Kiesecker, J. M. and Hudson, P. J. (2006). Negative effects of changing temperature on amphibian immunity under field conditions. Func. Ecol. 20, 819-828.
66. Rolff, J. (2001). Effects of age and gender on immune function of dragonflies (Odonata, Lestidae) from a wild population. Can. J. Zool. 79, 2176-2180.
67. Saino, N., Bolzern, A. M. and Møller, A. P. (1997). Immunocompetence, ornamentation, and viability of male barn swallows (Hirundo rustica). Proc. Natl. Acad. Sci. 94, 549-552.
68. Shelby, J. A., Mendonça, M. T., Horne, B. D. and Seigel, R. A. (2000). Seasonal variation in reproductive steroids of male and female yellow-blotched map turtles, Graptemys flavimaculata. Gen. Comp. Endocrinol. 119, 43-51.
69. 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.
70. Sunyer, J. O. and Lambris, J. D. (1998). Evolution and diversity of the complement system of poikilothermic vertebrates. Immunol. Rev. 166, 39-57.
71. Taub, D. D. and Longo, D. L. (2005). Insights into thymic aging and regeneration. Immuno. Rev. 205, 72-93.
72. Tieleman, B. I., Williams, J. B., Ricklefs, R. E. and Klasing, K. C. (2005). Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. R Soc. Lond., B, Biol. Sci. 272, 1715-1720.
73. Ujvari, B. and Madsen, T. (2005). Age, parasites, and condition affect humoral immune response in tropical pythons. Behav. Ecol. 17, 20-24.
74. Wilbur, H. M. (1975). A growth model for the turtle, Chrysemys picta. Copeia 1975, 337-343.
75. Zapata, A. G., Varas, A. and Torroba, M. (1992). Seasonal variations in the immune system of lower vertebrates. Immunol. Today 13, 142-147.