Can. J. Zool. 87(12): 1138–1146 (2009)  |  doi:10.1139/Z09-103  |  Published by NRC Research Press / Publié par les Presses scientifiques du CNRC  

Stress and reproduction in Boiga irregularis with notes on the ultrastructure of the sexual segment of the kidney in squamates

D. S. Siegel, R. D. Aldridge, C. S. Clark, E. H. Poldemann, and K. M. Gribbins

Abstract: The reproductive tract of wild-caught male Boiga irregularis (Merrem, 1802) (Brown Treesnake) and the changes that result in these tissues from captivity are described. Wild-caught snakes were compared with snakes kept in captivity and sacrificed at approximately 10, 30, 50, and 60+ days. Snakes sacrificed after 10 days in captivity showed no differences in histological appearance or epithelial height in either the testis or sexual segment of the kidney (SSK) compared with wild snakes. Normal spermatogenic stages and SSK ultrastructure were observed in the testes and kidney from wild specimens and captive specimens after 10 days. In terms of the SSK, large electron-dense secretory vacuoles occupied the apices of the epithelial cells, while a basal nucleus, rough endoplasmic reticulum, and Golgi bodies filled the bases of these cells. All SSK cells were actively secretory in a mode that could most accurately be termed apocrine. At time of secretion, released vacuoles become diffuse and the apical membrane ruptures, spilling the SSK contents into the distal nephron lumen. Between 10 and 30 days in captivity, spermatogenesis and secretion in the SSK ceased and the epithelial height of both tissues decreased. At approximately 60 days, testicular epithelial height increased and spermatogenic activity was reestablished. The SSK, however, remained regressed at 60 days.

Résumé : Nous décrivons les changements histologiques dans l’appareil reproducteur de mâles de Boiga irregularis (Merrem, 1802) (le serpent arboricole brun) capturés en nature et les modifications qui se produisent dans ces tissus à cause de la captivité. Nous comparons des serpents capturés en nature à des serpents gardés en captivité et sacrifiés environ aux jours 10, 30, 50 et 60+. Les serpents sacrifiés après 10 jours en captivité ne montrent aucune différence ni dans l’apparence histologique, ni dans la hauteur de l’épithélium, dans ni le testicule, ni le segment sexuel du rein (SSK) par rapport à des serpents sauvages. Les stades normaux de la spermatogenèse et l’ultrastructure normale du SSK s’observent dans le testicule et le rein chez les individus sauvages et captifs après 10 jours. Dans le cas du SSK, de larges vacuoles sécrétrices opaques aux électrons occupent les apex des cellules épithéliales, alors qu’un noyau basal, un réticulum endoplasmique granulaire et des appareils de Golgi remplissent la base de ces cellules. Toutes les cellules du SSK sont sécrétrices selon un mode que l’on définirait de la manière la plus précise comme apocrine. Au moment de la libération de la sécrétion, les vacuoles deviennent diffuses et la membrane apicale se rompt, versant le contenu du SSK dans la lumière du néphron distal. Entre les jours 10 et 30 de la captivité, la spermatogenèse et la sécrétion du SSK cessent et la hauteur de l’épithélium des deux tissus diminue. À environ 60 jours, la hauteur de l’épithélium testiculaire augmente et la spermatogenèse recommence. Le SSK, cependant, demeure en régression après 60 jours.

[Traduit par la Rédaction]

Aldridge, R.D., and Arackal, A.A. 2005. Reproductive biology and stress of captivity in male brown treesnakes (Boiga irregularis) on Guam. Aust. J. Zool. 53(4): 249–256.

Bishop, J.E. 1959. A histological and histochemical study of the kidney tubule of the common garter snake, Thamnophis sirtalis, with special reference to the sexual segment in the male. J. Morphol. 104(2): 307–357.

Cuellar, O. 1966. Oviducal anatomy and sperm storage structures in lizards. J. Morphol. 119(1): 7–19.

Del Conte, E., and Tamayo, J.G. 1973. Ultrastructure of the sexual segments of the kidney in male and female lizards, Cnemidophorus l. lemniscatus (L.). Z. Zellforsch. 144(3): 325–337.

Devine, M.C. 1975. Copulatory plugs in snakes: enforced chastity. Science, 187(4179): 844–845.

Fox, W. 1965. A comparison of the male urogenital systems of blind snakes, Leptotyphlopidae and Typhlopidae. Herpetologica, 21: 241–256.

Fox, H. 1977. The urogenital system of reptiles. In Biology of the Reptilia, Vol. 6: Morphology E. Edited by C. Gans and T.S. Parsons. Academic Press, New York. pp. 1–157.

Graham, S.P. 2006. An integrative analysis of reproduction and stress in free-living male cottonmouths, Agkistrodon piscivorus. M.Sc. thesis, Center for Behavioral Neuroscience, Georgia State University, Georgia.

Gribbins, K.M., Mills, E.M., and Sever, D.M. 2007. Ultrastructural examination of spermiogenesis within the testis of the ground skink, Scincella laterale (Squamata, Sauria, Scincidae). J. Morphol. 268(2): 181–192.

Gribbins, K.M., Rheubert, J.L., Collier, M.H., Siegel, D.S., and Sever, D.M. 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(5): 461–476.

Jordan, M.A., and Rodda, G.H. 1994. Identification of sex in Boiga irregularis: implications for understanding population dynamics in Guam. J. Herpetol. 28(3): 381–384.

Kiernan, J.A. 1990. Histological and histochemical methods: theory and practice. Pergamon Press, Inc., New York.

Krohmer, R.W. 2004. Variation in seasonal ultrastructure of sexual granules in the renal sexual segment of the Northern Water Snake, Nerodia sipedon sipedon. J. Morphol. 261(1): 70–80.

Kühnel, W., and Krisch, B. 1974. On the sexual segment of the kidney in the snake (Natric natrix). Cell Tissue Res. 148(3): 417–429.

Mathies, T., Felix, T.A., and Lance, V.A. 2001. Effects of trapping and subsequent short-term confinement stress on plasma corticosterone in the brown treesnake (Boiga irregularis) on Guam. Gen. Comp. Endocrinol. 124(1): 106–114.

Mathies, T., Cruz, J.A., Lance, V.A., Miller, L.A., and Savidge, J.A. 2010. Reproductive biology of male brown treesnakes (Boiga irregularis) on Guam. J. Herpetol. In press.

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(2): 99–108.

Pandha, S.K., and Thapliyal, J.P. 1964. Effect of male hormone on the renal sex segment of castrated males of the lizard Calotes versicolor. Copeia, 1964(3): 579–581.

Prasad, M.R.N., and Reddy, P.R.K. 1972. Physiology of the sexual segment of the kidney in reptiles. Gen. Comp. Endocrinol. 3: 649–662.

Prasad, M.R.N., and Sanyal, M.K. 1969. Effect of sex hormones on the sexual segment of kidney and other accessory reproductive organs of the Indian house lizard Hemidactylus flaviviridis Ruppell. Gen. Comp. Endocrinol. 12(1): 110–118.

Rodda, G.H., and Fritts, T.H. 1992. The impact of the introduction of the colubrid snake Boiga irregularis on Guam’s lizards. J. Herpetol. 26(2): 166–174.

Rodda, G.H., Fritts, T.H., McCoid, M.J., and Campbell, E.W., III. 1999. An overview of the biology of the Brown Treesnake (Boiga irregularis), a costly introduced pest on Pacific islands. In Problem snake management: The Habu and the Brown Treesnake. Edited by G.H. Rodda, Y.Sawai, D.Chiszar, and H. Tanaka. Cornell University Press, Ithaca. pp. 44–80.

Saint-Girons, H. 1972. Morphologie comparee du segment sexuel du rein des squamates (Reptilia). Arch. Anat. Microsc. Morphol. Exp. 61: 243–266.

Savidge, J.A. 1987. Extinction of an island forest avifauna by an introduced snake. Ecology, 68(3): 660–668.

Schuett, G.W., and Grober, M.S. 2000. Post-fight levels of plasma lactate and corticosterone in male copperheads, Agkistrodon contortrix (Serpentes, Viperidae): differences between winners and losers. Physiol. Behav. 71(3–4): 335–341.

Schuett, G.W., Harlow, H.J., Rose, J.D., Van Kirk, E.A., and Murdoch, W.J. 1996. Levels of plasma corticosterone and testosterone in male copperheads (Agkistrodon contortrix) following staged fights. Horm. Behav. 30(1): 60–68.

Sever, D.M., and Hopkins, W.A. 2005. Renal sexual segment of the ground skink, Scincella laterale (Reptilia, Squamata, Scincidae). J. Morphol. 266(1): 46–59.

Sever, D.M., Stevens, R.A., Ryan, T.J., and Hamlett, W.C. 2002. Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). III. Sexual segment of the male kidney. J. Morphol. 252(3): 238–254.

Sever, D.M., Siegel, D.S., Bagwill, A., Eckstut, M.E., Alexander, L., Camus, A., and Morgan, C. 2008. Renal sexual segment of the Cottonmouth snake, Agkistrodon piscivorous (Reptilia, Squamata, Viperidae). J. Morphol. 269(6): 640–653.

Sykes, K.L., and Klukowski, M. 2009. Effects of acute temperature change, confinement and housing on plasma corticosterone in water snakes, Nerodia sipedon (Colubridae: Natricinae). J. Exp. Zool. 311A(3): 172–181.

Volsøe, H. 1944. Structure and seasonal variation of the male reproductive organs of Vipera berus (L.). Spolia Zoologica Musei Hauniensis V. Skrifter, Zoologisk Museum, Københavns Universitet.

Wiles, G.J. 1987. Current research and future management of Marianas fruit bats (Chiroptera: Pteropodidae) on Guam. Aust. Mammal. 10: 93–95.