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.

Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence

Micrurus surinamensis is an aquatic member of the genus Micrurus. This species is known for its highly specialized venom and distinctive diet, mostly made of aquatic vertebrates. Here, we explore both external (head and body) and skull shape morphologies in M.surinamensis, comparing it with two terrestrial species of the genus (M.lemniscatus and M.spixii) and to aquatic and terrestrial species of distantly related groups. We use both traditional and geometric morphometrics to determine whether the presence of similar traits in head shape morphology is rather the result of adaptive convergences between M.surinamensis and other aquatic species, or whether it is the product of phylogenetic conservatism within the genus. Results from both traditional and geometric morphometrics show that M.surinamensis can be considered convergent with aquatic species, mainly in the skull shape. Micrurus surinamensis differs from the two terrestrial species of Micrurus by having a wider head, smaller distance between nostrils, and a long tail. Geometric morphometric analysis shows that despite having an extremely conserved skull and mandible shape, M.surinamensis shows a longer supratemporal and quadrate bones than in terrestrial Micrurus, indicating a larger gape for this species. A more kinetic skull combined with a larger gape would allow M.surinamensis to feed on fish, which represent larger and wider prey that contrast with the elongate prey, which compose the main diet of species in the genus Micrurus. Our results illustrate the importance of both phylogenetic conservatism and adaptation in shaping species morphology.

Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence

Micrurus surinamensis is an aquatic member of the genus Micrurus. This species is known for its highly specialized venom and distinctive diet, mostly made of aquatic vertebrates. Here, we explore both external (head and body) and skull shape morphologies in M.surinamensis, comparing it with two terrestrial species of the genus (M.lemniscatus and M.spixii) and to aquatic and terrestrial species of distantly related groups. We use both traditional and geometric morphometrics to determine whether the presence of similar traits in head shape morphology is rather the result of adaptive convergences between M.surinamensis and other aquatic species, or whether it is the product of phylogenetic conservatism within the genus. Results from both traditional and geometric morphometrics show that M.surinamensis can be considered convergent with aquatic species, mainly in the skull shape. Micrurus surinamensis differs from the two terrestrial species of Micrurus by having a wider head, smaller distance between nostrils, and a long tail. Geometric morphometric analysis shows that despite having an extremely conserved skull and mandible shape, M.surinamensis shows a longer supratemporal and quadrate bones than in terrestrial Micrurus, indicating a larger gape for this species. A more kinetic skull combined with a larger gape would allow M.surinamensis to feed on fish, which represent larger and wider prey that contrast with the elongate prey, which compose the main diet of species in the genus Micrurus. Our results illustrate the importance of both phylogenetic conservatism and adaptation in shaping species morphology.

Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae).

Neotropical "goo-eating" dipsadine snakes display a set of morphological and histo-chemical adaptations linked to the capture of their soft-bodied, viscous invertebrate prey. Within this group, species from the genus Sibynomorphus feed chiefly on snails and slugs. Here, we analyzed a series of skull and mandible characters in S. mikanii, S. neuwiedi and S. turgidus using geometric morphometrics, with the aim of assessing morphological adaptations related to slug- and snail-feeding in that genus. We further compared the results with Leptodeira annulata, a species that feeds on vertebrates. To evaluate shape differences of the skull and mandible between species we performed a multivariate analysis of variance and a linear discriminant analysis. Our results show that the narrow, elongate skull in S. mikanii may help with slug ingestion, while asymmetry in teeth number and mandibular shape in S. neuwiedi and S. turgidus are likely related to snail feeding.

Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae)

Neotropical "goo-eating" dipsadine snakes display a set of morphological and histo-chemical adaptations linked to the capture of their soft-bodied, viscous invertebrate prey. Within this group, species from the genus Sibynomorphus feed chiefly on snails and slugs. Here, we analyzed a series of skull and mandible characters in S. mikanii, S. neuwiedi and S. turgidus using geometric morphometrics, with the aim of assessing morphological adaptations related to slug- and snail-feeding in that genus. We further compared the results with Leptodeira annulata, a species that feeds on vertebrates. To evaluate shape differences of the skull and mandible between species we performed a multivariate analysis of variance and a linear discriminant analysis. Our results show that the narrow, elongate skull in S. mikanii may help with slug ingestion, while asymmetry in teeth number and mandibular shape in S. neuwiedi and S. turgidus are likely related to snail feeding.

Morphological variation in siphlophis worontzowi (Squamata: Serpentes: Dipsadidae) from the Brazilian Amazon

The Neotropical snake Siphlophis worontzowi was described based on a single specimen from Rio Amana, Amazonas state in the western portion of the Brazilian Amazon, but has subsequently become known from Bolivia and Peru as well. Here, we report a new morphological data set of S. worontzowi (meristic, morphometric, pholidosis, colour pattern, and hemipenial characters) and new geographic localities. Geographical variation and sexual polymorphism are analysed and described. Siphlophis worontzowi can be distinguished from its congeners by the combination of the following characters: dorsal scale rows 19-19-15, dorsals with two apical pits; undifferentiated vertebral scales; 3 postoculars; long loreal; 2+3 temporals; 8 supralabials, with the third, fourth and fifth contacting the orbit; 9 infralabials, first four pairs contacting chin shields; 14-17 prediastemal and 2 postdiastemal maxillary teeth; 21 mandibular teeth, with 4-5 larger than others; 2 or 3 preventrals; 221-243 ventrals; 93-119 subcaudals; body black with 12-22 conspicuous yellowish or reddish vertebral spots, and black head with one or two conspicuous reddish or orange nuchal spots when alive; hemipenis with Y-shaped and T-shaped conditions; intrasulcar surface with a row of three enlarged spines in the proximal region of each lobe. Additionally, we provide detailed descriptions of the hemipenis, and discuss its polymorphic condition in the genus Siphlophis.

Polychromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil / Policromatismo das populações de Corallus hortulanus (Squamata: Boidae) ao sul da Bacia Amazônica, Brasil

The Amazon tree boa Corallus hortulanus is known for featuring a wide variation in color pattern and design markings. Although there are studies on its polychromatism, none of them addresses the geographic variation in the color pattern of this species. The aim of this study was to describe the chromatic variation found in the populations of C. hortulanus from the southern Amazon Basin and its relationship with geographic distribution of the species. Analysis of both design markings and color patterns on 112 C. hortulanus specimens from the southern Amazon Basin interfluves resulted in the identification of six distinct morphotypes. Grayish-brown coloration and elongated diamond-shaped patterns were the most frequent patterns. Two morphotypes showed a tendency of correlation with the geographical distribution of those species found in Madeira and Juruá Rivers. The small sample size does not allow for a robust conclusion on the possible cause of geographic variation. The distribution of morphological patterns of C. hortullanus in the Amazon Basin suggest that there is gene flow between populations, regardless of geographical distance and natural barriers. The variation in color pattern and markings may represent a phenotypic response to the characteristics of different habitats occupied by the species.

Corallus hortulanus é uma serpente conhecida por apresentar grande variação no padrão de coloração e desenho. Apesar de estudos relacionados ao seu policromatismo, nenhum deles abordou a variação geográfica no padrão de cor desta espécie. O objetivo deste estudo foi descrever a variação cromática das populações de C. hortulanus na Calha sul do Rio Amazonas e verificar a correlação entre a distribuição geográfica e a variação encontrada. A partir da análise do padrão de desenho e cor de 112 espécimes de C. hortulanus procedentes dos interflúvios (área entre dois rios) da Calha Sul foram descritos seis morfotipos. Dos seis morfotipos descritos, a cor marrom-acinzentado e o padrão de desenho losango alongado foram os mais comuns entre as populações analisadas. Dois morfotipos apresentaram uma tendência de correlação com a distribuição geográfica, estando relacionados aos rios Madeira e Juruá, embora o número de amostras tenha sido pequeno. A distribuição dos padrões morfológicos de C. hortullanus na Bacia Amazônica revelou que existe fluxo gênico entre as populações, independentemente da distância geográfica e das barreiras naturais. Provavelmente, o padrão de cor e desenho seja uma resposta fenotípica às pressões nos diferentes ambientes ocupados pela espécie.

A new species of monadal coral snake of the genus Micrurus (Serpentes, Elapidae) from western Amazon.

We described a new species of monadal coral snake of the genus Micrurus from the region of Tabatinga and Leticia, along the boundaries of Brazil, Colombia, and Peru. The new species can be distinguished from the other congeners by the combination of the following characters: absence of a pale nuchal collar; black cephalic-cap extending from rostral to firstdorsal scale and enclosing white tipped prefrontal scales; upper half of first to four supralabials and postoculars black; tricolor body coloration, with 27-31 black rings bordered by narrower white rings and 27-31 red rings; tail coloration similar to body, with alternating black rings bordered by irregular narrow white rings, red rings of the same width as the black rings; ventral scales 205-225; subcaudal scales 39-47.

The real identity of Leptodiranycthemera Werner, 1901 from Ecuador: a junior synonym of Oxyrhopuspetolarius (Linnaeus, 1758) (Serpentes, Dipsadidae).

Leptodiranycthemera Werner, 1901, was described from a specimen collected in Ecuador. No information on the holotype was published after its description. In the most recent review of Leptodeira, Leptodiranycthemera was considered to be a synonym of Leptodeiraannulataannulata, although the author emphasized that the holotype was lost and did not include the pholidotic data from the original description in his account of Leptodeiraannulataannulata. Since this review, a number of authors have accepted this synonymy. Recently, analyzing specimens of Leptodeira in the Museum für Naturkunde, Berlin, Germany, we discovered the holotype of Leptodiranycthemera. This holotype is re-described here, and its correct identity is determined. Based on the analysis of meristic characters and the color of the holotype, we recognize Leptodiranycthemera as a junior synonym of Oxyrhopuspetolarius.

A new species of Amerotyphlops from Northeastern Brazil, with comments on distribution of related species.

We describe a new species of Amerotyphlops from an upland forest enclave in the state of Paraíba, Northeastern Brazil. The new species is distinguished from the other seven South American species of Amerotyphlops by the combination of the following characters: nasal suture incomplete; rostral scale oval and yellowish cream with some dark brown spots; four supralabial scales; three infralabial scales; rows of scales around the body 18/18/18; middorsal scales from 204 to 225; dorsum with twelve to thirteen rows of scales dark brown and belly with four to five rows of scales immaculate yellowish cream; caudal spine dark brown; subcaudal scales 8-10 in female and 11-13 in males; maximum total length 233 mm. The new species is morphologically similar to A. amoipira and A. paucisquamus, sharing 18/18/18 rows of scales around the body and a small overlap of counts of middorsal scales.

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.

Envenomation by Micrurus coral snakes in the Brazilian Amazon region: report of two cases / Envenenamento por coral do gênero Micrurus na Amazônia brasileira: relato de dois casos

Two cases of proven coral snake bites were reported in Belém, Pará State, Brazil. The first case was a severe one caused by Micrurus surinamensis. The patient required mechanical ventilation due to acute respiratory failure. The second case showed just mild signs of envenomation caused by Micrurus filiformis. Both patients received specific Micrurus antivenom and were discharged without further complications. Coral snake bites are scarcely reported in the Amazon region and there is a broad spectrum of clinical manifestations, varying from extremely mild to those which may rapidly lead to death if the patient is not treated as soon as possible.

Dois acidentes por coral verdadeira são descritos em Belém, Pará. O primeiro caso foi decorrente de envenenamento por Micrurus surinamensis, no qual a vítima necessitou ventilação mecânica por insuficiência respiratória. O segundo, causado por Micrurus filiformis, apresentou apenas manifestações leves. Ambos os pacientes receberam soro antielapídico específico e evoluíram sem complicações. Acidentes por coral verdadeira na região Amazônica são raramente descritos e podem cursar com um largo espectro de alterações, que variam desde quadros de envenenamento muito leves até manifestações com risco de óbito.

Envenomation by Micrurus coral snakes in the Brazilian Amazon region: report of two cases.

Two cases of proven coral snake bites were reported in Belém, Pará State, Brazil. The first case was a severe one caused by Micrurus surinamensis. The patient required mechanical ventilation due to acute respiratory failure. The second case showed just mild signs of envenomation caused by Micrurus filiformis. Both patients received specific Micrurus antivenom and were discharged without further complications. Coral snake bites are scarcely reported in the Amazon region and there is a broad spectrum of clinical manifestations, varying from extremely mild to those which may rapidly lead to death if the patient is not treated as soon as possible.

Serpentes da Bacia Petrolífera de Urucu, município de Coari, Amazonas, Brasil / Snakes of the Urucu Petrol Basin, municipality of Coari, Amazonas, Brasil

Um inventário estruturado de serpentes foi realizado na Base Operacional Geólogo Pedro de Moura (BOGPM), localizada na Bacia Petrolífera de Urucu, Município de Coari, Amazonas, nos anos de 2003, 2004 e 2007. Nas quatro expedições realizadas (51 dias de coleta) foram registradas 47 espécies de serpentes, pertencentes a sete famílias e 33 gêneros. Foram utilizados quatro métodos complementares de amostragem de serpentes: armadilha de interceptação e queda, encontros ocasionais, procura limitada por tempo a pé e procura limitada por tempo de carro. Das 47 espécies coletadas, Liophis reginae (n= 14), Philodryas viridissima (n= 9), Philodryas boulengeri (n= 7) e Oxybelis fulgidus (n= 7) foram as mais abundantes em toda região. O maior número de espécies e espécimes foi registrado pela procura limitada por tempo de carro (52,8%). Estudos anteriores indicam que as localidades ao sul do Rio Amazonas (como região Leste do Pará, Usina Hidrelétrica de Tucuruí, Estado do Pará, e de Samuel, Estado de Rondônia) apresentam maior riqueza quando comparadas às regiões ao norte do Amazonas (como Município de Manaus, Reserva do INPA-WWF e Usina Hidrelétrica de Balbina, Estado do Amazonas). Desta forma, é possível inferir que o levantamento das serpentes da região de Urucu ainda não esteja completo, sendo necessário um maior esforço de coleta para que novos registros sejam adicionados para a área.

A structured snake inventory was carried out at the Base Operacional Geólogo Pedro de Moura (BOGPM), located at the Urucu Petrol Basin, Municipality of Coari, Amazonas, during 2003, 2004 and 2007. Throughout four sampling expeditions (51 collection days), seven species of snakes, belonging to seven families and 33 genera, were recorded. Four complementary sampling methods were used: pitfall traps with drift fence, occasional encounters, time-limited search on foot and time-limited search by car. Of the 47 collected species Liophis reginae (n= 14), Philodryas viridissima (n= 9), Philodryas boulengeri (n= 7) and Oxybelis fulgidus (n= 7) were the most abundant in the region. The highest number of species and specimens was obtained by the time-limited search by car (n=52.8%). Previous studies indicate that localities south of the Amazonas river (such as the eastern region of Pará and Tucuruí, state of Para, and Samuel Hydroelectric Plants, state of Rondônia) present a greater richness when compared to those north of the Amazonas river (such as the mucipality of Manaus, INPA-WWF Reserve and Balbina Hydroelectric Plant, state of Amazonas).Thus, it is possible to infer that the snake inventory in Urucu region is not yet complete, requiring more sampling efforts so that new records can be obtained for the area.

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.