A subterranean generalist predator: diet of the soil-dwelling caecilian Gegeneophis ramaswamii (Amphibia; Gymnophiona; Caeciliidae) in southern India

Biologists have paid relatively little attention to subterranean predators, especially their ecology. Although diets of some subterranean lower vertebrates suggest specialisation, there remains a lack of quantitative data. The diet of the caecilian amphibian Gegeneophis ramaswamii was investigated through analyses of gut contents of 67 specimens collected in randomised surveys at three localities in Kerala, southern India, in early and mid-monsoon. Although termites were the most frequently ingested items in the mid-monsoon, the specialist predator hypothesis was rejected because of differences in diet found in early monsoon samples, when earthworms contributed the greatest mass. That guts of some G. ramaswamii contained many individuals of only a single dietary taxon was interpreted as feeding on patchily distributed prey rather than specialisation. No ontogenetic differences in diet were apparent, but more sampling is required to investigate this further. Subadults largely feed on fewer items of the same prey as adults, though there is an indication that subadult diet is less diverse. The data do not support differences between male and female diet. High densities of G. ramaswamii, and perhaps of other terrestrial caecilians and subterranean lower vertebrates feeding on soil-ecosystem engineers (termites, earthworms and ants), might substantially impact soil ecology.     

The caecilian amphibian Scolecomorphus kirkii Boulenger as prey of the burrowing asp Atractaspis aterrima Günther: trophic relationships of fossorial vertebrates

A report is given of an adult caecilian, Scolecomorphus kirkii, found in the gut of a specimen of the snake Atractaspis aterrima from the Udzungwa Mountains, Tanzania. Both predator and prey are largely fossorial in soil, and their ecology is poorly known, such that this is the first reported predator of any scolecomorphid caecilian. The caecilian was ingested head first and much of the flesh from the anterior of the specimen had been digested. The prey/predator mass ratio is 0.48. This value is substantially higher than reported for A. aterrima from West Africa, and refutes the notion that this species feeds only on small prey. Most reported predators of caecilians are snakes, and a brief review is presented.     

Evidence of seasonal migration in a tropical subterranean vertebrate

Many animals undergo migrations that depend on a range of biotic or abiotic factors provoking daily, seasonal or annual movement of individuals and/or populations. Temperate amphibians frequently have their life cycles dominated by annual temperature fluctuations, but in the tropics it is often presumed that distinct rainy seasons will influence amphibians more than small changes in temperature. Here, we direct the seasonal changes in abundance hypothesis to a caecilian amphibian Boulengerula boulengeri found in monthly randomized quantitative surveys in the top 30 cm of soil. Meteorological data are used to interpret the significant changes found in relation to rainfall and temperature variables. Instead of the expected correlation of migration with rainfall, we find that frequency varies significantly and positively with temperature. In addition, data on the depth at which individual caecilians are collected suggest that animals undergo a vertical (rather than horizontal) migration within the soil. This is the first example of vertical migrations with temperature (as opposed to rainfall) of any tropical subterranean fauna. We discuss the possible influences that stimulate migration in this species (abiotic factors, feeding, reproduction and predation). The ecology of caecilians has lagged behind that of all other tetrapods, and this study has importance for future ecological studies, as well as biodiversity assessments and monitoring methodologies.     

Sexual size dimorphism in caecilian amphibians: analysis, review and directions for future research

Sexual dimorphism, widespread in the animal kingdom, describes differences between the sexes in size, shape and many other traits. Sexual size dimorphism (SSD) plays a significant role in understanding life history evolution and mating systems. The snakelike morphology of limbless caecilian amphibians lacking obvious secondary sexual characters (in contrast to frogs and salamanders) impedes accurate intrasexual comparisons. In this study, sexual size dimorphism in the oviparous caecilian Ichthyophis cf. kohtaoensis, a phylogenetically basal caecilian, was analysed. Females were larger in all body and head characters tested. However, when adjusted to body size (total length), females differed only in their cloacal shape. Clutch volume was positively correlated to female body size, thus female fecundity increased with body size supporting the hypothesis of a fecundity-selected SSD in the oviparous Ichthyophis cf. kohtaoensis. A review of the present SSD data for caecilians shows that many species are monomorphic for body size but show dimorphism in head size, while other species demonstrate female-biased SSD. Male-biased SSD has not been reported for caecilians. To understand life history evolution in caecilians, further studies on the reproductive biology of other taxa are urgently needed, in particular for rhinatrematids and uraeotyphlids. New data will allow phylogenetically controlled comparative analyses to fully explore the pattern of SSD among caecilian lineages.     

Frequency of independent origins of viviparity among caecilians (Gymnophiona): evidence from the first 'live-bearing' Asian amphibian

Viviparity is reported for Gegeneophis seshachari (Gymnophiona: Caeciliidae) from a gravid female containing four oviductal foetuses. The oviducts are highly vascularized and contain patches of thickened, layered tissue similar to foetal gut contents. Gegeneophis seshachari probably resemble other viviparous caecilians in having foetuses that ingest thickened oviduct lining using specialized deciduous teeth. This is the first report of viviparity in Asian amphibians and Indo-Seychellean caeciliids. Gegeneophis is the only caecilian genus known to include oviparous and viviparous species, and G. seshachari is the smallest known viviparous caecilian. Phylogenetic analysis of mitochondrial DNA sequences supports assignment of G. seshachari to a monophyletic Gegeneophis. Character optimization indicates that viviparity has evolved independently at least four times within Gymnophiona--a rate of incidence relative to the number of extant species that is higher than for other vertebrate groups except squamate reptiles. Our findings strengthen the proposal that caecilian reproduction demands further attention.     

Phylogenetic relationships of Indian caecilians (Amphibia: Gymnophiona) inferred from mitochondrial rRNA gene sequences

India has a diverse caecilian fauna, including representatives of three of the six currently recognized families, the Caeciliidae, Ichthyophiidae, the endemic Uraeotyphlidae, but previous molecular phylogenetic studies of caecilians have not included sequences for any Indian caecilians. Partial 12S and 16S mitochondrial gene sequences were obtained for a single representative of each of the caecilian families found in India and aligned against previously reported sequences for 13 caecilian species. The resulting alignment (16 taxa, 1200 sites, of which 288 cannot be aligned unambiguously) was analyzed using parsimony, maximum-likelihood, and distance methods. As judged by bootstrap proportions, decay indices, and leaf stabilities, well-supported relationships of the Indian caecilians are recovered from the alignment. The data (1) corroborate the hypothesis, based on morphology, that the Uraeotyphlidae and Ichthyophiidae are sister taxa, (2) recover a monophyletic Ichthyophiidae, including Indian and South East Asian representatives, and (3) place the Indian caeciliid Gegeneophis ramaswamii as the sister group of the caeciliid caecilians of the Seychelles. Rough estimates of divergence times suggest an origin of the Uraeotyphlidae and Ichthyophiidae while India was isolated from Laurasia and Africa and are most consistent with an Indian origin of these families and subsequent dispersal of ichthyophiids into South East Asia.     

Evolutionary Origin and Host Range of Plagiotoma lumbrici (Ciliophora,Hypotrichia), an Obligate Gut Symbiont of Lumbricid Earthworms

Four common earthworm species, the anecic Lumbricus terrestris, the endogeic Octolasion tyrteum as well as the epigeic Eisenia fetida and Dendrobaena veneta, were examined for the presence of the microbial gut symbiont Plagiotoma lumbrici. The evolutionary origin of this endobiotic microbe was reconstructed, using the 18S rRNA gene, the ITS1‐5.8S‐ITS2 region, and the first two domains of the 28S rRNA gene. Plagiotoma lumbrici was exclusively detected in the anecic Lumbricus terrestris. Multigene analyses and the ITS2 secondary structure robustly determined the phylogenetic home of Plagiotoma lumbrici populations within the oxytrichid Dorsomarginalia (Spirotrichea: Hypotrichia) as a sister taxon of the free‐living Hemiurosomoida longa. This indicates that earthworms obtained their gut endosymbiont by ingesting soil/leaf litter containing oxytrichine ciliates that became adapted to the intestinal tract of earthworms. Interestingly, according to the literature data, Plagiotoma lumbrici was detected in multiple anecic and some epigeic but never in endogeic earthworms. These observations suggest that Plagiotoma lumbrici might be adapted to certain gut conditions and the lifestyle of anecic Lumbricidae, such as Lumbricus, Aporrectodea, and Scherotheca, as well as of some co‐occurring epigeic Lumbricus species.     

The Braincase of Eocaecilia micropodia (Lissamphibia,Gymnophiona) and the Origin of Caecilians

The scant fossil record of caecilians has obscured the origin and evolution of this lissamphibian group. Eocaecilia micropodia from the Lower Jurassic of North America remains the only stem-group caecilian with an almost complete skull preserved. However, this taxon has been controversial, engendering re-evaluation of traits considered to be plesiomorphic for extant caecilians. Both the validity of the placement of E. micropodia as a stem caecilian and estimates of the plesiomorphic condition of extant caecilians have been questioned. In order to address these issues, the braincase of E. micropodia was examined via micro-computed tomography. The braincase is considered to be a more reliable phylogenetic indicator than peripheral regions of the skull. These data reveal significant new information, including the possession of an ossified nasal septum, ossified anterior wall of the sphenethmoid, long anterolateral processes on the sphenethmoid, and paired olfactory nerve foramina, which are known only to occur in extant caecilians; the latter are possibly related to the evolution of the tentacle, a caecilian autapomorphy. A phylogenetic analysis that included 64 non-amniote taxa and 308 characters represents the first extensive test of the phylogenetic affinities of E. micropodia. The results place E. micropodia securely on the stem of extant caecilians, representing a clade within Temnospondyli that is the sister taxon to batrachians plus Gerobatrachus. Ancestral character state reconstruction confirms the braincase of E. micropodia to be largely representative of the plesiomorphic condition of extant caecilians. Additionally, the results refine the context within which the evolution of the caecilian form can be evaluated. The robust construction and pattern of the dermal skull of E. micropodia is interpreted as symplesiomorphic with advanced dissorophoid temnospondyls, rather than being autapomorphic in its robust construction. Together these data increase confidence in incorporating E. micropodia into discussions of caecilian evolution.     

A field guide to the caecilians of the Western Ghats, India

Caecilians are legless amphibians quite characteristic of the Western Ghats. Fourteen out of 16 Indian species occur in the Western Ghats and all are endemic. The present paper deals with the biology of caecilians with reference to external morphology and general breeding behaviour. It consolidates information on 26 morphological parameters which are used in caecilian identification. Metric multidimensional scaling of 16 species of caecilians using pair-wise euclidian distances calculated on the basis of 11 important morphometric parameters clearly depicts morphological distances between different species and more so the genera, thereby validating the classification. A field guide has been developed for the identification of caecilians based on a survey made all over the Western Ghats, observation of holotypes at the Natural History Museum, London and review of the literature. The study also reveals the microhabitat requirements of the caecilians. Further, the localities of caecilian distribution in the Western Ghats are mapped. The taxonomy of Indian caecilians is discussed.     

A mitogenomic perspective on the phylogeny and biogeography of living caecilians (Amphibia: Gymnophiona)

The caecilians, members of the amphibian Order Gymnophiona, are the least known Order of tetrapods, and their intra-relationships, especially within its largest group, the Family Caeciliidae (57% of all caecilian species), remain controversial. We sequenced thirteen complete caecilian mitochondrial genomes, including twelve species of caeciliids, using a universal primer set strategy. These new sequences, together with eight published caecilian mitochondrial genomes, were analyzed by maximum parsimony, partitioned maximum-likelihood and partitioned Bayesian approaches at both nucleotide and amino acid levels, to study the intra-relationships of caecilians. An additional multiple gene dataset including most of the caecilian nucleotide sequences currently available in GenBank produced phylogenetic results that are fully compatible with those based on the mitogenomic data. Our phylogenetic results are summarized as follow. The caecilian family Rhinatrematidae is the sister taxon to all other caecilians. Beyond Rhinatrematidae, a clade comprising the Ichthyophlidae and Uraeotyphlidae is separated from a clade containing all remaining caecilians (Scolecomorphidae, Typhlonectidae and Caeciliidae). Within this large clade, Scolecomorphidae is the sister taxon of Typhlonectidae and Caeciliidae but this placement did not receive strong support in all analyses. Caeciliidae is paraphyletic with regard to Typhlonectidae, and can be divided into three well-supported groups: Caeciliidae group 1 contains the African caeciliids Boulengerula and Herpele; Caeciliidae group 2 contains Caecilia and Oscaecilia and it is the sister taxon of Typhlonectidae; Caeciliidae group 3 comprises the remaining species of caeciliids. The mitochondrial genome data were also used to calculate divergence times for caecilian evolution using the penalized likelihood method implemented in the program R8S. The newly obtained dating results are compatible with (but a little older than) previous time estimates mainly based on nuclear gene data. The mitogenomic time tree of caecilians suggests that the initial diversification of extant caecilians most probably took place in Late Triassic about 228 (195–260) Ma. Caeciliids currently distributed in India and the Seychelles diverged from their African and American relatives most probably in Late Jurassic about 138 (112–165) Ma, fairly close to the time (130 Ma) when Madagascar–India–Seychelles separated from Africa and South America. The split between the Indian caeciliid Gegeneophis and Seychellean caeciliids occurred about 103 (78–125) Ma, predated the rifting of India and the Seychelles (65 Ma).     

Drought stress in rice (Oryza sativa L.) is enhanced in the presence of the compacting earthworm Millsonia anomala

Earthworms increase growth of most plant species through a number of poorly investigated mechanisms. We tested the hypothesis that earthworm modifications of soil structure and the resulting changes in water availability to plants explain this positive effect. Addition of endogeic earthworms Millsonia anomala induced a 40% increase in shoot biomass production and a 13% increase in CO₂ assimilation rate of well watered rice plants grown in pots. Conversely, when plants were subjected to water deficit, presence of earthworms had no effect on shoot biomass production and a negative impact on CO₂ assimilation rate (−21%). Early stomatal closure in presence of earthworms indicated lower water availability. The hypothesis that earthworms improve plant biomass production through soil physical structure modification was thus rejected. Three hypotheses were tested to explain this decrease in water availability: (i) a decrease in soil water retention capacity, (ii) an increase in evaporation from the soil or/and (iii) an increase in plant transpiration. Results showed that earthworms significantly reduced soil water retention capacity by more than 6%, but had no effect on evaporation rate. Water losses through transpiration were greater in the presence of earthworms when the soil was maintained at field capacity, but this was not the case under drought conditions. This experiment showed that the endogeic compacting earthworm M. anomala significantly increased plant photosynthesis by an undetermined mechanism under well-watered conditions. However, photosynthesis was reduced under drought conditions due to reduced soil water retention capacity.     

Externally measured condition versus internal organ mass in the caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae)

The relationship between externally measured condition (mass x length(-3)) and the mass of internal major organs in the caecilian Gegeneophis ramaswamii is investigated, based on a collection of 67 specimens from three southern Indian localities in the early and mid-monsoon. Condition in juveniles (< 90 mm total length) is higher than in subadults (90-170 mm) and adults (> 170 mm). The relationship between condition and total length is consistent in subadults, but variable in adults, and these differences indicate that the delimitation of these ontogenetic stages has some biological meaning. Adult females have fat bodies which fluctuate in mass, but not in relation to their body size. On average, adult females have heavier fat bodies and lighter gut contents than adult males, but there are no significant differences between subadult males and females. Gravid females are predicted to have a notably greater condition. There is no consistent relationship between condition and any major internal organ, but there is some significant variation among samples grouped by sampling time and locality. More sampling throughout the year is required to clarify the complex relationships between condition and internal organs, and before externally measured condition from ecological studies of living animals can be readily interpreted. However, its utility in helping to differentiate between ontogenic classes may be of immediate use.     

Plant and Litter Influences on Earthworm Abundance and Community Structure in a Tropical Wet Forest1

Plant communities differ in species composition and litter input. To examine the influence of plant species on the abundance and community structure of soil fauna, we sampled earthworms in areas close to and away from the bases of Dacryodes excelsa and Heliconia caribaea, two distinct plant communities within a tropical wet forest in Puerto Rico. We also carried out a litter manipulation experiment to examine the short–term responses of earthworms to litter removal and litter addition treatments. We found that: (1) the density and biomass of both soil–feeding endogeic and litter-feeding anccic worms did not differ between areas close to and away from Dacryodef trees (in contrast, the density and biomass of anecic worms was higher in areas away from Heliconia plants despite the lack of differences for endogeic worms); and (2) total dry weight of earthworms tended to be higher in the litter addition treatment than in the control within the Heliconia community. Our results suggest that Heliconia caribaea has a strong negative influence on anecic earthworms and that earthworms in the Heliconia community are more sensitive to litter input than in the Dacryodes community.     

Cellular migration and morphological complexity in the caecilian brain

The morphology of the tectum mesencephali and the medial pallium is studied in species representing the six families of caecilians (Amphibia: Gymnophiona) in order to determine whether differences in brain morphology are related to function, phylogenetic history, or life history strategies. In general, the caecilian tectum is characterized by simplification in having little to no lamination and few migrated cells. The degree of morphological complexity differs between species and between brain regions. Our data suggest that changes in brain morphology are due to a mosaic of different influences. We did not find a strict correlation between visual system reduction and tectal morphologies. However, phylogenetic effects exist. The greatest degree of morphological complexity is found in members of the Rhinatrematidae, a family that is considered basal to the lineage. Thus, simplification of brain morphology in caecilians must be considered a secondary or derived rather than a primitive feature. Direct development and miniaturization are correlated with the greatest simplification in the tectum mesencephali and medial pallium. There is a relationship between differences in brain morphology and heterochrony in caecilians, as in other amphibians. J. Morphol. 231:11–27, 1997. © 1997 Wiley-Liss, Inc.     

Functional domains in soils

Soil processes are significantly regulated by biological activities. Soil ecosystem engineers (predominantly termites, earthworms and ants) and roots produce biogenic structures, aggregates or pores that determine the structure and architecture of soil. The sum of structures produced by a population or community of invertebrate engineers creates a specific environment defined here as a functional domain. Functional domains are characterized by (i) the nature and spatial array of the biogenic structures, solid aggregates, mounds or constructs and pores of different shapes or sizes; (ii) the specific communities of smaller organisms from the meso- and microfauna and micro-organisms that they host; and (iii) the spatial and temporal scales at which soil processes operate. The regulation of processes caused by the physical organization of the soil environment and the redistribution of organic resources have been described and quantified in several studies. In soil, the relative importance of regulation imposed by ecosystem engineering is likely to be greater than regulation by trophic relationships because of the specific ecological constraints observed in this environment when compared to above-ground conditions.     

One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona)

Maternal dermatophagy, the eating of maternal skin by offspring, is an unusual form of parental investment involving co-evolved specializations of both maternal skin and offspring dentition, which has been recently discovered in an African caecilian amphibian. Here we report the discovery of this form of parental care in a second, distantly related Neotropical species Siphonops annulatus, where it is characterized by the same syndrome of maternal and offspring specializations. The detailed similarities of skin feeding in different caecilian species provide strong evidence of its homology, implying its presence in the last common ancestor of these species. Biogeographic considerations, the separation of Africa and South American land masses and inferred timescales of amphibian diversification all suggest that skin feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100 Myr. These inferences support the hypotheses that (i) maternal dermatophagy is widespread in oviparous direct-developing caecilians, and (ii) that viviparous caecilians that feed on the hypertrophied maternal oviduct evolved from skin-feeding ancestors. In addition to skin-feeding, young S. annulatus were observed to congregate around, and imbibe liquid exuded from, the maternal cloacal opening.     

Nest mounds of red wood ants (Formicaaquilonia): hot spots for litter-dwelling earthworms

A previously undocumented association between earthworms and red wood ants (Formicaaquilonia Yarr.) was found during an investigation of the influence of wood ants on the distribution and abundance of soil animals in boreal forest soil. Ant nest mounds and the surrounding soil of the ant territories were sampled. The ant nest mound surface (the uppermost 5-cm layer) harboured a much more abundant earthworm community than the surrounding soil; the biomass of the earthworms was about 7 times higher in the nests than in the soil. Dendrodrilusrubidus dominated the earthworm community in the nests, while in soils Dendrobaenaoctaedra was more abundant. Favorable temperature, moisture and pH (Ca content), together with abundant food supply (microbes and decomposing litter) are likely to make a nest mound a preferred habitat for earthworms, provided that they are not preyed upon by the ants. We also conducted laboratory experiments to study antipredation mechanisms of earthworms against ants. The experiments showed that earthworms do not escape predation by avoiding contact with ants in their nests. The earthworm mucus repelled the ants, suggesting a chemical defence against predation. Earthworms probably prevent the nest mounds from becoming overgrown by moulds and fungi, indicating possible mutualistic relationships between the earthworms and the ants. Received: 21 November 1996 / Accepted: 3 April 1997     

Diet is the primary determinant of bacterial community structure in the guts of higher termites

The gut microbiota of termites plays critical roles in the symbiotic digestion of lignocellulose. While phylogenetically ‘lower termites’ are characterized by a unique association with cellulolytic flagellates, higher termites (family Termitidae) harbour exclusively prokaryotic communities in their dilated hindguts. Unlike the more primitive termite families, which primarily feed on wood, they have adapted to a variety of lignocellulosic food sources in different stages of humification, ranging from sound wood to soil organic matter. In this study, we comparatively analysed representatives of different taxonomic lineages and feeding groups of higher termites to identify the major drivers of bacterial community structure in the termite gut, using amplicon libraries of 16S rRNA genes from 18 species of higher termites. In all analyses, the wood‐feeding species were clearly separated from humus and soil feeders, irrespective of their taxonomic affiliation, offering compelling evidence that diet is the primary determinant of bacterial community structure. Within each diet group, however, gut communities of termites from the same subfamily were more similar than those of distantly related species. A highly resolved classification using a curated reference database revealed only few genus‐level taxa whose distribution patterns indicated specificity for certain host lineages, limiting any possible cospeciation between the gut microbiota and host to short evolutionary timescales. Rather, the observed patterns in the host‐specific distribution of the bacterial lineages in termite guts are best explained by diet‐related differences in the availability of microhabitats and functional niches.     

A comparative study of locomotion in the caecilians Dermophis mexicanus and Typhlonectes natans (Amphibia: Gymnophiona)

We compared locomotion of two species of caecilian using x-ray videography of the animals traversing smooth-sided channels and a pegboard. Two channel widths were used, a body width channel and a body width + 20% channel. The terrestrial caecilian, Dermophis mexicanus , used internal concertina locomotion in both channels and lateral undulation on the pegboard. The aquatic caecilian, Typhlonectes natans , was not able to move at all in the body width channel. In the wider channel Typhlonectes proceeded at the same speed as Dermophis while using normal, rather than internal, concertina locomotion. On the pegboard, Typhlonectes used lateral undulation and achieved 2.5 times the speed managed by Dermophis. A phylogenetic analysis of this, and other, evidence shows that (1) internal concertina evolved in the ancestor to extant caecilians and (2) internal concertina locomotion was secondarily lost in the aquatic caecilians.     

Evolutionary relationships of the lungless caecilian Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae)

Appreciation of the diversity of caecilian amphibians has recently been enhanced by the discovery of a radically divergent aquatic caecilian of the Neotropical Typhlonectidae. Atretochoana eiselti is the largest lungless tetrapod and the only lungless caecilian, and it possesses a suite of remarkable cranial modifications that set it apart from all other caecilians. Numerical phylogenetic analyses, using 141 morphological characters, were performed in order to resolve the evolutionary relationships of Atretochoana and representatives of all other typhlonectid genera. These analyses yield a single most parsimonious tree, (Chthonerpeton (Nectocaecilia (Typhlonectes natans, Typhlonectes compressicauda) (Potomotyphlus, Atretochoana)))) , that is both well resolved and, as judged by Bremer support and by bootstrapping, is well supported. This tree is used as a basis for interpreting ecological shifts and associated morphological evolution within the Typhlonectidae. The available data suggest that the rate of morphological evolution in the Atretochoana lineage is significandy greater than that in other typhlonectid lineages.