Reproductive strategies of the semifossorial snake Atractus zebrinus from the Atlantic Forest


  • Lucas Henrique Carvalho Siqueira
  • Jade Lima-Santos
  • Karina Maria Pereira Silva

Palabras clave:

Female sperm storage, Reproductive cycle, Secretive snakes, Sexual dimorphism, Spermiogenesis


 Secretive snakes (e.g., fossorial or semifossorial) show morphological adaptations that may constrain potential reproductive output. However, females can store sperm in the reproductive tract, increasing their reproductive potential. Thus, studies on the reproduction of fossorial and semifossorial species are of great interest for a complete understanding of snake reproductive strategies. Here, we investigate the reproductive strategies of the semifossorial snake Atractus zebrinus through macroscopic and histological analyzes of the male and female reproductive tracts. Females were larger and had more ventral scales than males, the most common pattern in snakes, and apparently conserved in the genera. The female reproductive cycle was seasonal, with gravid females occurring in spring and summer. Rainfall seems to be the major factor driving female reproductive seasonality, and sperm storage in the infundibular receptacles may ensure fertilization and multiple paternity. The male reproductive cycle was aseasonal. Spermiation, hypertrophy of the sexual segment of the kidney, and sperm storage in the ductus deferentia occurred over several months. This aseasonal reproduction in males may enhance paternity by increasing the species mating chances.


Abegg, A.D.; Passos, P.; Mario-Da-Rosa, C.; Azevedo W. Dos S.; Malta-Borges, L. & Bubadué J.M. 2020. Sexual dimorphism, ontogeny and static allometry of a semi-fossorial snake (genus Atractus). Zoologischer Anzeiger 287: 95-104.

Abramoff, M.D.; Magalhães P.J. & Ram, S.J. 2004. Image processing with ImageJ. Biophotonics International 11: 36- 42. ttps://

Aldridge, R.D.; Jellen, B.C.; Siegel, D.S. & Wisniewski, S.S. 2011. The Sexual Segment of the Kidney: 477-509. In: Aldridge, R.D. & Sever, D.M. (Eds), Reproductive Biology and Phylogeny of Snakes. Science Publishers, Enfield.

Aldridge, R.D. & Duvall, D. 2002. Evolution of the mating season in the pitvipers of North America. Herpetological Monographs 16: 1-25.

Almeida-Santos, S.M.; Braz, H.B.; Santos, L.C.; Sueiro, L.R.; Barros, V.A.; Rojas, C.A. & Kasperoviczus, K.N. 2014. Biologia reprodutiva de serpentes: recomendações para a coleta e análise de dados. Herpetologia Brasileira 3: 14-24

Alves, F.Q.; Argolo, A.J.S. & Jim, J. 2005. Biologia reprodutiva de Dipsas neivai e Dipsas catesbyi (Sentzen) (Serpentes, Colubridae) no sudeste da Bahia, Brasil. Revista Brasileira de Zoologia 22: 573-579.

Angarita-Sierra, T. & López-Hurtado C.A. 2020. Exploring the reproductive ecology of the tropical semifossorial snake Ninia atrata. Zoological research, 41: 157. 10.24272/j. issn.2095-8137.2020.015

Arnold, S.J. 1988. Quantitative genetics and selection in natural populations: microevolution of vertebral numbers in the Garter snake Thamnophis elegans: 619-637. In: Weir, B.S.; Eisen, E.J.; Goodman, M.M. & Namkoong, G. (Eds), Proceedings of the Second International Conference on Quantitative Genetics. Sinauer Associates Inc, Sunderland. Balestrin, R.L. & Di-Bernardo, M. 2005. Reproductive biology of Atractus reticulatus (Boulenger, 1885) (Serpentes, Colubridae) in southern Brazil. Herpetological Journal 15: 195-199.

Barbo, F.E.; Marques, O.A.V. & Sawaya, R.J. 2011. Diversity, natural history, and distribution of snakes in the municipality of São Paulo. South American Journal of Herpetology 6: 135-160.

Barros, V.A.; Rojas, C.A. & Ameida-Santos, S.M. 2014. Is rainfall seasonality important for reproductive strategies in viviparous Neotropical pit vipers? a case study with Bothrops leucurus from Brazil Atlantic Forest. Herpetological Journal 24: 67–75.

Barros, V.A.; Sueiro, L.R. & Almeida-Santos, S.M. 2012. Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns. Herpetological Journal 22: 97-104.

Barros, F.C.; Herrel, A. & Kohlsdorf, T. 2011. Head shape evolution in Gymnophthalmidae: does habitat use constrain the evolution of cranial design in fossorial lizards? Journal of Evolutionary Biology 24: 2423-2433.

Bellini, G.P.; Arzamendia, V. & Giraudo, A.R. 2013. Ecology of Thamnodynastes hypoconia in subtropical-temperate South America. Herpetologica 69: 67-79. doi: https://doi. org/10.1655/HERPETOLOGICA-D-12-00027

Bizerra, A.F.; Marques, O.A.V. & Sazima, I. 2005. Reproduction and feeding of the colubrid snake. Amphibia-Reptilia 26: 33–38. Doi: 10.1163/1568538053693350

Böhm, M. et al. 2013. The conservation status of the world’s reptiles. Biological Conservation 157: 372–385. doi. org/10.1016/j.biocon.2012.07.015

Braz, H.B.; Kasperoviczus, K.N. & Guedes, T.B. 2019. Reproductive Biology of the Fossorial Snake Apostolepis gaboi (Elapomorphini): A Threatened and Poorly Known

Species from the Caatinga Region. South American Journal of Herpetology 14: 37-47.

Braz, H.B.; Kasperoviczus, K.N. & Almeida-Santos, S.M. 2014. Reproductive ecology and diet of the fossorial snake Phalotris lativittatus in the Brazilian Cerrado. Herpetological Journal 24: 49-57.

Brown, G.P. & Shine, R. 2006. Why do most tropical animals reproduce seasonally? Testing hypotheses on an Australian snake. Ecology 87: 133-143.

Costa, H.C. & Bérnils, R.S. 2018. Répteis do Brasil e suas Unidades Federativas: Lista de espécies. Herpetologia Brasileira 8:.

Crews, D. & Moore, M.C. 1986. Evolution of mechanisms controlling mating behavior. Science 231: 121-125.

Crews, D. & Garstka, W.R. 1982. The Ecological Physiology of a Garter Snake. Scientific American 247: 158-168. doi. org/10.1038/scientificamerican1182-158

Cyriak, V.P. & Kodandaramaiah, U. 2018. Digging their own macroevolutionary grave: fossoriality as an evolutionary dead end in snakes. Journal of Evolutionary Biology 31: 587-598.

DeNardo, D.F. & Taylor, E.N. 2011. Hormones and reproduction in free-ranging snakes: 265-287. In Aldridge, R.D. & Sever, D.M. (Eds.), Reproductive Biology and Phylogeny of Snakes, FL: CRC Press, Boca Raton.

De Resende, F.C. & Nascimento, L.B. 2015. The Female Reproductive Cycle of the Neotropical Snake Atractus pantostictus (Fernandes and Puorto, 1993) from South‐eastern Brazil. Anatomia, histologia, embryologia 44: 225- 235.

Dowling, H.G. 1951. A proposed standard system of counting ventrals in snakes. British Journal of Herpetology 1: 97-99.

Fernandes, R.; Freire, E.M.X. & Puorto, G. 2000. Geographic variation of the Brazilian atlantic rain forest snake Atractus maculatus (Günther, 1858) with the revalidation of Rhabdosoma zebrinum Jan, 1862 (Serpentes: Colubridae). Boletim do Museu Nacional Nova Série Zoologia 419: 1-8.

Fernandes, R. & Puorto, G. 1993. A new species of Atractus from Brazil and the status of A. guentheri (Serpentes: Colubridae). Memórias do Instituto Butantan 55: 7-14.

Ferreira-Silva, C.; Ribeiro, S.C.; De Alcantara, E.P. & Ávila, R.W. 2019. Natural history of the rare and endangered snake Atractus ronnie (Serpentes: Colubridae) in northeastern Brazil. Phyllomedusa 18: 77-87.

Friesen, C.R.; Kahrl, A.F. & Olsson, M. 2020. Sperm competition in squamate reptiles: Sperm competition in lizards and snakes. Philosophical Transactions of the Royal Society B: Biological Sciences 375. rstb.2020.0079rstb20200079

Friesen, C.R.; Shine, R., Krohmer, R.W. & Mason, R.T. 2013. Not

just a chastity belt: The functional significance of mating plugs in garter snakes, revisited. Biological Journal of the Linnean Society 109: 893-907.

García-Cobos, D.; Crawford, A.J. & Ramírez-Pinilla, M.P. 2021. Reproductive phenology in a Neotropical aquatic snake shows marked seasonality influenced by rainfall patterns. Journal of Natural History 54: 1845-1862.

Giraudo, A.R. & Scrocchi, G.J. 2000. The genus Atractus (Serpentes: Colubridae) in north-eastern Argentina. Herpetological Journal 10: 81-90.

Goldberg, S.R. 2004. Reproduction of the coffee snake, Ninia maculata (Serpentes: Colubridae), From Costa Rica. Texas Journal of Science 56: 81-84.

Grazziotin, F.G.; Zaher, H.; Murphy, R.W.; Scrocchi, G.; Benavides, M.A.; Zhang, Y. & Bonatto, S.L. 2012. Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics 28: 437–459. doi. org/10.1111/j.1096-0031.2012.00393.x

Gualdrón-Durán, L.E.; Calvo-Castellanos, M.F. & Ramírez- Pinilla, M.P. 2019. Annual Reproductive Activity and Morphology of the Reproductive System of an Andean Population of Atractus (Serpentes, Colubridae). South American Journal of Herpetoly 14: 58. sajh-d-16-00054.1

Junqueira, L.C. & Carneiro, J. 2013. Biologia celular e molecular. Guanabara Koogan, Rio de Janeiro.

King, R.B. 1989. Sexual dimorphism in snake tail length: sexual selection, natural selection, or morphological constraint? Biological Journal of the Linnean Society 38: 133-154.

Khouri, R. S.; Almeida-Santos, S. M. & Fernandes D. S. 2020. Anatomy of the reproductive system of a population of Amerotyphlops brongersmianus from southeastern Brazil (Serpentes: Scolecophidia). The Anatomical Record 330: 2485–2496. DOI: 10.1002/ar.24382.

Krohmer, R.W. 2004. Variation in seasonal ultrastructure of sexual granules in the renal sexual segment of the northern water snake, Nerodia sipedon sipedon. Journal of Morphology 261: 70-80.

Levine, B.A.; Schuett, G.W. & Booth, W. 2021. Exceptional long-term sperm storage by a female vertebrate. PLOS ONE 16(6): e0252049.

Lindell, L.E.; Forsman, A. & Merilä, J. 1993. Variation in number of vertebral scales in snakes: effects on body size, growth rate and survival in the Adder, Vipera berus. Journal of Zoology 1993: 101-115.

Loebens, L.; Almeida-Santos, S.M. & Cechin, S.Z. 2020. Reproductive biology of the Sword Snake Tomodon dorsatus (Serpentes: Dipsadidae) in South Brazil: comparisons within the tribe Tachymenini. Amphibia-Reptilia 41: 445-459. doi. org/10.1163/15685381-bja10012

Loebens, L.; Rojas, C.A.; Almeida-Santos, S.M. & Cechin, S.Z. 2017. Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: Female reproductive cycle. Acta Zoologica 99: 105-114.

Loebens, L.; Cechin, S.Z.; Theis, T.F.; Moura, L.B. & Almeida- Santos, S.M. 2016. Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: Male reproductive cycle. Acta Zoologica 98, 329–339. doi: 10.1111/azo.12172

Lovich, J.E. & Gibbons, J.W.; 1992. A review of techniques for quantifying sexual size dimorphism. Growth, Development and Aging 56: 269-281.

Lutterschmidt, D.I. & Masob, R.T. 2009. Endocrine mechanisms mediating temperature-induced reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis). Journal of Experimental Biology 212: 3108-3118.

Manes, M.E.; Noriega, T.; Casal F.C. & Apichela, S. 2007. Ovarian changes during the reproductive cycle of the Tupinambis merianae lizard raised in a temperate environment. Cuadernos de Herpetología 21: 21-29.

Marques, O.A.V.; Eterovic, A. & Sazima, I. 2019. Serpentes da Mata Atlântica: guia ilustrado para as florestas costeiras do Brasil. Ponto A Editora, Cotia.

Marques, O.A.V. & Puorto, G. 1998. Feeding, reproduction and growth in the crowned snake. Amphibia-Reptilia 19: 311- 318.

Marques, O.A.V. 1996. Reproduction, seasonal activity and growth of the coral snake, Micrurus corallinus (Elapidae), in the southeastern Atlantic Forest in Brazil. Amphibia-Reptilia 17: 277-285.

Martins, M. & Oliveira, M.E. 1993. The snakes of the genus Atractus Wagler (Reptilia: Squamata: Colubridae) from the Manaus region, central Amazonia, Brazil. Zoologische Mededelingen 67: 21-40.

Mathies, T. 2011. Reproductive cycles of tropical snakes: 511- 550. In: Aldridge, R.D. & Sever, D.M. (Eds), Reproductive biology and phylogeny of snakes. CRC Press, Boca Raton.

Mendonça, F. & Danni-Oliveira, I.M. 2007. Climatologia: Noções básicas e climas do Brasil. Oficina de Textos, São Paulo.

Meneses-Pelayo, E. & Passos. P. 2019. New Polychromatic Species of Atractus (Serpentes: Dipsadidae) from the Eastern Portion of the Colombian Andes. Copeia 2019: 250-261. doi. org/10.1643/CH-18-163

Myers, C.W. 2003. Rare snakes-five new species from eastern Panama: reviews of northern Atractus and southern Geophis (Colubridae: Dipsadinae). American Museum Novitates 2003: 1-47.

Navas, C.A.; Antoniazzi, M.M.; Carvalho, J.E.; Chaui-Berlink, J.G.; James, R.S.; Jared, C.; Kohlsdorf, T.; Pai-Silva, M.D. & Wilson, R.S. 2004. Morphological

and physiological specialization for digging in amphisbaenians, an ancient lineage of fossorial vertebrates. Journal of Experimental Biology 207: 2433-2441

Nogueira, C.C et al. 2019. Atlas of Brazilian snakes: Verified point-locality maps to mitigate the Wallacean shortfall in a megadiverse snake fauna. South American Journal of Herpetology, 14: 1–274. 2994/ SAJH-D-19-00120.1.

Passos, P.; Prudente, A. L.C.; Ramos, L.O.; Caicedo-Portilla, J.R. & Lynch, J.D. 2018. Species delimitations in the Atractus collaris complex (Serpentes: Dipsadidae). Zootaxa, 4392: 491–520.

Passos, P.; Echevarría, L.Y. & Venegas, P.J. 2013. Morphological variation of Atractus carrioni (Serpentes: Dipsadidae). South American Journal of Herpetology 8: 109-120.

Passos, P.; Fernandes, R.; Bernils, R.S. & Moura-Leite, J.D. 2010a. Taxonomic revision of the Brazilian Atlantic Forest Atractus (Reptilia: Serpentes: Dipsadidae). Zootaxa 23: 64-63.

Passos, P.; Dobiey, M. & Venegas, P.J. 2010b. Variation and natural history notes on giant groundsnake, Atractus gigas (Serpentes: Dipsadidae). South American Journal of Herpetology 5: 73-82.

Perkins, M.J. & Palmer, B.D. 1996. Histology and functional morphology of the oviduct of an oviparous snake, Diadophis

punctatus. Journal of Morphology 227: 67-79.

Pizzatto, L.; Cantor, M., Oliveira, J.L; Marques, O.A.V.; Capovilla, V. & Martins, M. 2008. Reproductive Ecology of Dipsadine Snakes, With Emphasis on South American Species. Herpetologica, 64: 168-179.

Pizzatto, L. & Marques, O.A.V. 2002. Reproductive biology of the false coral snake Oxyrhopus guibei (Colubridae) from southeastern Brazil. Amphibia-Reptilia 23: 495-504. doi. org/10.1163/15685380260462392

Pizzatto, L. & Marques, O.A.V. 2006. Interpopulational variation in reproductive cycle and activity of the water snake Liophis miliaris (Colubridae) in Brazil. Herpetological Journal 16: 353-362.

Pleguezuelos, J.M. & Feriche, M. 1999. Reproductive ecology of the horseshoe whip snake (Coluber hippocrepis) in the Iberian Peninsula. Journal of Herpetology 33: 202–207. doi. org/10.2307/1565715

Pough, F.H. 1980. The advantages of ectothermy for tetrapods. American Naturalist 115: 92-112.

R Development Core Team. 2021. R: A language and environment for statistical computing. Retrieved from

Rivas, J.A. & Burghardt, G.M. 2001. Understanding sexual size dimorphism in snakes: wearing the snake’s shoes. Animal Behavior 61: 1-6.

Rojas, C.A.; Barros, V.A. & Almeida-Santos, S.M. 2017. A histological and ultrastructural investigation of the female reproductive system of the water snake (Erythrolamprus miliaris): Oviductal cycle and sperm storage. Acta Zoologica 2017: 1-12.

Rojas, C.A, Barros, V.A & Almeida-Santos, S.M. 2015. Sperm storage and morphofunctional bases of the female reproductive tract of the snake Philodryas patagoniensis from southeastern Brazil. Zoomorphology 134: 577-586.

Rojas, C.A.; Barros, V.A. & Almeida-Santos S.M. 2013. The reproductive cycle of the male sleep snake Sibynomorphus mikanii (Schlegel, 1837) from southeastern Brazil. Journal of Morphology 274: 215-228.

Saint-Girons, H. 1982. Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica 38: 5-16.

Saint-Girons, H. 1957. Le cycle sexuel chez Vipera aspis dans l'ouest de la France. Bulletin Biologique de la France et de la Belgique 91: 284–350.

Sandoval, M.; Palomas, S.; Ayarragaray, M. & Álvarez, B.B. 2009. Nesting site, clutch size and development of Atractus reticulatus (Serpentes, Colubridae) from Corrientes, Argentina. Herpetological Bulletin 109: 11-16.

Schuett, G.W.; Harlow, H.J.; Rose, J.D.;Van Kirk, E.A. & Murdoch; W.J. 1997. Annual cycle of plasma testosterone in male copperheads, Agkistrodon contortrix (Serpentes, Viperidae): Relationship to timing of spermatogenesis, mating, and agonistic behavior. General and Comparative Endocrinology 105: 417-424.

Sever, D.M. & Hopkins, W.A. 2005. Renal sexual segment of the ground skink, Scincella laterale (Reptilia, Squamata, Scincidae). Journal of Morphology 266: 46-59.

Shine, R.; Olsson, M.M.; Moore, I.T.; Lemaster, M.P. & Mason, R.T. 1999. Why do male snakes have longer tails than females? Proceedings of the Royal Society B 266: 2147-2151.

Shine, R. 1994. Sexual size dimorphism in snakes revisited. Copeia 1994: 326-346.

Shine R. 1993. Sexual dimorphism in snakes: 49-86. In: Seigel, R.A. & Collins, J.T. (Eds), Snakes: Ecology and Behavior, McGraw-Hill, New York.

Shine R. 1978. Growth rates and sexual maturation in six species of Australian Elapid snakes. Herpetologica 34: 73-79.

Siegel, D.S.; Miralles, A.; Chabarria, R.E. & Aldridge, R.D. 2011. Female reproductive anatomy: Cloaca, Oviduct, and Sperm storage: 347-409. In: Aldridge R. D.; & Sever, D.M. (Eds.). Reproductive Biology and Phylogeny of Snakes. CRC Press, Boca Raton.

Siegel, D.S. & Sever, D.M. 2008. Sperm Aggregations in female Agkistrodon piscivorus (Reptilia, Squamata): A histological and ultrastructural investigation. Journal of Morphology 269: 189-206.

Silva, K.M.P.; Silva, K.B.; Sueiro, L.R.; Oliveira, M.E.E.S. & Almeida-Santos, S.M. 2019a. Reproductive biology of Bothrops atrox (Serpentes, Viperidae, Crotalinae) from the Brazilian Amazon. Herpetologica 75: 198-207.

Silva, K.M.P.; Barros, V.A.; Rojas, C.A. & Almeida‐Santos, S.M. 2019b. Infundibular sperm storage and uterine muscular twisting in the Amazonian lancehead, Bothrops atrox. The Anatomical Record 303: 3145-3154 .

Silva, K.M.P.; Braz, H.B.; Kasperoviczus, K.N.; Marques, O.A.V. & Almeida-Santos, S.M. 2020. Reproduction in the pitviper Bothrops jararacussu: Large females increase their reproductive output while small males increase their potential to mate. Zoology, 142, 125816. https://doi. org/10.1016/j.zool.2020.125816

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). General and Comparative Endocrinology 136: 328-337. ygcen.2004.01.008

Teixeira, V.H.S.; Quintela, F.M. & Loebmann, D. 2020. Reproductive biology of Erythrolamprus jaegeri coralliventris (Serpentes: Dipsadidae) in the Brazilian Coastal Pampa. Anais da Academia Brasileira de Ciências 92: e20181383. DOI 10.1590/0001-3765202020181383.

Travaglia-Cardoso, S.R. & Maia, D.C. 2012. Clutch size and incubation period of Atractus pantostictus (Fernandes & Puorto, 1993) (Serpentes: Dipsadidae). Biologia Geral e Experimental 12: 5-6.

Uller, T. & Olsson, M. 2008. Multiple paternity in reptiles: Patterns and processes. Molecular Ecology 17: 2566-2580.

Vieira, S.; Romero De Perez, G. & Ramirez-Pinilla, M.P. 2010. Ultrastructure of the ovarian follicles in the placentotrophic Andean Lizard of the genus Mabuya (Squamata: Scincidae). Journal of Morphology 271: 738-749.

Vitt, L.J. 1992. Diversity of Reproductive Strategies Among Brazilian Lizards and Snakes: The Significance of Lineage and Adaptation: 135 – 149: In Hamlet, W.C. (Ed.), Reproductive Biology of South American Vertebrates II, Springer-V.

Zaher, H. et al. 2019. Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PloS One 14. pone.0216148

Zanella, N. & D’agostini, F. 2018. Ecology of the snake Atractus paraguayensis (Dipsadidae) in southern Brazil. Zoologia 35: e12487




Cómo citar

Carvalho Siqueira, L. H. ., Lima-Santos, J. ., & Pereira Silva, K. M. . (2022). Reproductive strategies of the semifossorial snake Atractus zebrinus from the Atlantic Forest. Cuadernos De Herpetología, 36(1). Recuperado a partir de