Did I mention that 2008 is the Year of the Frog? Well, believe it or don’t, another major conservation effort directed at the world’s amphibians kicks off in January 2008, and in an effort to bring all you wonderful Tet Zoo readers up to speed on amphibian diversity before it launches, we need to get through ALL of the world’s amphibian groups first. But that’s not as bad as it sounds. Besides anurans – which we’ve nearly covered in entirety – there are only two other groups, and here we look in detail at one of them.
With apologies to those who already have privileged knowledge…. if I told you that there was a group of living tetrapods that have sensory tentacles, sometimes sport protrusible eyes, sometimes lack eyes entirely, often exhibit sophisticated parental care and may even feed their babies on a specially grown layer of nutritious epidermal skin, are incredibly long-bodied yet often lack tails, and sometimes possess large, anatomically complex, eversible male sexual organs, you might wonder which recreational drugs I was taking. The fact is, I’m talking about a very real – albeit very poorly known – group of living tetrapods: the caecilians.
All extant caecilians (pronounce it ‘say-see-lee-un’) are long-bodied, limbless, superficially worm-like amphibians with reduced eyes. They are predominantly fossorial (adapted for burrowing), although some are aquatic or semiaquatic and some terrestrial species have aquatic larvae. Limb girdles are entirely absent and skin folds (annulae) encircle the body. Despite their mostly fossorial habits some species are visually striking, being blue, purple, green, bright orange, yellow, or with bright yellow lateral stripes [image of bright orange caeciliid Schistometopum thomense from the Gulf of Guinea shown below]. Others are decorated with blotches, or have a head that is lighter in colour than the body. Poison glands are present (some species may even be quite toxic to humans), so it’s likely that the bright colours are aposematic. While the smallest species (like the caeciliid Idiocranium russelli from Cameroon) are mature at just 70 mm, the largest – the very slender-bodied Caecilia thompsoni from Colombia – reaches 1.5 m [C. thompsoni shown in adjacent image; photo by Taran Grant].
In the most primitive living caecilians (the South American rhinatrematids), a short tail is present and the mouth is located at the front of the head; in the more advanced groups no tail is present and the mouth is situated further back, slung underneath the head. It’s mostly assumed that caecilians are generalist predators of soil invertebrates such as earthworms, ants and termites – animals that have been termed ‘soil ecosystem engineers’ by ecologists. However, it’s also been argued that some caecilians are specialists (preying specifically on termites, earthworms or beetle pupae), or even detritivores, ingesting leaf humus and other plant fragments (Hebrard et al. 1992). This last proposal would be radical given that amphibians are essentially all carnivorous as adults, and a later study showed that soil and detritus recovered from the gut contents of the species concerned (the east African caeciliid Boulengerula taitana) originated from its earthworm prey (Gaborieau & Measey 2004). Small vertebrates including frogs, lizards, burrowing snakes (Presswell et al. 2002) and possibly rodents sometimes fall prey to the larger species. Caecilians themselves are preyed upon by burrowing snakes, fish (Gazola Da Silva et al. 2007), and by introduced animals like chickens, pigs and the tenrecs that have been introduced to the Seychelles.
Caecilians occur throughout the humid tropical regions of the world: in South America, equatorial eastern and western Africa, and tropical Asia including the Philippines and the western Indo-Australian archipelago. They also inhabit the Seychelles. The absence of caecilians from central equatorial Africa and Madagascar is odd and we should consider the possibility that they might await discovery in these areas. Generally assumed to be rare and highly elusive, some studies have shown that at least some caecilian species can be abundant if searched for (Measey 2004), and in fact present in sufficient numbers to be (presumably) ecologically significant, especially so given their effects on soil ecosystem engineers (Jones et al. 2006).
It stands to reason that, because of their fossoriality, we know relatively little about caecilians, and because many species are poorly known and poorly represented in zoological collections, confusion about their systematics and taxonomy has been rife. A nice example is provided by the tropical American caeciliid Gymnopis* syntrema: in a paper subtitled ‘a comedy of errors’, Nussbaum (1988) argued that ‘six different binomial names have been applied to this species; it has been assigned to seven genera, two subfamilies of a single family, and three families’ (p. 921). Currently, 33 genera and about 175 caecilian species are recognised, so this isn’t a huge group. Until 1968 all caecilians were united in one ‘family’ – Caeciliidae** – but later work by Edward H. Taylor (read on) and Ronald A. Nussbaum proposed that this should be divided into six ‘families’ (Rhinatrematidae, Ichthyophiidae, Uraeotyphlidae, Scolecomorphidae, Caeciliidae and Typhlonectidae). Multiple other families and other suprageneric groups were recognised by a few authors during the 1980s, but were later rejected as artificial or erroneous (Nussbaum & Wilkinson 1989). Frost et al. (2006) argued for a new classification where only three ‘families’ are recognised, but in a major recent review Wilkinson & Nussbaum (2006) continued to use all six.
* Not a typo, though of course some workers have inadvertently spelt it Gymnophis [sic].
** Little known is that a family of psocopteran insects has also been called Caeciliidae, and it was recommended by the ICZN that the caecilian group therefore go by the older spelling Caeciliaidae (psocopterans are booklice, bookflies and so on. I keep lots of them in my office). Nussbaum & Wilkinson (1989) argued that this decision was inappropriate because Rafinesque, the author of Caeciliaidae, never associated any generic name with this group (he only named it for an Italian vernacular name: ‘Ceciliani’), nor did he specify its intended content. Despite these objections, Nussbaum & Wilkinson (1989) continued to use Caeciliaidae following the ICZN’s ruling, although other authors did not. In 1996 the ICZN changed the ruling such that Caeciliidae became reinstated for the amphibians; the alternative name Caeciliusidae is now used for the psocopterans (Wilkinson & Nussbaum 2006). A caeciliusid is shown in the adjacent image – perhaps the only non-tetrapod I’ve featured so far on Tet Zoo.
There are very few good non-technical sources where you can read up on caecilians: the only one I can readily recommend is Nussbaum (2000). A major volume devoted entirely to caecilians, Taylor’s 1968 848-pp The Caecilians of the World: A Taxonomic Review, is cited in just about every bit of caecilian literature and proved instrumental in initiating new interest in the taxonomy and phylogeny of the group. I thought about getting hold of a copy recently, but gave up when I discovered that it can’t be obtained for less than £138 ($275). A German book, Die Blindwühlen, was published on the group in 1996 (Himstedt 1996), and a French one – Les Gymnophiones, ces curieux Amphibiens – in 2000 (Exbrayat 2000) [image above shows someone's pet Ichthyophis].
Tentacles and protrusible eyes
In some details, caecilian anatomy is surreal. Easily the weirdest features have to be the tentacles: unique to the group, these are paired sensory structures that emerge from a cavity on the side of the snout between the eye and nostril. They are always quite easy to see, even in the smallest species (in the image above of a captive Ichthyophis, you can see the pale tip of the retracted tentacle half-way between the eye and nostril). No other tetrapod has anything like this. Derived from the tear duct, extrinsic eye muscles and other orbital structures, the tentacles are connected to the vomeronasal organs and presumably allow the animals to test their environment for sensory clues.
The caecilian skull is generally bullet-shaped, robust, thick-boned and with strongly adhering skin [adjacent image, showing the skull of the American caeciliid Dermophis mexicanus, is from DigiMorph]. Their recurved teeth are sometimes sharp-keeled and bicusped (but wait for part II). The eyes of caecilians are sometimes visible beneath the skin and set within bony sockets (e.g., Ichthyophis), are sometimes hidden beneath the bones of the skull (e.g., Scolecomorphus), and are sometimes completely absent (e.g., Boulengerula). While the tentacle is often located close to the nostril and some distance from the eye, the eye and tentacle are close in position in some species. Scolecomorphids, containing only Scolecomorphus and Crotaphatrema, are unique to equatorial Africa and have a particularly large tentacular opening located near the tip of the snout, ahead of the under-slung mouth. The close position of the eye and tentacle mean that they’ve become connected: in its resting position, the eye is located beneath the lateral surface of the skull, but full extrusion of the tentacle causes the eye to move out of the skull and down the tentacle (O’Reilly et al. 1996). An area of the tentacle lacking in pigmentation presumably allows light to reach the retina. Scolecomorphids are the only tetrapods that can deliberately move their eyes out of their skulls. Scolecomorphids are also unusual in lacking a stapes.
Caecilians are also unique in that they have two sets of jaw-closing muscles: in addition to the adductor mandibulae muscles that are located at the back of the jaws, they also use their interhyoideus posterior muscles in jaw closure. These muscles are located in the neck and are attached to the retroarticular process at the posterior end of the lower jaw: they close it by pulling down and backwards on the retroarticular process (Nussbaum 1983). Other tetrapods possess interhyoideus posterior muscles, but they aren’t used in jaw closing, so why have caecilians co-opted them for this use? The answer might be that, in evolving a rigid, box-like skull specialised for burrowing, caecilians have had to reduce and close the temporal fossae that originally housed the adductor mandibulae muscles. To compensate for the weakened power provided by the now reduced adductor mandibulae, caecilians have switched to using the interhyoideus posterior as well – a classic example of exaptation (where an existing structure is co-opted for a new function) [adjacent image, from Wilkinson & Nussbaum (2006), shows the variation in caecilian cranial and interhyoideus posterior morphology].
Of course, this isn’t where it ends – we still have the weird sexual organs to look at yet, plus the stegokrotaphy, zygokrotaphy, the whole ‘out of India’ thing, the viviparity, dermatotrophy and matrotrophy, and the biggest lungless tetrapod ever (the bizarre Atretochoana, shown at the very top of the article). Be sure to tune in to the next thrilling installment of Tetrapod Zoology!
Refs – –
Exbrayat, J.-M. 2000. Les Gymnophiones, ces curieux Amphibiens. Edition Boubée, Paris.
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.
Gaborieau, O. & Measey, G. J. 2004. Termitivore or detritivore? A quantitative investigation into the diet of the east African caecilian Boulengerula taitanus (Amphibia: Gymnophiona: Caeciliidae). Animal Biology 54, 45-56.
Gazola Da Silva, F. F., Mott, T., Garey, M. V., & Vutule, J. R. S. 2007. Chthonerpeton viviparum Parker & Wettstein, 1929 (Amphibia, Gymnophiona, Typhlonectidae) in Paraná state, Brazil and the first record of predation of this species by Hoplias malabaricus (Bloch, 1794) (Actinopterygii, Erythrinidae). Pan-American Journal of Aquatic Science 2, 261-262.
Hebrard, J., Maloiy, G. & Alliangana, D. 1992. Notes on the habitat and diet of Afrocaecilia taitana (Amphibia, Gymnophiona). Journal of Herpetology 26, 513-515.
Himstedt, W. 1996. Die Blindwühlen. Westarp, Magdeburg.
Jones, D. T., Loader, S. P. & Gower, D. J. 2006. Trophic ecology of east African caecilians (Amphibia: Gymnophiona), and their impact on forest soil invertebrates. Journal of Zoology 268, 117-126.
Measey, G. J. 2004. Are caecilians rare? An east African perspective. Journal of East African Natural History 93, 1-21.
Nussbaum, R. A. 1983. The evolution of a unique dual jaw-closing mechanism in caecilians (Amphibia: Gymnophiona) and its bearing on caecilian ancestry. Journal of Zoology 199, 545-554.
– . 1988. On the status of Copeotyphlinus syntremus, Gymnopis oligozona, and Minascaecilia sartoria (Gymnophiona, Caeciliidae): a comedy of errors. Copeia 1988, 921-928.
– . 2000. Caecilians. In Cogger, H. G., Gould, E., Forshaw, J., McKay, G. & Zweifel, R. G. (consultant eds) Encyclopedia of Animals: Mammals, Birds, Reptiles, Amphibians. Fog City Press (San Francisco), pp. 492-499.
– . & Wilkinson, M. 1989. On the classification and phylogeny of caecilians (Amphibia: Gymnophiona), a critical review. Herpetological Monographs 3, 1-42.
O’Reilly, J. C., Nussbaum, R. A. & Boone, D. 1996. Vertebrate with protrusible eyes. Nature 382, 33.
Presswell, B., Gower, D. J., Oommen, O. V., Measey, G. J. & Wilkinson, M. 2002. Scolecophidian snakes in the diets of south Asian caecilian amphibians. Herpetological Journal 12, 123-126.
Wilkinson, M. & 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.