Caecilian Species Research Articles

Genomic SNPs resolve the phylogeny of an ancient amphibian island radiation from the Seychelles

Unusually for oceanic islands, the granitic Seychelles host multiple lineages of endemic amphibians. This includes an ancient (likely ca. 60 million years) radiation of eight caecilian species, most of which occur on multiple islands.These caecilians have a complicated taxonomic history and their phylogenetic inter-species relationships have been difficult to resolve. Double-digest RAD sequencing (ddRADseq) has been applied extensively to phylogeography and increasingly to phylogenetics but its utility for resolving ancient divergences is less well established. To address this, we applied ddRADseq to generate a genome-wide SNP panel for phylogenomic analyses of the Seychelles caecilians, whose phylogeny has so far not been satisfactorily resolved with traditional DNA markers. Based on 129,154 SNPs, we resolved deep and shallow splits, with strong support. Our findings demonstrate the capability of genome-wide SNPs for evolutionary inference at multiple taxonomic levels and support the recently proposed synonymy of Grandisonia Taylor, 1968 with Hypogeophis Peters, 1879. We revealed three clades of Hypogeophis (large-, medium- and short-bodied) and identify a single origin of the diminutive, stocky-bodied and pointy-snouted phenotype.

The first fossil record of an aquatic caecilian (Gymnophiona: Typhlonectidae)

Abstract The lissamphibian clade Gymnophiona includes approximately 220 recognized modern species known by the English vernacular as caecilians and characterized by their elongated and annulated bodies, without girdles or limbs. Fossils of caecilians are particularly rare and mostly limited to isolated vertebrae. Until now, only four bona fide Gymnophionomorpha species have been named based on fossils. Only one of these (Apodops pricei) is a crown-group caecilian, but its affinities with modern caecilians are uncertain because the material is limited to one damaged vertebra and is currently lost. Here we describe a new genus and species of caecilian from the Oligocene Tremembé Formation, Brazil, based on a partially preserved fossil skeleton (including elements of the skull and postcranium) that is damaged but still partly articulated. We investigated the fossil caecilian’s anatomy using high-resolution microcomputed tomography, and then compared it to the osteology of modern species. We interpret the fossil as a member of Typhlonectidae, a family of caecilians well known for their aquatic and semi-aquatic lifestyles. This new record represents the first record for caecilians from the Oligocene and also the first fossil species confidently assigned to an extant caecilian family.

A New Species of Caecilian in the Genus Boulengerula from Endau Hill in South-Eastern Kenya

A New Species of Caecilian in the Genus Boulengerula from Endau Hill in South-Eastern Kenya

Resistance Is Not Futile: Widespread Convergent Evolution of Resistance to Alpha-Neurotoxic Snake Venoms in Caecilians (Amphibia: Gymnophiona).

Predatory innovations impose reciprocal selection pressures upon prey. The evolution of snake venom alpha-neurotoxins has triggered the corresponding evolution of resistance in the post-synaptic nicotinic acetylcholine receptors of prey in a complex chemical arms race. All other things being equal, animals like caecilians (an Order of legless amphibians) are quite vulnerable to predation by fossorial elapid snakes and their powerful alpha-neurotoxic venoms; thus, they are under strong selective pressure. Here, we sequenced the nicotinic acetylcholine receptor alpha-1 subunit of 37 caecilian species, representing all currently known families of caecilians from across the Americas, Africa, and Asia, including species endemic to the Seychelles. Three types of resistance were identified: (1) steric hindrance from N-glycosylated asparagines; (2) secondary structural changes due to the replacement of proline by another amino acid; and (3) electrostatic charge repulsion of the positively charged neurotoxins, through the introduction of a positively charged amino acid into the toxin-binding site. We demonstrated that resistance to alpha-neurotoxins convergently evolved at least fifteen times across the caecilian tree (three times in Africa, seven times in the Americas, and five times in Asia). Additionally, as several species were shown to possess multiple resistance modifications acting synergistically, caecilians must have undergone at least 20 separate events involving the origin of toxin resistance. On the other hand, resistance in non-caecilian amphibians was found to be limited to five origins. Together, the mutations underlying resistance in caecilians constitute a robust signature of positive selection which strongly correlates with elapid presence through both space (sympatry with caecilian-eating elapids) and time (Cenozoic radiation of elapids). Our study demonstrates the extent of convergent evolution that can be expected when a single widespread predatory adaptation triggers parallel evolutionary arms races at a global scale.

A survey of amphibians at Liwagu Water Catchment Area, Tambunan, Sabah, Malaysia

This paper presents the inventory of frogs collected at Liwagu Water Catchment, Tambunan, Sabah. The specimens were collected along trails using the Visual Encounter Survey (VES) and hand-grabbing technique. The process of collecting and recording data was done according to the standard method for handling amphibians. A total of 15 species of anurans and one species of caecilian were recorded. The assemblage was dominated by anurans from Ranidae (39%).

The anatomy of the head muscles in caecilians (Amphibia: Gymnophiona): Variation in relation to phylogeny and ecology?

In limbless fossorial vertebrates such as caecilians (Gymnophiona), head-first burrowing imposes severe constraints on the morphology and overall size of the head. As such, caecilians developed a unique jaw-closing system involving the large and well-developed m. interhyoideus posterior, which is positioned in such a way that it does not significantly increase head diameter. Caecilians also possess unique muscles among amphibians. Understanding the diversity in the architecture and size of the cranial muscles may provide insights into how a typical amphibian system was adapted for a head-first burrowing lifestyle. In this study, we use dissection and non-destructive contrast-enhanced micro-computed tomography (μCT) scanning to describe and compare the cranial musculature of 13 species of caecilians. Our results show that the general organization of the head musculature is rather constant across extant caecilians. However, the early-diverging Rhinatrema bivittatum mainly relies on the 'ancestral' amphibian jaw-closing mechanism dominated by the m. adductores mandibulae, whereas other caecilians switched to the use of the derived dual jaw-closing mechanism involving the additional recruitment of the m. interhyoideus posterior. Additionally, the aquatic Typhlonectes show a greater investment in hyoid musculature than terrestrial caecilians, which is likely related to greater demands for ventilating their large lungs, and perhaps also an increased use of suction feeding. In addition to three-dimensional interactive models, our study provides the required quantitative data to permit the generation of accurate biomechanical models allowing the testing of further functional hypotheses.

Regional differences in vertebral shape along the axial skeleton in caecilians (Amphibia: Gymnophiona).

Caecilians are elongate, limbless and annulated amphibians that, as far as is known, all have an at least partly fossorial lifestyle. It has been suggested that elongate limbless vertebrates show little morphological differentiation throughout the postcranial skeleton. However, relatively few studies have explored the axial skeleton in limbless tetrapods. In this study, we used μCT data and three-dimensional geometric morphometrics to explore regional differences in vertebral shape across a broad range of caecilian species. Our results highlight substantial differences in vertebral shape along the axial skeleton, with anterior vertebrae being short and bulky, whereas posterior vertebrae are more elongated. This study shows that despite being limbless, elongate tetrapods such as caecilians still show regional heterogeneity in the shape of individual vertebrae along the vertebral column. Further studies are needed, however, to understand the possible causes and functional consequences of the observed variation in vertebral shape in caecilians.

Investigating the Effect of Disturbance on Prey Consumption in Captive Congo Caecilians Herpele squalostoma

Maintaining Gymnophiona in captivity provides opportunities to study the behaviour and life-history of this poorly known Order, and to investigate and provide species-appropriate welfare guidelines, which are currently lacking. This study focuses on the terrestrial caecilian Herpele squalostoma to investigate its sensitivity to disturbances associated with routine husbandry needed for monitoring and maintaining adequate wellbeing in captivity. Fossorial caecilians gradually pollute their environment in captivity with waste products, and substrate must be replaced at intervals; doing so disturbs the animals directly and via destruction of burrow networks. As inappetence is frequently associated with stress in amphibians, the percentage consumption of offered food types, river shrimp (Palaemon varians) and brown crickets (Gryllus assimilis), was measured as an indicator of putative stress following three routine substrate changes up to 297 days post-substrate change. Mean daily variation in substrate temperatures were also recorded in order to account for environmental influences on food consumption, along with nitrogenous waste in tank substrate prior to a substrate change and fresh top soil in order to understand the trade-off between dealing with waste accumulation and disturbing animals. We found a significant negative effect of substrate disturbance on food intake, but no significant effect of prey type. Variations in daily soil temperatures did not have a significant effect on food intake, but mean substrate temperature did. Additionally, substrate nitrogenous waste testing indicated little difference between fresh and tank substrate. In conclusion, this study provides a basis from which to develop further welfare assessment for this and other rarely kept and rarely observed terrestrial caecilian species.

REVIEW OF HISTOLOGIC LESIONS AND MORTALITY IN RIO CAUCA CAECILIANS (TYPHLONECTES NATANS) OVER A 22-YEAR PERIOD

Rio Cauca caecilians (Typhlonectes natans) are a unique, fully aquatic species of amphibian from the order Gymnophiona. They are housed in several zoological institutions and aquaria with limited information available regarding health and disease. This retrospective study evaluates common pathologic findings and causes of mortality of Rio Cauca caecilians from three different institutions over a 22-y period. Comparisons to previous medical health surveys were conducted with evaluation according to age class and sex to determine whether the primary causes of mortality and common histologic findings have remained similar over time and between institutions. Between 1997 and 2019, the 62 mortalities included males (15/62; 24.2%), females (26/62; 41.9%), and undetermined sex (21/62; 33.9%). The majority of examined individuals were adult (38/62; 61.3%), followed by juveniles (13/62; 21.0%), neonates (9/62; 14.5%), and undetermined age class (2/62; 3.2%). Thirteen (21.0%) individuals were euthanatized. Adult females (16/62; 25.48%) represented the largest group. In adults, the most common lesion and contributor to death was renal disease (28/38; 73.7%) followed by skin disease (16/38; 42.1%), including oomycete dermatitis (8/38; 21.1%) from Saprolegnia sp. Other common findings included bacterial dermatitis, gastrointestinal nematodiasis, and adrenal hyperplasia. This retrospective study will provide a useful reference to help guide veterinary care, management decisions, and collection management planning for this caecilian species in managed care.

Amphibians and reptiles of Wildsumaco Wildlife Sanctuary, Napo Province, Ecuador

We conducted a long-term inventory of the herpetofauna of Wildsumaco Wildlife Sanctuary in the eastern part of the Napo Province in Ecuador. This private preserve is about 500 ha in size and is located on the southern slopes of Volcán Sumaco. The preserve contains primary forest, secondary forest, and pasture habitats. Based mostly on nocturnal transect sampling we documented 39 species of amphibians including one species of salamander, two species of caecilians, and 36 species of frogs. Rain frogs (Pristimantis Jiminez de la Espada, 1871) were diverse with 14 species documented. A diverse species assemblage of 45 reptile species was also documented on the preserve. Six amphibian species found were listed by the IUCN Red List. At least three species exhibited substantial geographic range extensions and seven species showed elevational range extensions. We discovered several undescribed species including one salamander, three frogs, one lizard, and one snake.

Global assessment of artificial habitat use by amphibian species

Human modification of natural landscapes is a key threatening process contributing to the decline of global biodiversity. Amphibians are particularly vulnerable to this threat, with over a third of species threatened as a direct result. However, some habitat modifications may be less detrimental than others, with some species known to successfully thrive in certain artificial habitats while others undergo further declines. Yet, recognizing how amphibians respond to different habitat modifications remains limited, particularly on a global scale. Herein, we examine the known artificial habitat associations of amphibian species globally, demonstrating artificial habitat use is dependent on their conservation status, life history, taxonomic order, and geographical location. Approximately one-third of all amphibians were found to use artificial habitats, including nearly half of all non-threatened and one-sixth of threatened species, with usage decreasing as conservation status increased. Terrestrial, generalist, and caecilian species were much more likely to use artificial habitats. Non-threatened species were more likely to utilize artificial habitats such as aquaculture ponds, pastureland, canals, excavations, urban areas, and rural gardens. Plantations, heavily degraded former forests, and wastewater treatment areas contained a greater proportion of threatened species, particularly in Afrotropical, Indomalayan, and Oceanian regions. Countries with the most amphibians utilizing artificial habitats were Brazil, Colombia, Peru, Madagascar, and Ecuador. However, the greatest number of threatened species using artificial habitats were found in Mexico, Madagascar, India, Sri Lanka, and China. We highlight the potential value or threat of each artificial habitat type, which may be used to better focus valuable conservation efforts.

First confirmed record of caecilians (Amphibia: Gymnophiona) from the Himalayan Kingdom of Bhutan

The world currently recognizes 214 species of Caecilians (Amphibia: Gymnophiona) most of which occur in the wet tropics and some adjacent subtropical regions. Of the ten-family classification known, three occur in Asia, viz. Chikilidae (endemic to northeast India, Indotyphlidae (India’s Western and Eastern Ghats) and Ichthyophiidae. However, until this report, there were no confirmed reports of any caecilian species from Bhutan, although their presence has been assumed likely given their occurrence in adjacent countries. This report provides the first confirmed report of caecilians in Bhutan with work to identify the species to be carried on later with further research.

A new genus and species of rhinatrematid caecilian (Amphibia: Gymnophiona: Rhinatrematidae) from Ecuador

A new genus and species of rhinatrematid caecilian, Amazops amazops gen. et sp. nov., is described based on a single specimen from Orellana, Ecuador collected in 1990. Among other features the new taxon differs from all other rhinatrematid caecilians in having less than four annular grooves interrupted in the region of the vent and in the squamosal contributing to the bony margin of the orbit. A consideration of its distinctive morphology suggests that it is plausible that the new taxon is the sister taxon of all other rhinatrematid caecilians. That the genus is known from a single specimen, and that this is the first new rhinatrematid species from the Andes described for more than 50 years, highlights the poor sampling (collecting) of rhinatrematid caecilians and limited knowledge of their diversity.

Taxonomic status of the Guyanese endemic caecilian Caecilia pressula Taylor, 1968 (Amphibia: Gymnophiona: Caeciliidae)

The taxonomic status of the poorly known Neotropical caecilian species Caecilia pressula Taylor, 1968 is reconsidered based on examination of the type series. The single reported diagnostic feature, a laterally compressed body, that purportedly distinguishes C. pressula from Caecilia tentaculata Linnaeus, 1758 is not consistent across the seven specimens that constitute the type series and the only reported specimens, is variable in the Holotype depending on how it is held, and is considered to be artefactual. Caecilia pressula is considered to be a junior synonym of Caecilia tentaculata. Dentitional features of the smallest and presumed youngest specimens in the type series provide evidence that C. tentaculata practices maternal dermatophagy.

The roles of vicariance and isolation by distance in shaping biotic diversification across an ancient archipelago: evidence from a Seychelles caecilian amphibian

BackgroundIsland systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investigating evolutionary patterns and processes shaping biotic diversification have focused on more recent (emergent) rather than ancient oceanic archipelagos. Here, we focus on the granitic islands of the Seychelles, which are unusual among island systems because they have been isolated for a long time and are home to a monophyletic radiation of caecilian amphibians that has been separated from its extant sister lineage for ca. 65–62 Ma. We selected the most widespread Seychelles caecilian species, Hypogeophis rostratus, to investigate intraspecific morphological and genetic (mitochondrial and nuclear) variation across the archipelago (782 samples from nine islands) to identify patterns and test processes that shaped their evolutionary history within the Seychelles.ResultsOverall a signal of strong geographic structuring with distinct northern- and southern-island clusters were identified across all datasets. We suggest that these distinct groups have been isolated for ca. 1.26 Ma years without subsequent migration between them. Populations from the somewhat geographically isolated island of Frégate showed contrasting relationships to other islands based on genetic and morphological data, clustering alternatively with northern-island (genetic) and southern-island (morphological) populations.ConclusionsAlthough variation in H. rostratus across the Seychelles is explained more by isolation-by-distance than by adaptation, the genetic-morphological incongruence for affinities of Frégate H. rostratus might be caused by local adaptation over-riding the signal from their vicariant history. Our findings highlight the need of integrative approaches to investigate fine-scale geographic structuring to uncover underlying diversity and to better understand evolutionary processes on ancient, continental islands.

Insights into the skin of caecilian amphibians from gene expression profiles

BackgroundGene expression profiles can provide insights into the molecular machinery behind tissue functions and, in turn, can further our understanding of environmental responses, and developmental and evolutionary processes. During vertebrate evolution, the skin has played a crucial role, displaying a wide diversity of essential functions. To unravel the molecular basis of skin specialisations and adaptations, we compared gene expression in the skin with eight other tissues in a phylogenetically and ecologically diverse species sample of one of the most neglected vertebrate groups, the caecilian amphibians (order Gymnophiona).ResultsThe skin of the five studied caecilian species showed a distinct gene expression profile reflecting its developmental origin and showing similarities to other epithelial tissues. We identified 59 sequences with conserved enhanced expression in the skin that might be associated with caecilian dermal specialisations. Some of the up-regulated genes shared expression patterns with human skin and potentially are involved in skin functions across vertebrates. Variation trends in gene expression were detected between mid and posterior body skin suggesting different functions between body regions. Several candidate biologically active peptides were also annotated.ConclusionsOur study provides the first atlas of differentially expressed sequences in caecilian tissues and a baseline to explore the molecular basis of the skin functions in caecilian amphibians, and more broadly in vertebrates.

Identification of toxic metabolites produced by Batrachochytrium dendrobatidis fungus

Batrachochytrium dendrobatidis, or Bd, is a fungus that causes chytridiomycosis in amphibians, a disease responsible for the rapid decline in amphibian populations globally. The pervasiveness and mortality rates of the Bd fungus has spurred researchers to discover why the fungus is so lethal in various species of frogs, salamanders, and caecilians. While it is known that the fungus affects the skin of amphibians and causes death through suffocation via populating in the pores of adult amphibians, little is known about the active compounds in the fungus. An understanding of the methods of infection will aid in the creation of safe ways to treat amphibians and prevent further outbreaks. To determine the metabolites excreted by the fungus, the culture medium was filtered, dried, and analyzed by LCMS. A Daphnia assay was developed in order to aid bioactivity‐guided fractionation. Preliminary data suggests the presence of several compounds of interest in the dried metabolites. The masses of the peaks of interest were used to guide further isolation and identification of compounds.Support or Funding InformationFunded by a SURF grant from the University of Tampa

POSTMORTEM FINDINGS IN EIGHT SPECIES OF CAPTIVE CAECILIAN (AMPHIBIA: GYMNOPHIONA) OVER A TEN-YEAR PERIOD.

Between July 2007 and June 2017 there were 86 deaths in the populations of eight caecilian species at the Zoological Society of London (ZSL) London Zoo. The mortality rate (deaths per animal-year at risk) ranged from 0.03 in the Congo caecilian (Herpele squalostoma) to 0.85 in Kaup's caecilian (Potomotyphlus kaupii). Among the 73 individuals examined post mortem, no cause of death or primary diagnosis could be established in 35 cases, but of the others the most common cause of death was dermatitis (22 cases). When all significant pathological findings were considered, skin lesions of varying types were again the commonest (56 cases), particularly among the aquatic species: Typhlonectes compressicauda (18 out of 21 cases), T. natans (8/10) and P. kaupii (12/14). Other common findings were poor gut-fill (35 cases), kidney and gastrointestinal lesions (10 cases each), generalized congestion (8 cases) and poor body condition (6 cases). This review adds to the growing body of knowledge regarding the presentations and causes of disease in captive caecilians.

Dietary Partitioning in Two Co-occurring Caecilian Species (Geotrypetes seraphini and Herpele squalostoma) in Central Africa.

SynopsisTrophic interactions among fossorial vertebrates remain poorly explored in tropical ecosystems. While caecilian species can co-occur, whether and how sympatric species partition dietary or other resources are largely unknown. Based on specimens collected during field surveys in southern Cameroon, we conducted a dietary analysis of two co-occurring caecilian species, Geotrypetes seraphini and Herpele squalostoma. We find a negligible overlap in the adult diets of these two species. Earthworms dominated the diet of adult G. seraphini, whereas we found that mole crickets were the most frequent prey items in adult H. squalostoma. The dietary breadth of adult G. seraphini is smaller than that of H. squalostoma, which consumes a variety of hard-bodied prey including mole crickets, cockroaches, beetles, and crabs. Juvenile diets were similar between these species and mostly contained earthworms and ants. We did not detect significant ontogenetic dietary shifts in either species, though adults generally consumed a broader diversity of prey. As adults, G. seraphini and H. squalostoma may partition prey categories by consuming soft-bodied and hard-bodied prey, respectively. Because most caecilians are likely opportunistic predators, we expect that sympatric species partition dietary resources either by preference for different soil layers or ability to consume different prey categories.

A first screening of chytrid fungus Batrachochytrium in amphibians in French zoos

Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) screening was carried out in captive amphibians in order to establish the presence of these fungal pathogens in French zoos. Over a period of 3 years, 437 skin swabs were collected at eight French zoos and one private breeding centre [38 species of Anura, 7 species and 2 subspecies of Urodela (salamanders and newts), and 1 caecilian species] and these were analysed using qPCR. None of the samples revealed the presence of Bsal. Bd was detected four times on three species – American bullfrog Lithobates catesbeianus, Common midwife toad Alytes obstetricans and Yellow‐bellied toad Bombina variegata – all of which originated from or were in contact with the natural environment.