Corticosterone suppresses immune activity in territorial Galápagos marine iguanas during reproduction

Hormones and Behavior

Volumn 47, Issue 4, 2005, Pages 419-429

  Berger, Silke ^a   Martin II, Lynn B ^b   Wikelski, Martin ^b   Romero, L Michael ^c   Kalko, Elisabeth K V ^a   Vitousek, Maren N ^b   Rödl, Thomas ^b  

^a UNIVERSITY OF ULM   (Germany)

^b PRINCETON UNIVERSITY   (United States)

^c TUFTS UNIVERSITY   (United States)

Author keywords

Corticosterone; Iguana; Immunocompetence; Phytohemagglutinin; Resource allocation; Testosterone; Trade off

Indexed keywords

CORTICOSTERONE; PHYTOHEMAGGLUTININ; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; BODY CONSTITUTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EDEMA; HEMATOCRIT; HORMONAL REGULATION; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOCOMPETENCE; LIZARD; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTION; SEXUAL BEHAVIOR; SKIN TEST; TERRITORIALITY; TESTOSTERONE BLOOD LEVEL;

EID: 15044344733     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2004.11.011     Document Type: Article

References (88)

1. W.B. Amand Avian Clinical Hematology and Blood Chemistry 1986 Saunders Philadelphia
2. V. Apanius Stress and immune defense A.P. Moller M. Milinski P.J.B. Slater Stress and Behavior 1998 Academic Press San Diego 133 153
3. L.D. Beletsky, G.H. Orians, and J.C. Wingfield Relationships of steroid hormones and polygyny to territorial status breeding experience and reproductive success in male red-winged blackbirds Auk 106 1989 107 117
4. S.D. Bilbo, F.S. Dhabhar, K. Viswanathan, A. Saul, S.M. Yellon, and R.J. Nelson Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function Proc. Natl. Acad. Sci. U. S. A. 99 2002 4067 4072
5. S. Braude, Z. Tang-Martinez, and G.T. Taylor Stress, testosterone, and the immunoredistribution hypothesis Behav. Ecol. 10 1999 333 350
6. C.W. Breuner, and M. Orchinik Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain J. Neuroendocrinol. 13 2001 412 420
7. C.C. Carpenter The marine iguana of the Galápagos islands, its behavior and ecology Proc. Calif. Acad. Sci. 34 1966 329 376
8. J.M. Casto, Jr. Val Nolan, and E.D. Ketterson Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis) Am. Nat. 157 2001 408 420
9. M.A. Chappell, M. Zuk, T.S. Johnsen, and T.H. Kwan Mate choice and aerobic capacity in red junglefowl Behaviour 134 1997 511 529
10. M. Cucco, R. Ottonelli, M. Raviola, and G. Malacarne Variations of body mass and immune function in response to food unpredictability in magpies Acta Oecol. 23 2002 271 276
11. Dellinger, T., 1991. Aufwand, Kosten und Nutzen der Fortpflanzung bei Meerechsen (Amblyrhynchus cristatus). Dissertation. University Munich.
12. G.E. Demas, V. Chefer, M.I. Talan, and R.J. Nelson Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice Am. J. Physiol. 273 1997 1631 1637
13. F.S. Dhabhar, and B.S. McEwen Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking Brain Behav. Immun. 11 1997 286 306
14. F.S. Dhabhar, A.H. Miller, B.S. McEwen, and R.L. Spencer Effects of stress on immune cell distribution: dynamics and hormonal mechanisms J. Immunol. 154 1995 5511 5527
15. D.L. Duffy, G.E. Bentley, D.L. Drazen, and G.F. Ball Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings Behav. Ecol. 11 2002 654 662
16. I. Eibl-Eibesfeldt The fighting of the marine iguanas Philos. Trans. R. Soc., B 251 1966 475 476
17. S.B. Emerson Male advertisement calls: behavioral variation and physiological processes M.J. Ryan Anuran Communication 2001 Smithsonian Institution Press Washington, DC 36 44
18. M.R. Evans, A.R. Goldsmith, and S.R.A. Norris The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus) Behav. Ecol. Sociobiol. 47 2000 156 163
19. J.T. Fitzsimons, and S. Kaufman Cellular and extracellular dehydration and angiotensin as stimuli to drinking in the common iguana (Iguana iguana) J. Physiol. 265 1977 443 463
20. I. Folstad, and A.J. Karter Parasites, bright males, and the immunocompetence handicap Am. Nat. 139 1992 603 622
21. N. Goto, H. Kodoma, K. Okada, and Y. Fujimoto Suppression of phytohemagglutinin skin response in thymectomized chickens Poultry Sci. 57 1978 246 250
22. W. Goymann, and J.C. Wingfield Allostatic load, social status and stress hormones: the costs of social status matter Anim. Behav. 67 2004 591 602
23. M. Grassman, and D.L. Hess Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: II. Responses to acute stress in the laboratory J. Exp. Zool. 264 1992 183 188
24. N. Greenberg, and J.C. Wingfield Stress and reproduction: reciprocal relationships D.O. Norris R.E Jones Hormones and Reproduction in Fishes, Amphibians, and Reptiles 1987 Plenum Press New York 461 503
25. N. Greenberg, T. Chen, and D. Crews Social status, gonadal state, and the adrenal stress response in the lizard Anolis carolinensis Horm. Behav. 18 1984 1 11
26. C.G. Greenman, L.B. Martin II, and M. Hau Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus) Physiol. Biochem. Zool. 78 2005 (in press)
27. L.J. Guillete, A. Cree, and A.A. Rooney Biology of stress: interactions with reproduction, immunology, and intermediary metabolism C. Warwick F.L. Frye J.B. Murphy Health and Welfare of Captive Reptiles 1995 Chapman and Hall New York 32 70
28. L. Gustafsson, A. Qvarnstrom, and B.C. Sheldon Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers Nature 375 1995 311 313
29. G. Haggag, M.E.-H. Mohammed, and R. Hassan Seasonal variation of hematocrit value and erythrocyte sedimentation rate in the hibernating desert reptile Varanus griseus B Fac. Sci. Cairo 1974 205 212
30. W.D. Hamilton, and M. Zuk Heritable true fitness and bright birds a role for parasites? Science 218 1982 384 387
31. S.A. Hanssen, D. Hasselquist, I. Folstad, and K.E. Erikstad Costs of immunity: immune responsiveness reduces survival in a vertebrate Proc. R. Soc., B 271 2004 (online)
32. D. Hasselquist, J.A. Marsh, P.W. Sherman, and J.C. Wingfield Is avian humoral immunocompetence suppressed by testosterone? Behav. Ecol. Sociobiol. 45 1999 167 175
33. N. Hillgarth, and J.C. Wingfield Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection N.E. Beckage Parasites and Pathogens: Effects on Host Hormones and Behavior 1997 Chapman and Hall New York 143 155
34. D.H. Jennings, M.C. Moore, R. Knapp, L. Matthews, and M. Orchinik Plasma steroid-binding globulin mediation of differences in stress reactivity in alternative male phenotypes in tree lizards, Urosaurus ornatus Gen. Comp. Endocrinol. 120 2000 289 299
35. A.S. Kitaysky, J.C. Wingfield, and J.F. Piatt Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes Funct. Ecol. 13 1999 577 584
36. W.A. Laurie Effects of the 1982-83 El Niño-Southern Oscillation event on marine iguana (Amblyrhynchus cristatus) populations in the Galápagos islands P. Glynn Global Ecological Consequences of the 1982-83 El Niño-Southern Oscillation 1989 Elsevier New York 121 141
37. K.M. Lindström, D. Krakower, J.O. Lundström, and B. Silverin The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): an experimental test of the immunocompetence-handicap hypothesis Proc. R. Soc., B 268 2001 207 211
38. R.L. Lochmiller, and C. Deerenberg Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88 2000 87 98
39. C. Manzo, M. Zerani, A. Gobbetti, F.M.M. Di, and F. Angelini Is corticosterone involved in the reproductive processes of the male lizard, Podarcis sicula sicula Horm. Behav. 28 1994 117 129
40. L.B. Martin, A. Scheuerlein, and M. Wikelski Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. B. 270 2003 153 158
41. B.S. McEwen, and J.C. Wingfield The concept of allostasis in biology and biomedicine Horm. Behav. 43 2003 2 15
42. I.T. Moore, and T.S. Jessop Stress, reproduction, and adrenocortical modulation in amphibians and reptiles Horm. Behav. 43 2003 39 47
43. M.C. Moore, C.W. Thompson, and C.A. Marler Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard Urosaurus ornatus Gen. Comp. Endocrinol. 81 1991 217 226
44. I.T. Moore, J.P. Lerner, D.T. Lerner, and R.T. Mason Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus Physiol. Biochem. Zool. 73 2000 307 312
45. M.C. Moore, D. Painter, S.K. Woodley, E.L. Lacy, D.H. Jennings, and M. Wikelski Neuroendocrine mechanisms of alternative male reproductive tactics in marine iguanas Am. Zool. 40 2000 1137
46. L.A. Morici, R.M. Elsey, and V.A. Lance Effect of long-term corticosterone implants on growth and immune function in juvenile alligators, Alligator mississippiensis J. Exp. Zool. 279 1997 156 162
47. F. Munoz, A. Galvan, M. Lerma, and M. De la Fuente Seasonal changes in peripheral blood leukocyte functions of the turtle Mauremys caspica and their relationship with corticosterone, 17-beta-estradiol and testosterone serum levels Vet. Immunol. Immunop. 77 2000 27 42
48. Nelson, K., 2003. Testing the relative plasticity hypothesis in a lekking lizard with alternative mating strategies. Dissertation. University of Illinois.
49. R.J. Nelson, and G.E. Demas Seasonal changes in immune function Q. Rev. Biol. 71 1996 511 548
50. R.J. Nelson, and S.L. Klein Environmental and social influences on seasonal breeding and immune function K. Wallen J.E. Schneider Reproduction in context 2000 MIT Press Cambridge 219 256
51. M. Olsson, E. Wapstra, T. Madsen, and B. Silverin Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards Proc. R. Soc., B 267 2000 2339 2343
52. J. Partecke, A. von Haeseler, and M. Wikelski Territory establishment in lekking marine iguanas, Amblyrhynchus cristatus: support for the hotshot mechanism Behav. Ecol. Sociobiol. 51 2002 579 587
53. A. Peters Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free living males with high testosterone are more immunocompetent Proc. R. Soc., B 276 2000 883 889
54. A. Poiani, A.R. Goldsmith, and M.R. Evans Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model Behav. Ecol. Sociobiol. 47 2000 230 242
55. J. Potti, J. Moreno, S. Merino, O. Frias, and R. Rodriguez Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca Oecologia 120 1999 1 8
56. L. Råberg, M. Grahn, D. Hasselquist, and E. Svensson On the adaptive significance of stress-induced immunosuppression Proc. R. Soc., B 265 1998 1637 1641
57. L. Råberg, J.-A. Nilsson, P. Ilmonen, M. Stjernman, and D. Hasselquist The cost of an immune response: vaccination reduces parental effort Ecol. Lett. 3 2000 382 386
58. M.C. Rigby, and Y. Moret Life-history trade-offs with immune defense R. Poulin S. Morand A. Skorping Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality 2000 Elsevier Science B. V. New York 129 142
59. L.M. Romero Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates Gen. Comp. Endocrinol. 128 2002 1 24
60. L.M. Romero, and M. Wikelski Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events Proc. Natl. Acad. Sci. U. S. A. 98 2001 7366 7370
61. A.H. Saad, and R. El Ridi Endogenous corticosteroids mediate seasonal cyclic changes in immunity of lizards Immunobiology 177 1988 390 403
62. A.H. Saad, R.E. Ridi, S.E. Deeb, and M.A.W. Soliman Effect of hydrocortisone on immune system of the lizard Chalcides ocellatus. Effect on cellular and humoral immune responses Dev. Comp. Immunol. 10 1986 235 246
63. A.H. Saad, N.A. Khalek, and R.E. Ridi Blood testosterone level a season-dependent factor regulating immune reactivity in lizards Immunobiology 180 1990 184 194
64. N. Saino, A.P. Møller, and A.M. Bolzern Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis Behav. Ecol. 6 1995 397 404
65. A. Salvador, J.P. Veiga, J. Martin, P. Lopez, M. Abelenda, and M. Puerta The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation Behav. Ecol. 7 1996 145 150
66. R.M. Sapolsky Neuroendocrinology of the stress-response J.U.B. Becker S.M. Breedlove D. Crews Behavioral Endocrinology 1992 MIT Press Cambridge, MA 287 324
67. B.C. Sheldon, and S. Verhulst Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology Trends Ecol. Evol. 11 1996 317 321
68. E. Svensson, B. Sinervo, and T. Comendant Density-dependent competition and selection on immune function in genetic lizard morphs Proc. Natl. Acad. Sci. U. S. A. 98 2001 12561 12565
69. E.M. Tarlow, M. Hau, D.J. Anderson, and M. Wikelski Diel changes in plasma melatonin and corticosterone concentrations in tropical Nazca boobies (Sula granti) in relation to moon phase and age Gen. Comp. Endocrinol. 133 2003 297 304
70. R.R. Tokarz Effects of corticosterone treatment on male aggressive behavior in a lizard Anolis sagrei Horm. Behav. 21 1987 358 370
71. K.G.K. Trillmich The mating system of the marine iguana Amblyrhynchus cristatus Z. Tierpsychol. 63 1983 141 172
72. F. Trillmich, and K.G.K. Trillmich The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny Biol. J. Linn. Soc. 21 1984 209 216
73. S. Verhulst, S.J. Dieleman, and H.K. Parmentier A tradeoff between immunocompetence and sexual ornamentation in domestic fowl P. Natl. Acad. Sci. U. S. A. 96 1999 4478 4481
74. M. Wikelski, and S. Baeurle Pre-copulatory ejaculation solves time constraints during copulations in marine iguanas Proc. R. Soc., B 263 1996 439 444
75. M. Wikelski, and M. Hau Is there an endogenous tidal foraging rhythm in marine iguanas? J. Biol. Rhythms 10 1995 335 350
76. M. Wikelski, and F. Trillmich Foraging strategies of the Galapagos marine iguana (Amblyrhynchus cristatus): adapting behavioral rules to ontogenetic size change Behaviour 128 1994 255 279
77. M. Wikelski, B. Gall, and F. Trillmich Ontogenetic changes in food intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus) Oecologia 94 1993 373 379
78. M. Wikelski, C. Carbone, and F. Trillmich Lekking in marine iguanas: female grouping and male reproductive strategies Anim. Behav. 52 1996 581 596
79. M. Wikelski, C. Carbone, P.A. Bednekoff, S. Choudhury, and S. Tebbich Why is female choice not unanimous? Insights from costly mate sampling in marine iguanas Ethology 107 2001 623 638
80. M. Wikelski, S.S. Steiger, B. Gall, and K.N. Nelson Sex, drugs and mating role: testosterone-induced phenotype-switching in Galápagos marine iguanas Behav. Ecol. 16 2005 260 268
81. J.C. Wingfield Modulation of the adrenocortical response to stress in birds K.G. Davey R.E. Peter S.S. Tobe Perspectives in Comparative Endocrinology 1994 National Research Council of Canada Ottawa 520 528
82. J.C. Wingfield, and D. Farner The determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding Steroids 26 1975 311 327
83. J.C. Wingfield, R.F. Hegner, A.M.J. Dufty, and G.F. Ball The challenge hypothesis theoretical implications for patterns of testosterone secretion mating systems and breeding strategies Am. Nat. 136 1990 829 846
84. J.C. Wingfield, C.M. Vleck, and M.C. Moore Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert J. Exp. Zool. 264 1992 419 428
85. J.C. Wingfield, D.L. Maney, C.W. Breuner, J.D. Jacobs, S. Lynn, M. Ramenofsky, and R.D. Richardson Ecological bases of hormone-behavior interactions: the "emergency life history stage" Am. Zool. 38 1998 191 206
86. S.K. Woodley, D.L. Painter, M.C. Moore, M. Wikelski, and L.M. Romero Effect of tidal cycle and food intake on the baseline corticosterone rhythm in intertidally foraging marine iguanas Gen. Comp. Endocrinol. 132 2003 216 222
87. M. Zuk, and T.S. Johnsen Social environment and immunity in male red jungle fowl Behav. Ecol. 11 2000 146 153
88. M. Zuk, T.S. Johnsen, and T. Maclarty Endocrine-immune interactions, ornaments and mate choice in red jungle fowl Proc. R. Soc., B 260 1995 205 210