Embryonic development of the neotropical pit viper Bothrops atrox (Serpentes: Viperidae: Crotalinae), with emphasis on pit organ morphogenesis and its evolution in snakes.

BACKGROUND: Bothrops atrox is a pit viper with a loreal pit organ, and its embryological development remains undescribed. Here, we provide a comprehensive description of the embryology of B. atrox, focusing on the loreal pit organ and cephalic scales. RESULTS: We characterized 13 developmental stages of B. atrox based on external features consistent with the embryogenesis of previously described snake species. The loreal pit organ originates from the circumorbital region and migrates to its final position. In Crotalinae, the pit organ first becomes visible at stage 28, whereas in Pythonidae labial, pit organs appear at Stage 35. Pit organs evolved independently three times in Serpentes, encompassing Boidae, Pythonidae, and Crotalinae. Boidae lacks embryological information for pit organs. Furthermore, we observed that head scalation onset occurs at Stage 33 in B. atrox, with fusion of scales surrounding the loreal pit organ. CONCLUSIONS: The embryology of pit organs in Pythonidae and Boidae species remains poorly understood. Our detailed embryological descriptions are critical for proposing developmental scenarios for pit organs and guiding future research on these structures.

Unwrapping broken tails: Biological and environmental correlates of predation pressure in limbless reptiles.

Studying species interactions in nature often requires elaborated logistics and intense fieldwork. The difficulties in such task might hinder our ability to answer questions on how biotic interactions change with the environment. Fortunately, a workaround to this problem lies within scientific collections. For some animals, the inspection of preserved specimens can reveal the scars of past antagonistic encounters, such as predation attempts. A common defensive behaviour that leaves scars on animals is autotomy, the loss of a body appendage to escape predation. By knowing the collection site of preserved specimens, it is possible to assess the influence of organismal biology and the surrounding environment in the occurrence of autotomy. We gathered data on tail loss for 8189 preserved specimens of 33 snake and 11 amphisbaenian species to investigate biological and environmental correlates of autotomy in reptiles. We applied generalized linear mixed effect models to evaluate whether body size, sex, life-stage, habitat use, activity pattern, biome, tropicality, temperature and precipitation affect the probability of tail loss in limbless reptiles. We observed autotomy in 23.6% of examined specimens, with 18.7% of amphisbaenian and 33.4% of snake specimens showing tail loss. The probability of tail loss did not differ between snakes and amphisbaenians, but it was higher among large-sized specimens, particularly in adults and females. Chance of tail loss was higher for diurnal and arboreal species, and among specimens collected in warmer regions, but it was unaffected by biome, precipitation, and tropicality. Autotomy in limbless reptiles was affected by size-dependent factors that interplay with ontogeny and sexual dimorphism, although size-independent effects of life-stage and sex also shaped behavioural responses to predators. The increase in probability of tail loss with verticality and diurnality suggests a risk-balance mechanism between species habitat use and activity pattern. Although autotomy is more likely in warmer regions, it seems unrelated to seasonal differences in snakes and amphisbaenians activity. Our findings reveal several processes related to predator-prey interactions involving limbless reptiles, demonstrating the importance of scientific collections to unveil ecological mechanisms at different spatio-temporal scales.

Co-occurrence patterns between false coral snake Atractus latifrons (Günther, 1868) (Serpentes: Dipsadidae) and venomous coral snakes from the Amazon.

Batesian mimicry may result in remarkable cases of phenotypic convergence that represent classic examples of evolution through natural selection. The existence of mimicry systems among coral snakes, however, remains controversial because of contradictions between the predictions of mimetic theory and the empirical patterns of co-occurrence and species abundance. Here, we analyze the geographic distribution of coral snake species of the genus Micrurus and populations of the false coral snake Atractus latifrons in Amazonia, and perform ecological niche modeling (ENM) analyzes to generate potential geographic distributions of species of Micrurus and A. latifrons, identify patterns of co-occurrence and assess whether the distribution of A. latifrons coincides with the distribution of Micrurus species, which could suggest the existence of a possible mimetic relationship between the species. We identified six Micrurus species that may represent mimetic models for A. latifrons. The results of the co-occurrence analysis corroborates the results from ENM, indicating that chromatic patterns of A. latifrons and their respective model species are aggregated. Our study suggests that all color patterns of A. latifrons - including the tricolor monads, and the more common tricolor dyads and tricolor tetrads - may benefit from the resemblance with other Micrurus species as perfect and imperfect mimics.

Patterns, biases and prospects in the distribution and diversity of Neotropical snakes.

Motivation: We generated a novel database of Neotropical snakes (one of the world's richest herpetofauna) combining the most comprehensive, manually compiled distribution dataset with publicly available data. We assess, for the first time, the diversity patterns for all Neotropical snakes as well as sampling density and sampling biases. Main types of variables contained: We compiled three databases of species occurrences: a dataset downloaded from the Global Biodiversity Information Facility (GBIF), a verified dataset built through taxonomic work and specialized literature, and a combined dataset comprising a cleaned version of the GBIF dataset merged with the verified dataset. Spatial location and grain: Neotropics, Behrmann projection equivalent to 1° × 1°. Time period: Specimens housed in museums during the last 150 years. Major taxa studied: Squamata: Serpentes. Software format: Geographical information system (GIS). Results: The combined dataset provides the most comprehensive distribution database for Neotropical snakes to date. It contains 147,515 records for 886 species across 12 families, representing 74% of all species of snakes, spanning 27 countries in the Americas. Species richness and phylogenetic diversity show overall similar patterns. Amazonia is the least sampled Neotropical region, whereas most well-sampled sites are located near large universities and scientific collections. We provide a list and updated maps of geographical distribution of all snake species surveyed. Main conclusions: The biodiversity metrics of Neotropical snakes reflect patterns previously documented for other vertebrates, suggesting that similar factors may determine the diversity of both ectothermic and endothermic animals. We suggest conservation strategies for high-diversity areas and sampling efforts be directed towards Amazonia and poorly known species.

A new species of Imantodes Duméril, 1853 (Serpentes, Dipsadidae) from the Eastern Cordillera of Colombia.

We describe a new species of Imantodes, morphologically similar to I. chocoensis, from the Eastern Cordillera of Colombia. This new species is distinguished from all congeners by the following combination of morphological characters: smooth dorsal scale rows 17/17/15; apical pits absent; infralabials 12-13; ventrals 227-236; subcaudals 147-148; presence of loreal scale; cloacal plate divided; dark temporal stripe on the suture between the lower edge of temporal scales and upper region of supralabials; dorsum of body light brown with dark brown transversal streaks, weakly evident in lateral view; hemipenis in situ extending to the level of 11th subcaudal and reaches the 10th subcaudal when everted; hemipenis with sulcus spermaticus expanded at the base of capitulum and extending distally. Additionally, we discuss the lateral expansion of the sulcus spermaticus in the new species, similar to that of species of Leptodeira.

Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes.

BACKGROUND: Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as "goo-eating snakes". Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e.g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells. RESULTS: Here, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system. CONCLUSIONS: The acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.

A new species of triadal coral snake of the genus Micrurus Wagler, 1824 (Serpentes: Elapidae) from northeastern Brazil.

The genus Micrurus comprises 123 currently recognized taxa (species and subspecies) that are traditionally arranged in four species groups diagnosable mainly by color pattern characteristics. Here, we describe a new species of triadal coral snake from northeastern Brazil. The new species is distinguished from other sympatric triadal congeners (M. lemniscatus carvalhoi, M. ibiboboca and M. brasiliensis) mainly by the entirely black parietals and by a suite of external characters and hemipenial morphology. The new species appears to be restricted to tropical ombrophilous lowland coastal forests of northeastern Brazil and all recently collected specimens are known to occur in small forest patches surrounded by periurban environment, which calls for an urgent evaluation on its conservation status.

Embryonic development of the pelvic girdle and hindlimb skeletal elements in Anilius scytale (Linnaeus, 1758) (Serpentes: Aniliidae).

Anilius scytale is the sister lineage of all other alethinophidian snakes. Morphology of the hind limb complex in adult A. scytale (Aniliidae) has been documented. We herein, for the first time, describe the embryology of the skeletal elements of its hind limb and pelvic girdle and contextualize the evolution of these structures. We identified pregnant females of A. scytale in the Herpetology Collection of the Museu Paraense Emílio Goeldi and separated 40 embryos. The embryos were sequentially staged using external and internal anatomy, collectively comprising a developmental series representing six stages. We cleared-stained one specimen of stages 31, 34, 36, and 37. Using the embryological information gleaned from A. scytale, we reinterpret evidence relating to the ossification of the pelvis and hindlimbs. In A. scytale hindlimb buds develop as transient structures that developed before Stage 30 and regresses in subsequent stages. There is no external or internal evidence of the forelimb or scapular girdle. From Stage 31 onwards the ischium, pubis, ilium, femur and zeugopodial cartilages are visible. Pubis and femur ossify towards the end of embryonic life, and cloacal spurs do not develop in the embryo. Skeletal elements of the hindlimb and pelvic girdle develop initially in the ventral zone of the cloaca-tail region. In subsequent stages the hindlimb and pelvic girdle elements migrate dorsally, with the pubis/ischium positioned medial to the ribs. A similar process may be associated with the achievement of the condition of the pelvic girdle in adults of scolecophidians, pythonids and boids.

A new dwarf gecko of the genus Pseudogonatodes (Squamata: Sphaerodactylidae) from the eastern slope of the Andean Cordillera de Mrida in northern South America.

Pseudogonatodes is a poorly known genus of small bodied, diurnal, ground-dwelling geckos widely distributed in northern South America. No additional species have been described in over two decades. Herein we describe a new species from the eastern slope of the Cordillera de Mrida in the Venezuelan Andes. The new species is readily diagnosable morphologically from the other seven recognized species of Pseudogonatodes by having a single postnasal scalea putative autapomorphy. Furthermore, it is characterized by a unique combination of phenotypic characters that includes granular dorsal scales, three large postrostrals, five to six loreals, mental U-shaped, four to six postmentals, 2629 ventrals between anterior levels of fore- and hind limbs, third lamella under fourth toe not distinctly enlarged, and subcaudal pattern 11. In addition to characterizing the external morphology, we present a description of the skull, based on 3D digital models reconstructed from high resolution computed microtomography scans. The discovery of this new species highlights the still underestimated diversity of this group of Neotropical dwarf geckos and underscores the need for further studies on its systematics and taxonomy.

Morphological variation and affinities of the poorly known snake Atractus caxiuana (Serpentes: Dipsadidae) .

Atractus caxiuana was recently described based on three specimens (two males and one female) from the Floresta Nacional de Caxiuanã, municipality of Melgaço, state of Pará, in the eastern portion of the Brazilian Amazon. Apart from the type series, no additional samples are known for the species. In this study, we report new specimens of A. caxiuana, providing new morphological data (meristic, morphometric, pholidosis, colour pattern, and hemipenis) and localities. We relate the variability displayed by the characters analyzed to sexual dimorphism, geographic variation, and ontogeny. Additionally, we provide detailed comparisons with A. collaris and putative sister species, and propose a new species group to accommodate this distinct and possible monophyletic assemblage. 

Unveiling underestimated species diversity within the Central American Coralsnake, a medically important complex of venomous taxa.

Coralsnakes of the genus Micrurus are a diverse group of venomous snakes ranging from the southern United States to southern South America. Much uncertainty remains over the genus diversity, and understanding Micrurus systematics is of medical importance. In particular, the widespread Micrurus nigrocinctus spans from Mexico throughout Central America and into Colombia, with a number of described subspecies. This study provides new insights into the phylogenetic relationships within M. nigrocinctus by examining sequence data from a broad sampling of specimens from Mexico, Guatemala, Honduras, Nicaragua, Costa Rica, and Panama. The recovered phylogenetic relationships suggest that M. nigrocinctus is a species complex originating in the Pliocene and composed of at least three distinct species-level lineages. In addition, recovery of highly divergent clades supports the elevation of some currently recognized subspecies to the full species rank while others may require synonymization.

Sexual dimorphism and allometry in malacophagus snakes (Dipsadidae: Dipsadinae).

Sexual dimorphism in snakes is generally described in association with body or tail size and scale counts, with relatively few studies addressing intrasexual divergence in the skull. Here, we analyzed sexual dimorphism in the size and shape of skull and body in three malacophagous dipsadine snakes, Dipsas mikanii, Dipsas neuwiedi and Dipsas turgida, as well as allometric effect on these components. We used linear and geometric analysis to assess: (1) if there is sexual dimorphism in cranial components; (2) if there are differences between the sexes regarding body and tail size, number of ventral and subcaudal scales; (3) whether there is covariation between cranial components and body size; (4) if there are changes in cranial shape associated with increased size; and (5) whether there is an allometric relationship between body and tail size. Our results showed that all three species are dimorphic in cranial shape and size (except D. turgida for cranial size), with females having longer and thinner skulls than males. In the three species, the female skull was negatively allometric, whereas the male skull was isometric. Allometry related to cranial shape was significant only in males of D. turgida, which showed greater snout robustness and eye size associated with enlargement of the skull. Females of D. mikanii and D. neuwiedi were significantly larger than males. Only males of D. neuwiedi showed positive allometry for the tail, while dimorphism related to scale counts followed the pattern found in most snakes, with females having a greater number of ventrals and males subcaudals (except D. neuwiedi in the latter case). Based on our results, we hypothesize that patterns of sexual dimorphism and skull allometry in malacophagous snakes may be explained both by aspects related to diet and reproduction. Meanwhile, patterns associated with body size reflect advantages related to fecundity favoring greater reproductive success of females.

Synergistic effects of climate and landscape change on the conservation of Amazonian lizards.

The leading causes of the worldwide decline in biodiversity are global warming, allied with natural habitat loss and fragmentation. Here, we propose an analysis of the synergistic effects of these two factors in 63 species of Amazonian lizards. We predicted that the high-climatic suitability areas of species would be significantly impacted by different deforestation scenarios and the resultant landscape structure and considered that forest-dwelling species would be especially susceptible to deforestation scenarios. We also pointed out species threatened by both drivers and suggested critical areas for their future conservation. According to our results, most species will face future reductions in suitable areas for their occurrence according to five different patterns, two of which represent significant risks for 15 species. Some of these species already deal with severe habitat loss and fragmentation of their current distribution ranges, whereas others will suffer a considerable area reduction related to future range shifts. We emphasize the importance of protected areas (PAs), especially indigenous lands, and the need to plan combined strategies involving PAs' maintenance and possible implementation of ecological corridors. Finally, we highlight eight species of thermoconformer lizards that constitute present and future conservation concerns related to the combined effects of climate change and habitat loss and that should be carefully evaluated in extinction risk assessments.

Taxonomic revision of the Erythrolamprus reginae species group, with description of a new species from Guiana Shield (Serpentes: Xenodontinae).

We perform a review of the Erythrolamprus reginae species group and putative related taxa (E. dorsocorallinus, E. zweifeli, and E. oligolepis), based on external morphology and hemipenial characters. We infer species boundaries among taxa traditionally associated with this group, recognizing two nominal subspecies (Erythrolamprus reginae reginae and E. r. macrosomus) in the species level. We propose the synonymy of E. r. semilineatus with E. reginae and recognize the validity of the related taxa, such as: E. dorsocorallinus, E. zweifeli, and E. oligolepis. In addition, two specimens occurring in the state Amapá, Brazil, are herein described as a new species. Therefore, we provide an identification key for the species of the group and discuss some of the combination of morphological features useful to delimitate the species of this group, in comparison with other representatives of the genus Erythrolamprus.

Taxonomy of the Micrurus spixii species complex (Serpentes, Elapidae).

Historically, the Micrurus spixii species complex comprises four subspecies (M. s. spixii, M. s. martiusi, M. s. obscurus, and M. s. princeps), however, recently, some authors have considered only two full species (M. spixii and M. obscurus). In this paper, we report data on meristic, morphometric, color pattern in life and after preservation, cranial osteology, and hemipenis morphology to Micrurus spixii species complex. We examined 358 specimens throughout the geographical distribution, including the type-series of all taxa. Differences in color pattern and morphology of hemipenis and skull support the existence of only two diagnosable taxa, M. spixii and M. obscurus, both considered here as a full species. We corroborate the synonymy of Micrurus s. martiusi and M. spixii based on wide overlap of meristic and morphometric characters, as well as the similarities of color pattern, hemipenis and skull characters. We can distinguished M. spixii from M. obscurus (in parenthesis) by the combination of the following characters: black cephalic cap (vs. cephalic cap absent, with red parietal region), hemipenial body with spines dispersed on the asulcate surface (vs. spines arranged in rows on the asulcate surface), capitate condition of hemipenis (vs. organ partially-capitate), narrow parietal bone with posterior angular borders (vs. enlarged parietal bone with elliptical posterior border), and relatively long venom inoculating fangs (vs. relatively short venom inoculating fangs).

Dataset from the Snakes (Serpentes, Reptiles) collection of the Museu Paraense Emílio Goeldi, Pará, Brazil.

BACKGROUND: We present a dataset with information from the snake collection of the Museu Paraense Emílio Goeldi, known as the "Ophidia Collection". This collection currently has 26,728 specimens of snakes, including 9 families, 66 genera and 220 species. For the most part, it represents material from the Amazon Region. Specimens are preserved mostly in wet (alcohol) preparation, with some samples preserved in dry form, as is the case of the shells and skeletons of turtles. The dataset is now available for public consultation on the Global Biodiversity Information Facility portal (https://doi.org/10.15468/lt0wet). NEW INFORMATION: The Herpetological collection of Museu Paraense Emílio Goeldi comprises the largest collection of its kind in the Amazon region with about 100,000 specimens of amphibians and reptiles (chelonians, alligators, lizards, snakes and amphisbaenians). This collection currently has 26,728 specimens of snakes, including 9 families, 66 genera and 220 species, some of which are endemic to the Amazon rainforest region. The Museu Paraense Emílio Goeldi is the second oldest institution of science in Brazil in activity, founded in 1866.

Oral glands in dipsadine "goo-eater" snakes: morphology and histochemistry of the infralabial glands in Atractus reticulatus, Dipsas indica, and Sibynomorphus mikanii.

Although snake infralabial glands are generally constituted of mucous cells, among dipsadines, they are much more developed and predominantly serous in nature, possibly due to the peculiar feeding habits of some species of this group, the "goo-eaters", which feed on soft and viscous invertebrates. We compared the morphology and histochemistry of the infralabial glands of three goo-eater species of Southeast Brazil, Atractus reticulatus, Dipsas indica and Sibynomorphus mikanii. In A. reticulatus the glands are formed by mixed acini composed of mucous and seromucous cells and in D. indica, they are composed of mucous tubules and seromucous acini. In S. mikanii the glands are organized in seromucous acini; mucous cells are restricted to the gland anterior region and to the duct lining epithelium. Ultrastructurally, secretory granule electron density varies from low to moderate, depending on their mucous or seromucous nature. The results indicate a large morphological and histochemical variation in the infralabial glands, probably reflecting differences in the secretion chemical composition and in feeding specialization among the three species. The protein content in the secretory cells can be related with the presence of toxins that can be used in chemical prey immobilization or detaching of snails from their shells.

Species delimitations in the Atractus collaris complex (Serpentes: Dipsadidae).

We reassessed the taxonomic status of the species in the Atractus collaris complex (A. alphonsehogei, A. collaris, A. limitaneus, and A. gaigeae) on the basis of congruence between quantitative and qualitative morphological characters (meristic, morphometric, color pattern, hemipenis, and scale microdematoglyphics) along its wide geographical distribution. Our results support the recognition of three species with apparently fixed diagnostic characters. We propose the synonymization of Atractus limitaneus with A. collaris based on the wide overlap of all morphological character systems here analyzed, as well as on the basis of examination of the holotype and two topotypes of A. limitaneus. Finally, we discuss the geographical variation and morphological distinction of A. alphonsehogei, A. collaris and A. gaigeae. Furthermore, we provide a dichotomous key for all recognized species in the A. collaris species group.

Phylogenetic and morphological evidence reveals the association between diet and the evolution of the venom delivery system in Neotropical goo-eating snakes

Advanced endoglyptodont snakes share a complex but homologous venom delivery system associated with the upperjaw and its dentition. Recently, a remarkable novel lower jaw venom delivery system was described for the Neotropicaldipsadine radiation of goo-eating snakes. While most dipsadines are opistoglyphous and exhibit large, mainly serousvenom glands associated with the upper jaw and supralabial glands, goo-eating dipsadine snakes are aglyphous and lackserous upper labial venom glands. Here, we provide new morphological and histological information on the oral glandsand maxillary dentition of representatives of the major lineages of dipsadines that help trace the evolutionary steps thatshaped the venom delivery system of dipsadines. We performed a maximum likelihood analysis on a molecular datasetthat includes 443 terminals and seven loci. Our results show that goo-eating dipsadines form a monophyletic assemblagethat includes the genusAdelphicosfor the first time, along withGeophis,Atractus,Ninia,Chersodromus,Tropidodipsas,Sibon, andDipsas. We also provide the first evidence of a complete shift from an upper jaw to a lower jaw venomdelivery system associated with their specialized feeding behaviour. Unlike other dipsadines who exhibit typicalendoglyptodont anteroposteriorly ridged posterior maxillary teeth, goo-eating dipsadines have uniform lateromediallyridged teeth throughout their maxilla. Our results indicate that the loss of the endoglyptodont venom delivery systemoccurred in the most recent common ancestor of goo-eating dipsadines, probably resulting from the loss of theembryonic posterior maxillary lamina responsible for the development of the venom delivery system.

Intense male-male ritual combat In the Micrurus ibiboboca complex (Elapidae) from Northeastern South America

Snakes engaged in agonistic encounters may employ visual and tactile displays that sometimes culminate in ritual combat. Here, we describe novel male-male ritual combat behaviors in South American coral snakes in the Micrurus ibiboboca complex based on the largest observational dataset of ritual combat for any species of the genus Micrurus. The dataset includes 85 photographs and four videographs from six respective observation records of male snakes. We observed four of these fights during the daytime and two during the night. All observations were random encounters in different natural environments during transitional dry seasons (i.e., early dry season between April and June in the west, and the early wet season between August and September on the east coast). During each respective period, precipitation is < 100 mm and is accompanied with decreasing and increasing temperatures, respectively. The following behaviors were observed: recognition, ascent, and alignment. These were followed by orientation, entwining and twisting, rolling, and hovering; then, oblique display stances and topping (including lyre-shaped positioning and dorsal hyperextension). The topping attempts were from high oblique display positions with one male attempting to force the head of the other down. We also observed snapping, where snake opponents twist the heads of each other creating a quick snap-like sound. We suggest these complex ritual displays communicate dominance between snakes.