Geographic variation in timekeeping systems among three populations of garter snakes (Thamnophis sirtalis) in a common garden

Physiological and Biochemical Zoology

Volumn 81, Issue 6, 2008, Pages 810-825

  Lutterschmidt, Deborah I ^a,b   Mason, Robert T ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; MELATONIN;

COURTSHIP; ENVIRONMENTAL CHANGE; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL CUE; GARDEN; GEOGRAPHICAL VARIATION; INTERPOPULATION VARIATION; PHYSIOLOGICAL RESPONSE; REPRODUCTIVE BEHAVIOR; SNAKE;

ACCLIMATIZATION; ANIMAL; ARTICLE; BLOOD; CIRCADIAN RHYTHM; ECOSYSTEM; FEMALE; HIBERNATION; MALE; PHOTOPERIODICITY; PHYSIOLOGY; SEASON; SEXUAL BEHAVIOR; SNAKE;

ACCLIMATIZATION; ANIMALS; CIRCADIAN RHYTHM; COLUBRIDAE; CORTICOSTERONE; ECOSYSTEM; FEMALE; HIBERNATION; MALE; MELATONIN; PHOTOPERIOD; SEASONS; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; THAMNOPHIS; THAMNOPHIS SIRTALIS; THAMNOPHIS SIRTALIS CONCINNUS; THAMNOPHIS SIRTALIS PARIETALIS; THAMNOPHIS SIRTALIS SIRTALIS;

EID: 55549096364     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/589900     Document Type: Article

References (95)

1. Aleksiuk M. and P.T. Gregory. 1974. Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 1974:681-689.
2. Axelrod J. 1974. The pineal gland: a neurochemical transducer. Science 184:1341-1348.
3. Benshoff H.M., G.C. Brainard, M.D. Rollag, and G.R. Lynch. 1987. Suppression of pineal melatonin in Peromyscus leucopus by different monochromatic wavelengths of visible and nearultraviolet light (UV-A). Brain Res 420:397-402.
4. Bittman E.L., R.J. Demsey, and F.J. Karsch. 1983. Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113:2276-2283.
5. Bona-Gallo A. and P. Licht. 1983. Effect of temperature on sexual receptivity and ovarian recrudescence in the garter snake, Thamnophis sirtalis parietalis. Herpetologica 39:173-182.
6. Brown J.L., S.-H. Li, and N. Bhagabati. 1999. Long-term trend toward earlier breeding in an American bird: a response to global warming? Proc Natl Acad Sci USA 96:5565-5569.
7. Cagnoli C.M., C. Atabay, E. Kharlamova, and H. Manev. 1995. Melatonin protects neurons from singlet oxygen-induced apoptosis. J Pineal Res 18:222-226.
8. Camazine B., W. Garstka, R. Tokarz, and D. Crews. 1980. Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Horm Behav 14:358-372.
9. Carter D.S. and B.D. Goldman. 1983. Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter. Endocrinology 113:1261-1267.
10. Cease A.J., D.I. Lutterschmidt, and R.T. Mason. 2007. Corticosterone and the transition from courtship behavior to dispersal in male red-sided garter snakes (Thamnophis sirtalis parietalis). Gen Comp Endocrinol 150:124-131.
11. Crews D. 1984. Gamete production, sex hormone secretion, and mating behavior uncoupled. Horm Behav 18:22-28.
12. Crews D., B. Camazine, M. Diamond, R. Mason, R.R. Tokarz, and W.R. Garstka. 1984. Hormonal independence of courtship behavior in the male garter snake. Horm Behav 18:29-41.
13. Crews D. and C. Gans. 1992. The interaction of hormones, brain, and behavior: an emerging discipline in herpetology. Pp. 1-23 in C. Gans and D. Crews, eds. Biology of the Reptilia. Vol. 18. Hormones, Brain, and Behavior. University of Chicago Press, Chicago.
14. Crews D. and W.R. Garstka. 1982. The ecological physiology of reproduction in the garter snake. Sci Am 247:158-168.
15. Crews D., V. Hingorani, and R.J. Nelson. 1988. Role of the pineal gland in the control of annual reproductive behavioral and physiological cycles in the red-sided garter snake (Thamnophis sirtalis parietalis). J Biol Rhythms 3:293-302.
16. de Queiroz A., R. Lawson, and J.A. Lemos-Espinal. 2002. Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: howmuch DNA sequence is enough? Mol Phylogenet Evol 22:315-329.
17. Dubbels R., R.J. Reiter, E. Klende, A. Goebel, E. Schnakenberg, C. Ehlers, H.W. Schiwara, and W. Schloot. 1995. Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J Pineal Res 18:28-31.
18. Dunn O.J. 1964. Multiple contrasts using rank sums. Technometrics 6:241-252.
19. Dunn P.O. and D.W. Winkler. 1999. Climate change has affected the breeding date of tree swallows throughout North America. Proc R Soc B 266:2487.
20. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125:1-15.
21. Field A. 2005. Discovering Statistics Using SPSS. Sage, London.
22. Firth B.T. and D.J. Kennaway. 1987. Melatonin content of the pineal, parietal eye and blood plasma of the lizard, Trachydosaurus rugosus: effects of constant and fluctuating temperature. Brain Res 404:313-318.
23. Firth B.T., M.B. Thompson, D.J. Kennaway, and I. Belan. 1989. Thermal sensitivity of reptilian melatonin rhythms: "cold" tuatara vs. "warm" skink. Am J Physiol 256:R1160-R1163.
24. Forchhammer M.C., E. Post, and N.C. Stenseth. 1998. Breeding phenology and climate. Nature 391:29-30.
25. García-Allegue R., J.A. Madrid, and F.J. Sánchez- Vázquez. 2001. Melatonin rhythms in European sea bass plasma and eye: influence of seasonal photoperiod and water temperature. J Pineal Res 31:68-75.
26. Garstka W.R., B. Camazine, and D. Crews. 1982. Interactions of behavior and physiology during the annual reproductive cycle of the red-sided garter snake, Thamnophis sirtalis parietalis. Herpetologica 38:104-123.
27. Goldman B., E. Gwinner, F.J. Karsch, D. Saunders, I. Zucker, and G.F. Ball. 2004. Circannual rhythms and photoperiodism. Pp. 107-142 in J.C. Dunlap, J.J. Loros, and P.J. DeCoursey, eds. Chronobiology: Biological Timekeeping. Sinauer, Sunderland, MA.
28. Groggel D.J. and J.H. Skillings. 1986. Distribution-free tests for main effects in multifactor designs. Am Stat 40:99-102.
29. Harvey R.E., J.G. Phillips, and T.R. Hall. 1984. Stress and adrenal function. J Exp Zool 232:633-646.
30. Hau M., L.M. Romero, J.D. Brawn, and T.J. Van't Hof. 2002. Effect of polar day on plasma profiles of melatonin, testosterone, and estradiol in high-Arctic Lapland longspurs. Gen Comp Endocrinol 126:101-112.
31. Hyde L.L. and H. Underwood. 2000. Effects of melatonin administration on the circadian activity rhythm of the lizard Anolis carolinensis. Physiol Behav 71:183-192.
32. Idler D.R. 1972. Steroids in Non-mammalian Vertebrates. Academic Press, New York.
33. Intergovernmental Panel on Climate Change (IPCC). 2001. Climate Change 2001: Impacts, Adaptation, and Vulnerability. Intergovernmental Panel on Climate Change Technical Summary. IPCC Secretariat, Geneva.
34. Jasnow A.M., K.L. Huhman, T.J. Bartness, and G.E. Demas. 2002. Short days and exogenous melatonin increase aggression of male Syrian hamsters (Mesocricetus auratus). Horm Behav 42:13-20.
35. Jessop T.S., C.J. Limpus, and J.M. Whittier. 2002. Nocturnal activity in the green sea turtle alters daily profiles of melatonin and corticosterone. Horm Behav 41:357-365.
36. Joy J.E. and D. Crews. 1985. Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis). J Comp Psychol 99:145-149.
37. Khan R., S. Daya, and B. Potgieter. 1990. Evidence for a modulation of the stress response by the pineal gland. Experientia 46:860-862.
38. Khare P.V., M.K. Satralkar, C. Vanlalnghaka, V.L. Keny, M.S. Kasture, A.J. Shivagaje, R.J. Barnabas, and D.S. Joshi. 2005. Altitudinal variation in the circadian rhythm of oviposition in Drosophila ananassae. Chronobiol Int 22:45-57.
39. Kirby A.W., M. Clayton, P. Rivera, and C.A. Comperatore. 1999. Melatonin and the reduction or alleviation of stress. J Pineal Res 27:78-85.
40. Krohmer R.W., M. Grassman, and D. Crews. 1987. Annual reproductive cycle in the male red-sided garter snake, Thamnophis sirtalis parietalis: field and laboratory studies. Gen Comp Endocrinol 68:64-75.
41. Krotewicz M., A. Lewinski, and E. Wajs. 1992. The inhibitory effect of late-afternoon melatonin injections, but not of melatonin-containing subcutaneous implants, on thyroid hormone secretion in male Wistar rats. Neuroendocrinol Lett 14:405-409.
42. Landys-Ciannelli M.M., M. Ramenofsky, T. Piersma, J. Jukema, Castricum Ringing Group, and J.C.Wingfield. 2002. Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiol Biochem Zool 75:101-110.
43. Leary C.J., T.S. Jessop, A.M. Garcia, and R. Knapp. 2004. Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans. Behav Ecol 15:313-320.
44. LeMaster M.P. and R.T Mason. 2002. Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J Chem Ecol 28:1269-1285.
45. Lincoln G.A., H. Andersson, and A. Loudon. 2003. Clock genes in calendar cells as the basis of annual timekeeping in mammals: a unifying hypothesis. J Endocrinol 179:1-13.
46. Lutterschmidt D.I. 2006. Chronobiology of Garter Snakes: Environmental and Hormonal Cues Mediating Hibernation and Reproduction. PhD diss. Oregon State University, Corvallis.
47. Lutterschmidt D.I., M.P. LeMaster, and R.T. Mason. 2004. Effects of melatonin on the behavioral and hormonal responses of red-sided garter snakes (Thamnophis sirtalis parietalis) to exogenous corticosterone. Horm Behav 46:692-702.
48. _. 2006. Minimal over-wintering temperatures of red-sided garter snakes (Thamnophis sirtalis parietalis): a possible cue for emergence? Can J Zool 84:771-777.
49. Lutterschmidt D.I., W.I. Lutterschmidt, N.B. Ford, and V.H. Hutchison. 2002. Behavioral thermoregulation and the role of melatonin in a nocturnal snake. Horm Behav 41:41-50.
50. Lutterschmidt D.I., W.I. Lutterschmidt, and V.H. Hutchison. 1997. Melatonin and chlorpromazine: thermal selection and metabolic rate in the bullsnake, Pituophis melanoleucus. Comp Biochem Physiol 118C:271-277.
51. _. 2003. Melatonin and thermoregulation in ectothermic vertebrates: a review. Can J Zool 81:1-13.
52. Lutterschmidt W.I., D.I. Lutterschmidt, C.R. Tracy, and V.H. Hutchison. 1998. Time course analyses of the thermoregulatory responses to melatonin and chlorpromazine in bullsnakes (Pituophis melanoleucus). J Therm Biol 23:319-327.
53. Lutterschmidt D.I. and R.T. Mason. 2005. A serotonin receptor antagonist, but not melatonin, modulates hormonal responses to capture stress in two populations of garter snakes (Thamnophis sirtalis parietalis and Thamnophis sirtalis concinnus). Gen Comp Endocrinol 141:259-270.
54. Maestroni G.J.M., A. Conti, and W. Pierpaoli. 1989. Melatonin, stress, and the immune system. Pineal Res Rev 7:203-226.
55. Mendonça M.T., A.J. Tousignant, and D. Crews. 1996a. Courting and noncourting male red-sided garter snakes, Thamnophis sirtalis parietalis: plasma melatonin levels and the effects of pinealectomy. Horm Behav 30:176-185.
56. _. 1996b. Pinealectomy, melatonin, and courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis). J Exp Zool 274:63-74.
57. Michael T.P., P.A. Salomé, H.J. Yu, T.R. Spencer, E.L. Sharp, M.A. McPeek, J.M. Alonso, J.R. Ecker, and C.R. McClung. 2003. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049-1053.
58. Moore I.T., M.J. Greene, and R.T. Mason. 2001. Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male garter snake, Thamnophis sirtalis. J Exp Zool 289:99-108.
59. Moore I.T. and T.S. Jessop. 2003. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39-47.
60. Moore I.T., M.P. LeMaster, and R.T. Mason. 2000a. Behavioural and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis. Anim Behav 59:529-534.
61. Moore I.T., J.P. Lerner, D.T. Lerner, and R.T. Mason. 2000b. Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus. Physiol Biochem Zool 73:307-312.
62. Moore I.T. and R.T. Mason. 2001. Behavioral and hormonal responses to corticosterone in the male red-sided garter snake, Thamnophis sirtalis parietalis. Physiol Behav 72:669-674.
63. Moss R., J. Oswald, and D. Baines. 2001. Climate change and breeding success: decline of the capercaillie in Scotland. J Anim Ecol 70:47-61.
64. Nelson R.J., R.T. Mason, R.W. Krohmer, and D. Crews. 1987. Pinealectomy blocks vernal courtship behavior in red-sided garter snakes. Physiol Behav 39:231-233.
65. Oliveira C., A. Ortega, J.F. López-Olmeda, L.M. Vera, and F.J. Sánchez-Vázquez. 2007. Influence of constant light and darkness, light intensity, and light spectrum on plasma melatonin rhythms in Senegal sole. Chronobiol Int 24:615-627.
66. O'Reilly K.M. and J.C. Wingfield. 1995. Spring and autumn migration in arctic shorebirds: same distance, different strategies. Am Zool 35:222-233.
67. Pottinger T.G. 1999. The impact of stress on animal reproductive activities. Pp. 130-177 in P.H.M. Baum, ed. Stress Physiology in Animals. CRC, Boca Raton, FL.
68. Reierth E., T.J. Van't Hof, and K.A. Stokkan. 1999. Seasonal and daily variations in plasma melatonin in the high-arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). J Biol Rhythms 14:314-319.
69. Reiter R.J. 1996. Functional aspects of the pineal hormone melatonin in combating cell and tissue damage induced by free radicals. Eur J Endocrinol 134:412-420.
70. Reneerkens J., R.I.G. Morrison, M. Ramenofsky, T. Piersma, and J.C. Wingfield. 2002. Baseline and stress-induced levels of corticosterone during different life cycle substages in a shorebird on the high arctic breeding grounds. Physiol Biochem Zool 75:200-208.
71. Root T.L., J.T. Price, K.R. Hall, S.H. Schneider, C. Rosenzweig, and J.A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57-60.
72. Sapolsky R.M. 1992. Neuroendocrinology of the stress response. Pp. 287-324 in J.B. Becker, ed. Behavioral Endocrinology. MIT Press, Cambridge, MA.
73. Sawilowsky S.S., R.C. Blair, and J.J. Higgins. 1989. An investigation of the Type I error and power properties of the rank transform procedure in factorial ANOVA. J Educ Stat 14:255-267.
74. Schramm B.G., M. Casares, and V.A. Lance. 1999. Steroid levels and reproductive cycle of the Galapagos tortoise, Geochelone nigra, living under seminatural conditions on Santa Cruz Island (Galapagos). Gen Comp Endocrinol 114:108-120.
75. Schwabl H., J.C. Wingfield, and D.S. Farner. 1985. Influence of weather on endocrine state and behavior in European blackbirds (Turdus merula). Z Tierpsychol 68:244-252.
76. Sheskin D.J. 2007. Handbook of Parametric and Nonparametric Statistical Procedures. Chapman & Hall/CRC, Boca Raton, FL.
77. Silverin B. and J.C. Wingfield. 1998. Adrenocortical responses to stress in breeding pied flycatchers, Ficedula hypoleuca: relation to latitude, sex, and mating status. J Avian Biol 29: 228-234.
78. Sokal R.R. and F.J. Rohlf. 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W.H. Freeman, New York.
79. SPSS. 2006. SPSS. Version 15.0. SPSS, Chicago.
80. Systat. 2005. SigmaStat 3.11. Systat Software, Point Richmond, CA.
81. Tamarkin L., C.J. Baird, and O.F. Almeida. 1985. Melatonin: a coordinating signal for mammalian reproduction? Science 227:714-720.
82. Tennant A. 1997. A Field Guide to Snakes of Florida. Gulf, Houston, TX.
83. Tilden A.R. and V.H. Hutchison. 1993. Influence of photoperiod and temperature on serum melatonin in the diamondback water snake, Nerodia rhombifera. Gen Comp Endocrinol 92:347-354.
84. Toothaker L.E. 1993. Multiple Comparisons Procedures. Sage, Thousand Oaks, CA.
85. Visser M.E. 2008. Keeping up with a warming world: assessing the rate of adaptation to climate change. Proc R Soc B 275:649-659.
86. Weil M.R. 1985. Comparison of plasma and testicular testosterone levels during the active season in the common garter snake, Thamnophis sirtalis (L.). Comp Biochem Physiol A 81:585-587.
87. Whittier J.M., R.T. Mason, and D. Crews. 1987. Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: relationship to mating and gestation. Gen Comp Endocrinol 67:33-43.
88. Wilson B.S. and J.C. Wingfield. 1992. Correlation between female reproductive condition and plasma corticosterone in the lizard Uta Stansburiana. Copeia 1992:691-697.
89. _. 1994. Seasonal and interpopulational variation in plasma levels of corticosterone in the side-blotched lizard (Uta Stansburiana). Physiol Zool 67:1025-1049.
90. Wingfield J.C. 1988. Changes in reproductive function of freeliving birds in direct response to environmental perturbations. Pp. 121-148 in M.H. Stetson, ed. Processing of Environmental Information in Vertebrates. Springer, New York.
91. Wingfield J.C., D.L. Maney, C.W. Breuner, J.D. Jacobs, S. Lynn, M. Ramenofsky, and R.D. Richardson. 1998. Ecological bases of hormone-behavior interactions: the "emergency life history stage." Am Zool 38:191-206.
92. Woolley S.C., J.T. Sakata, and D. Crews. 2004. Evolutionary insights into the regulation of courtship behavior in male amphibians and reptiles. Physiol Behav 83:347-360.
93. Wright M.L., A. Pikula, L.J. Cykowski, and K. Kuliga. 1996. Effect of melatonin on the anuran thyroid gland: follicle cell proliferation, morphometry, and subsequent thyroid hormone secretion in vitro after melatonin treatment in vivo. Gen Comp Endocrinol 103:182-191.
94. Zar J.H. 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.
95. Zerani M. and A. Gobbetti. 1993. Corticosterone during the annual reproductive cycle and in sexual behavior in the crested newt, Triturus carnifex. Horm Behav 27:29-37.