Gymnophiona (Caecilians)

Andrew R Milner, Birkbeck College, London, UK

The order Gymnophiona (also sometimes called Apoda or Caecilia) is a group of highly specialized tropical fossorial (burrowing) amphibians. Because most are burrowers, they are rarely seen and, until the last two decades, little was known of their biology. They have no widely used common names and are generally called caecilians. They are found in tropical South America, Africa, the Seychelles, the Indian subcontinent and parts of southeast Asia, but are absent from Madagascar and Australasia.

Introductory article
Article Contents
. Basic Design . Diversity and Lifestyles . Fossil Record and Phylogeny

Basic Design
Caecilians share the characteristics of Lissamphibia including a pulmocutaneous circulatory system associated with respiratory gas exchange through the skin, toxinsecreting granular glands in the skin, pedicellate teeth, very reduced straight ribs, and vertebrae composed predominantly of membrane bone without a cartilage precursor. Caecilians resemble earthworms supercially, having long, apparently segmented, bodies, tiny eyes and no tympana, no limbs or girdles, and a short or absent postcloacal tail. The skin is smooth and contains mucous and granular glands. It is arranged in annuli (rings) separated by annular grooves which range from two per segment in primitive caecilians to one per segment in advanced forms. In primitive caecilians, these grooves contain rows of thin bony disc-like dermal scales, homologous to the dermal scales of shes. Such scales are absent in other living amphibians and in various advanced caecilians, having apparently been lost more than once. The skull is highly modied, apparently as a consequence of the role of the head in burrowing. It is fairly compact and cylindrical, and several elements fuse during development. The orbit is tiny and ahead of it is the tentacular fossa for a sensory tentacle, this opening sometimes being larger than the orbit, and sometimes conuent with it. The skull roof is solid, without temporal fossae, except in the primitive Rhinotrematidae. The palate is dominated by a broad parasphenoid and the occiput is largely made up of a single composite os basale. Advanced caecilians have a long retroarticular process on the mandible. This is associated with a unique jaw-closing mechanism in which the jaw is closed by a downward and backward pull on the retroarticular process by the muscularis interhyoideus, which arises from the lower trunk wall. The dentition is unusual in that there is a double row of teeth on upper and lower jaws. The upper tooth rows are on the premaxillae and maxillopalatine outer edges, while the inner tooth row is on the vomers and inner maxillopalatine ramus. On the lower jaws, the outer tooth row is on the dentary and the inner tooth row is on the splenial. These tooth rows interlock, the dentary row

between upper rows, to give a crimping bite. The teeth are pedicellate as in most lissamphibians, but vary greatly in crown structure. Some are bicuspid the typical lissamphibian condition but others are monocuspid. They are frequently curved medially and have sharp cutting edges. In viviparous forms, the fetus has a distinctive dentition in which the crowns are spatulate with 516 tiny spiky cusps per tooth. The eyes are reduced but are always functional as lightsensitive structures. The lens varies from functional to absent and some of the musculature may be lost, but parts of the optical system are modied to support a sensor that is characteristic of the group the sensory tentacle, found in a pit just ahead of the orbit. The sensory tentacle is olfactory and can be extended ahead of the animal. Its retractor muscles and innervation are modied from those found in the orbits of other vertebrates and it is lubricated by the Harderian gland, squeezed by the levator bulbi muscle. In scolecomorphids, the association is so close that the eye is embedded in the tentacle and can be protruded with the tentacle. The trunk is long, 95285 trunk vertebrae, and the postcloacal tail varies from 12 vertebrae in length in primitive forms to absent in most advanced forms in which the cloaca is terminal. The ribs are small and doubleheaded. There is no trace of pectoral or pelvic girdles, or limbs, in any modern caecilian. The fundamental locomotor mechanism appears to be internal concertina-crawling in burrows and lateral undulation on the surface. Aquatic typhlonectines use only lateral undulation. The internal concertina-crawling is, in part, powered hydrostatically by vertical body muscles squeezing body uid and causing the body to become rigid and elongate. A crossed-helix array of tendons turns this pressure into a powerful forward thrust of the head, necessary for pushing through soil. Respiration may be by buccopharyngeal, cutaneous and/or pulmonary gas exchange. Caecilians vary between possession of symmetrical lungs, asymmetrical lungs, one lung or no lungs. Buccopharyngeal breathing is certainly fundamental for the group but the long body does provide a more favourable surfacevolume ratio for cutaneous exchange than in most amphibians.
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Gymnophiona (Caecilians)

Fertilization is internal, the male having an intromittent organ comprising an eversible cloaca. Primitive caecilians lay large yolky eggs in a burrow in wet ground near streams, sometimes guarding the eggs until they hatch. The larvae are aquatic and retain a lateral-line system, one or more pairs of gill slits but do not have external gills. In advanced caecilians, viviparity predominates, with up to 20 young developing in the mothers oviducts. The fetuses respire by large external gills which are appressed to the vascular oviduct wall of the mother. When their yolk sacs are exhausted, they continue to feed by rasping at secretory tissue in the mothers oviduct wall, which produces a milklike nutrient. The fetal dentition is an adaptation for this. They metamorphose before birth, losing the gills and larval teeth and acquiring the adult dentition.

gills that are resorbed before birth. Typhlonectines are believed to be secondarily aquatic and derived from burrowing caeciliid ancestors.

Fossil Record and Phylogeny

Morphological analysis of the relationships of living amphibians suggests that caecilians are slightly more distantly related to frogs and salamanders than the latter groups are to each other, whereas molecular analyses indicate that caecilians are closer relatives of salamanders. They might have diverged from other amphibians at any time between the late Permian and the end of the Triassic. The earliest fossil form is Eocaecilia from the Lower Jurassic Kayenta Formation of Arizona. This was already a long-bodied burrower, with a caecilian-type skull bearing a tentacular fossa. However, it retained girdles and small limbs, pleurocentrum-dominated endochondral vertebrae and several primitive skull elements lost in modern forms. The only later fossils described to date are isolated caeciliid-type vertebrae from the Mid-Cretaceous of the Sudan and the Palaeocene of Brazil and Bolivia. All our understanding of caecilian phylogeny comes from analyses of the modern taxa. Diversication of the caecilian crown group appears to have largely taken place in Gondwana during the Mesozoic. The presence of caecilians on the Seychelles a Gondwanan platelet isolated since the Cretaceous is the most obvious testimony of this. The most primitive living family is the South American Rhinatrematidae, which retains temporal fossae between the parietals and squamosals like other lissamphibians but unlike other caecilians. It is followed by an Asian clade comprising the Ichthyophiidae and Uraeotyphlidae which share with higher caecilians the possession of a solidly roofed skull. All three families retain short tails and dermal scales and all are oviparous with aquatic larvae. The higher caecilians, the scolecomorphids and caeciliids, have gained a long retroarticular process on the mandible and lost or fused the pterygoid in the palate. They have all lost the tail and most have lost the scales; most are viviparous though some caecilids remain oviparous. It appears that the South American rhinotrematids, the Asian ichthyophiids and uraeotyphlids, and the African scolecomorphids are the relicts of a rst radiation within Gondwana, while the Caeciliidae represent a second radiation, overlapping all the more primitive families in range. Both radiations took place before the separation of South America, Africa, the Seychelles and India as evidenced by their present distributions. The southeast Asian ichthyophiids are assumed to represent range extensions from India after it fused with the rest of Asia in the late Cretaceous or early Tertiary.

Diversity and Lifestyles

In 1995, caecilian diversity was estimated at 164 species. Most species grow to 300 mm but some reach only 50 mm and one species of Caecilia reaches 1500 mm. Most live in wet soil or leaf-litter and are opportunistic carnivores, feeding on worms, arthropods and small vertebrates. Caecilians have skin toxins but are recorded as prey for snakes and birds. Five families are recognized, four being small families, all more primitive than the Caeciliidae, and all endemic to specic continents. The Rhinatrematidae are small burrowing forms from South America. Where known, they have aquatic larvae. The Ichthyophiidae and Uraeotyphlidae are smallmedium burrowers from India (both families), Sri Lanka and southeast Asia (ichthyophiids). They lay large yolky eggs and have aquatic larvae. The Scolecomorphidae is a small family of medium-sized viviparous burrowers from subSaharan Africa. It is monogeneric, comprising the highly derived genus Scolecomorphus, which has a very modied skull suggestive of a dierent burrowing mechanism. The Caeciliidae is a large and diverse family found across tropical South America, Africa, the Seychelles and the Indian subcontinent. It contains about two-thirds of the known species and is currently divided into three subfamilies: the Caeciliinae for a few South American genera with enlarged upper marginal dentition; the Typhlonectinae for a group of specialized aquatic genera, also from South America (see below); and the Dermophinae which is a large, rather miscellaneous, grade of genera of obscure relationships. The family diversity extends to patterns of reproduction, including both oviparous and viviparous forms. Members of the subfamily Typhlonectinae are large (700 mm) aquatic caeciliids. The posterior trunk is laterally compressed for swimming. Despite their aquatic lifestyle, they do not have free-living larvae. They are viviparous, with the young developing in the oviduct and respiring through unique large membranous external
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Gymnophiona (Caecilians)

Further Reading
Billo R and Wake MH (1987) Tentacle development in Dermophis mexicanus (Amphibia, Gymnophiona) with an hypothesis of tentacle origin. Journal of Morphology 192: 101111. Duellman WE and Trueb L (1986) Biology of Amphibians. New York: McGraw-Hill. Evans SE, Milner AR and Werner C (1996) Sirenid salamanders and a gymnophionan amphibian from the Cretaceous of the Sudan. Palaeontology 39: 7795. Hedges SB, Nussbaum RL and Maxson LR (1993) Caecilian phylogeny and biogeography inferred from mitochondrial DNA sequences of the 12S rRNA and 16S rRNA gene. Herpetological Monographs 7: 6476. Jenkins FA and Walsh DM (1993) An early Jurassic caecilian with limbs. Nature 365: 246250.

OReilly JC, Nussbaum RA and Boone D (1996) Vertebrate with protrusible eyes. Nature 382: 33. OReilly JC, Ritter DA and Carrier DR (1997) Hydrostatic locomotion in a limbless tetrapod. Nature 386: 269272. Summers AP and OReilly JC (1997) A comparative study of locomotion in the caecilians Dermophis mexicanus and Typhlonectes natans (Amphibia: Gymnophiona). Zoological Journal of the Linnean Society 121: 6576. Wake MH (1977) Fetal maintenance and its evolutionary signicance in the Amphibia: Gymnophiona. Journal of Herpetology 11: 379386. Wake MH (1985) The comparative morphology and evolution of the eyes of caecilians (Amphibia, Gymnophiona). Zoomorphology 105: 277295.

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net