Animal Reproduction (AR)
Animal Reproduction (AR)
Original Articles

Hormonal and ultrasonographic characterization of the seasonal reproductive cycle of male and female Crotalus durissus terrificus

Priscilla M. Matayoshi, Priscilla M. Souza, Vinícius P.O. Gasparotto, Michelle S. Araujo, Carla R.B. Simões, Fabiana F. Souza, Eunice Oba, Vânia M.V. Machado, Rui S.F. Júnior, Nereu C. Prestes

Downloads: 0
Views: 35


Research concerning to characterize seasonal reproductive cycle in males and females of Crotalus durissus terrificus by ultrasound and hormonal measurement. Reproductive aspects (follicular and testicular cycles, and pregnancy) from 28 adult snakes (14 males and 14 females) during different months of the years were studied. Snakes housed individually in cages in an environment with controlled luminosity and humidity, and fed monthly. Females were examined by ultrasound during quiescence and active follicular phase, and pregnancy for follicular and embryo/fetal development. Males were evaluated to testicular echotexture and measurements during reproductive and non-reproductive season. The blood samples were collected from males and females for serum testosterone and progesterone determination, respectively. In 77% males the testes were identified by ultrasound and found increased size during summer, decreased serum testosterone in winter, and positive correlation between serum testosterone and testes size. There was no change in testicular echotexture in according to season. Testosterone concentration was decreased during winter and it was positively correlated with testes size. In 71% females, were observed follicular development (vitellogenesis) and gestation since winter to spring by ultrasonography. Parturition occurred mainly in summer. Pregnancy length was 123.0 ± 11.4 days, with mean 6.9 ± 1.5 newborns/female, and there was gradual increase of serum progesterone during this period. There was no variation in progesterone concentration in non-gravid females. Males and females Tropical Rattlesnake show seasonal variation of reproductive cycle and was clear a biennial cycle in female. The ultrasonography can be considered an essential tool to accomplish the follicular development, pregnancy and testicular alterations in Tropical Rattlesnake.


follicle, gestation, progesterone, rattlesnake, testosterone.


Almeida-Santos SM, Salomão MG. 1997. Long-term sperm storage in the female neotropical rattlesnake Crotalus durissus terrificus (Viperidae, Crotalinae). Jpn J Herpetol, 17:46-52.

Almeida-Santos SM, Aguiar LFSA, Balestrin RL. 1998. Micrurus frontalis (Coral Snake). Male Combat. Herpetol Rev, 29:242.

Almeida-Santos SM, Orsi AM. 2002. Reproductive cycle of Crotalus durissus and Bothrops jararaca (Serpentes, Viperidae): morphology and function of the oviduct. Rev Bras Reprod Anim, 26:109-112.

Almeida-Santos SM, Salomão MG. 2002. Reproduction in neotropical pitvipers, with emphasis on species of the genus Bothrops. In Schuett GW, Höggren M, Douglas ME, Greene HW (Eds.). Biology of the vipers Carmel: Indiana. Eagle Mountain Publishing. pp.445-462.

Almeida-Santos SM, Abdalla FMF, Silveira PF, Yamanouye N, Breno MC, Salomão MG. 2004. Reproductive cycle of the neotropical Crotalus durissus terrificus: I. Seasonal levels and interplay between steroid hormones and vasotocinase. Gen Comp Endocrinol, 139:143-150.

Almeida-Santos SM. 2005. Reproductive models serpents: sperm storage and placentation in Crotalus durissus and Bothrops jararaca (Serpentes: Viperidae). [in Portugueses]. São Paulo, Brazil: University of São Paulo. Thesis.

Augusto AQ. 2007. Ultrasonography. In Cubas ZS, Silva JCR, Catão-Dias JL (Eds.). Wild Animals Treaty [in Portuguese]. São Paulo, Brazil: Roca. pp.879-895.

Banzato T, Hellebuyck A, Van Caelenberg JH, Saunders AZ. 2013. A review of diagnostic imaging of snakes and lizards. Vet Rec, 173:43-49.

Bertona M, Chiaraviglio M. 2003. Reproductive biology, mating aggregations, and sexual dimorphism of the argentine boa constrictor (Boa constrictor occidentalis). J Herpetol, 37:510-516.

Betkowski SE. 2006. Study of serum progesterone and estradiol levels and monitoration of rattlesnakes ovaries ultrasound characteristics (Crotalus durissus terrificus) kept in captivity over 12-month period [in Portuguese]. São Paulo, Brazil: University of São Paulo. Dissertation.

Blem CR. 1982. Biennial reproduction in snakes: an alternative hypothesis. Copeia, 4:961-963.

Bonnet X, Naulleou G, Bradshaw D, Shine R. 2001. Changes in plasma progesterone in relation to vitellogenesis and gestation in the viviparous snake Vipera aspis. Gen Comp Endocrinol, 121:84-94.

Calvete JJ, Sanz L, Pérez A, Borges A, Vargas AM, Lomonte B, Angulo Y, Gutiérrez JM, Chalkidis HM, Mourão RHV, Furtado MFD, Moura da Silva AM. 2011. Snake population venomics and antivenomics of Bothrops atrox: Paedomorphism along its transamazonian dispersal and implications of geographic venom variability on snakebite management. J Proteomics, 74:510-527.

Chiaraviglio M, Sironi M, Cervantes R, Berona M., Lucino S. 1998. Imagenes de ultrasonido de estruturas reproductivas em Boa constrictor occidentalis (Serpentes: Boidae). Gayana Zool, 62:91-95.

Cunha MR, Menezes FA, Santos GR, Pinto CAL, Barraviera B, Margins VCA, Plepis AMG, Ferreira Jr RS. 2015. Hydroxyapatite and a new fibrin sealant derived from snake venom as scaffold to treatment of cranial defects in rats. Mat Res, 18:196-203.

Cura JE, Blanzaco DP, Brisson C, Cura MA, Cabrol R, Larrateguy L, Mendez C, Sechi JC, Silveira JS, Theiller E, De Roodt AR, Vidal JC. 2002. Phase I and pharmacokinetics study of crotoxin (Cytotoxic PLA2, NSC-624244) in patients with advanced cancer. Clin Cancer Res, 8(4): 1033-41.

Denardo DF, K Autumn. 2001. Effect of male presence on reproductive activity in captive female blood Pythons, Python Curtus Copeia 4, 1138-1141.

Girling JE. 2002. The reptilian oviduct: a review of structure and function and directions for future research. J Exp Zool, 293:141-170.

Gnudi G, Volta A, Di Ianni F, Bonazzi M, Manfredi S, Bertoni G. 2009. Use of ultrasonography and contrast radiography for snake gender determination. Vet Radiol Ultrasound, 50:309-311.

Greenberg N, Wingfield J. 1987. Stress and reproduction: reciprocal relationships. In Norris DO, Jones RE (Eds.). Hormones and Reproduction in Fishes, Amphibians, and Reptiles. New York, USA: Plenum Press. pp.461-503.

Grumbles JS, Rostal DC. 1997. Diagnostic imaging: ultrasonography. In: Ackerman, L. (Ed.), The Biology, Husbandry and Health Care of Reptiles: The Health Care of Reptiles, 3. T.F.H. Publications Inc., New Jersey, pp. 613-627.

Hoss SK, Schuett GW, Early RL, Smith LL. 2011. Reproduction in male Crotalus adamanteus beauvois (Eastern Diamond-backed Rattlesnake): relationship of plasma testosterone to testis and kidney dimensions and the mating season. Southeast Nat, 10:95-108.

Isaza R, Ackerman N, Jacobson RE. 1993. Ultrasound imaging of the coelomic structures in the Boa constrictor. Vet Radiol Ultrasound, 34:445-450.

January-Cinquini TRF. 2004. Reproductive capacity of Bothrops jararaca (Serpentes, Viperidae). Iheringia Sér Zool, 94:429-431.

Kumar S, Kumar S, Beh, Y, Gupta RK. 2014. Development and standardization of ELISA as pre-screen test for the potency estimation during commercial production of antisnake venom serum (ASVS). Am J Biomed Sci, 6:20-31.

Lance VA, Rostal DC, Elsey RM, Trosclair III PL. 2009. Ultrassonography of reproductive structures and hormonal correlates of follicular development in female American alligators, Alligator mississippiensis, in southwest Louisiana. Gen Comp Endocrinol, 162:251-256.

Lind CM, Beaupre SJ. 2014. Natural variation in steroid hormone profiles of male Timber Rattlesnakes, Crotalus horridus, in northwest Arkansas. Gen Comp Endocrinol, 206:72-79.

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.

Neto FCP, Guerra PC, Costa FB, Araujo AVC, Miglino MA, Bombonato PP, Vulcano LC, Alves FR. 2009. Ultra-sonografia do fígado, aparelho renal e reprodutivo da jibóia (Boa constrictor). Pesq Vet Bras, 29:317-321.

Neves MS, Sousa DRT, Ferreira MPSBC, Frota MZM, Souza JVB, Lozano JLL. 2015. Evaluation of antifungal activity of snake venoms from the Amazon forest. J. Yeast Fungal Res, 6:11-16.

Nudel BC, Perdoménico C, Iácono R, Cascone O. 2012. Optimization by factorial analysis of caprylic acid precipitation of non-immunoglobulins from hyperimmune equine plasma for antivenom preparation.Toxicon, 59:68-73.

Pizzatto L. 2006. Ecomorphology and reproductive strategies in Boidae (Serpentes), with emphasis on Neotropical species [in Portugueses]. São Paulo, Brazil: University of Campinas. Tesis.

Raiti P. 2000. Transcoelomic ultrasonography of the reproductive tract reptile. Exotic DVM Vet. Mag, 1:27-32.

Ramirez-Bautista A, Gutierrez-Mayen G. 2003. Reproductive ecology of Sceloporus utiformis (Sauria: phrynosomatidae) from the tropical dry forest of Mexico. J Herpetol, 37:1-10.

Redrobe S, Wilkinson RJ. 2002. Reptile and amphibian anatomy and imaging. In Redrobe S, Meredith A. (Eds.). Manual of Exotic Pets. Catalunha, Spain: Graphs. pp. 193-207.

Reeks TA, Fry BG, Alewood PF. 2015. Privileged frameworks from snake venom. Cell Mol Life Sci, 72:1939-1958.

Root CR, Spaulding KA. 1994. Diagnostic imaging theriogenology companion animals. Semin Vet Med Surg, 9:7-27.

Salomão MG, Almeida-Santos SM. 2002. The reproductive cycle in male Neotropical Rattlesnake (Crotalus durissus terrificus). In Schuett GW, Hoggren M, Douglas ME, Green HW (Eds.). Biology of the Vipers. Utah, USA: Eagle Mountain Pub Lc. pp. 507-514.

Schuett GW. 1992. Is long-term storage an important component of the reproductive biology of temperate pitvipers? In Campbell JA, Brodie Jr ED (Eds). Biology of the Pitvipers. Texas, USA: Selva. pp.169-184.

Seigel RA, Ford NB. 1987. Reproductive ecology. In Seigel RA, Collins JT, Novak SS. (Eds.). Snakes: ecology and evolutionary biology. New York, USA: Mcmillan. pp. 210-252.

Shine R. 2003. Reproductive strategies in snakes. Proc Biol Sci, 270:995-1004.

Soares MA, Pujatti PB, Fortes-Dias CL, Antonelli L, RG Santos. 2010. Crotalus durissus terrificus venom as a source of antitumoral agents. J Venom Anim Toxins Incl Trop Dis, 16(3):480-492.

Stahlschmidt Z, Brashears J, Denaro D. 2011. The use of ultrasonography to assess reproductive investment and output in pythons. Biol J Linnean Soc, 103:772-778.

Stetter MD. 2006. Ultrasonography. In Mader, DR (Ed.). Reptile in Medicine and Surgery. Philadelphia, USA: WB Saunders. pp. 665-674.

Taylor EN, Denardo DF. 2005. Reproductive ecology of Western Diamond-backed Rattlesnakes (Crotalus atrox) in the Sonoran Desert. Copeia, 1:152-158.

Yamanouye N, Silveira PF, Abdalla FMF, Almeida-Santos SM, Breno MC, Salomão MG. 2004. Reproductive cycle of the neotropical Crotalus durissus terrificus: II. Establishment and maintenance of the uterine muscular twisting, a strategy for long-term sperm storage. Gen Comp Endocrinol, 139:151-157.

Zacariotti RL. 2004. Longitudinal study of rattlesnake (Crotalus durissus terrificus) spermogram and serum testosterone levels coming from nature São Paulo state [in Portuguese]. São Paulo, Brazil: University of São Paulo. Dissertation.

5c07e7370e8825a47b0e27c2 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections