Testosterone Level, Testicular Histology and Reproductive Events Of Caucasian Pit Viper, Gloydius Halys Caucasicus (Serpentes: Viperidae)
The steroid hormones regulate the reproductive physiology of animals and may influence by habitat and seasonal conditions. In this study, body weight and length, testosterone concentration and testicular histology were measured in Caucasian pit viper from Lar region, Tehran province, during summer and autumn seasons in year 2014. Serum samples were collected from 24 anesthetized snakes and testicles were removed and fixed for histological study. Enzyme immunoassay (ELISA) was conducted on serum samples to determine concentrations of testosterone (T) and standard histological procedure was performed on gonads. Results indicated that body weights and lengths in summer and fall seasons were respectively 49.88±9.6 gr, 50.25±7.4 cm and 42.75±4.5gr, 43.25±2.3 cm, serum testosterone level in summer, 29.3± 5.12 ng/ml was more than fall, 13.75±2.80 ng/ml at P≤0.05.The numbers of spermatogonias, spermatocytes and spermatids in summer were more than fall and statistically different at P≤0.05. The leydig cells number and diameter in fall were more than summer but differences were not significant.There were significant differences between seminiferous tubules diameter, germinal epithelial height and tunica albuginea thickness in summer as compared to fall at P≤0.05. The data suggest male Caucasian pit-viper of Lar region of Tehran displaying estival spermatogenesis and some relationship was revealed between T level and snake's body weight, and high level of T coincide with the mating period
2. Maurel D.and Boissin J. 1981. Comparative mechanisms of physiological, metabolical and eco-ethological adaptation to the winter season ih two wild European mammals: the European Badge (Meles meles L.) and red fox (Vulpes vulpes L.)In: Adaptation to terrestrial environments by Margaris NS. , Faraggitaki, MA. and Reiter RJ. . University of Texas, Health Sciences Center, San Antonio Texas, Plenum Press 1982. NY. Lond. Part 2 , pp: 219-231.
3. Saboureau M., Boissin J. (1978) Seasonal Changes and Environmental Control of Testicular Function in the Hedgehog,Erinaceus europaeus L.. In: Assenmacher I., Farner D.S. (eds) Environmental Endocrinology. Proceedings in Life Sciences. Springer, Berlin, Heidelberg.
4. 5- Duvall D, Arnold SJ, Schuett GW. Pitviper mating systems: Ecological potential, sexual selection and micro-evolution. In: Campbell JA, Jr. Brodie ED. Eds. The Biology of the Pitvipers. Tyler: Selva Press 1992; 321-336.
5. 6- Goldberg, E.A S.R., Parker, W.S., 1975. Seasonal testicular histology of the colubrid
6. Gondos B, Berndtson WE. Postnatal and pubertal development. In:
7. Prestt, I.1971. An ecological study of the viper Vipera berus in southern Britain. J. Zool. (Lond.) 164 (3), 373–418 1971.
8. Nilson,G. 19980. Male reproductive cycle of the European adder, Vipera brus, and its relation to annual activity patterns. Copeia, 729.
9. Schuett, G. W. 1992. Is long-term sperm storage an important component of the reproductive biology of temperate pitvipers? p. 169–184. In: Biology of the pitvipers. J. A. Campbell, and E. D. Brodie Jr. (eds.), Selva, Tyler, TX.
10. Aldridge, R.D., Duvall, D., 2002. Evolution of the mating season in the pitvipers of North America. Herpetol. Monographs 16, 1–25.
11. Shcuett GW. Carlisle SL. Holycross AT. O'leile, JK. Hardy D L. Vankirk SR. E A., and Mordoch WJ.2002.Mating system of male Mojave Rattlesnakes (Crotalus scutulatus) seasonal timming of mating, agonistic behavior,spermatogenesis, sexual segment of the kidney and plasma sex steroids. Biology of Vipers, 515- 532.
12. 13. Schuett GW. Repp RA.Taylor EN. DeNardo DF. Earley RL.Van Kirk EA.Murdoch WJ. 2006. Winter profile of plasma sex steroid levels in free-living male western diamond-backed rattlesnakes, Crotalus atrox(Serpentes: Viperidae).Gen Comp Endocrinol. 149(1):72-80.
13. 14- Schuett, G.W., Hardy Sr., D.L., Greene, H.W., Earley, R.L., Grober, M.S., Van Kirk, E.A.,Murdoch, W.J., 2005. Sympatric rattlesnakes with contrasting mating systems
14. scutulatus): seasonal timing of mating, agonistic behavior, spermatogenesis,sexual segment of the kidney, and plasma sex steroids. In: Schuett, G.W.,Hِggren, M., Douglas, M.E., Greene, H.W. (Eds.), Biology of the Vipers. EagleMountain Publishing, LC, Eagle Mountain, Utah, pp. 515–532.
15. Saint Girons H. 1982. Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica 38: 5–16.
16. Johnson L, Varner DD, Tatum ME, Scrutch field WL. 1991. Season but not age affects Sertoli cell number in adult stallion. Biol Reprod. 45(3):404-10.
17. Johnson LF, Jacob JS, Torrance P. 1982. Annual testicular and androgenic cycles of the Cottonmouth (Agkistrodon piscivorus) in Alabama. Herpetologica, 38:16-25.
18. Tinkle, D. W. 1962. Reproductive potential and cycles in female Crotalus atrox from northwestern Texas.Copeia 1962:306–313.
19. 19-Aldridge, R.D., 2002. The link between mating season and male reproductive anatomy in the rattlesnakes Crotalusviridisoreganus and Crotalusviridishelleri. J.Herpetol. 36, 295–300.
20. Gibbons DW (1989) Seasonal reproductive success of the moorhen Gallinula chloropus: the importance of male weight. Ibis 131: 57–68.
21. Goldberg, S.R. 2000. Reproduction in the longnose snake, Rhinocheilus lecontei (Serpentes: Colubridae). Texas Journal of Science 52:319-326.
22. 23.Goldberg, S. R. 1999a. Reproduction in the tiger rattlesnake, Crotalus tigris (Serpentes: Viperidae). Tex. J. Sci 51:31–36.
23. 25.Goldberg, S. R. 1999b. Reproduction in the blacktail rattlesnake, Crotalus molossus (Serpentes: Viperidae).Ibid 51:323–328.
24. 26. Goldberg, S. R. and P. C. Rosen. 2000. Reproduction in the Mojave Rattlesnake, Crotalus scutulatus(Serpentes: Viperidae). Tex. J. Sci 52:101–109.
25. Goldberg, S. R. 2000. Reproduction in the twin-spotted rattlesnake, Crotalus pricei (Serpentes: Viperidae).West. North American Nat 60:98–100.
26. Aldridge, R. D. 1979. Seasonal spermatogenesis in sympatric Crotalus viridis and Arizona elegans in New Mexico. J. Herpetol 13:187–192.
27. 28. Holycross AT. and Goldberg SR. 2001.Reproduction in Northern Populations of the Ridgenose Rattlesnake, Crotalus willardi (Serpentes: Viperidae). . Copeia 2001(2):473-481.
28. 30. Hartmann MT, Marques OAV, Almeida-Santos SM. 2004. Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpents, Viperidea). Amphibian Reptile 25(1): 77- 85.
29. 31- Tourmente M, Gomendio M, Roldan ERS, et al. Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 2009; 63(10): 2513-2524.
30. 32. Bahri S, Shiravi AH, Todehdehghan F.Reproductive cycle of female Pit Viper(Gloydius halys caucasicus) in Iran.SCIREA J Anim Husb Vet. Med.
32. Shakoori S, Todehdehghan F, Shiravi AH, Hojati V. The assessment of captive breeding in the Caucasian viper (Gloydius halys caucasicus) in Iran. Journal of Entomology and Zoology Studies.2015;3(2):257-259.
33. 34- Mozafari SZ, Shiravi AH, Todehdehghan F. Evaluation of reproductive parameters ofvas deferens sperms in Caucasian snake (Gloydiushalyscaucasicus). Vet Res Forum. 2012;3(2):
34. Schuett G. W., Harlow H. J., Rose J. D., Van Kirk E. A., Murdoch W. J., 1997. Annualcycle of testosterone in male copperheads, Agkistrodon contortix (Serpentes: Viperidae): relationship to timing of spermatogenesis, mating, and agonistic behavior. Gen. Comp. Endocrinol. 105, 417–424.
35. Graham SP.,EarleyRL., Hoss SK., Schuett WG.,Matthew S. Grober MS. 2008. The reproductive biology of male cottonmouths (Agkistrodonpiscivorus): Do plasma steroid hormones predict the mating season? General and Comparative Endocrinology, 159: 226–235.
36. 37- Taylor, E. N., DeNardo, D. F., Jennings, D. H. 2004. Seasonal steroid hormone levels and their relation to reproduction in the western diamond-backed rattlesnake, Crotalus atrox (Serpentes: Viperidae). Gen. Comp. Endocrinol.136, 328–337.
37. Saint-Girons, H., Bradshaw, S.D., Bradshaw, F.J., 1993. Sexual activity and plasma levels of sex steroids in the aspic viper Vipera aspis.(Reptilia, Viperidae). Gen. Comp.Endocrinol. 91,
38. 38.. Moore, I., LeMaster, M. and Mason, RT. 2000. Behavioural and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis. Anim. Behav. 59, 529–534.
39. Crew D. 1991. Trans -seasonal action of androgen in the control of spring courtship behavior in male red sided gartter snakes. Proceedinf of the National Academy of Sciences. 88: 3545- 3548.
40. Lind CM (2009) The relationship between seasonal steroid hormone concentrations and the reproductive cycle in the northern pacific rattlesnake, Crotalus oreganus. Masters thesis. The Faculty of California Polytechnic State University.
41. Lind CM, Husak JF, Eikenaar C, Moore IT, Taylor EN (2010) The relationship between plasma steroid hormone concentrations and the reproductive cycle in the northern pacific rattlesnake, Crotalus oreganus. Gen Comp Endocrinol. 166:590–599.
42. Bronson, F. H. 1998. Energy balance and ovulation: small cages versus natural habitats. Repr Fert Dev10:127–137.
43. 45. Bonnet X, Naulleau G. 1996. Are body reserves important for reproduction in males dark green snake (Coluber viridiflavus)? Herpetologica 52: 137–146.
44. 46. Albon SD, Mitchell B, Huby BJ, Brown D.1986. Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. J Zool Lond 209: 447–460
45. 49. Bonnet X, Naulleau G. 1996. Are body reserves important for reproduction in males dark green snake (Coluber viridiflavus)? Herpetologica 52: 137–146.
46. 50 Bonnet, X., Naulleau, G., and Lourdais, O. (2000). The benefits of complementary techniques: Using capture–recapture and physiological approaches to understand costs of reproduction in the asp viper. In G. Schuett and M. Ho¨ggren (Eds.), Biology of the Vipers
47. 51. Shine R. Harlow PS. Elphick MJ. Olsson MM. Mason RT.2000. Conflicts between courtship and thermoregulation: The thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, Colubridae).Physiol Biochem Zool, 73, 508–516.
48. 51. Fleury F . Naulleau G, 1987.Relations between hibernation and the resumption of endocrine, testicular and thyroid activities, in Vipera aspis L. (Reptilia, Viperidae)]. Gen Comp Endocrinol, 68(2):271-7.
49. 52. Naulleau G, Fleury F, Boissin J.1987.Annual cycles in plasma testosterone and thyroxine in the male aspic viper Vipera aspis L., (Reptilia, Viperidae), in relation to the sexual cycle and hibernation. Gen Comp Endocrinol. 65(2):254-63.
50. 53. Bona-Gallo A, Licht P, Mackenzie DS, Lofts B. 1980. Annual cycles in levels of pituitary and plasma gonadotropin, gonadal steroids, and thyroid activity in the Chinese cobra (Naja naja). Gen Comp Endocrinol 42: 477–493.
51. 54. Krohmer RW. 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(1):64-75.
52. 55. Aldridge RD., James J. Greenhaw JJ. Michael V. PlummerMV.1990 .The male reproductive cycle of the rough green snake (Opheodrys aestivus). Amphibia- Reptilia, 11(1990): 165-172.
53. 59. Aubret F., Bonnet X., Shine R., and Lourdais O. (2002). Fat is sexy for females but not males: The influence of body reserves on reproduction in snakes (Vipera aspis). Hormones and Behavior 42, 135–147.
54. 60- Gribbins, KM., Rheubert ,JL., Collier ,MH., Siegel DS., , David M. Sever, DM. 2008. Histological analysis of spermatogenesis and the germ cell development strategy within the testis of the male Western Cottonmouth Snake, Agkistrodon piscivorus leucostoma. Ann Anat 190, 461—476.
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