RESUMEN
The reproductive cycle of Crotalus durissus is markedly seasonal and synchronous between individuals. The start of vitellogenesis occurs at the end of the summer and coincides with copulation. However, given that the copulation is dissociated from ovulation, sperm storage is obligatory in females. In viperids, sperm storage in the female reproductive tract is reported to occur in two regions: (1) the posterior infundibulum, which presents sperm storage glands; and (2) the nonglandular uterus where sperm is stored in crypts by means of the uterine muscular twisting (UMT). The mechanisms that allow the survival of sperm in the female reproductive tract of snakes are still unknown. In this study, we investigated five regions of the reproductive tract of C. durissus, searching for the presence of spermatozoa and sperm storage structures in different oviductal portions. Additionally, we used histological techniques to verify the occurrence of hypertrophy of the infundibular and uterine glands during the processes of vitellogenesis, as well as histochemical techniques to investigate the nature of the secretion produced in the nonglandular uterus and posterior infundibulum. Storage sperm were observed in the nonglandular uterus and although the posterior infundibulum had storage receptacles, sperm were not observed in that region. Both sperm storage regions presented granules testing positive for acidic and neutral polysaccharides, in vitellogenic and previtellogenic females. This presence of guaranteeing conditions for sperm storage. Histochemical analysis revealed the possible storage capacity of sperm in the nonglandular uterus. In addition, the UMT was observed in all the females with storage sperm, which assures the maintenance of sperm in the nonglandular uterus until ovulation.
RESUMEN
We describe the seasonal variation in the male reproductive cycle of Bothrops pubescens, a pitviper from southern Brazil. All specimens were collected in the state of Rio Grande do Sul, a region with climates varying from subtropical to subtemperate and temperate. We characterized male reproduction considering histological analyses of the testes, sexual segment of the kidneys (SSK), and ductus deferens, as well as macroscopic indicators of reproductive activity (testes volume and ductus deferens width in the distal portion) to allow comparisons. We also evaluated the seasonal variation of epithelial height and tubule diameter of the testes and SSK. These reproductive parameters showed significant seasonal variation, with a high increase in summer and a peak in autumn for spermatogenic and SSK activity. Courtship behavior occurs on March (end of summer/beginning of autumn), in synchrony with sperm production and SSK hypertrophy. Sperm storage occurred in the ductus deferens throughout the year. We detected an ampulla ductus deferentis in the distal portion of the ductus deferens in some individuals. Male B. pubescens exhibit a seasonal reproductive cycle, and the use of microscopic methods was highly informative for supporting this conclusion.
Nós descrevemos a variação sazonal no ciclo reprodutivo de Bothrops pubescens, uma espécie de serpente da subfamília Crotalinae, da região Sul do Brasil. Os machos foram amostrados no estado do Rio Grande do Sul, que é uma região com climas variando de subtropical a subtemperado e temperado. Os ciclos dos testículos, segmento sexual renal (SSR) e ducto deferente foram caracterizados utilizando análises histológicas para descrever o ciclo reprodutivo dos machos. Nós também avaliamos indicadores macroscópicos da atividade reprodutiva (volume do testículo e largura do ducto deferente na região distal) para fins de comparação. Considerando os dados histológicos, foram avaliadas as variações sazonais da altura do epitélio e diâmetro dos túbulos tanto dos testículos quanto do SSR. Estes parâmetros reprodutivos apresentaram variação sazonal significativa, com grande aumento no verão e pico no outono, tanto para a atividade espermatogênica quanto para o SSR. Corte em vida livre ocorre em março (fim do verão/início do outono), em sincronia com a produção de esperma e a hipertrofia do SSR. Estocagem de esperma ocorreu no ducto deferente ao longo do ano. A ampulla ductus deferentis foi observada na porção distal do ducto deferente de alguns indivíduos. O ciclo reprodutivo dos machos de B. pubescens é sazonal e o uso de métodos microscópicos foi essencial para chegar a esta conclusão.
RESUMEN
In Squamata, the sexual segment of the male kidney (SSK) produces secretory granules that are transmitted to the female tract during copulation. Here, we investigate the morphology of SSK in various species of the pitviper-genus Bothrops, a medically relevant clade of Neotropical snakes, using histology, histochemistry, as well as scanning and transmission electron microscopy. We also evaluated the relationship of SSK hypertrophy with spermatogenesis and storage of sperm. The SSK in Bothrops consists of tall columnar epithelial cells filled with electron-dense secretory granules. These granules are apparently released into the lumen by an apocrine secretory process. In general, the ultrastructural morphology of SSK in Bothrops is similar to those described for other pitvipers in the genus Agkistrodon. In most Bothrops males, the SSK produces carbohydrates and proteins, and occurs in all lobes of the kidney, occupying most of the kidney mass. In contrast, intersexual females (with male copulatory organs) of Bothrops insularis had a smaller SSK diameter than males and did not show hypertrophy. The seasonal development of SSK in Bothrops species seems to be driven by environmental factors rather than phylogeny, since sister species exhibited periods of hypertrophy at different months. In most Bothrops males, hypertrophy occurs at various seasons of the year (spring, summer, autumn), even in winter, and seasonal changes in SSK do not necessarily accompany spermatogenesis.
RESUMEN
We examined four suspected cases of facultative parthenogenesis in three species of a neotropical lineage of pitvipers of the Bothrops atrox group. Reproduction without mating was observed in captive females of B. atrox, B. moojeni and B. leucurus housed alone for seven years (the two former species) and nine years (the latter one). In addition to the observation of captivity data, we investigated molecularly this phenomenon using heterologous microsatellites. DNA was extracted from the mothers’ scales or liver, from embryo and newborn fragments, and yolked ova. Four of the microsatellites showed good amplification using Polymerase Chain Reaction and informative band segregation patterns among each mother and respective offspring. Captivity information, litter characteristics (comparison of the number of newborns, embryos and yolked ova) and molecular data altogether agreed with facultative parthenogenesis predictions in at least three out of the four mothers studied: B. atrox (ID#933) was heterozygous for three out of the four markers, and the sons S1 and S2 were homozygous; B. moojeni (BUT86) was heterozygous for two out of four markers, offspring S1, S3, E2, and E4, and O1 to O6 were homozygous; and B. leucurus (MJJS503) was heterozygous for three out of four markers, and son E1 and O1 were homozygous. B. moojeni (BUT44) was homozygous for all loci analyzed in the mother and offspring, which although not informative is also consistent with parthenogenesis. This study represents the first molecular confirmation of different pitviper species undergoing facultative parthenogenesis among Neotropical endemic snakes.
RESUMEN
Reproductive traits vary widely within and among snake species, and are influenced by a range of factors. However, additional studies are needed on several species, especially on tropical snake faunas, to fully understand the patterns of reproductive variation in snakes. Here, we characterized the reproductive biology of B. jararacussu from southeastern and southern Brazil. We combined macroscopic and microscopic examinations of the reproductive system of museum specimens with observations of free-ranging snakes to characterize size at sexual maturity, sexual size dimorphism (SSD), reproductive output, and male and female reproductive cycles. We compared our data with published literature and discuss the factors that may play a role in shaping the reproductive patterns in the species and the genus. Bothrops jararacussu shares several characteristics with its congeners such as autumn mating season, obligatory sperm storage in the female reproductive tract, seasonal timing of parturition (summer-autumn), female-biased SSD, maturity at larger body sizes in females, and a positive relationship between body size and litter size. These characteristics seem phylogenetically conserved in Bothrops. On the other hand, B. jararacussu exhibits some unique characteristics such as a high degree of SSD (one of the highest values recorded in snakes), a large female body size, and a large litter and offspring size, which are among the largest recorded in the genus. Moreover, larger females reproduce more frequently than smaller conspecifics. These characteristics may be collectively interpreted as the result of a strong selection for increased fecundity. Other peculiarities of the species include an asynchrony between spermiogenesis (summer-autumn) and the peak of SSK hypertrophy (autumn to spring) and a prolonged production of SSK granules. Because SSK hypertrophy and mating are androgen-dependent in snakes, the prolonged SSK hypertrophy suggests that male B. jararacussu may prolong their potential to mate (compared with its congeners), which may increase their reproductive success. Our results and previous literature collectively suggest that, in Bothrops, the evolution of SSD is driven by fecundity selection, variation in reproductive output is influenced by variation in female body size, and the timing of spermiogenesis is influenced by other factors in addition to temperature. We also suggest that male Bothrops have undergone multiple evolutionary shifts in the timing of spermiogenesis.
RESUMEN
Although knowledge about the reproduction of snakes of the genus Bothrops has increased recently, many questions remain regarding sperm storage by these neotropical pitvipers. The relationship between two known sperm storage sites—the nonglandular uterus and the infundibulum—has yet to be detailed for Bothrops. In addition, the formation of uterine muscular twisting (UMT) and its function in sperm storage in the nonglandular uterus have been questioned. This article presents data on both sperm storage sites (posterior infundibulum and nonglandular uterus) in the Amazonian lancehead, Bothrops atrox, aiming to address the role of UMT in bothropoid reproduction considering female reproductive stages, timing of sperm storage, and morphology and histochemistry of sperm receptacles. The oviduct of B. atrox is composed of the infundibulum (anterior and posterior), the glandular uterus, the nonglandular uterus and the pouch. Sperm storage occurs in the posterior infundibulum and nonglandular uterus in vitellogenic females. In the posterior infundibulum sperm is stored in receptacles, while in the nonglandular uterus it is stored in crypts in the UMT of vitellogenic females. Both sperm storage sites possess granules testing positive for neutral mucopolysaccharides in the presence of spermatozoa, possibly favoring the conditions for spermatozoa surveillance during sperm storage in the reproductive tract.
RESUMEN
Reproductive seasonality is common among snakes, with mating, pregnancy, and birth or oviposition occurring only during few months of the year and modulated mainly by two environmental phenomena—temperature and rainfall. Species of Bothrops inhabit regions with varied climatic conditions, including those that are tropical, subtropical, equatorial, and semiarid. Bothrops atrox is an endemic and widespread species of the Amazon rain forest. Such habitat is characterized by an equatorial climate with little variability in temperature and humidity, but marked seasonality in intense precipitation. We investigated several aspects of the reproductive biology of B. atrox, including the reproductive cycle, the sexual segment of the kidney (SSK), sperm storage, and the possible influence of temperature and rainfall on pregnancy duration, birth, and spermatogenesis. Specifically, we examined museum specimens to describe sexual dimorphism, litter size, and male and female urogenital cycles through macroscopic and histological analyses. Females of B. atrox exhibited follicular recrudescence mainly from January to April (part of the wet season). Pregnant females were found throughout the year (except May), but births were found to occur mainly at the end of the dry season (August–October). Males exhibited SSK hypertrophy and sperm production in the wet season (November–April). Females were found to be larger than males, but males of B. atrox—as with other members of the B. atrox species complex—obtain relatively larger body sizes when compared with other species of Bothrops, which might be an adaptive response to male–male combat in this species. Together, our results show that B. atrox from Amazonia has a unique reproductive strategy (for each sex) among pit vipers, indicating greater reproductive plasticity when compared with its congeners.
RESUMEN
Although knowledge about the reproduction of snakes of the genus Bothrops has increased recently, many questions remain regarding sperm storage by these neotropical pitvipers. The relationship between two known sperm storage sites—the nonglandular uterus and the infundibulum—has yet to be detailed for Bothrops. In addition, the formation of uterine muscular twisting (UMT) and its function in sperm storage in the nonglandular uterus have been questioned. This article presents data on both sperm storage sites (posterior infundibulum and nonglandular uterus) in the Amazonian lancehead, Bothrops atrox, aiming to address the role of UMT in bothropoid reproduction considering female reproductive stages, timing of sperm storage, and morphology and histochemistry of sperm receptacles. The oviduct of B. atrox is composed of the infundibulum (anterior and posterior), the glandular uterus, the nonglandular uterus and the pouch. Sperm storage occurs in the posterior infundibulum and nonglandular uterus in vitellogenic females. In the posterior infundibulum sperm is stored in receptacles, while in the nonglandular uterus it is stored in crypts in the UMT of vitellogenic females. Both sperm storage sites possess granules testing positive for neutral mucopolysaccharides in the presence of spermatozoa, possibly favoring the conditions for spermatozoa surveillance during sperm storage in the reproductive tract.
RESUMEN
Reproductive seasonality is common among snakes, with mating, pregnancy, and birth or oviposition occurring only during few months of the year and modulated mainly by two environmental phenomena—temperature and rainfall. Species of Bothrops inhabit regions with varied climatic conditions, including those that are tropical, subtropical, equatorial, and semiarid. Bothrops atrox is an endemic and widespread species of the Amazon rain forest. Such habitat is characterized by an equatorial climate with little variability in temperature and humidity, but marked seasonality in intense precipitation. We investigated several aspects of the reproductive biology of B. atrox, including the reproductive cycle, the sexual segment of the kidney (SSK), sperm storage, and the possible influence of temperature and rainfall on pregnancy duration, birth, and spermatogenesis. Specifically, we examined museum specimens to describe sexual dimorphism, litter size, and male and female urogenital cycles through macroscopic and histological analyses. Females of B. atrox exhibited follicular recrudescence mainly from January to April (part of the wet season). Pregnant females were found throughout the year (except May), but births were found to occur mainly at the end of the dry season (August–October). Males exhibited SSK hypertrophy and sperm production in the wet season (November–April). Females were found to be larger than males, but males of B. atrox—as with other members of the B. atrox species complex—obtain relatively larger body sizes when compared with other species of Bothrops, which might be an adaptive response to male–male combat in this species. Together, our results show that B. atrox from Amazonia has a unique reproductive strategy (for each sex) among pit vipers, indicating greater reproductive plasticity when compared with its congeners.
RESUMEN
Centipedes are part of the diet of several snake species of the genus Bothrops. However, reports on predation of centipedes by snakes are normally incomplete, and important data for natural history studies as the species identification and size of the prey are rarely published. The aim of this work was to report the presence of the centipede Scolopendra viridicornis in the digestive tract of the Amazon pit viper B. atrox. The snake specimen is an immature female from Aripuanã, state of Mato Grosso, Brazil, having a 623 mm snout-vent length. The centipede is an adult Scolopendra viridicornis, estimated to be 190 mm long, and found in the snake's stomach. The success in preying on this large and potentially dangerous centipede could be explained by the snake's dimensions, large enough for overpowering the prey, but still retaining characteristics of youth, such as venom with specific action against specific prey items.
Lacraias fazem parte da dieta de diversas espécies de serpentes do gênero Bothrops. Entretanto, informações importantes para estudos de história natural, como identificação da espécie e tamanho de presas, são raramente publicados. O objetivo desse trabalho é registrar a presença de uma lacraia Scolopendra viridicornis, no trato digestivo de uma jararaca da Amazônia, Bothrops atrox. A serpente estudada é uma fêmea imatura, com 623 mm de comprimento rostro-cloacal, proveniente de Aripuanã, estado de Mato Grosso, Brasil. A lacraia é um adulto de Scolopendra viridicornis parcialmente digerida, com aproximadamente 190 mm de comprimento. O sucesso na predação dessa grande e perigosa presa pode ser explicado pelas dimensões da serpente, que é grande o suficiente para dominar a presa, mas ainda retém características juvenis, como veneno com ação específica em determinados ítens alimentares.
Asunto(s)
Animales , Bothrops/metabolismo , DietaRESUMEN
Centipedes are part of the diet of several snake species of the genus Bothrops. However, reports on predation of centipedes by snakes are normally incomplete, and important data for natural history studies as the species identification and size of the prey are rarely published. The aim of this work was to report the presence of the centipede Scolopendra viridicornis in the digestive tract of the Amazon pit viper B. atrox. The snake specimen is an immature female from Aripuana, state of Mato Grosso, Brazil, having a 623 mm snout-vent length. The centipede is an adult Scolopendra viridicornis, estimated to be 190 mm long, and found in the snake's stomach. The success in preying on this large and potentially dangerous centipede could be explained by the snake's dimensions, large enough for overpowering the prey, but still retaining characteristics of youth, such as venom with specific action against specific prey items.
Lacraias fazem parte da dieta de diversas espécies de serpentes do gênero Bothrops. Entretanto, informações importantes para estudos de história natural, como identificação da espécie e tamanho de presas, são raramente publicados. O objetivo desse trabalho é registrar a presença de uma lacraia Scolopendra viridicornis, no trato digestivo de uma jararaca da Amazônia, Bothrops atrox. A serpente estudada é uma fêmea imatura, com 623 mm de comprimento rostro-cloacal, proveniente de Aripuanã, estado de Mato Grosso, Brasil. A lacraia é um adulto de Scolopendra viridicornis parcialmente digerida, com aproximadamente 190 mm de comprimento. O sucesso na predação dessa grande e perigosa presa pode ser explicado pelas dimensões da serpente, que é grande o suficiente para dominar a presa, mas ainda retém características juvenis, como veneno com ação específica em determinados ítens alimentares.
