Effects of pregnancy on the body temperature of the South American rattlesnake, Crotalus durissus, in Southeastern Brazil

Changes in the body temperature (Tb) of reproductive females are well documented in squamate reptiles. However, the direction of these changes varies among species. Pregnant females may exhibit a lower or higher (and less variable) Tb than nonpregnant females. In some species, pregnancy has no detectable effect on female Tb. In this study, we compared the Tb of female rattlesnakes (Crotalus durissus) in different reproductive statuses (pregnant and nonpregnant) to investigate whether pregnancy influences Tb. We measured the Tb of female rattlesnakes kept in a semi-natural outdoor enclosure during summer and spring 2016 and summer 2017. Pregnant females selected a higher mean Tb than nonpregnant females. Moreover, we found significant differences in Tb among seasons. Body temperatures in summer 2017 were higher than in other seasons; however, reproductive status did not influence Tb variance. Therefore, our results agree with the hypothesis that females change their thermoregulatory behavior during pregnancy. Female rattlesnakes may increase their Tb during pregnancy to increase offspring fitness or to maximize their lifetime fitness.

Reproductive ecology of the Amaral's blind snake trilepida koppesi in an area of Cerrado in south-eastern Brazil

Studies on reproductive biology have largely contributed to the understanding of snake ecology. However, detailed reproductive data are scarce for many groups, particularly blind snakes. Here, we describe the reproductive biology of Trilepida koppesi (Leptotyphlopidae), a widely distributed species in the savannas of south-central Brazil. We describe its macro- and microscopic reproductive anatomy, female reproductive cycle, potential clutch size, seasonal activity, and sexual dimorphism of a population from south-eastern Brazil. Males have plurilobulated testes. Spermiogenesis occurs in early spring (October), when gonads and kidneys show a textured surface, the sexual segment of the kidney is hypertrophied, and the ductus deferentia are opaque and packed with sperm. Females have only the right oviduct, which shows developed epithelium and uterine glands in spring. Mating likely occurs in spring (October–December), and females store sperm in infundibular receptacles until ovulation between late spring and early summer. Potential clutch size ranges from three to five eggs. Females grow larger than males. The synchrony between spermiogenesis and mating defines the male cycle as prenuptial, which is considered the ancestral state of Squamata. These results agree with the hypothesis of conservative parameters for the group.

First report of male–male combat in free-ranging amazonian common lanceheads (Bothrops atrox)

In many snakes, males engage in agonistic interactions (male–male combat) apparently to establish dominant–subordinate relationships to gain priority access to reproductive females. In the Neotropical genus Bothrops Wagler, 1824 (∼45 species), male–male combat has been recorded only in three species of the monophyletic Bothrops atrox group. However, most male combats recorded in this clade occurred in captivity, an environment that facilitates the emergence of agonistic interactions. Here, we provide the first record of male–male combat in free-ranging Amazonian Common Lanceheads (Bothrops atrox (Linnaeus, 1758)) and discuss the implications of this observation for the species mating system. During fieldwork, we found one immature female and five active adult males, two of them fighting. These observations suggest that reproductive male B. atrox actively search and compete for widely dispersed and scarce receptive females.

Reproduction in the pitviper Bothrops jararacussu: large females increase their reproductive output while small males increase their potential to mate

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.

Atlas of Brazilian snakes: verified point-locality maps to mitigate the wallacean shortfall in a megadiverse snake fauna

Accurate and detailed species distribution maps are fundamental for documenting and interpreting biological diversity. For snakes, an ecologically diverse group of reptiles, syntheses and detailed data on distribution patterns remain scarce. We present the first comprehensive collection of detailed, voucher-based, point-locality, range maps for all described and documented Brazilian snakes, with the major aim of mitigating the Wallacean shortfall and as a contribution towards a better understanding of this rich, threatened, and poorly studied megadiverse fauna. We recorded a total of 412 snake species in Brazil on the basis of an extensive and verified point-locality database of 163,498 entries and 75,681 unique records (available here as Online Supporting Information). Our results reveal previously undocumented patterns of distribution, sampling effort, richness, and endemism levels, resulting in a more objective view of snake diversity in the Neotropics. Apart from these achievements, we understand that the most relevant and enduring contribution of the present atlas is to stimulate researchers to publish corrections, additions, and new discoveries.

Reproductive biology of the fossorial snake apostolepis gaboi (Elapomorphini): a threatened and poorly known species from the caatinga region

Knowledge of reproductive biology is essential to understand the intrinsic traits of any species and to elaborate effective conservation strategies, particularly for threatened species. Despite recent advances, knowledge on the reproductive biology of snakes remains deficient for most species, especially for tropical fossorial taxa. Apostolepis gaboi is a psammophilous, fossorial, and threatened snake endemic of the Quaternary Sand Dunes of the São Francisco River, Caatinga domain. Here, we present information on its reproductive biology based on macroscopic and microscopic data obtained from the examination of all specimens preserved in Brazilian museums. Specifically, we addressed sexual maturity, sexual dimorphism, clutch size, timing of gametogenesis, activity of the sexual segment of the kidney (SSK), and female sperm storage. Apostolepis gaboi is one of the smallest species of the genus. Females attain sexual maturity at larger body sizes and grow larger than males. However, adult females have relatively shorter tails than males. We found no sexual dimorphism in body circumference and head size. Clutch size is small and averages 4.5 eggs. All males from the wet season showed testes in spermiogenesis, ductus deferentia packed of sperm, and SSK hypertrophied and secretory. Secondary vitellogenesis also occurs in the wet season. Moreover, females in early vitellogenesis from the wet season showed sperm stored in the posterior infundibulum. Mating occurs in the second half of the wet season, as suggested by the finding of aggregations of sperm in the uterine lumen of a female in early secondary vitellogenesis. Mating is associated with gonadal activity in males. Sperm storage confers flexibility for females to ovulate at the most suitable time in an unpredictable habitat such as the Caatinga. Apostolepis gaboi exhibits similarities (association between mating and spermiogenesis, small clutch) and differences (absence of sexual dimorphism in head size and stoutness) compared with another Elapomorphini species. Lastly, we argue that some of the intrinsic traits of A. gaboi (small clutch and small body size) may increase its vulnerability to extinction, raising additional concerns to its conservation.

Atlas of Brazilian snakes: verified point-locality maps to mitigate the wallacean shortfall in a megadiverse snake fauna

Accurate and detailed species distribution maps are fundamental for documenting and interpreting biological diversity. For snakes, an ecologically diverse group of reptiles, syntheses and detailed data on distribution patterns remain scarce. We present the first comprehensive collection of detailed, voucher-based, point-locality, range maps for all described and documented Brazilian snakes, with the major aim of mitigating the Wallacean shortfall and as a contribution towards a better understanding of this rich, threatened, and poorly studied megadiverse fauna. We recorded a total of 412 snake species in Brazil on the basis of an extensive and verified point-locality database of 163,498 entries and 75,681 unique records (available here as Online Supporting Information). Our results reveal previously undocumented patterns of distribution, sampling effort, richness, and endemism levels, resulting in a more objective view of snake diversity in the Neotropics. Apart from these achievements, we understand that the most relevant and enduring contribution of the present atlas is to stimulate researchers to publish corrections, additions, and new discoveries.

Reproductive biology of the fossorial snake apostolepis gaboi (Elapomorphini): a threatened and poorly known species from the caatinga region

Knowledge of reproductive biology is essential to understand the intrinsic traits of any species and to elaborate effective conservation strategies, particularly for threatened species. Despite recent advances, knowledge on the reproductive biology of snakes remains deficient for most species, especially for tropical fossorial taxa. Apostolepis gaboi is a psammophilous, fossorial, and threatened snake endemic of the Quaternary Sand Dunes of the São Francisco River, Caatinga domain. Here, we present information on its reproductive biology based on macroscopic and microscopic data obtained from the examination of all specimens preserved in Brazilian museums. Specifically, we addressed sexual maturity, sexual dimorphism, clutch size, timing of gametogenesis, activity of the sexual segment of the kidney (SSK), and female sperm storage. Apostolepis gaboi is one of the smallest species of the genus. Females attain sexual maturity at larger body sizes and grow larger than males. However, adult females have relatively shorter tails than males. We found no sexual dimorphism in body circumference and head size. Clutch size is small and averages 4.5 eggs. All males from the wet season showed testes in spermiogenesis, ductus deferentia packed of sperm, and SSK hypertrophied and secretory. Secondary vitellogenesis also occurs in the wet season. Moreover, females in early vitellogenesis from the wet season showed sperm stored in the posterior infundibulum. Mating occurs in the second half of the wet season, as suggested by the finding of aggregations of sperm in the uterine lumen of a female in early secondary vitellogenesis. Mating is associated with gonadal activity in males. Sperm storage confers flexibility for females to ovulate at the most suitable time in an unpredictable habitat such as the Caatinga. Apostolepis gaboi exhibits similarities (association between mating and spermiogenesis, small clutch) and differences (absence of sexual dimorphism in head size and stoutness) compared with another Elapomorphini species. Lastly, we argue that some of the intrinsic traits of A. gaboi (small clutch and small body size) may increase its vulnerability to extinction, raising additional concerns to its conservation.

How does oocyte uptake occur? A macroscopic study of the ovarian and oviductal modifications for egg capture in the coral-snake Micrurus corallinus

The processes of follicular development, ovulation, egg capture, and egg transport vary among vertebrates. Therefore, analysis of the reproductive tract of several lineages is needed for understanding the evolutionary changes of the reproductive system. In turtles, the ovulated eggs are released into the coelomic cavity and taken up by one of the two oviducts, a phenomenon called extrauterine migration of eggs. However, the process of egg uptake in lizards is different. The egg is ovulated directly into the infundibulum, and oocyte uptake by the contralateral oviduct rarely occurs. The same pattern has been hypothesized to occur in snakes. To test this hypothesis, we analyzed the reproductive tract of female Micrurus corallinus preserved in zoological collections. We examined the anatomical characteristics of the infundibulum and ovary and compared the reproductive output between the ovaries to verify the mechanism of egg capture and the anatomical viability of extrauterine migration of eggs. The reproductive output of the right ovary was higher than that of the left ovary, and the higher number of eggs in the right oviduct is due exclusively to the production of the ipsilateral ovary. Several anatomical features prevent extrauterine migration of eggs, including the asymmetry of the reproductive system, the arrangement of the ovarian follicles in a single row, and the formation of a wrapping around the ovary and infundibulum by the visceral pleuroperitoneum membrane (preventing against ectopic eggs). Therefore, the hypothesis of egg capture by the contralateral oviduct is anatomically infeasible in M. corallinus and possibly in other snakes.

How does oocyte uptake occur? A macroscopic study of the ovarian and oviductal modifications for egg capture in the coral-snake Micrurus corallinus

The processes of follicular development, ovulation, egg capture, and egg transport vary among vertebrates. Therefore, analysis of the reproductive tract of several lineages is needed for understanding the evolutionary changes of the reproductive system. In turtles, the ovulated eggs are released into the coelomic cavity and taken up by one of the two oviducts, a phenomenon called extrauterine migration of eggs. However, the process of egg uptake in lizards is different. The egg is ovulated directly into the infundibulum, and oocyte uptake by the contralateral oviduct rarely occurs. The same pattern has been hypothesized to occur in snakes. To test this hypothesis, we analyzed the reproductive tract of female Micrurus corallinus preserved in zoological collections. We examined the anatomical characteristics of the infundibulum and ovary and compared the reproductive output between the ovaries to verify the mechanism of egg capture and the anatomical viability of extrauterine migration of eggs. The reproductive output of the right ovary was higher than that of the left ovary, and the higher number of eggs in the right oviduct is due exclusively to the production of the ipsilateral ovary. Several anatomical features prevent extrauterine migration of eggs, including the asymmetry of the reproductive system, the arrangement of the ovarian follicles in a single row, and the formation of a wrapping around the ovary and infundibulum by the visceral pleuroperitoneum membrane (preventing against ectopic eggs). Therefore, the hypothesis of egg capture by the contralateral oviduct is anatomically infeasible in M. corallinus and possibly in other snakes.

Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicops spp.)

The evolution of viviparity requires eggshell thinning to bring together the maternal uterus and extraembryonic membranes to form placentae for physiological exchanges. Eggshell thinning likely involves reduced activity of the uterine glands that secrete it. We tested these hypotheses by comparing the uterine and eggshell structure and histochemistry among oviparous and viviparous water snakes (Helicops) using phylogenetic methods. Eggshell thinning occurred convergently in all three origins of viviparity in Helicops and was accomplished by the loss of the mineral layer and thinning of the shell membrane. Uterine glands secrete the shell membrane in both oviparous and viviparous Helicops. These glands increase during vitellogenesis regardless of the reproductive mode, but they always reach smaller sizes in viviparous forms. As there is no phylogenetic signal in eggshell thickness and gland dimensions, we conclude that interspecific differences are related to reproductive mode and not phylogeny. Therefore, our results support the hypothesis that eggshell thinning is associated with the evolution of viviparity and that such thinning result from a reduction in gland size in viviparous taxa. Interestingly, the shell membrane thickness of viviparous females of the reproductively bimodal Helicops angulatus is intermediate between their oviparous and viviparous congeners. Thus, although eggshell thinning is required by the evolution of viviparity, a nearly complete loss of this structure is not. However, uterine gland dimensions are similar across viviparous Helicops. Fewer glands or their functional repurposing may explain the thinner shell membrane in viviparous species of Helicops in comparison to viviparous females of the bimodal H. angulatus.

Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicops spp.)

The evolution of viviparity requires eggshell thinning to bring together the maternal uterus and extraembryonic membranes to form placentae for physiological exchanges. Eggshell thinning likely involves reduced activity of the uterine glands that secrete it. We tested these hypotheses by comparing the uterine and eggshell structure and histochemistry among oviparous and viviparous water snakes (Helicops) using phylogenetic methods. Eggshell thinning occurred convergently in all three origins of viviparity in Helicops and was accomplished by the loss of the mineral layer and thinning of the shell membrane. Uterine glands secrete the shell membrane in both oviparous and viviparous Helicops. These glands increase during vitellogenesis regardless of the reproductive mode, but they always reach smaller sizes in viviparous forms. As there is no phylogenetic signal in eggshell thickness and gland dimensions, we conclude that interspecific differences are related to reproductive mode and not phylogeny. Therefore, our results support the hypothesis that eggshell thinning is associated with the evolution of viviparity and that such thinning result from a reduction in gland size in viviparous taxa. Interestingly, the shell membrane thickness of viviparous females of the reproductively bimodal Helicops angulatus is intermediate between their oviparous and viviparous congeners. Thus, although eggshell thinning is required by the evolution of viviparity, a nearly complete loss of this structure is not. However, uterine gland dimensions are similar across viviparous Helicops. Fewer glands or their functional repurposing may explain the thinner shell membrane in viviparous species of Helicops in comparison to viviparous females of the bimodal H. angulatus.

Reproductive modes of the South American water snakes: A study system for the evolution of viviparity in squamate reptiles

Viviparity has evolved at least 115 times in squamates and these multiple origins have raised a series of functional and evolutionary questions. Ideally, testing evolutionary hypotheses on squamate viviparity requires focusing on closely related taxa that exhibit both reproductive modes. South American water snakes of the tribe Hydropsini (genera Hydrops, Pseudoeryx, and Helicops) are a potential model system for studying the evolution of viviparity. However, available information about reproductive modes in this group is often confusing and contradictory. Herein, we identify the reproductive modes of the Hydropsini species by combining original data taken from both museum and live specimens with a critical review of the published literature. In addition, we mapped the reproductive modes on different phylogenetic hypotheses to identify origins of viviparity. The genus Hydrops is exclusively oviparous. Contrary to previous suggestions, we found Pseudoeryx plicatilis to be oviparous, and available evidence suggests that females of the species remain with eggs throughout incubation. Our results show that reproductive mode varies only in the genus Helicops. Two Helicops species are oviparous and eight species are viviparous. Interestingly, we also found that one species (Helicops angulatus) exhibits both reproductive modes. Intraspecific variation in reproductive mode is a rare phenomenon in squamates, and H. angulatus is the only snake species in which reproductive bimodality has been confirmed. H. angulatus is oviparous from northern to mid-eastern and north-eastern South America, and viviparous from north-western to mid-western South America. The allopatric distribution of oviparous and viviparous forms of H. angulatus does not support the hypothesis of facultative changes in the reproductive mode. Geographic variation in the embryonic stage at oviposition is likely to occur in H. angulatus. Ancestral state reconstructions suggest that oviparity is plesiomorphic in Hydropsini, as well as in the bimodal genus Helicops, and that viviparity has evolved independently at least three times in Helicops. We argue that the water snakes of the tribe Hydropsini (and more importantly, the genus Helicops and the bimodal H. angulatus) are an excellent model to test hypotheses on the evolution of squamate viviparity