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Reproductive cycles of neotropical boid snakes evaluated by ultrasound
Abstract
Snakes have increasingly been bred as pets around the world. Few studies have addressed the reproduction of boid snakes, and no study has addressed their reproductive cycles in captivity. Thus, this paper describes the reproductive aspects of Brazilian boids in captivity. We used ultrasonography to characterize the reproductive cycle of four boid species in captivity in the Southern Hemisphere: the anaconda (Eunectes murinus), the red-tailed boa (Boa constrictor constrictor), the Amazon tree boa (Corallus hortulanus), and the rainbow boa (Epicrates cenchria). Nonvitellogenic follicles occurred from January to December in anaconda and red-tailed boa and for a shorter period from September to February in Amazon tree boa and from January to May in rainbow boa. Vitellogenesis occurred from late June to late March in E. murinus in year-round (12 months), from March to March in Amazon tree boa, from late September to late March in red-tailed boa, and from late March to late September in rainbow boa. Mating occurred from late March to late September in red-tailed boa and rainbow boa and from late September to late March in Amazon tree boa. No mating was observed in anacondas, but a female probably underwent parthenogenesis. Births occurred in July in anaconda and in March to July in Amazon tree boa and from December to March in red-tailed boa and rainbow boa. In males, increases in testicular size were associated with the mating season. Ultrasonography proved to be a safe and noninvasive technique to study the reproductive cycle of giant snakes in captivity.
HIGHLIGHTS
• A method of diagnosing the reproductive phases that determined an ovulatory and gestational development reproductive standard.
• In males was possible to relate the size of the testicles with the reproductive season.
• Ultrasound examination showed an easy and inexpensive method of diagnosis.
... Chorioallantoic capillaries are closely aligned with maternal capillaries, so gas exchange is still thought to be its primary function in viviparous squamates, although the transport of inorganic ions [11,13] and histotrophic transfer [14] are also functions. Ultrasonography is a very important diagnostic tool in any veterinary field, with many potential uses in reptile medicine [2,15]. This technique is considered safe for the patient; it is also a non-invasive method for the evaluation of anatomical position, size, and organ structure. ...
... Depth and contrast were adjusted to optimize the structure display. Ultrasound features included the dimensions and echogenicity of the ovarian follicles and the development and viability of the embryonic structures, as well as any cases of follicular regression and the evaluation of possible nonfertilized, yellowish eggs, known as slugs [15]. The viability of the embryonic structures was studied using color and power Doppler. ...
... Professional reptile breeding is becoming increasingly important, and it is therefore particularly useful to develop reliable techniques to monitor reproduction and gestation, maximizing the potential of the breeding itself [2,15,21,22]. In the present study, behavioral data were integrated with ultrasonography, a noninvasive diagnostic technique, minimizing animal stress. ...
The Boa constrictor is one of the most common reptiles bred in captivity. To achieve a successful breeding season, thorough knowledge of the females’ reproductive activity is necessary. In this regard, information on the Boa constrictor is still rather scarce. The aim of the present study was to monitor the ovarian activity and the embryonic development of boas by ultrasound. We performed brief scans on thirty non-anaesthetized snakes using a portable ultrasound system and a 7.5–10 MHz linear array transducer (Esaote MyLab™ Classic). Ultrasound features, dimensions, and echogenicity of the preovulatory and postovulatory follicles were determined. As gestation progresses, the postovulatory follicle size increases, and the embryonic silhouette becomes increasingly recognizable. During the second month after ovulation, by using color Doppler, early embryos’ heart activity could be evaluated. It is possible to highlight vascular connections between the mother and the membrane covering the embryonic structures. Ultrasound also allows one to identify follicular regression or slugs (nonfertilized eggs) early. The present study suggests that ultrasound could be an excellent noninvasive technique to evaluate the reproductive activity of Boa constrictor, allowing us to precisely identify the correct time for mating, monitor embryo development and viability, and allow the early diagnosis of follicular regression.
... The timing of our observations coincides with that of previous reports on courtship and mating (Pizzatto & , 2007;Garcia & Almeida-Santos, 2021). Moreover, three mated females from the Cornélio Procópio breeding facility gave birth to a total of 51 offspring in the summer, similar to that reported in the literature (Garcia & Almeida-Santos, 2021). ...
... The timing of our observations coincides with that of previous reports on courtship and mating (Pizzatto & , 2007;Garcia & Almeida-Santos, 2021). Moreover, three mated females from the Cornélio Procópio breeding facility gave birth to a total of 51 offspring in the summer, similar to that reported in the literature (Garcia & Almeida-Santos, 2021). These results contrast with those of Gadd (1983), who reported unsuccessful parturition after courtship and mating with little use of spurs. ...
... Few studies have been published on species of Boidae using histological and tissue morphology evidence (Bento et al. 2024a(Bento et al. , 2024bPinheiro et al., 2020). Most existing studies have focused solely on reproductive aspects using macroscopic data (Bertona & Chiaraviglio, 2003;Garcia & Almeida-Santos, 2021;Pizzatto & Marques, 2007). Similarly, species of Pythonidae, which include large constrictor snakes, often exhibit convergent biological traits with Boidae (Murphy & Henderson, 1997;Reed & Rodda, 2009;Reynolds et al., 2014), are equally underrepresented in studies involving microscopic analyses of their reproductive aspects (Currylow et al., 2022;Shine et al., 1998Shine et al., , 1999. ...
Although the reproduction of some Boidae snakes has been studied through the macroscopic anatomy of the gonads, without microscopic morphology, there is little precision in describing reproductive cycles, especially for males. The relationship between the reproductive cycle—gametogenesis and reproductive seasonality throughout the year—has yet to be detailed for many Boidae species. We present macroscopic and histological data on the reproductive tracts of both male and viviparous female Corallus hortulana (Linnaeus 1758) (Amazon Tree Boa) from the Brazilian Amazon rainforest. Males present spermiogenesis and spermiation mainly during January and June (wet season to beginning‐dry season). Contrary to common assumption, we speculate that sperm production in C. hortulana, even in the tropical Amazon, is likely energetically demanding, influenced by rainfall, given that testicular involution occurred between May and November (most of the driest months of the year). Females present ovarian follicles in processes of vitellogenesis from December to August (wet season and part of the dry season). However, newborns are found in the wild mainly in the wet season, characterizing the cycle of female C. hortulana as seasonal. Unprecedentedly, we present the first microscopic description of the pouch and non‐glandular uterus in a Boidae species. The cells that compose the epithelial tissue of the non‐glandular uterus have been suggested for maintaining and supporting spermatozoa (sperm storage) in snakes, but we found no evidence that sperm storage occurs in this portion of the oviduct in C. hortulana. This study not only improves our understanding of reproductive biology in a boid, but because several aspects of reproductive cycles are conservative in the family (e.g., season of birth of newborn snakes), it aids in the development of effective conservation policies for endangered species such as Corallus cropanii, the rarest Boidae in the Americas.
We used ultrasonography and radiography to assess the sexual organs and characterize the reproductive cycle of captive golden lancehead ( Bothrops insularis ) and Alcatrazes lancehead ( B. alcatraz ), two endangered island snake species in Brazil. We assessed 46‐ individuals of golden lancehead and 12 of Alcatrazes lancehead kept in captivity between 2014 and 2020. Follicular development was similar between species, but follicles in Alcatrazes lancehead were smaller than in the golden lanceheads. Female golden lanceheads produced 24 live young, seven stillborn and 73 undeveloped eggs. Parturition of live young occurred between midsummer (February) and early autumn and gestation averaged 8 months. Female Alcatrazes lanceheads produced four live young in midsummer, and one undeveloped egg in early autumn. Males and females of both species have seasonal and biennial reproductive cycles. Sperm storage in both sexes is essential to coordinate male and female cycles. The data obtained with golden lancehead and Alcatrazes lancehead in captivity, demonstrate a degree of conservatism, following data from other Bothrops .
Os criadouros comerciais legalizados desestimulam o tráfico ilegal e impactam positivamente na população de serpentes, oferecendo o reforço populacional, além da oferta de animais saudáveis, dóceis, bem tratados com a devida legalização na qual apoia as ações do IBAMA (Instituto brasileiro do meio ambiente e dos recursos naturais). A ultrassonografia vem sendo utilizada para o diagnóstico gestacional e de alterações reprodutivas em diversas espécies, sendo uma ferramenta não invasiva. Este trabalho teve como objetivo realizar a avaliação reprodutiva em jiboias arco-íris da caatinga (Epicrates assisi) com o auxílio de ultrassonografia, para a classificação dos órgãos e aferição de medidas e determinação de parâmetros de normalidade. Foram utilizados 3 exemplares de jiboia arco-íris da caatinga (E. assisi) pertencentes ao criatório legalizado Pet’s Serpentes e Companhia. Das 3 fêmeas utilizadas no projeto, duas encontraram-se prenhas e uma com folículos primários. Na primeira Epicrates assisi, foi visualizado um possível ovo reabsorvido e 7 ovos viáveis, já na segunda fêmea foram contados 8 ovos viáveis. A última espécime apresentou em topografia ovariana, folículos primários em formas de esferas agrupadas em formato de ‘cacho de uva’, indicando estar apta para a cruza, mas com diagnóstico gestacional negativo. O exame ultrassonográfico é uma ferramenta de fácil diagnostico servindo com grande utilidade para avaliar e determinar o processo gestacional das serpentes E. assisis, sendo como uma grande aliada gerando informações acerca do período reprodutivo e o momento na qual gestação se encontra.
Zoos and aquariums are culturally and historically important places where families enjoy their leisure time and scientists study exotic animals. Many contain buildings of great architectural merit. Some people consider zoos little more than animal prisons, while others believe they play an important role in conservation and education. Zoos have been the subject of a vast number of academic studies, whose results are scattered throughout the literature. This interdisciplinary volume brings together research on animal behaviour, visitor studies, zoo history, human-animal relationships, veterinary medicine, welfare, education, enclosure design, reproduction, legislation, and zoo management conducted at around 200 institutions located throughout the world. The book is neither 'pro-' nor 'anti-' zoo and attempts to strike a balance between praising zoos for the good work they have done in the conservation of some species, while recognising that they face many challenges in making themselves relevant in the modern world.
The golden lancehead (Bothrops insularis) is a critically endangered snake endemic to Queimada Grande Island, southeastern Brazil. Captive breeding programs are vital for the conservation of this species. This study evaluates the gestation of two females golden lanceheads using radiography and ultrasonography. The first female was collected on the island while reproductively active (late vitellogenesis or early pregnancy) and kept in captivity. This female gave birth to five neonates after an 8-month gestation period, which is longer than estimates based on specimens preserved in museums. The second female copulated in captivity in July and probably ovulated in October. In this case, no embryonic development was detected, and the female deposited 14 undeveloped eggs approximately 6 months after ovulation.
Background Folliculinum is a homeopathic sarcode medication that is mainly used for regulating the estrous cycle and reproductive function. In snakes, it is common to observe low frequencies of reproduction. Ovulation is related to follicular size and morphology, and follicle homogeneity may indicate the absence of problems such as dystocia (egg retention) or follicular stasis.
Objective The objective of the present study was to report on follicular stage changes in two ball pythons, Python regius (Shaw, 1802), which were treated using Folliculinum 6cH in a zoological park setting.
Methods Two female pythons – one weighing 2.8 kg, the other weighing 2.5 kg, and neither with a history of reproduction – were examined by ultrasound to enable viewing of ovarian follicles in different phases and sizes. Folliculinum 6cH, two globules diluted in 200 mL of water, was administered, targeted to the eyes and nostril regions.
Results Even given the slow metabolism of reptiles, ultrasound revealed an improvement in follicle homogeneity between 6 and 15 days after the start of homeopathy in both snakes; there was also improved weight gain in both animals. The MOdified NARanjo Criteria for Homeopathy (MONARCH) score was +8 in each of the cases, suggesting a causal relationship between the use of homeopathic medicine and clinical outcome.
Conclusion Folliculinum 6cH may have promoted stabilization of follicle size and enabled folliculogenesis in two ball pythons.
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.
RESUMO As serpentes pertencem ao segundo maior grupo dentro dos répteis, podendo apresentar sazonalidade quanto à espermatogênese, com produção descontínua ou contínua. O presente trabalho tem como objetivo caracterizar aspectos da biologia reprodutiva de Boa constrictor constrictor com base nos achados histológicos dos testículos nos períodos de máxima atividade (período de gametogênese) e quiescência. Os testículos de dois espécimes de Boa c. constrictor (7767 e 11752) foram cortados a uma espessura de 3μm em micrótomo, corados com azul de toluidina 1%, fotodocumentados e descritos. A presença de espermatozoides na luz do túbulo seminífero no indivíduo 7767 indica um período de máxima gametogênese, enquanto o lúmen dos túbulos seminíferos pouco evidentes, sem a presença de espermatozoides e de células gaméticas em divisão, caracteriza o indivíduo 11752 em período quiescente. Mediante os achados histológicos descritos no presente estudo, concluiu-se que Boa c. constrictor apresenta sazonalidade em relação à gametogênese, sendo esse padrão de sazonalidade associado ao período de cópulas relatado em literatura característico de serpentes com padrão pré-nupcial.
We present an updated checklist of Brazilian reptile species and, for the first time, its confirmed
presence in federation units (26 states and the Federal District). Brazil has the third richest reptile fauna in
the world, with 795 species: 36 Testudines, 6 Crocodylia, and 753 Squamata (72 amphisbaenians, 276 “lizards”,
and 405 snakes). If subspecies are counted, these numbers increase to 842 taxa. Almost half (47%) of
the Brazilian reptiles are endemic to the country, mainly amphisbaenians (76%), followed by lizards (54%),
snakes (40%), and chelonians (16%). Nomenclatural changes and taxa included or excluded since the last
checklist are discussed, as well as dubious or invalid state records.
In reptiles, the mode of reproduction is typically sexual. However, facultative parthenogenesis occurs in some Squamata, such as Komodo dragon (Varanus komodoensis) and Burmese python (Python bivittatus). Here, we report facultative parthenogenesis in the green anaconda (Eunectes murinus). We found two fully developed female neonates and 17 undeveloped eggs in the oviduct of a female anaconda isolated from other individuals for eight years and two months at Ueno Zoo, Japan. To clarify the zygosity of the neonates, we analyzed 18 microsatellite markers of which 16 were informative. We observed only maternal alleles and no paternal alleles for all 16 markers. To examine the possibility of the long-term sperm storage, we estimated allele frequencies in a putative parental stock by genotyping five unrelated founders. If all founders, including the mother, are originated from a single Mendelian population, then the probability that the neonates were produced by sexual reproduction with an unrelated male via long-term sperm storage was infinitesimally small (2.31E-32 per clutch). We also examined samples from two additional offspring that the mother delivered eight years before her death. We consistently observed paternal alleles in these elder offspring, indicating that the mother had switched from sexual reproduction to asexual reproduction during the eight years of isolation. This is the first case of parthenogenesis in Eunectes to be validated by DNA analysis, and suggests that facultative parthenogenesis is widespread in the Boidae.
Parthenogenesis has been documented across a variety of vertebrate taxa. Within snakes, a group for which the largest number of cases has been documented, both obligate and facultative types of parthenogenesis exists, but the obligate form appears to be restricted to a single basal species of blind snake, Indotyphlops braminus. In contrast, a number of snake species that otherwise reproduce sexually have been found capable of facultative parthenogenesis. Because original documentation of this phenomenon was restricted to subjects held in captivity and isolated from males, facultative parthenogenesis was attributed as a captive syndrome. However, its recent discovery in nature shifts the paradigm and identifies this form of reproduction as a potentially
important feature of vertebrate evolution. In light of the growing number of documented cases of parthenogenesis, it is now possible to review the phylogenetic distribution in snakes and thus identify subtle variations and commonalities that may exist through the characterization of its
emerging properties. Based on our findings, we propose partitioning facultative parthenogenesis in snakes into two categories, type A and type B, based on the sex of the progeny produced, their
viability, sex-chromosome morphology, ploidy, and their phylogenetic position. Furthermore, we introduce a hypothesis (directionality of heterogamety hypothesis) to explain the production of female-only parthenogens in basal alethinophidian snakes and male-only parthenogens in caenophidian (advanced) snakes.
Keywords: Automixis – Facultative parthenogenesis – Obligate parthenogenesis – Sex chromosomes morphology – Sex-determination – Genomics – Serpentes – Squamates
A reprodução faz parte do ciclo de vida dos animais permitindo a perpetuação e a conservação das espécies. Em serpentes, existe uma escassez de informações técnicas a respeito do ciclo reprodutivo. Este estudo teve o objetivo de avaliar o aparelho reprodutivo por meio da ultrassonografia em serpentes vivíparas cativas da família Boidae, permitindo diagnosticar as diferentes fases reprodutivas. Foram avaliadas ultrassonograficamente onze serpentes adultas de quatro espécies da família Boidae: Eunectes murinus, Boa constrictor constrictor, Corallus hortulanus e Epicrates cenchria pertencentes ao acervo do Museu Biológico do Instituto Butantan, São Paulo Brasil. Para a avaliação ultrassonográfica, as serpentes foram contidas fisicamente com gancho herpetológico e depois manualmente por aproximadamente 15 minutos. A avaliação foi feita aplicando-se gel acústico sobre a pele e posicionando o transdutor na linha lateral-ventral direita e esquerda, em região medial do corpo em sentido crânio-caudal. O exame ultrassonográfico permitiu avaliar todo o ciclo reprodutivo nas serpentes. Nas avaliações ultrassonográficas das fêmeas pode-se definir as fases de desenvolvimento ovariano e ovidutal. Os folículos ovarianos durante a fase pré-vitelogênica foram visualizados como homogêneos e anecogênicos, em forma de "cacho de uva". Já na fase vitelogênica, os folículos estavam maiores e mais ecogênicos seguidos uns dos outros, como um "colar de pérolas". Quando não houve cópula, os folículos foram reabsorvidos dentro do ovário retornando a fase pré-vitelogênica. Na fase pós ovulatória foram visualizados três estágios bem definidos de desenvolvimento fetal dentro do oviduto: 1) logo após a ovulação (e fecundação), somente o vitelo foi visualizado; 2) o vitelo ocupava 60% e o feto 40% do ovo e 3) o feto estava formado e não havia vitelo. Nos machos, os testículos foram visualizados como uma imagem homogênea e hipoecogênica quando se encontravam em estágio reprodutivo. Quando não estavam reprodutivos não era possível visualizar a imagem do testículo devido ao seu tamanho. A avaliação ultrassonográfica do aparelho reprodutor em serpentes demonstrou ser uma técnica de diagnóstico segura, não invasiva e que permite o acompanhamento das principais fases reprodutivas
Male-male combat is a ritualized behaviour occurring mainly during the mating season (Greene, 1997; Schuett, 1997; Schuett et al., 2001) which is widespread among snake families including Boidae, Elapidae, Viperidae and Colubridae (Shine, 1978, 1994). Male-male combat is an example of intrasexual selection in which males compete for access to females. Typically, the two opponents attempt to physically subdue one another by exerting pressures (e.g., pushing, flipping, entwining) on the anterior part of their body in an attempt to bring their adversary to the ground. (Carpenter, 1977). Among boid snakes male-male combat is recorded in only one erycinae (Eryx colubrinus – see Schuett et al., 2001), 21 pythoninae (see Shine, 1994; Schuett et al., 2001) and 14 boinae species – nine of these being Neotropical (see Shine, 1994; Schuett et al., 2001). The genus Epicrates includes ten species and combat is recorded for six, including the Brazilian E. c. cenchria (Shine, 1994; Schuett & Schuett, 1995; Schuett et al., 2001). Despite the existence of many records in boid snakes, detailed descriptions of combat behaviour are only available for the pythoninae (Python molurus ; Baker et al., 1979) and the boinae Sanzinia madagascariensis. Here we provide a description of combat in three captive male Epicrates cenchria crassus. This mainly terrestrial species feeds on small mammals (Pizzatto L., unpubl. data), and inhabits the Brazilian cerrado, a savanna-like vegetation, where it is probably associated with riparian forests (Peters et al., 1986; Henderson et al., 1995). The three snakes came from unknown localities in São Paulo State, southeastern Brazil and were maintained in captivity in Bandeirantes city (-50°03'W, -23°02'S), Paraná State, southern Brazil. Male 1 and male 2 were obtained in 1999 and male 3 was obtained in early 2001. These snakes were maintained in individual cages (1.0 m x 0.50 m x 0.40 m) made of wood with screen in the front. Cages were contiguous and disposed side by side in the same room, thereby preventing visual contacts between the experimental subjects. Room temperature was ca. 30–32°C in spring/summer and 22–25°C in autumn/winter. We used heating pads when the temperature fell below 25°C, and sprayed the cages with water when the humidity was low. Water was provided ad libitum, and snakes were fed once a week (one or two young rats). We measured each snake in June 2004: Male 1 was 1130 mm in SVL and weighed 845 g, male 2 was 910 mm in SVL and 800 g, and male 3 was 1060 mm SVL and 910 g. All males were adults (L. Pizzatto, unpl. data). We used the terminology used by Carpenter et al. (1976) for the combat phases. In April/May in 2001, we observed high snake activity in the cages and decided to introduce males to one another, simultaneously, in the same cage. Then, male 1 and 3 started a combat behaviour. Although male 2 was in the cage with the other 2 snakes it did not engage in combat. The end of the combat was initiated when the loser (male 3) withdrew itself from the fight and became inactive. After trials, all snakes were returned to their individual cages. Male-male ritualized combat in the Brazilian rainbow boa, Epicrates cenchria crassus
Currently, wild animals have been received special attention for domestic breeding. In Wild Animal Medicine, ultrasonographic exams could be considered as a tool to diagnose and prevent disease. Ultrasonographic examination of twenty snakes (Boa constrictor) was performed in order to describe the morphological and ultrasonography appearance of their coelomic structures. Examination by ultrasonography revealed the parechymal liver ranging from slightly hypoechogenic to hyperechogenic, with echogenic margins and homogeneous echotexture in total scanning of this organ. The kidney was accessible for examination by sagittal ultrasound, showing an ellipsoid shape, a hyperechogenic capsule with a thin and regular wall. Ultrasonographic scanning of ovarian follicle showed an ovoid shape, as well as a thin, regular and slightly hyperechogenic edge. No evident structures from male reproductive system were identified by ultrasound examination because of their similar echogenic appearance to the tissues around and the "body fat" that lies in this region. Examination by ultrasound of the coelomic structures was a fast and repeatable technique, which provides useful data to recognize the morphology, sintopy and ultrasonographic appearance of organs such as liver, kidneys and vitellogenic follicles.
Sperm quantity and quality were examined in 2 populations (from Mar de Cobo and Necochea, Argentina) of the subterranean rodent Ctenomys talarum (tuco-tuco) for which polygyny was confirmed as their mating system. Nonetheless, differential population attributes allow us to propose that polygyny may be exerted at different levels. Mean epididymal sperm counts were not different, but the Necochea population was characterized by higher variance in sperm counts. Low sperm production, with little variance, in the Mar de Cobo population is consistent with a more extreme polygyny, with aggression playing an important role in the males securing monopolization of females. In the Necochea population, where males were less likely to maintain female exclusivity, subordinant males are not driven away and may invest more in sperm production than in male-male interactions. However, C. talarum males from both populations produce high-quality sperm cells, based on their motility, percentage of live sperm cells, and morphology.
We present natural history information on 66 species of snakes found in the forests of the Manaus region, Central Amazonia, Brazil. For each species, we provide information on size, color pattern, habitat and microhabitat, feeding habits, reproduction, and defense. We also include a partial summary of the information available in the literature for Amazonian localities. Our results are based on nearly 800 captures or sightings of snakes made from 1990-95 at localities around Manaus, mostly at a primary forest reserve 25 km north of Manaus. Field data at this reserve were obtained during over 2600 person-h of visually searching for snakes, ca. 1600 of which occurred during time-constrained search. Temperature and relative humidity in Manaus are high and the amount of annual rainfall (2075 mm/yr) is relatively small, with a long dry season (4-7 mo). Of the 65 species for which information is available, 28 (42%) are primarily terrestrial, 20 (30%) fossorial and/or cryptozoic, 13 (20%) arboreal, and four (6%) aquatic, although many species use more than one microhabitat when active. Nearly all inactive snakes were found on vegetation. In relation to time of activity, 26 (41 %) of the 62 species for which information is available seem to be strictly diurnal, 13 (21%) strictly nocturnal, and 23 (38%) both diurnal and nocturnal. The five prey types most commonly consumed by snakes in the Manaus region are vertebrates: lizards (consumed by 58% of the species), frogs (39%), mammals (23%), birds (18%), and snakes (16%). A cluster analysis combining data on microhabitat use, diel activity, and diet resulted in several groups of species with similar habits. All these "guilds" included closely related species, as well as distantly related ones that converge in habits. These combined results indicate that in addition to current ecological factors (e.g., predation pressure, differential prey availability in different microhabitats), historical factors (phylogeny and biogeography) may have played an important role in determining the current natural history patterns of this snake assemblage. A high diversity of defensive tactics was found in this assemblage, and phylogeny may be a strong determinant factor for the occurrence of defensive tactics in each species. Contradicting generalizations on the timing and length of reproductive season in Amazonian snakes, juvenile recruitment seems to occur mainly during the rainy season in most species from the Manaus region, although some species seem to breed throughout the year. This may be a consequence of the prolonged dry season that occurs in the region, during which time some resources occur in limited supplies.
Among squamate reptiles, gravid females commonly are said to be able to resorb infertile and malformed eggs from their oviducts. This pattern, if it existed, would allow females to recycle nutrients from abortive attempts at reproduction, and to increase lifetime reproductive potential by modulating reproductive effort according to environmental circumstances. However, a review of the literature reveals that evidence for oviductal egg resorption is weak, and does not preclude other fates for abortive eggs (egg retention or expulsion). Furthermore, for the oviduct to resorb eggs would require that it have the functional properties of the digestive tract, properties that may be incompatible with its several reproductive functions. Future work should not assume oviductal egg resorption in squamates without definitive evidence that the eggs are not simply aborted or retained by females following absorption of water.
Boídeos ocorrem na América do Norte, Central e do Sul, África, incluindo Madagascar, Ásia, bem como em algumas ilhas do Pacífico. No Brazil, ocorrem ao longo de uma ampla variedade de hábitats e áreas climáticas. Este estudo apresenta dados reprodutivos e morfométicos para onze espécies e subespécies de boídeos brasileiros (Boa c. contrictor, B. c. amarali, Corallus caninus, Co. hortulanus, Co. cropanii, Epicrates c. cenchria, Ep c. assisi, Ep c. crassus, Eunectes murinus, Eu. deschauenseei and Eu. notaeus), incluindo dados morfométricos para os boídeos de Madagascar (Sanzinia madagascariensis e Acrantophis dumerili) e ilhas do Pacífico (Candoia carinata, Ca. aspera e Ca. bibroni). Essas serpentes de grande porte apresentam padrão conservativo em termos de sazonalidade do ciclo reprodutivo feminino, tamanho na maturidade, tamanhos relativos da ninhada e dos filhotes, e freqüência reprodutiva. O padrão reprodutivo dos Boidae é similar ao de Pythonidae. Os ciclos femininos são não anuais e sempre sazonais, geralmente com os nascimentos ocorrendo principalmente na primaveraverão. Estas serpentes apresentam dimorfismo sexual no comprimento corporal médio, tamanho da cabeça, comprimento do esporão e robustez. Em espécies nas quais os machos realizam combate ritual previamente à época de cópula não ocorre dimorfismo no tamanho corporal médio (i.e. subespécies de Ep. cenchria). O ciclo reprodutivo masculino dos boídeos é mais variável, podendo ser sazonal ou contínuo, dependendo da espécie.
Transverse ultrasound images from three live boa constrictors (Boa constrictor) were compared to the corresponding gross sections of a euthanized boa constrictor. The snakes were anesthetized, placed into dorsal recumbency, and imaged through the ventral scutes. Ultrasound images were produced with a real time, B-mode scanner and a linear 7.5-MHz transducer. The heart, liver, stomach, gall bladder, pancreas, kidneys, and fat body were the coelomic structures most consistently recognized ultrasonographically. Results of this study indicate that ultrasound is a useful imaging technique in snakes.
The Epicrates cenchria complex is endemic to the Neotropical region, occurring in mainland portions of Central and South America. The taxonomic status of the nine currently recognized subspecies (E. c. alvarezi, E. c. assisi, E. c. barbouri, E. c. cenchria, E. c. crassus, E. c. gaigei, E. c. hygrophilus, E. c. maurus, and E. c. polylepis), were evaluated based on external morphology, osteology, and hemipenis characters. Results obtained through quantitative and qualitative analyses support the recognition of E. alvarezi, E. assisi, E. cenchria, E. crassus, and E. maurus as distinct species based on statistically robust delimitation of species boundaries.
Male–male fighting (MMF) in snakes is a sexually dimorphic trait in adults that is expressed during breeding periods and
confers reproductive advantages to winners. This trait, however, is not ubiquitous among the approximately 2,700 species of
extant snakes, and past research shows evidence of taxonomic trends. We evaluated the phylogenetic distribution of MMF in
extant snakes using two previously published estimates of snake evolutionary history. We clearly identified multiple independent
gains and losses of MMF in snakes and phylogenetically important taxa for which information on MMF is lacking. We followed
this with two tests of the association of MMF with mode of prey capture using the concentrated-changes test (CCT) of Maddison
(1990), and a third test using the subtree decomposition method of Read and Nee (1995). In the CCT analyses, first we tested
whether MMF was randomly distributed with respect to mode of prey subjugation in snake lineages. This hypothesis was rejected,
with MMF being significantly more concentrated in taxa that subjugate prey by constriction and/or envenomation. Second, we
tested a more temporally exact hypothesis: whether changes in state of MMF were randomly distributed with respect to occurrences
of state changes in mode of prey subjugation. Results of this test depended on the exact test parameters used. In general,
however, this hypothesis also was rejected, suggesting that loss of constriction and/or envenomation typically results in
loss of MMF, or vice versa. Last, the subtree decomposition test indicated a significant correlation between evolution of
MMF and evolution of constriction and/or envenomation as the primary mode of prey subjugation. We propose that the relationship
between these states is not causal but results from both characters being independent adaptations to energy resource scarcity.
Until recently, facultative automictic parthenogenesis within the squamate reptiles exhibiting ZZ:ZW genetic sex determination
has resulted in single reproductive events producing male (ZZ) or female (ZW) offspring. With the recent discovery of viable
parthenogenetically produced female (WW) Boa constrictors, the existence of further parthenogenetic events resulting in WW
females was questioned. Here, we provide genetic evidence for consecutive virgin births by a female Colombian rainbow boa
(Epicrates maurus), resulting in the production of WW females likely through terminal fusion automixis. Samples were screened at 22 microsatellite
loci with 12 amplifying unambiguous products. Of these, maternal heterozygosity was observed in 4, with the offspring differentially
homozygous at each locus. This study documents the first record of parthenogenesis within the genus Epicrates, a second within the serpent lineage Boidae, and the third genetically confirmed case of consecutive virgin births of viable
offspring within any vertebrate lineage. Unlike the recent record in Boa constrictors, the female described here was isolated
from conspecifics from birth, demonstrating that males are not required to stimulate parthenogenetic reproduction in this
species and possibly other Boas.
Parthenogenesis in vertebrates is considered an evolutionary novelty. In snakes, all of which exhibit genetic sex determination with ZZ : ZW sex chromosomes, this rare form of asexual reproduction has failed to yield viable female WW offspring. Only through complex experimental manipulations have WW females been produced, and only in fish and amphibians. Through microsatellite DNA fingerprinting, we provide the first evidence of facultative parthenogenesis in a Boa constrictor, identifying multiple, viable, non-experimentally induced females for the first time in any vertebrate lineage. Although the elevated homozygosity of the offspring in relation to the mother suggests that the mechanism responsible may be terminal fusion automixis, no males were produced, potentially indicating maternal sex chromosome hemizygosity (WO). These findings provide the first evidence of parthenogenesis in the family Boidae (Boas), and suggest that WW females may be more common within basal reptilian lineages than previously assumed.
If selective forces on locomotor ability and reproductive biology differ among habitats, we expect to see relationships between habitat, morphology, and life-history traits. Comparative (phylogenetically based) analysis of data from 12 pythonid and 12 boid snake species reveals multiple evolutionary shifts in habitat use, notably in the evolution of arboreal habits. Compared to terrestrial and aquatic taxa of the same overall body size, arboreal species have narrower and more laterally compressed bodies and relatively longer tails. Offspring sizes are not affected by arboreality, but presumably reflecting space constraints within their narrow bodies, arboreal species (1) produce smaller clutch sizes relative to maternal body length and (2) have left and right ovaries that overlap little if at all along the length of the body (i.e., the right ovary is positioned anterior to the left ovary) whereas in terrestrial snakes the two ovaries overlap along much of their length. This modification of ovarian morphology in arboreal snakes presumably reduces the degree of bodily distension during vitellogenesis and pregnancy, thus enhancing climbing ability and camouflage among the branches.
Obtaining population-level life history data such as egg and clutch size in reptiles has most often required that individuals be sacrificed. This prevents a reexamination of individuals over intra-annual and inter-annual time scales, limiting insight into the effects of varying environmental conditions on reproductive output. Here, we test the use of a laptop-sized portable ultrasound imaging system as a nondestructive means for quantifying reproductive investment in five species of lizards with a range of body sizes, forms and life histories. Ultrasound scans produced egg counts that were accurate for clutch sizes of two to seven eggs, and provided good estimates (within 5.5+/-1.69 eggs, mean +/- s.e.m., relative error 21%) for clutch sizes of between 18 and 41 eggs. Egg measurements using virtual calipers produced average egg volumes that deviated from actual volumes by 0.09+/-0.01 cm(3) (relative error 25.9%), and estimated clutch volumes that differed from actual volumes by 1.03+/-0.26 cm(3) (relative error 29.5%). We also monitored development in five lizard species and found that changes in follicle and egg size and degree of embryonic development can be measured over periods of just a few days.
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, 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.
Both sexes mature at about 150 cm snout-vent length (SVL) prior to copulation. Reproductive activities occurred in spring (late September to early November). Two to 6 males aggregated around a single female; >1 male was seen to copulate with the same female, in the presence of other males. Mating aggregations lasted from 4-6 wk. Females oviposited in late December or early January inside "nests' of leaf litter and coiled around the eggs to incubate them. Clutch size varied between 9-54 eggs per clutch, and was positively correlated with maternal SVL. During reproduction, females lost c44% of their initial body weight; 2/3 was attributed to oviposition, 1/3 to metabolic costs and reduced feeding opportunities associated with incubation. Probably because of this high metabolic cost and the low energy intake associated with "ambush' foraging, females did not breed every year. -from Authors
Published and original data on the degree of sexual size dimorphism (SSD) were collated for 374 species of snakes from eight families, to test for predicted associations between SSD and other aspects of reproductive biology. Data on the occurrence and form of male-male combat were also reviewed. Because phylogenetic conservatism was evident in most of the characteristics studied, the data were analyzed in two ways: (1) I looked for general patterns by treating each species as an independent unit; and (2) I superimposed the data onto a phylogenetic framework so that I could calculate independent contrasts within each lineage. Male-male combat has been reported in 124 species of snakes, and this combat takes many forms. For example, biting is common in nonvenomous species. Males grow larger, relative to conspecific females, in species with male-male combat than in species not recorded to show this behavior, and this association remains significant when analysis is restricted to independent phylogenetic contrasts. On a proximate level, the larger size of males in species with combat is due primarily to a prolongation of male growth after maturation. Fecundity advantages of larger body sizes in females may also influence SSD, because the degree of SSD correlates with the rate at which litter sizes increase with body size. The evolution of viviparity is associated with a consistent shift toward larger female size relative to male size. However, my analyses suggest that a previously documented correlation between SSD and geographic distribution is due to phylogenetic conservatism rather than to any functional relationship between the two variables.
We provide data on sexual dimorphism, reproductive biology, and mating aggregations of the Argentine Boa Constrictor (Boa constrictor occidentalis), a poorly known, threatened species. Snakes were examined by ultrasound scanning between 1998 and 2001. Adult females were 14% longer and 51% more massive than adult males. Litter size averaged 25.05 and increased significantly with maternal body size. Reproductive activity was seasonal and associated, with vitellogenesis and spermatogenesis occurring during the dry season (April to September). The ratio of reproductive to nonreproductive females was 1:1, suggesting females do not reproduce annually in this population. Reproductive females were in better body condition (mass relative to body length) than nonreproductive females, indicating that a female's initial “decision” to reproduce in any given year may be driven by her body condition (storing enough energy for a long period before expending it on reproduction: “capital breeder”). Aggregated boas were found only during the dry season. The high proportion of solitary reproductive males and the operational sex ratio (male:female, 1.53:1) suggests a system of “prolonged mate-searching polygyny.”
A 22-year-old captive Brazilian rainbow boa (Epicrates cenchria cenchria) gave birth to four offspring after being housed with a vasectomized male. Sexual reproduction as a result of failed prior vasectomy, recanalization of the vas deferens, or prolonged sperm storage was ruled out using the clinical history, histopathology, and gross necropsy. Short tandem repeat (STR) DNA markers were genotyped in the male, female, and four offspring. None of the offspring possessed a diagnostic STR allele present in the potential sire. In addition, all offspring were homozygous at each STR locus evaluated, supporting parthenogenetic reproduction. This is the first report of parthenogenesis in a Brazilian rainbow boa and has implications for the conservation of reptiles maintained in captive breeding programs. Zoo Biol. 00:1-5, 2012. © 2012 Wiley Periodicals, Inc.
Reproductive investment and output are integral fitness components, often incorporated into life-history trade-off models and important to population dynamics. The trade-offs associated with reproduction can be dramatic in species such as snakes that make especially large investments into reproduction. Unfortunately, traditional methods used to determine reproductive investment and output are effective in many (but not all) situations. Thus, we used portable ultrasonography to serially estimate reproductive investment and reproductive output in three python species that exhibit significant variation in phylogeny, geographic range, body size, egg size, and clutch size: ball pythons (Python regius), Children's pythons (Antaresia childreni), and water pythons (Liasis fuscus). At each time point of measurement (range: 1–49 days pre-oviposition), ultrasound estimates of viable clutch size were highly accurate in all three species. However, ultrasound estimates of mean viable egg mass, and thus viable clutch mass, significantly differed from the actual values (range: 23–73% error). Interestingly, this error was considerably smaller as females approached oviposition, suggesting that female pythons transfer a significant amount of water into their eggs during the week before oviposition. Thus, water balance during late-stage egg development may be an integral part of reproductive success. The results obtained in the present study form the foundation for future assessments of reproductive investment, and also provide insight into the use of ultrasound technology to assist such efforts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 772–778.
Radiography and ultrasonography are important imaging tools for the morphologic and functional evaluation of internal organs and the diagnosis of reptilian diseases. The unique anatomy and architecture of the coelomic cavity and reptilian organs such as the respiratory tract will result in variations from the normal radiographic images seen in domestic animals and avian species. Radiography is the most commonly used imaging technique in reptiles to assess the respiratory tract, gastrointestinal tract, urinary tract, and skeletal system. Specific metabolic disorders (eg, metabolic bone disease in lizards and chelonians) as well as infectious disease processes can also be diagnosed using radiographic techniques. Advanced imaging techniques, such as contrast radiography, scintigraphy, and ultrasonography, are commonly used but may present some unique challenges in reptiles because of their anatomy and pathophysiology of diseases. Pathologic changes can only be recognized and diagnosed with a good understanding and knowledge of reptile anatomy and pathophysiology. Normal radiographic appearance of reptiles and the application of advanced radiography, including nuclear imaging and ultrasonographic techniques, will be presented.
Reproductive effort has been defined as the proportion of an organism's energy budget that is allocated to reproduction over a biologically meaningful time period. Historically, studies of reproductive bioenergetics considered energy content of gametes, but not costs of gamete production. Although metabolic costs of vitellogenesis (MCV) fundamentally reflect the primary bioenergetic cost of reproductive allocation in female reptiles, the few investigations that have considered costs of reproductive allocation have focused on metabolic costs of pregnancy (MCP) in viviparous species. We define MCP as energetic costs incurred by pregnant females, including all costs of maintaining gestation conditions necessary for embryogenesis. MCP by our definition do not include fetal costs of embryogenesis. We measured metabolic rates in five species of viviparous snakes (Agkistrodon contortrix, Boa constrictor, Eryx colubrinus, Nerodia sipedon, and Thamnophis sirtalis) during vitellogenesis and pregnancy in order to estimate MCV and MCP. Across all species, MCV were responsible for 30% increases in maternal metabolism. Phylogenetically-independent contrasts showed that MCV were significantly greater in B. constrictor than in other species, likely because B. constrictor yolk energy content was greater than that of other species. Estimates of MCP were not significantly different from zero in any species. In viviparous snakes, MCV appear to represent significant bioenergetic expenditures, while MCP do not. We suggest that MCV, together with yolk energy content, represent the most significant component of reptilian reproductive effort, and therefore deserve greater attention than MCP in studies of reptilian reproductive bioenergetics.
Thesis (Ph. D.)--University of Tennessee, Knoxville, 2000. Vita. Includes bibliographical references (leaves 267-284).
By employing histochemical techniques, the follicular atresia and problems of interstitial cells have been worked out in the ovaries of two species of snakes (Naja tripudians and Bungarus coeruleus). Large follicles with a polymorphic granulosa show more atresia from September to November. Details of morphological and histochemical changes in the yolk nucleus substance, mitochondria and lipid bodies of oocyte and granulosa have been described. During atresia the theca interna is greatly hypertrophied and is loaded with lipids consisting of first phospholipids, then phospholipids and triglycetides and finally triglycerides, cholesterol and its ester and little phospholipids. Finally the oocyte, zona pellucida, granulosa cells and most of the cells of theca interna regress and disappear, leaving behind some residual cells of theca interna. The histochemistry of normal and atretic follicle of snakes and lizards has also been compared and contrasted with that in mammals. The “interstitial cells” of snake ovary have been discussed in the light of recent researches carried out on similar cells in the mammalian ovary.
The majority of ovarian follicles undergo atresia, a hormonally controlled apoptotic process. Monitoring apoptotic DNA fragmentation provides a quantitative and sensitive endpoint to study the hormonal regulation of atresia in ovarian follicles. During follicle development, gonadotropins, together with local ovarian growth factors (IGF-I, EGF/TGF-alpha, basic FGF) and cytokine (interleukin-1 beta), as well as estrogens, activate different intracellular pathways to rescue follicles from apoptotic demise. In contrast, TNF-alpha, Fas ligand, presumably acting through receptors with a death domain, and androgens are atretogenic factors. These diverse hormonal signals probably converge on selective intracellular pathways (including genes of the bcl-2 and ICE families) to regulate apoptosis. With a constant loss of follicles from the original stockpile, the ovary provides a unique model for studying the hormonal regulation of apoptosis.
In lizards and snakes, the oviducts function in fertilization, sperm storage, egg transport, eggshell deposition, maintenance of the early embryo, and expulsion of the egg or fetus. In viviparous forms they also contribute to placentae responsible for gas exchange and nutrient provision to the fetus. Dissections of species of 30 genera coupled with data from the literature indicate that squamate oviducts vary interspecifically in seven macroscopic features, including the extent and nature of regional differentiation, vascular supply, topographic asymmetry, number of oviducts, vaginal pouches, and relationship to the cloaca. The uterus, infundibulum, and vagina differ histologically in their epithelia, glands, and myometrial layers. Season cyclicity occurs in all three oviductal regions, most prominently in the uterus, and is under endocrinological control. Regional and cytological specializations reflect the diverse functions performed by the oviduct. Definitive evidence for oviductal albumen production and egg resorption is lacking. In viviparous squamates, three uterine specializations may facilitate maternal-fetal gas exchange: an attenuated epithelium, reduced uterine glands (and a reduced shell membrane), and increased vascularization. Contrary to previous reports, pregnant uteri show no epithelial erosion or capillary exposure. Specializations for nutrient provision to the fetus include mucosal hypertrophy, enlarged glandular epithelia, and multicellular glands whose secretions are absorbed by the chorioallantois. Comparisons with other amniotes indicate that squamates inherited the oviduct as an organ with capabilities for egg uptake and transport, fertilization, eggshell deposition, and oviposition. Other features have evolved convergently among squamates: infundibular sperm receptacles, unilateral oviduct loss, uterine gestation, placentation, and specializations for placentotrophy. Cladistic analysis indicates that oviductal features associated with deposition of tertiary egg investments in reptiles reflect evolutionary convergence as well as secondary simplification, rather than a unidirectional trend towards increased specialization.
Internal fertilization and oviparity most likely are symplesiomorphies for modern reptiles, and viviparity has evolved independently numerous times in Sauria and Serpentes. Oviducal sperm storage is known in females of all taxa except Amphisbaenia. However, in Rhynchocephalia and Crocodilia, sperm storage is poorly studied, and specialized sperm storage tubules (Ssts) are unknown. We use the molecular phylogenetic hypothesis [(Chelonia+Archosauria) (Squamata)] to trace evolution of sperm storage characters. Ssts arose independently in Chelonia and Squamata. Turtles possess albumen-secreting glands in the anterior half of the oviduct (the tuba or isthmus), and the most distal of these glands also serve as Ssts; in addition, some turtles possess Ssts in the adjacent segment of the oviduct, the uterus. Squamates lack albumen-secreting glands, and the ancestral state is possession of Ssts in the posterior infundibulum (uterine tube). Secondarily, iguanids have evolved vaginal Ssts. In this paper, we present the first ultrastructural observations on vaginal Ssts in lizards, using Anolis sagrei (Polychrotidae). Proximally, the neck of these simple tubular glands continues the alternation of ciliated and secretory cells lining the lumen of the vagina. However, the epithelial cells of the distal sperm storage area are neither secretory nor ciliated. The Ssts of Anolis are more similar to those of birds more than to infundibular receptacles in snakes and lizards.
Operação cesariana realizada em Eunectes murinus (Linnaeus 1758), Serpentes
- Belluomini H. E.
Contribuição à biologia de Eunectes murinus (Linnaeus 1758), Serpentes: Observações sobre hábitos alimentares de “sucuris” em cativeiro
- Belluomini H. E.
Contribuição à biologia do gênero Eunectes Wagler, 1830. Serpentes Boidae. estudo de seis ninhadas de “sucuris”
- Belluomini H. E.