All Title Author
Keywords Abstract

Reproductive Biology of Bothrops erythromelas from the Brazilian Caatinga

DOI: 10.1155/2014/680861

Full-Text   Cite this paper   Add to My Lib


The reproductive biology of Bothrops erythromelas, a small pit viper from the Caatinga, a semiarid biome in Brazil, is described based on analysis of individuals deposited in zoological collections. Males are smaller and also attain sexual maturity at a smaller size than females. Female reproductive cycle is seasonal with an extended period of secondary vitellogenesis and births occurring in a restricted period from late spring to early summer. Sperm storage in females may probably occur in infundibular tubular glands and uterine muscular twisting (UMT), which is a polymorphic condition within B. erythromelas. Seasonal spermatogenesis in males is variable with some intraspecific variation regarding the male reproductive stage per season. Most males are reproductively active during spring/summer and reproductively quiescent during autumn/winter, although some individuals vary (e.g., show testicular spermatogenesis and active sexual segment of the kidneys (SSK) during winter). The SSK could be identified in every male. Most males showed highly hypertrophied SSK in spring/summer and moderately hypertrophied SSK in autumn/winter. The ampulla ductus deferentis was observed and histochemical reactions were conducted. We discuss the probable influence of the unique environmental conditions of the Caatinga region and phylogenetic inertia in the reproductive patterns of this snake species. 1. Introduction The Caatinga domain, a mosaic of thorny bushes and seasonal dry forest, is a semiarid biome exclusive to Brazil. It is characterized by an extremely irregular rainfall pattern with severe dry seasons in some years [1]. Reptiles that live in arid environments may show physiological, behavioral, ecological, and morphological adaptations related to water scarcity in the environment [2]. Recently, a long-term study in the field showed that timing of parturition is influenced by rainfall seasonality in Crotalus atrox, a pit viper species from the Sonoran Desert [3]. To our knowledge, few studies addressed questions related to the influence of rainfall in the determination of reproductive strategies in snakes [3, 4]. Pit viper species from the Caatinga region are good models to explore questions on the influence of environmental variables in the reproductive cycles because this region has unique characteristics regarding patterns of temperature and rainfall [1], and some data on reproduction of pit viper species from the Neotropical region including species from the Caatinga region are available for comparisons [4–9]. Bothrops erythromelas is a terrestrial and


[1]  A. N. Ab’Saber, Os domínios de natureza no Brasil: potencialidades paisagísticas, Atêlie Editorial, S?o Paulo, Brazil, 2003.
[2]  F. H. Pough, R. M. Andrews, J. E. Cadle, M. L. Crump, A. H. Savitzky, and K. D. Wells, Herpetology, Pearson Prentice Hall, Upper Saddle River, NJ, USA, 2004.
[3]  G. W. Schuett, R. A. Repp, S. K. Hoss, and H. W. Herrmann, “Environmentally cued parturition in a desert rattlesnake, Crotalus atrox,” Biological Journal of the Linnean Society, vol. 110, no. 4, pp. 866–877, 2013.
[4]  V. A. Barros, C. A. Rojas, and S. M. Almeida-Santos, “Is rainfall seasonality important for reproductve strategies in viviparous neotropical pit vipers? A case study with Bothrops leucurus from the Brazilian Atlantc Forest,” Herpetological Journal, vol. 24, no. 2, pp. 69–77, 2014.
[5]  S. M. Almeida-Santos and M. G. Salom?o, “Reproduction in neotropical pitvipers, with emphasis on species of the genus Bothrops,” in Biology of the Vipers, G. W. Schuett, M. H?ggren, M. E. Douglas, and H. W. Greene, Eds., Eagle Mountain Publishing, Eagle Mountain, Calif, USA, 2002.
[6]  V. A. Barros, L. R. Sueiro, and S. M. Almeida-Santos, “Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns,” Herpetological Journal, vol. 22, no. 2, pp. 97–104, 2012.
[7]  M. T. Hartmann, O. A. V. Marques, and S. M. Almeida-Santos, “Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae),” Amphibia Reptilia, vol. 25, no. 1, pp. 77–85, 2004.
[8]  C. Monteiro, C. E. Montgomery, F. Spina, R. J. Sawaya, and M. Martins, “Feeding, reproduction, and morphology of Bothrops mattogrossensis (Serpentes, Viperidae, Crotalinae) in the Brazilian Pantanal,” Journal of Herpetology, vol. 40, no. 3, pp. 408–413, 2006.
[9]  C. Nogueira, R. J. Sawaya, and M. Martins, “Ecology of the pitviper, Bothrops moojeni, in the Brazilian cerrado,” Journal of Herpetology, vol. 37, no. 4, pp. 653–659, 2003.
[10]  R. M. Lira-da-Silva, Y. F. Mise, L. L. Casais-e-Silva, J. Ulloa, B. Hamdan, and T. K. Brazil, “Serpentes de importancia médica do nordeste do Brasil,” Gazeta Médica da Bahia, vol. 79, pp. 7–20, 2009.
[11]  M. Martins, O. A. V. Marques, and I. Sazima, “Ecological and phylogenetic correlates of feeding habits in neotropical pitvipers of the genus Bothrops,” in Biology of the Vipers, G. W. Schuett, M. H?ggren, M. E. Douglas, and H. W. Greene, Eds., Eagle Mountain Publishing, Eagle Mountain, Utah, Utah, 2002.
[12]  M. T. Rodrigues, “Herpetofauna da caatinga,” in Ecologia e conserva??o da caatinga, I. R. Leal, M. Tabarelli, and J. M. C. Silva, Eds., Editora Universitária da UFPE Recife, Recife, Brazil, 2003.
[13]  M. Martins, M. S. Araujo, R. J. Sawaya, and R. Nunes, “Diversity and evolution of macrohabitat use, body size and morphology in a monophyletic group of Neotropical pitvipers (Bothrops),” Journal of Zoology, vol. 254, no. 4, pp. 529–538, 2001.
[14]  W. Wüster, M. G. Salom?o, J. A. Quijada-Mascare?as, and R. S. Thorpe, “Origin and evolution of the South American pitviper fauna: evidence from mitochondrial DNA sequence analysis,” in Biology of the Vipers, G. W. Schuett, M. H?ggren, M. E. Douglas, and H. W. Greene, Eds., Eagle Mountain Publishing, Eagle Mountain, Calif, USA, 2002.
[15]  R. M. Lira-da-Silva, L. L. Casais-e-Silva, I. B. Queiroz, and T. B. Nunes, “Contribui??o à biologia de serpentes da Bahia, Brasil. I- Vivíparas,” Revista Brasileira de Zoologia, vol. 11, no. 2, pp. 187–193, 1994.
[16]  W. P. Maddison and D. R. Maddison, “Mesquite: a modular system for evolutionary analysis,” Version 2.75, 2011,
[17]  P. A. Carrasco, C. I. Mattoni, G. C. Leynaud, and G. J. Scrocchi, “Morphology, phylogeny and taxonomy of South American bothropoid pitvipers (Serpentes, Viperidae),” Zoologica Scripta, vol. 41, no. 2, pp. 109–124, 2012.
[18]  R. D. Aldridge, “Oviductal anatomy and seasonal sperm storage in the southeastern crowned snake (Tantilla coronata),” Copeia, vol. 1992, pp. 1103–1106, 1992.
[19]  D. S. Siegel, A. Miralles, R. E. Chabarria, and R. D. Aldridge, “Female reproductive anatomy: cloaca, oviduct, and sperm storage,” in Reproductive Biology and Phylogeny of Snakes, R. D. Aldridge and D. M. Sever, Eds., Science Publishers, Enfield, Conn, USA, 2011.
[20]  T. Mathies, “Reproductive cycles of tropical snakes,” in Reproductive Biology and Phylogeny of Snakes, R. D. Aldridge and and D. M. Sever, Eds., Science Publishers, Enfield, NH, USA, 2011.
[21]  A. Cree, L. J. Guillette Jr., M. A. Brown, G. K. Chambers, J. F. Cockrem, and J. D. Newton, “Slow estradiol-induced vitellogenesis in the tuatara, Sphenodon punctatus,” Physiological Zoology, vol. 64, pp. 1234–1251, 1991.
[22]  C. J. Reading, “The influence of body condition and prey availability on female breeding success in the smooth snake (Coronella austriaca Laurenti),” Journal of Zoology, vol. 264, no. 1, pp. 61–67, 2004.
[23]  W. Fox, “Seminal receptacles of snakes,” The Anatomical Record, vol. 124, no. 3, pp. 519–539, 1956.
[24]  D. M. Sever and T. J. Ryan, “Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). I. Evidence for oviducal sperm storage,” Journal of Morphology, vol. 241, pp. 1–18, 1999.
[25]  W. Fox and H. C. Dessauer, “The single right oviduct and other urogenital structures of female Typhlops and Leptotyphlops,” Copeia, vol. 1962, no. 3, pp. 590–597, 1962.
[26]  A. P. Halpert, W. R. Garstka, and D. Crews, “Sperm transport and storage and its relation to the annual sexual cycle of the female red-sided garter snake, Thamnophis sirtalis parietalis,” Journal of Morphology, vol. 174, no. 2, pp. 149–159, 1982.
[27]  M. J. Perkins and B. D. Palmer, “Histology and functional morphology of the oviduct of an oviparous snake, Diadophis punctatus,” Journal of Morphology, vol. 227, no. 1, pp. 67–79, 1996.
[28]  W. Booth and G. W. Schuett, “Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis,” Biological Journal of the Linnean Society, vol. 104, no. 4, pp. 934–942, 2011.
[29]  K. M. P. Silva, Análise do comportamento reprodutivo de Bothrops spp. em cativeiro, Universidade de Franca, S?o Paulo, Brazil, 2009.
[30]  R. W. Krohmer, “Variation in seasonal ultrastructure of sexual granules in the renal sexual segment of the Northern Water Snake, Nerodia sipedon sipedon,” Journal of Morphology, vol. 261, no. 1, pp. 70–80, 2004.
[31]  C. A. Rojas, V. A. Barros, and S. M. Almeida-Santos, “The reproductive cycle of the male sleep snake Sibynomorphus mikanii (Schlegel, 1837) from southeastern brazil,” Journal of Morphology, vol. 274, no. 2, pp. 215–228, 2013.
[32]  X. Ji, C. X. Lin, L. H. Lin, Q. B. Qiu, and Y. Du, “Evolution of viviparity in warm-climate lizards: an experimental test of the maternal manipulation hypothesis,” Journal of Evolutionary Biology, vol. 20, no. 3, pp. 1037–1045, 2007.
[33]  R. D. Aldridge and D. Duvall, “Evolution of the mating season in the pitvipers of North America,” Herpetological Monographs, no. 16, pp. 1–25, 2002.
[34]  P. H. Valdujo, C. Nogueira, and M. Martins, “Ecology of Bothrops neuwiedi pauloensis (Serpentes: Viperidae: Crotalinae) in the Brazilian cerrado,” Journal of Herpetology, vol. 36, no. 2, pp. 169–176, 2002.
[35]  R. B. King, “Determinants of offspring number and size in the brown snake, Storeria dekayi,” Journal of Herpetology, vol. 27, no. 2, pp. 175–185, 1993.
[36]  R. Shine, “Reproductive strategies in snakes,” Proceedings of the Royal Society B: Biological Sciences, vol. 270, no. 1519, pp. 995–1004, 2003.
[37]  M. A. Akbarsha, V. Tamilarasan, B. Kadalmani, and P. Daisy, “Ultrastructural evidence for secretion from the epithelium of ampulla ductus deferentis of the fan-throated lizard Sitana ponticeriana Cuvier,” Journal of Morphology, vol. 266, no. 1, pp. 94–111, 2005.
[38]  S. E. Trauth and D. M. Sever, “Male urogenital ducts and cloacal anatomy,” in Reproductive Biology and Phylogeny of Snakes, R. D. Aldridge and D. M. Sever, Eds., Science Publishers, Enfield, Conn, USA, 2011.
[39]  H. Saint Girons, “Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles,” Herpetologica, vol. 38, no. 1, pp. 5–16, 1982.
[40]  M. Olsson, T. Madsen, and R. Shine, “Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus,” Proceedings of the Royal Society B: Biological Sciences, vol. 264, no. 1380, pp. 455–459, 1997.
[41]  C. Arzabe, “Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga,” Revista Brasileira de Zoologia, vol. 16, no. 3, pp. 851–864, 1999.
[42]  J. G. E. Lewis, The Biology of Centipedes, Cambridge University Press, Cambridge, UK, 1st edition, 1981.
[43]  W. S. Parker and M. V. Plummer, “Population ecology,” in Snakes: Ecology and Evolutionary Biology, R. A. Seigel, J. T. Collins, and S. S. Novak, Eds., MacMillan, New York, NY, USA, 1987.
[44]  R. Shine, “Sexual size dimorphism in snakes revisited,” Copeia, no. 2, pp. 326–346, 1994.
[45]  X. Bonnet, G. Naulleau, R. Shine, and O. Lourdais, “Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis,” Oikos, vol. 89, no. 3, pp. 509–518, 2000.
[46]  R. Shine, “Sexual size dimorphism and male combat in snakes,” Oecologia, vol. 33, no. 3, pp. 269–277, 1978.
[47]  M. E. Oliveira and M. Martins, “When and where to find a pitviper: activity patterns and habitat use of the lancehead, Bothrops atrox, in Central Amazonia, Brazil,” Herpetological Natural History, vol. 8, pp. 101–110, 2001.


comments powered by Disqus