Surreal caecilians part II: pass mum's skin, hold the mayo

Overall I'm pretty pleased with the attention that the first caecilian article received (it's here): it was in the Sb top five most active articles for most of today (Jan 4th), and elicited a decent amount of response. Thanks as always to everyone who commented and especially to those who added snippets of information - in particular Lars Dietz, David Marjanović, and of course Sordes for that invaluable fact about pugs and what happens when you shake them too hard. Anyway, last time we got as far as tentacles, protrusible eyes and the dual jaw-closing mechanism - but what about all the really weird stuff? Well here we go...

The sexual organs of caecilians are unique: in contrast to other amphibians, male caecilians are able to evert their cloaca to form a phallus, properly termed a phallodeum. Decorated with tuberosities, ridges, grooves, crests and/or spines, the phallodeum superficially recalls the eversible hemipenes of male snakes and lizards (which, unlike the phallodeum, are paired). The reduced tails or tailessness of caecilians mean, however, that their cloacae are either at, or very close to, the animal's posterior tip where a disk-like structure - the terminal shield - is present. It's been suggested that phallodeum morphology is species-specific in caecilians (as hemipenial morphology generally is in snakes and lizards), but this is difficult to confirm, is not true in all cases, and is confused by intraspecific and ontogenetic variation (Gower & Wilkinson 2002). However, closely related taxa do share similar details, and the phallodeum is likely to be a good systematic tool, har har (not my joke, I stole it from a Mark Wilkinson talk). Incidentally, we don't know much about the sex lives of caecilians, but sexual dimorphism is developed in some taxa, with males having proportionally larger heads, and with the sexes differing in counts of vertebrae and annuli in some species.

Of Neocaecilia, Diatremata and Teresomata

All caecilians more derived than rhinatrematids are united by a suite of characters, including a recessed mouth, a large retroarticular process on the lower jaw, and soft tissue characters of the heart, musculature and vasculature, and by molecular data (San Mauro et al. 2004, Frost et al. 2006, Wilkinson & Nussbaum 2006). Cannatella & Hillis (1993) termed this advanced group the Stegokrotaphia, a name based on the so-called stegokrotaphic skull configuration (stegokrotaphy is the condition where the skull is roofed entirely by bone and is devoid of openings). However, many members of this clade are not stegokrotaphic but zygokrotaphic (this refers to the condition where openings are present in the temporal region), so Wilkinson & Nussbaum (2006) argued that an anatomically neutral clade name would be more appropriate and coined Neocaecilia.

At the base of Neocaecilia are two closely related groups, the Indian uraeotyphlids and the ichthyophiids of India and SE Asia (including the Philippines and Indo-Malayan archipelago). Molecular and morphological characters indicate that these two groups form a clade: Frost et al. (2006) proposed that Uraeotyphlidae should therefore be sunk into Ichthyophiidae (Uraeotyphlidae is, after all, redundant as it only contains the taxon Uraeotyphylus), but Wilkinson & Nussbaum (2006) argued for the erection of a new ichthyophiid + uraeotyphlid clade, termed Diatremata. Ichthyophiids might be paraphyletic with respect to uraeotyphlids: in fact, some members of the 'genus' Ichthyophis are probably closer to Uraeotyphlus than they are to other Ichthyophis species (Gower et al. 2002). Like rhinatrematids, diatrematans possess a true tail, possess scales within their annular grooves, and are oviparous. The eggs hatch into aquatic gilled larvae that usually have small caudal fins, and in ichthyophiids at least the mother remains with the unhatched eggs in an underground chamber [adjacent image shows the Sri Lankan ichthyophiid I. glutinosus].

Phylogenetic work indicates that diatrematans were ancestrally Indian, and so far as we know they were unique to India prior to its collision in the early Cenozoic with mainland Asia (Gower et al. 2002). This 'out of India' hypothesis also applies to other amphibians (notably many neobatrachian clades), and I'll be coming back to it again in a little while. Some ichthyophiids have achieved a surprisingly wide distribution along the length of the Indian subcontinent: what was thought to be a complex of five similar Ichthyophis species was recently shown to represent one very wide-ranging, genetically homogenous one distributed across 1500 km and 12°; of latitude (Gower et al. 2007). Exactly how one species of caecilian got to be so widely distributed is a good question.

Neocaecilians more derived than diatrematans - the caeciliids, typhlonectids and scolecomorphids - were termed the Teresomata by Wilkinson & Nussbaum (2006). All members of Teresomata lack a tail and they have a tendency to lack the scales present in more basal caecilians; their monophyly is well corroborated by molecular data (San Mauro et al. 2004, Frost et al. 2006, Wilkinson & Nussbaum 2006). Both typhlonectids and scolecomorphids were found to be nested within caeciliids by Frost et al. (2006), and hence both were downgraded to caecillid 'subfamilies' by these authors. Teresomata is easily the most diverse, widespread and speciose caecilian clade, but the relationships between the bulk of the species - those within the paraphyletic Caeciliidae - remain uncertain. The Seychelles caeciliids (all species of which have been included in phylogenetic studies) have proved to represent a clade, with their closest relative being the Indian Gegeneophis [adjacent image doesn't show a teresomatan, but an Ichthyophis brooding eggs. From here. See below.]

Viviparity, dermatotrophy and matrotrophy

Most caeciliids are oviparous and the females guard the eggs [see image above]. In some species, gilled aquatic larvae are present, but in others the larval stage has been skipped and the babies hatch fully metamorphosed. Scolecomorphids also exhibit direct development. However, some caeciliids and the typhlonectids are viviparous and give birth to fully metamorphosed young. And here's where things get really interesting.

Recent work on the caeciliid Boulengerula taitana has shown that caecilians do something that, yet again, is unique among tetrapods; furthermore, there are indications that this habit is (or was) widespread among the group. B. taitana is oviparous and has direct-developing embryos. However, the babies don't emerge from their eggs as precocial miniature adults: instead, they are altricial, with poorly ossified skulls and vertebrae and weakly developed musculature that inhibits their movement. They have weird, multi-cusped teeth quite different from those of adults: the cusps on the juvenile teeth might be short and blunt, or elongate and strongly curved, like a grappling hook [one tooth is shown in the image below]. During the time that she broods these altricial, hook-toothed babies, the mother changes: she grows a particularly thick layer of epidermis that is rich in lipids. And so the babies crawl over her, digging their hooked little teeth into her skin, peeling it off, and eating it (Kupfer et al. 2006). That's what's happening in the adjacent image. Autodermatophagy - the eating of one's own shed skin - is common among amphibians, but dermatotrophy as a form of parental care is unique and it means that, like mammals, caecilians have evolved a sophisticated provisioning of the young by the mother. It might seem a totally unexpected discovery, but in fact maternal provisioning of the young was actually predicted by Alexander Kupfer and colleagues some years prior to its observation.

This isn't the end of the story. As mentioned a moment ago, some caeciliids are viviparous and give birth to well-developed young. But while in the ovidict, these babies possess unusual specialised teeth - quite similar to those used in dermatotrophy by B. taitana - that allow them to feed on the oviduct lining (a habit termed matrotrophy). These teeth are shed soon after birth. The discovery of specialised juvenile teeth in oviparous caeciliids now suggests that the teeth of matrotrophic species are exaptations from dermatotrophic ancestors: in other words, that the viviparous species that eat oviduct lining descend from oviparous species that ate maternal epidermis. It's therefore implied that dermatotrophy and the specialised teeth required for it were phylogenetically widespread in caecilians, extending back in the group's history to the Cretaceous and beyond (Kupfer et al. 2006). Many questions have been raised by this remarkable series of discoveries and we can look forward to hearing more about them in the future [apologies to all the other bloggers, like Carel, who covered this discovery when it was published in 2006].

The typhlonectids

Typhlonectids are aquatic and semiaquatic teresomatans of the American tropics, represented by five genera and 13 species. Due to the prevalence of one species (Typhlonectes natans) in the pet trade, they are (ironically) among the most familiar of caecilians [adjacent T. natans photo by Neil Phillips]. Uniquely, their embryonic gills have evolved into strange sac-like structures and a dorsal fin-like structure is present on the posterior part of the laterally compressed body (the exception is Nectocaecilia petersii from Venezuela, which lacks both lateral compression and a fin-like structure). Typhlonectids don't appear to protrude their tentacles and their tentacular opening is small, they lack scales, and they're viviparous, giving birth to fully metamorphosed babies.

Often imagined to be free-swimming animals that might hide in debris or under stones, wild typhlonectids inhabit aquatic mud burrows, though Nectocaecilia can travel across land and is best described as semiaquatic. Atretochoana eiselti, named in 1965 but not given its own genus until 1995, is remarkable in being lungless (it is apparently unique among caecilians in this regard) and, at over 800 mm long, in being the largest known lungless tetrapod. It's assumed that Atretochoana is fully aquatic, but nothing is known of its ecology or lifestyle: only two specimens are known, and neither came with good locality data (Nussbaum & Wilkinson 1995, Wilkinson & Nussbaum 1997, 1999, Wilkinson et al. 1998). There's a picture of its head at the top of the part I article: compared to other caecilians, its skull is compressed dorsoventrally and a posteriorly located jaw articulation gives it a particularly wide gape (of course, we don't know whether it gapes its jaws wide when alive as no one has ever reported seeing one!).

So there we have it - a remarkable but very poorly known group of tetrapods that exhibit some astounding morphological and behavioural features. These two articles have been, of course, but an introduction to these wonderful animals, and we will definitely be visiting them again in the future. As I mentioned in the first article, there really aren't any good, readily-accessible comprehensive works on caecilians. The good news is that, thanks to the wonders of open access and science for all, you can obtain lots of the primary literature for yourself from several of the world's leading caecilian workers: for Mark Wilkinson's homepage go here, for David Gower's go here, and for G. John Measey's go here.

And if you're interested in amphibian conservation and didn't already know it, did I mention that 2008 is Year of the Frog?

Refs - -

Cannatella, D. C. & Hillis, D. M. 2004. Amphibians: leading a life of slime. In Cracraft, J. and Donoghue, M. (eds), Assembling the Tree of Life. Oxford University Press (Oxford), pp. 430-450.

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297, 1-370.

Gower, D. J., Dharne, M., Bhatta, G., Giri, V., Vyas, R., Govindappa, V., Oommen, O. V., George, J., Shouche, Y. & Wilkinson, M. 2007. Remarkable genetic homogeneity in unstriped, long-tailed Ichthyophis along 1500 km of the Western Ghats, India. Journal of Zoology 272, 266-275.

- ., Kupfer, A., Oommen, O. V., Himstedt, W., Nussbaum, R. A., Loader, S. P., Presswell, B., Müller, H., Krishna, S. B, Boistel, R. & Wilkinson, M. 2002. A molecular phylogeny of ichthyophiid caecilians (Amphibia: Gymnophiona: Ichthyophiidae): out of India or out of South East Asia? Proceedings of the Royal Society of London B 269, 1563-1569.

- . & Wilkinson, M. 2002. Phallus morphology in caecilians (Amphibia, Gymnophiona) and its systematic utility. Bulletin of the Natural History Museum, London (Zoology) 68, 143-154.

Kupfer, A., Müller, H., Antoniazi, M. M., Jared, C., Greven, H., Nussbaum, R. A. & Wilkinson, M. 2006. Parental investment by skin feeding in a caecilian amphibian. Nature 440, 926-929.

Nussbaum, R. A. & Wilkinson, M. 1995. A new genus of lungless tetrapod: a radically divergent caecilian (Amphibia: Gymnophiona). Proceedings of the Royal Society of London B 261, 331-335.

San Mauro, D., Gower, D. J., Oommen, O. V., Wilkinson, M. & Zardoya, R. 2004. Phylogeny of caecilian amphibians (Gymnophiona) based on compete mitochondrial genomes and nuclear RAG1. Molecular Phylogenetics and Evolution 33, 413-427.

Wilkinson, M. & Nussbaum, R. A. 1997. Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae). Biological Journal of the Linnean Society 62, 39-109.

- . & Nussbaum, R. A. 1999. Evolutionary relationships of the lungless caecilian Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae). Zoological Journal of the Linnean Society 126, 191-223.

- . & Nussbaum, R. A. 2006. Caecilian phylogeny and classification. In Exbrayat, J.-M. (ed.) Reproductive Biology and Phylogeny of Amphibia Volume 3. Gymnophiona. Science Publishers Inc., pp. 39-78.

- ., Sebben, A., Schwartz, E. N. F. & Schwartz, C. 1998. The largest lungless tetrapod: report on a second specimen of the lungless caecilian Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae) from Brazil. Journal of Natural History 32, 617-627.