Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T09:21:50.287Z Has data issue: false hasContentIssue false

17 - The Evolution of Sperm-Storage Location in Squamata with Particular Reference to Snakes

from Part V - Anatomical and Functional Morphological Perspectives

Published online by Cambridge University Press:  30 July 2022

By
Henrique B. Braz  and
Selma M. Almeida-Santos
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
Get access

Summary

Females of many squamates maintain viable sperm in their reproductive tract after insemination. This 'female sperm storage' (FSS), has several advantages and clear implications for squamate evolution by dramatically influencing life histories, mating systems, and sexual selection and conflict. In this chapter, we summarize the literature on the anatomy of FSS and reconstruct the evolution of sperm-storage location in squamate reptiles. Our major aim is to provide insights into the evolution of FSS in squamates, with a particular focus on the origin and early evolution of snakes. Various lizard lineages store sperm exclusively in crypts or tubules in the posterior oviduct. Most ‘basal’ lizards (gekkotans) and all ‘basal’ snakes (scolecophidians) studied thus far store sperm in tubules in the anterior oviduct. A few gekkotans and most alethniophidian snake studied store (or potentially store) sperm in both oviductal regions. Some snakes apparently have evolved morphological adaptations to hold sperm in the posterior oviduct. Based on ancestral state reconstructions, we elaborate a scenario for the evolution of FSS in snakes.

Keywords

reproductionoviductfemale sperm storagefertilizationlizardsevolutionancestral stateanatomy
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 389 - 409
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Orr, T. J. and Brennan, P. L. R., Sperm storage: distinguishing selective processes and evaluating criteria. Trends in Ecology and Evolution, 30 (2015), 261–272.CrossRefGoogle ScholarPubMed
Schuett, G. W., Is long-term sperm storage an important component of the reproductive biology of temperate pitvipers? In Campbell, J. A. and Brodie, E. D., eds., Biology of the Pitvipers (Tyler: Selva Publishing, 1992), pp. 169–184.Google Scholar
Aldridge, R. D. and Duvall, D., Evolution of the mating season in the pitvipers of North America. Herpetolological Monographs, 16 (2002), 1–25.Google Scholar
Birkhead, T. R. and Møller, A. P., Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biological Journal of the Linnean Society, 50 (1993), 295–311.Google Scholar
Friesen, C. R., Kahrl, A. F., and Olsson, M., Sperm competition in squamate reptiles. Philosophical Transactions of the Royal Society, B Biological Sciences, 375 (2020), 20200079.CrossRefGoogle ScholarPubMed
Blackburn, D. G., Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. Journal of Experimental Zoology, 282 (1998), 560–617.Google Scholar
Girling, J. E., The reptilian oviduct: a review of structure and function and directions for future research. Journal of Experimental Zoology, 293 (2002), 141–170.CrossRefGoogle ScholarPubMed
Sever, D. M. and Hamlett, W. C., Female sperm storage in reptiles. Journal of Experimental Zoology, 292 (2002), 187–199.Google Scholar
Siegel, D. S., Miralles, A., Chabarria, R. E., and Aldridge, R. D., Female reproductive anatomy: cloaca, oviduct, and sperm storage. In Aldridge, R. D. and Sever, D. M., eds., Reproductive Biology and Phylogeny of Snakes (Enfield: Science Publishers, 2011), pp. 347–409.CrossRefGoogle Scholar
Siegel, D. S., Miralles, A., Rheubert, J. L., and Sever, D. M., Female reproductive anatomy: cloaca, oviduct and sperm storage. In Rheubert, J. L., Siegel, D. S., and Thauth, S. E., eds., Reproductive Biology and Phylogeny of Lizards and Tuatara (Boca Raton: CRC Press, 2014), pp. 144–195.Google Scholar
Eckstut, M. E., Sever, D. M., White, M. E., and Crother, B. I., Phylogenetic analysis of sperm storage in female squamates. In Dahnof, L. T., ed., Animal Reproduction: New Research Developments (New York: Nova Science Publishers, 2009), pp. 185–218.Google Scholar
Howarth, B., Sperm storage: as a function of the female reporductive tract. In Johnson, A. D. and Foley, C. W., eds., The Oviduct and Its Functions (New York: Academic Press, 1974), pp. 237–270.Google Scholar
Fox, H., Urinogenital System. In Gans, C. and Parsons, T. S., eds., Biology of the Reptilia, Vol. 6. Morphology (London and New York: Academic Press, 1977), pp. 81–96.Google Scholar
Gist, D. H. and Jones, J. M., Storage of sperm in the reptilian oviduct. Scanning Microscopy, 1 (1987), 1839–1849.Google Scholar
Barros, V. A., Sueiro, L. R., and Almeida-Santos, S. M., Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns. Herpetological Journal, 22 (2012), 97–104.Google Scholar
Barros, V. A., Rojas, C. A., and Almeida-Santos, S. M., Reproductive biology of Bothrops erythromelas from the Brazilian Caatinga. Advances in Zoology, 2014 (2014), 1–11.Google Scholar
Bassi, E. A., Coeti, R. Z., and Almeida-Santos, S. M., Reproductive cycle and sperm storage of female coral snakes, Micrurus corallinus and Micrurus frontalis . Amphibia-Reptilia, 41 (2019), 1–15.Google Scholar
Braz, H. B., Kasperoviczus, K. N., and Guedes, T. B., 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 (2019), 37–47.CrossRefGoogle Scholar
Silva, K. M. P.,Barros, V. A., Rojas, C. A., and Almeida-Santos, S. M., Infundibular sperm storage and uterine muscular twisting in the Amazonian lancehead, Bothrops atrox . Anatomical Record, 303 (2020), 3145–3154.CrossRefGoogle ScholarPubMed
Silva, K. M. P., Silva, K. B., Sueiro, L. R., Oliveira, M. E. E. S., and Almeida-Santos, S. M., Reproductive biology of Bothrops atrox (Serpentes, Viperidae, Crotalinae) from the Brazilian Amazon. Herpetologica, 74 (2019), 198–207.CrossRefGoogle Scholar
Loebens, L., Almeida-Santos, S. M., and Cechin, S. Z., Reproductive biology of the sword snake Tomodon dorsatus (Serpentes: Dipsadidae) in South Brazil: comparisons within the tribe Tachymenini. Amphibia-Reptilia, 41 (2020), 1–15.CrossRefGoogle Scholar
Gualdrón-Durán, L. E., Calvo-Castellanos, M. F., and Ramírez-Pinilla, M. P., Annual reproductive activity and morphology of the reproductive system of an Andean population of Atractus (Serpentes, Colubridae). South American Journal of Herpetology, 14 (2019), 58–70.Google Scholar
Silva, K. M. P., Braz, H. B., Kasperoviczus, K. N., Marques, O. A. V., and Almeida-Santos, S. M., Reproduction in the pitviper Bothrops jararacussu: large females increase their reproductive output while small males increase their potential to mate. Zoology, 142 (2020), 125816.Google Scholar
Muniz‐da‐Silva, D. F., Passos, J., Siegel, D. S., and Santos-Almeida, S. M., Caudal oviduct coiling in a viperid snake, Crotalus durissus . Acta Zoologica, 101 (2020), 69–77.CrossRefGoogle Scholar
Khouri, R. S., Almeida‐Santos, S. M., and Fernandes, D. S., Anatomy of the reproductive system of a population of Amerotyphlops brongersmianus from southeastern Brazil (Serpentes: Scolecophidia). Anatomical Record, 303 (2020), 2485–2496.Google Scholar
Villagrán-Santa, M., Mendoza-Cruz, E., Granados-González, G., Rheubert, J. L., and Hernández-Gallegos, O., Sperm storage in the viviparous lizard Sceloporus bicanthalis (Squamata: Phrynosomatidae), a species with continuous spermatogenesis. Zoomorphology, 136 (2017), 85–93.CrossRefGoogle Scholar
Barros, V. A., Rojas, C. A., and Almeida-Santos, S. M., Is rainfall seasonality important for reproductive strategies in viviparous Neotropical pitvipers? A case study with Bothrops leucurus from the Brazilian Atlantic Forest. Herpetological Journal, 24 (2014), 69–77.Google Scholar
Melo, G. C., Nascimento, L. B., and Galdino, C. A. B., Lizard reproductive biology beyond the gonads: an investigation of sperm storage structures and renal sexual segments. Zoology, 135 (2019), 125690.Google Scholar
Migliore, S. N., Biologia reprodutiva de Enyalius perditus (Jackson, 1978) e Enyalius iheringii Boulenger, 1885 (Squamata: Leiosauridae). Unpublished Masters dissertation, Universidade de São Paulo, 2016.Google Scholar
Souza, E. and Almeida‐Santos, S. M., Reproduction in the bushmaster (Lachesis muta): Uterine muscular coiling and female sperm storage. Acta Zoologica, 2020.Google Scholar
Migliore, S. N., Estratégias reprodutivas de lagartos Mabuyinae do Brasil . Unpublished PhD thesis, Universidade de São Paulo, 2021.Google Scholar
Khouri, R. S., Fiorillo, B. F., Braz, H. B., et al., Reproductive ecology of the Amaral’s Blind Snake Trilepida koppesi in an area of Cerrado in south-eastern Brazil. Herpetological Journal, 32 (2022), 70–79.Google Scholar
Kasperoviczus, KN. Evolução das estratégias reprodutivas de Bothrops jararaca (Serpentes: Viperidae). Unpubished PhD thesis, Universidade de São Paulo, 2013.Google Scholar
de Resende, F. C. and Nascimento, L. B., The female reproductive cycle of the Neotropical snake Atractus pantostictus (Fernandes and Puorto, 1993) from south-eastern Brazil. Anatomia Histologia Embryologia , 44 (2015), 225–235.CrossRefGoogle Scholar
Amaral, F. M., Estratégias reprodutivas da serpente Bothrops alternatus: influência de fatores ambientais. Unpublished Masters dissertation, Universidade de São Paulo, 2015.Google Scholar
Rojas, C. A., Barros, V. A., and Almeida-Santos, S. M., Sperm storage and morphofunctional bases of the female reproductive tract of the snake Philodryas patagoniensis from southeastern Brazil. Zoomorphology, 134 (2015), 577–586.Google Scholar
Rojas, C. A., Barros, V. A., and Almeida-Santos, S. M., A histological and ultrastructural investigation of the female reproductive system of the water snake (Erythrolamprus miliaris): Oviductal cycle and sperm storage. Acta Zoologica, 100 (2019), 69–80.CrossRefGoogle Scholar
Almeida-Santos, S. M., Barros, V. A., Rojas, C. A., Sueiro, L. R., and Nomura, R. H. C., Reproductive biology of the Brazilian lancehead, Bothrops moojeni (Serpentes, Viperidae), from the state of São Paulo, southeastern Brazil. South American Journal of Herpetology, 12 (2017), 174–181.CrossRefGoogle Scholar
Loebens, L., Rojas, C. A., Almeida-Santos, S. M., and Cechin, S. Z., Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: Female reproductive cycle. Acta Zoologica , 99 (2018), 105–114.CrossRefGoogle Scholar
Pyron, R. A., Burbrink, F. T., and Wiens, J. J., A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13 (2013), 93.Google Scholar
Zaher, H., Murphy, R. W., Arredondo, J. C., et al., Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS ONE, 14 (2019), e0216148.Google Scholar
Burbrink, F. T., Grazziotin, F. G., Pyron, R. A., et al., Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology, 69 (2020), 502–520.Google Scholar
Cuellar, O., Oviducal anatomy and sperm storage structures in lizards. Journal of Morphology, 119 (1966), 7–19.Google Scholar
Fox, W., Special tubules for sperm storage in female lizards. Nature, 198 (1963), 500–501.CrossRefGoogle Scholar
Shantakumari, T. R., Sarkar, H. B. D., and Shivanandappa, T., Histology and histochemistry of the oviductal sperm storage pockets of the agamid lizard Calotes versicolor . Journal of Morphology, 203 (1990), 97–106.Google Scholar
Amey, A. P. and Whittier, J. M., The annual reproductive cycle and sperm storage in the bearded dragon, Pogona barbata. Australian Journal of Zoology, 48 (2000), 411.CrossRefGoogle Scholar
Uribe, M. C. A., Velasco, S. R., Guillette, L. J., and Estrada, E. F., Oviduct histology of the lizard, Ctenosaura pectinata. Copeia, 1988 (1988), 1035–1042.Google Scholar
Guillette, L. J. and Jones, R. E.. Ovarian, oviductal, and placental morphology of the reproductively bimodal lizard, Sceloporus aeneus . Journal of Morphology, 184 (1985), 85–98.Google Scholar
Yaron, Z., Effects of ovariectomy and steroid replacement on the genital tract of the viviparous lizard, Xantusia vigilis . Journal of Morphology, 136 (1972), 313–325.CrossRefGoogle ScholarPubMed
Halpert, A. P., Garstka, W. R., and Crews, D., 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, 174 (1982), 149–159.CrossRefGoogle Scholar
Aldridge, R. D., Oviductal anatomy and seasonal sperm storage in the southeastern crowned snake (Tantilla coronata). Copeia, 1992 (1992), 1103–1106.CrossRefGoogle Scholar
Sever, D. M. and Ryan, T. J., Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea): Part I. Evidence for oviducal sperm storage. Journal of Morphology, 241 (1999), 1–18.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Sever, D. M., Ryan, T. J., Morris, T., Patton, D., and Swafford, S., Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). II. Annual oviducal cycle. Journal of Morphology, 245 (2000), 146–160.Google Scholar
Almeida-Santos, S. M. and Salomão, M. G., Long-term sperm storage in the female Neotropical rattlesnake Crotalus durissus terrificus (Viperidae: Crotalinae). Japanese Journal of Herpetology, 17 (1997), 46–52.Google Scholar
Ludwig, M. and Rahn, H., Sperm storage and copulatory adjustment in the prairie rattlesnake. Copeia, 1943 (1943), 15–18.Google Scholar
Nilson, G. and Andrén, C., Function of renal sex secretion and male hierarchy in the adder, Vipera berus, during reproduction. Hormones and Behavior, 16 (1982), 404–413.Google Scholar
Almeida-Santos, S. M. and Salomão, M. G., Reproduction in Neotropical pitvipers, with emphasis on species of the genus Bothrops . In Schuett, G. W., Höggren, M., Douglas, M. E., et al., eds., Biology of the Vipers (Carmel: Eagle Mountain Publishing, 2002), pp. 445–462.Google Scholar
Nunes, S. F., Kaefer, I. L., Leite, P. T., and Cechin, S. Z., Reproductive and feeding biology of the pitviper Rhinocerophis alternatus from subtropical Brazil. Herpetological Journal, 20 (2010), 31–39.Google Scholar
Kasperoviczus, K. N., Biologia reprodutiva da jararaca ilhoa, Bothrops insularis (Serpentes: Viperidae), da Ilha da Queimada Grande, São Paulo . Unpublished Masters dissertation, Universidade de São Paulo, 2009.Google Scholar
Yamanouye, N., Silveira, P. F., Abdalla, F. M. F., et al., Reproductive cycle of the Neotropical Crotalus durissus terrificus: II. Establishment and maintenance of the uterine muscular twisting, a strategy for long-term sperm storage. General and Comparative Endocrinology, 139 (2004), 151–157.Google Scholar
Almeida-Santos, S. M., Abdalla, F. M. F, Silveira, P. F., et al., Reproductive cycle of the Neotropical Crotalus durissus terrificus: I. Seasonal levels and interplay between steroid hormones and vasotocinase. General and Comparative Endocrinology, 139 (2004), 143–150.CrossRefGoogle ScholarPubMed
Stille, B., Madsen, T., and Niklasson, M., Multiple paternity in the adder, Vipera berus . Oikos, 47 (1986), 173–175.Google Scholar
Siegel, D. S. and Sever, D. M., Utero-muscular twisting and sperm storage in viperids. Herpetological Conservation and Biology, 1 (2006), 87–92.Google Scholar
Andrén, C. and Nilson, G., The copulatory plug of the adder, Vipera berus : Does it keep sperm in or out? Oikos, 49 (1987), 230.Google Scholar
Fox, W., Seminal receptacles of snakes. Anatomical Record, 124 (1956), 519–539.Google Scholar
Bull, K. H., Mason, R. T., and Whittier, J., Seasonal testicular development and sperm storage in tropical and subtropical populations of the brown tree snake (Boiga irregularis). Australian Journal of Zoology, 45 (1997), 479.Google Scholar
Thongboon, L., Senarat, S., Kettratad, J., et al., Morphology and histology of female reproductive tract of the dog-faced water snake Cerberus rynchops (Schneider, 1799). Maejo Internation Journal of Science and Technology, 14 (2020), 11–26.Google Scholar
Saint Girons, H., Le cycle sexuel chez Vipera aspis (L.) dans l’ouest de la France. Bulletin Biologique de la France et de la Belgique, 91 (1957), 284–350.Google Scholar
Saint Girons, H., Le cycle reproducteur de la Vipère à cornes Cerastes cerastes (L.) dans la nature et en captivité. Bulletin de la Société Zoologique de France, 87 (1962), 41–51.Google Scholar
Saint Girons, H. and Duguy, R., Le cycle sexuel de Lacerta muralis L. en plaine et en montagne. Bulletin du Muséum National d’Histoire Naturelle, 42 (1970), 690–695.Google Scholar
Devine, M., Copulatory plugs in snakes: enforced chastity. Science, 187 (1975), 844–845.Google Scholar
Uribe, M. C., González-Porter, G., Palmer, B. D., and Guilette, L. J., Cyclic histological changes of the oviductal-cloacal junction in the viviparous snake Toluca lineata . Journal of Morphology, 237 (1998), 91–100.Google Scholar
Barros, V. A., Rojas, C. A., and Almeida-Santos, S. M., Mating plugs and male sperm storage in Bothrops cotiara (Serpentes, Viperidae). Herpetological Journal, 27 (2017), 63–67.Google Scholar
, H. A. J in den Bosch, , First record of mating plugs in lizards. Amphibia-Reptilia, 15 (1994), 89–93.Google Scholar
Kasperoviczus, K. N. and Almeida‐Santos, S. M., Copulatory plugs in Neotropical viperid snakes. 7th World Congress of Herpetology, Vancouver, abstracts (2012), 11–12.Google Scholar
Devine, M. C., Potential for sperm competition in reptiles: behavioral and physiological consequences. In Smith, R. L., ed., Sperm Competition and the Evolution of Animal Mating Systems (Orlando: Academic Press, 1984), pp. 509–521.Google Scholar
Shine, R., Olsson, M., and Mason, R., Chastity belts in gartersnakes: the functional significance of mating plugs. Biological Journal of the Linnean Society, 70 (2000), 377–390.Google Scholar
Friesen, C. R., Shine, R., Krohmer, R. W., and Mason, R. T., Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited. Biological Journal of the Linnean Society, 109 (2013), 893–907.Google Scholar
Hoffman, L. H. and Wimsatt, W. A., Histochemical and electron microscopic observations on the sperm receptacles in the garter snake oviduct. American Journal of Anatomy, 134 (1972), 71–95.Google Scholar
Jacobi, L., Ovoviviparie bei einheimischen Eidechsen. Zeitschrift für wissenschaftliche Zoologie, 148 (1936), 401–464.Google Scholar
Saint Girons, H., Sperm survival and transport in the female genital tract of reptiles. In Hafez, E. S. E. and Thibault, C. G., eds., The Biology of Spermatozoa (Basel: Karger, 1975), pp. 105–113.Google Scholar
Fox, W. and Dessauer, H. C., The single right oviduct and other urogenital structures of female Typhlops and Leptotyphlops . Copeia, 1962 (1962), 590–597.Google Scholar
Srinivas, S. R., Hegde, S. N., Sarkar, H. B. D., and Shivanandappa, T., Sperm storage in the oviduct of the tropical rock lizard, Psammophilus dorsalis . Journal of Morphology, 224 (1995), 293–301.Google Scholar
Marinho, C. E., Almeida-Santos, S. M., Yamasaki, S. C., and Silveira, P. F., Peptidase activities in the semen from the ductus deferens and uterus of the neotropical rattlesnake Crotalus durissus terrificus . Journal of Comparative Physiology B, 179 (2009), 635–642.Google Scholar
Aldridge, R. D., Jellen, B. C., Siegel, D. S., and Wisniewski, S. S., The sexual segment of the kidney. In Aldridge, R. D. and Sever, D. M., eds., Reproductive Biology and Phylogeny of Snakes (Enfield: Science Publishers, 2011), pp. 477–509.Google Scholar
Siegel, D. S. and Sever, D. M., Sperm aggregations in female Agkistrodon piscivorus (Reptilia: Squamata): A histological and ultrastructural investigation. Journal of Morphology 269 (2008), 189–206.Google Scholar
Rahn, H., Sperm viability in the uterus of the garter snake, Thamnophis. Copeia, 1940 (1940), 109–115.Google Scholar
Maddison, W. P. and Maddison, D. R., Mesquite: A modular system for evolutionary analysis. Version 3.61 , http://mesquiteproject.org (2019).Google Scholar
Zheng, Y. and Wiens, J. J., Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Molecular Phylogenetics and Evolution, 94 (2016), 537–547.CrossRefGoogle Scholar
Alencar, L. R. V., Quental, T. B., Grazziotin, F. G., et al., Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution, 105 (2016), 50–62.Google Scholar
Saint Girons, H., Deplacements et survie des spermatozoides chez les reptiles. Colloques de l’Institut National de la Santé et de la Recherche Médicale, 26 (1973), 259–282.Google Scholar
Gabe, M. and Saint Girons, H., Contribution a l’histologie de Sphenodon punctatus Gray (Paris: Éditions du Centre National de la Recherche Scientifique, 1964).Google Scholar
Cree, A., Cockrem, J. F., and Guillette, L. J., Reproductive cycles of male and female tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. Journal of Zoology 226 (1992), 199–217.CrossRefGoogle Scholar
Wiens, J. J., Hutter, C. R., Mulcahy, D. G., et al., Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biology Letters, 8 (2012), 1043–1046.Google Scholar
Miralles, A., Marin, J., Markus, D., et al., Molecular evidence for the paraphyly of Scolecophidia and its evolutionary implications. Journal of Evolutionary Biology, 31 (2018), 1782–1793.Google Scholar
Simões, B. F., Sampaio, F. L., Jared, C.., et al., Visual system evolution and the nature of the ancestral snake. Journal of Evolutionary Biology, 28 (2015), 1309–1320.Google Scholar
Withers, P. C., Physiological correlates of limblessness and fossoriality in scincid lizards. Copeia, 1981 (1981), 197–204.Google Scholar
Gans, C., Studies on amphisbaenids (Amphisbaenia, Reptilia). 1. A taxonomic revision of the Trogonophinae, and a functional interpretation of the amphisbaenid adaptive pattern. Bulletin of the American Museum of Natural History, 119 (1960), 129–204.Google Scholar
Webb, J. K., Shine, R., Branch, W. R., and Harlow, P. S., Life-history strategies in basal snakes: reproduction and dietary habits of the African thread snake Leptotyphlops scutifrons (Serpentes: Leptotyphlopidae). Journal of Zoology, 250 (2000), 321–327.Google Scholar
Webb, J. K., Branch, W. R., and Shine, R., Dietary habits and reproductive biology of typhlopid snakes from southern Africa. Journal of Herpetology 35 (2001), 558–567.CrossRefGoogle Scholar
Sawaya, R. J., Marques, O. A. V., and Martins, M., Composição e história natural das serpentes de Cerrado de Itirapina, São Paulo, sudeste do Brasil. Biota Neotropica, 8 (2008), 127–149.Google Scholar
Parpinelli, L. and Marques, O. A. V., Seasonal and daily activity in the pale-headed blindsnake Liotyphlops beui (Serpentes: Anomalepidae) in southeastern Brazil. South American Journal of Herpetology, 3 (2008), 207–212.CrossRefGoogle Scholar
Shine, R. and Webb, J. K., Natural history of Australian typhlopid snakes. Journal of Herpetology, 24 (1990), 357–363.CrossRefGoogle Scholar
Parpinelli, L. and Marques, O. A. V., Reproductive biology and food habits of the blindsnake Liotyphlops beui (Scolecophidia: Anomalepididae). South American Journal of Herpetology, 10 (2015), 205–210.Google Scholar
Saint Girons, H., Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica, 38 (1982), 5–16.Google Scholar
Aldridge, R. D., Goldberg, S. R., Wisniewski, S. S., Bufalino, A. P., and Dillman, C. B., The reproductive cycle and estrus in the colubrid snakes of temperate North America. Contemporary Herpetology, 2009 (2009), 1–31.Google Scholar
Smyth, M. and Smith, M. J., Obligatory sperm storage in the skink Hemiergis peronii . Science, 161 (1968), 575–576.Google Scholar
Bertona, M. and Chiaraviglio, M., Reproductive biology, mating aggregations, and sexual dimorphism of the Argentine boa constrictor (Boa constrictor occidentalis). Journal of Herpetology, 37 (2003), 510–516.Google Scholar
Cechin, S. Z. and Oliveira, J. L., Sibynomorphus ventrimaculatus (Southern Snail-eater). Mating. Herpetological Review, 34 (2003), 73.Google Scholar
Marques, O. A. V., Muniz-Da-Silva, D. F., Barbo, F. E., et al., Ecology of the colubrid snake Spilotes pullatus from the Atlantic Forest of southeastern Brazil. Herpetologica, 70 (2014), 407–416.Google Scholar
Shine, R., Comparative ecology of three Australian snake species of the genus Cacophis (Serpentes: Elapidae). Copeia, 1980 (1980), 831–838.Google Scholar
Shine, R., Haagner, G. V., Branch, W. R., Harlow, P. S., and Webb, J. K., Natural history of the African shieldnose snake Aspidelaps scutatus (Serpentes, Elapidae). Journal of Herpetology, 30 (1996), 361–366.Google Scholar
Yokoyama, F. and Yoshida, H., The reproductive cycle of the female habu, Trimeresurus flavoviridis . Journal of Herpetology, 28 (1994), 54–59.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×