Endocrine mechanisms mediating temperature-induced reproductive behavior in red-sided garter snakes (Thamnophis sirtalisparietalis)

Journal of Experimental Biology

Volumn 212, Issue 19, 2009, Pages 3108-3118

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

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Androgen; Corticosterone; Courtship behavior; Diel rhythm; Estradiol; Hibernation; Melatonin; Reptile; Winter dormancy

Indexed keywords

CORTICOSTERONE; MELATONIN; SEX HORMONE;

ANIMAL; ARTICLE; ENDOCRINE SYSTEM; FEMALE; HIBERNATION; MALE; METABOLISM; PHOTOPERIODICITY; PHYSIOLOGY; SEXUAL BEHAVIOR; SNAKE; TEMPERATURE;

ANIMALS; COLUBRIDAE; CORTICOSTERONE; ENDOCRINE SYSTEM; FEMALE; GONADAL STEROID HORMONES; HIBERNATION; MALE; MELATONIN; PHOTOPERIOD; SEXUAL BEHAVIOR, ANIMAL; TEMPERATURE;

REPTILIA; SERPENTES; THAMNOPHIS; THAMNOPHIS SIRTALIS PARIETALIS;

EID: 70349136588     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.033100     Document Type: Article

References (63)

1. Aleksiuk, M. and Gregory, P. T. (1974). Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 681-689.
2. Axelrod, J. (1974). The pineal gland: a neurochemical transducer. Science 184, 1341-1348.
3. Barriga, C., Marchena, J. M., Lea, R. W., Harvey, S. and Rodriguez, A. B. (2002). Effect of stress and dexamethasone treatment on clrcadian rhythms of melatonin and corticosterone in ring dove (Streptopelia risoria). Mol. Cell Biochem. 232, 27-31. (Pubitemid 34413878)
4. Benshoff, H. M., Brainard, G. C., Rollag, M. D. and Lynch, G. R. (1987). Suppression of pineal melatonin In Peromyscus leucopus by different monochromatic wavelengths of visible and near-ultraviolet light (UV-A). Brain Res. 420, 397-402.
5. Bittman, E. L., Demsey, R. J. and Karsch, F. J. (1983). Pineal melatonin secretion drives the reproductive response to daylength In the ewe. Endocrinology 113, 2276-2283.
6. Bona-Gallo, A. and Licht, P. (1983). Effect of temperature on sexual receptivity and ovarian recrudescence in the garter snake, Thamnophis sirtalis parietalis. Herpetologica 39, 173-182.
7. Brotto, L. A., Gorzalka, B. B. and LaMarre, A. K. (2001). Melatonin protects against the effects of chronic stress on sexual behavior In male rats. NeuroReport 12, 3465-3469.
8. Camazine, B., Garstka, W., Tokarz, R. and Crews, D. (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 Goldman, B. D. (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., Lutterschmidt, D. I. and Mason, R. T. (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. Crawford, K. M. (1991). The winter environment of painted turtles, Chrysemys picta: temperature, dissolved oxygen, and potential cues for emergence. Can. J. Zool. 69, 2493-2498.
12. Crews, D. (1984). Gamete production, sex hormone secretion, and mating behavior uncoupled. Horm. Behav. 18, 22-28.
13. Crews, D. (1991). Trans-seasonal action of androgen In the control of spring courtship In male red-sided garter snakes. Proc. Natl. Acad. Sci. USA 88, 3545-3548.
14. Crews, D. and Garstka, W. R. (1982). The ecological physiology of reproduction in the garter snake. Sci. Am. 247, 158-168.
15. Crews, D., Camazine, B., Diamond, M., Mason, R., Tokarz, R. R. and Garstka, W. R. (1984). Hormonal independence of courtship behavior In the male garter snake. Horm. Behav. 18, 29-41.
16. Crews, D., Hingorani, V. and Nelson, R. J. (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.
17. Etheridge, K., Wit, L. C. and Sellers, J. C. (1983). Hibernation in the lizard Cnemidophorus sexlineatus (Lacertilla: Teildae). Copeia 206-214.
18. Field, A. (2005). Discovering Statistics Using SPSS. London: Sage Publications.
19. García-Allegue, R., Madrid, J. A. and Sánchez- Vázquez, F. J. (2001). Melatonin rhythms In European sea bass plasma and eye: influence of seasonal photoperiod and water temperature. J. Pineal Res. 31, 68-75.
20. Garstka, W. R., Camazine, B. and Crews, D. (1982). Interactions of behavior and physiology during the annual reproductive cycle of the red-sided garter snake, Thamnophis sirtalis parietalis. Herpetologica 38, 104-123
21. Grobman, A. B. (1990). The effect of soil temperatures on emergence from hibernation of Terrapene carolina and T ornata. Am. Midi. Nat. 124, 366-371.
22. Hawley, A. W. L. and Aleksiuk, M. (1975). Thermal regulation of spring mating behavior In the red-sided garter snake (Thamnophis sirtalis parietalis). Can. J. Zool. 53, 768-776.
23. Hawley, A. W. L. and Aleksiuk, M. (1976). The influence of photoperlod and temperature on seasonal testicular recrudescence in the red-sided garter snake (Thamnophis sirtalis parietalis). Comp. Biochem. Physiol. 53A, 215-221.
24. Idler, D. R. (1972). Steroids In Non-mammalian Vertebrates. New York: Academic Press.
25. Jacob, S. J. and Painter, C. W. (1980). Overwinter thermal ecology of Crotalus viridis In the north-central plains of New Mexico. Copeia 799-805.
26. Joy, J. E. and Crews, D. (1985). Social dynamics of group courtship behavior In male red-sided garter snakes (Thamnophis sirtalis parietalis). J. Comp. Psychol. 99, 145-149.
27. Krohmer, R. W. and Crews, D. (1987). Temperature activation of courtship behavior in the male red-sided garter snake (Thamnophis sirtalis parietalis): role of the anterior hypothalamus-preoptic area. Behav. Neurosci. 101, 228-236. (Pubitemid 17077266)
28. Krohmer, R. W., Grassman, M. and Crews, D. (1987). Annual reproductive cycle in the male red-sided garter snake, Thamnophis sirtalis parietalis: field and laboratory studies. Gen. Comp. Endocrinol. 68, 64-75. (Pubitemid 17140338)
29. LeMaster, M. P. and Mason, R. T. (2002). Variation In a female sexual attractiveness pheromone controls male mate choice in garter snakes. J. Chem. Ecol. 28, 1269-1285.
30. Levey, I. L. (1973). Effects of pinealectomy and melatonin injections at different seasons on ovarian activity In the lizard Anolis carolinensis. J. Exp. Zool. 185, 169-174.
31. Licht, P. (1984). Seasonal cycles in reptilian reproductive physiology. In Marshall's Physiology of Reproduction (ed. E. Lamming), pp. 206-282. Edinburgh: Churchill Livingstone.
32. Lutterschmidt, D. I. and Mason, R. T. (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.
33. Lutterschmidt, D. I. and Mason, R. T. (2008). Geographic variation In timekeeping systems of three populations of garter snakes (Thamnophis sirtalis) in a common garden. Physiol. Biochem. Zool. 81, 810-825.
34. Lutterschmidt, D. I., LeMaster, M. P. and Mason, R. T. (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.
35. Lutterschmidt, D. I., LeMaster, M. P. and Mason, R. T. (2006). Minimal overwintering temperatures of red-sided garter snakes (Thamnophis sirtalis parietalis): a possible cue for emergence? Can. J. Zool. 84, 771-777.
36. Macartney, J. M., Larsen, K. W. and Gregory, P. T. (1989). Body temperatures and movements of hibernating snakes (Crotalus and Thamnophis) and thermal gradients of natural hibernacula. Can. J. Zool. 67, 108-114.
37. Maestroni, G. J. M., Conti, A. and Pierpaoli, W. (1989). Melatonin, stress, and the immune system. Pineal Res. Rev. 7, 203-226.
38. Mayer, I., Bornestaf, C. and Borg, B. (1997). Melatonin In non-mammalian vertebrates: physiological role In reproduction? Comp. Biochem. Physiol. 118A, 515-531. (Pubitemid 28009894)
39. Mendonça, M. T. and Crews, D. (1996). Effects of ovariectomy and estrogen replacement on attractivity and receptivity In a dissociated pattern breeder, the redsided garter snake (Thamnophis sirtalis parietalis). J. Comp. Physiol. 178A, 373-381. (Pubitemid 3022949)
40. Mendonça, M. T., Tousignant, A. J. and Crews, D. (1996a). Pinealectomy, melatonin, and courtship behavior In male red-sided garter snakes (Thamnophis sirtalis parietalis). J. Exp. Zool. 274, 63-74.
41. Mendonça, M. T., Tousignant, A. J. and Crews, D. (1996b). Courting and noncourtlng male red-sided garter snakes, Thamnophis sirtalis parietalis: plasma melatonin levels and the effects of pinealectomy. Horm. Behav. 30, 176-185.
42. Moore, I. T. and Jessop, T. S. (2003). Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm. Behav. 43, 39-47.
43. Moore, I. T. and Mason, R. T. (2001). Behavioral and hormonal responses to corticosterone In the male red-sided garter snake, Thamnophis sirtalis parietalis. Physiol. Behav. 72, 669-674.
44. Moore, I. T., LeMaster, M. P. and Mason, R. T. (2000). Behavioural and hormonal responses to capture stress In the male red-sided garter snake, Thamnophis sirtalis parietalis. Anim. Behav. 59, 529-534.
45. Moore, I. T., Greene, M. J. and Mason, R. T. (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.
46. Moyer, R. W., Firth, B. T. and Kennaway, D. J. (1995). Effect of constant temperatures, darkness and light on the secretion of melatonin by pineal expiants and retinas in the gecko Christinus marmoratus. Brain Res. 675, 345-348.
47. Nelson, R. J., Mason, R. T., Krohmer, R. W. and Crews, D. (1987). Pinealectomy blocks vernal courtship behavior In red-sided garter snakes. Physiol. Behav. 39, 231-233.
48. Oliveira, C., Ortega, A., López-Olmeda, J. F., Vera, L. M. and Sánchez-Vázquez, F. J. (2007). Influence of constant light and darkness, light intensity, and light spectrum on plasma melatonin rhythms in Senegal sole. Chronobiol. Int. 24, 615-627. (Pubitemid 47263092)
49. Otsuka, M., Kato, K., Murai, I., Asai, S., Iwasaki, A. and Arakawa, Y. (2001). Roles of nocturnal melatonin and the pineal gland in modulation of water-immersion restraint stress-induced gastric mucosal lesions In rats. J. Pineal Res. 30, 82-86. (Pubitemid 32176210)
50. Rawding, R. S. and Hutchison, V. H. (1992). Influence of temperature and photoperiod on plasma melatonin in the mudpuppy, Necturus maculosus. Gen. Comp. Endocrinol. 88, 364-374.
51. Sheskin, D. J. (2007). Handbook of Parametric and Nonparametric Statistical Procedures. Boca Raton, FL: Chapman & Hall.
52. Silverin, B. and Wingfield, J. C. (1998). Adrenocortical responses to stress in breeding Pled Flycatchers, Ficedula hypoleuca: relation to latitude, sex, and mating status. J. Avian Biol. 29, 228-234. (Pubitemid 28443725)
53. Tilden, A. R. and Hutchison, V. H. (1993). Influence of photoperiod and temperature on serum melatonin In the diamondback water snake, Nerodia rhombifera. Gen. Comp. Endocrinol. 92, 347-354.
54. Toothaker, L. E. (1993). Multiple Comparisons Procedures. Sage: Thousand Oaks, CA, USA.
55. Turek, F. W. and Van Cauter, E. (1994). Rhythms In reproduction. In Physiology of Reproduction (ed. E. Knobil and J. D. Neil), pp. 487-550. New York: Raven Press.
56. Underwood, H. (1985a). Pineal melatonin rhythms in the lizard Anolis carolinensis: effects of light and temperature cycles. J. Comp. Physiol. A 157, 57-65.
57. Underwood, H. (1985b). Annual testicular cycle of the lizard Anolis carolinensis: effects of pinealectomy and melatonin. J. Exp. Zool. 233, 235-242.
58. Vivien-Roels, B., Pévet, P. and Claustrat, B. (1988). Pineal and circulating melatonin rhythms In the box turtle, Terrapene carolina triunguis: effect of photoperiod, light pulse, and environmental temperature. Gen. Comp. Endocrinol. 9, 163-173. (Pubitemid 18045837)
59. Whittier, J. M., Mason, R. T., Crews, D. and Licht, P. (1987a). Role of light and temperature in the regulation of reproduction in the red-sided garter snake, Thamnophis sirtalis parietalis. Can. J. Zool. 65, 2090-2096.
60. Whittier, J. M., Mason, R. T. and Crews, D. (1987b). Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: relationship to mating and gestation. Gen. Comp. Endocrinol. 67, 33-43.
61. Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M. and Richardson, R. D. (1998). Ecological bases of hormonebehavior interactions: the "emergency life history stage." Am. Zool. 38, 191-206.
62. Woolley. S. C., Sakata, J. T. and Crews, D. (2004). Evolutionary insights into the regulation of courtship behavior In male amphibians and reptiles. Physiol. Behav. 83, 347-360.
63. Zar, J. H. (1999). Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.