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Benjamin T. Swan

Scott Wright

Biology 117-002

Spring 2009

Animal Diversity: Order Gymnophiona

Odd Amphibian Out: On the Diversity of Order Gymnophiona

Everything about Order Gymnophiona would seem to conspire to make them as non-

descript and forgettable as possible. The third branch of Class Amphibia, they are neither highly

speciose (making up approximately 4% of amphibian species), nor particularly prominent in

literature. Modest in appearance, they all resemble large worms or, alternately, eyeless snakes,

and live out their lives either as subterranean (fossorial) or, in some groups, aquatic predators. To

further compound matters, caecilians are confined to the tropics, and even there many are elusive

enough that experienced researchers may go years without encountering a single specimen of a

species. Indeed, many species are known by only one example, sometimes decades nor nearly a

century old. Yet, despite these factors, what sparse investigations have been made into this order

have found a highly adapted, quite curious group with a number of compelling derived features

which are well worthy of study, not only for their own merit, but also for what they may tell us

about the process of evolution.

Caecilians are thought to be a quite ancient group with origins dating to more than 120

million years ago. This would place them on the super-continent of Gondwana, with

fragmentation of that land mass providing for the order’s current wide tropical distribution.

(Jared, Navas, & Toledo, 1999) The earliest known specimen that can be confidently grouped with the

caecilians would be the Lower Jurassic’s Eocaecilia, which, while retaining modest limbs, displays many

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characteristics of the order, including a highly elongated body and, most tellingly, a skull morphology

which is strikingly reminiscent of that which allows for current caecilians to utilize the interhyoideus

posterior as the key jaw-closing muscle. Of the far later Paleozoic amphibians, the best candidate for

ancestral statues is the Rhynchonkos, a lepospondyl microsaur possessing an elongated body, reduced

limbs, and familiar skull. Paleontologist Robert Carroll summarized: “If we limit our consideration to the

caecilians, certainly their most parsimonious origin is from this microsaur.” (p. 1207).

Geographic Range and Habitat

Gymnophiona is a tropical order widely distributed across four continents as well as many

islands and island groups. Broad but not contiguous ranges may hint to a wider spread earlier in

the group’s history, with later events limiting zones of habitation. Family Caeciliidae, the largest

of the order with around 100 species (55% of all described caecilians) within 21 genera, occupies

a large expanse, from the tiny Seychelles Islands, through the Indian subcontinent and Africa, all

the way to South and Central America. The more basal and often aquatically inclined

Ichthyophiidae make up 2 genera and 29 species, all in Asia, from the Indian subcontinent and

Sri Lanka out through Southeast Asia, then island hopping through Borneo, Sumatra, and the

Philippines. Resembling the Ichthyophiidae and equipped with a tail, Uraeotyphlidae’s single

genus of 5 species is known only in southern India. The 2 genera and 6 species of

Scolecomorphiidae occupy a range along the coasts of central Africa, bifurcated by the great

continental interior. The short tailed burrowers of Rhinatrematidae, encompassing 9 species in 2

genera, dwell in South America. The other family endemic to the Americas, Typhlonectidae, is

the group of caecilians most closely associated with an aquatic lifestyle, and has 13 species of 5

genera distributed disjunctly in northern Argentina, southern Brazil, and the northern end of

South America. (Wells, 2007; Taylor, 1968)

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Caecilians can be found occupying a variety of habitats within their respective ranges, the

simple rule of thumb being that there must be sufficient moisture present to allow for easy

burrowing and forestall rapid dehydration through their water-permeable skin. Most species are

primarily terrestrial (fossorial), though some are adapted to aquatic life, and may live from sea-

level locations to those of moderate elevation, stalking through leaf litter, under rocks and logs,

and, naturally, underground. Oviparous species must obey the additional stricture of being able

to have ready access to streams and ponds for the development of their larvae, commonly laying

eggs in muddy burrows or under rocks or logs at the head of small springs. Ovoviviparous and

viviparous forms have no such direct dependence upon water. (Taylor, 1968; Jared, Navas, &

Toledo, 1999) Examinations of populations of I. cf. kohtaoensis provide evidence for some

degree of seasonal migration to accompany the tropical rainy and dry season cycles. This

includes horizontal migration to areas retaining significant moisture (e.g. pond beds, swampy

ground) and perhaps vertical migration (retreating to greater soils depths with presumably more

moisture). (Kupfer, Nabhitabhata, & Himstedt, 2005)

Physical Description and Diversity

Caecilians are best described as having the physical appearance of an eyeless snake or a

massive earthworm. Cylindrical, elongated amphibians having from 95-2851 vertebrae capable of

movement in any direction, all caecilian are limbless, lacking even any hint of a pelvic or

pectoral girdle. (Wells, 2007) Families considered more basal- Icthyophiidae, Rhinatrematidae,

and Uraeotyphlidae- possess a true tail (having both vertebrae and annular grooves), though the

more derived Caeciliaidae does not. (Jared, Navas, & Toledo, 1999) A lengthy body has left

caecilians with some notably pinched and extended organs, including the testes and lungs (the

1 Renous and Gasc give a mode of 100-110

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latter being some 50-75% of body length), with the left lung being severely reduced or absent

(similar to what is seen in some snakes). (Wells, 2007; Smits & Flanagin, 1994) Most are

moderately sized, though species may range from miniaturized forms such as the 100 mm

Idiocranium russeli2 to the impressive 1.5 m Caecilia thompsoni. (Wells, 2007) Although largely

fossorial, more aquatic variants, such as the Typhlonectes and Potomotyphlus of Typlonectidae

have significant morphological adaptations to such environs, including a “fin-like” laterally

flattened posterior body. Although none of the caecilians could be described as specialized

swimmers, some can stay immersed for up to 100 minutes (at 25 C).⁰ (Jared, Navas, & Toledo,

1999)

The integument is thickened and consists of two layers: the stratum spongisum (an outer

layer with mucous and granular glands, dermal scales, and chromatophores) and the stratum

compactum. Mucous secretions are hydrophilic, aiding in underground movement, moisture

retention, and trans-cutaneous respiration. Some Caeciliaidae, Ichthyophiidae, and T.

compressicaudus bear dermal scales which, in addition to providing protection, serve for

retaining water and adding a degree of rigidity and pressure for glandular excretions. (Jared,

Navas, & Toledo, 1999)

Caecilian skulls are well adapted to their burrowing lifestyle, being quite ossified, with a

judicious combination of bone fusion and loss giving a strong, flattened form for digging.

(Wells, 2007) All species show well developed sets of teeth in either three or four series (the

premaxillary-maxillary, prevomeropalatine, dentary [mandibular], and sometimes splenial), the

number of which is variable by species and genera. (Taylor, 1968) Teeth of the crown and

2 This is similar to the miniaturization phenomenon known in other amphibians. I. russeli also exhibits paedomorphism by means of retained vertebral and skull cartilage and the absence of certain late-developing bones. (Wells, 2007)

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pedicel are incurved and placed in single ranks, made for catching and holding onto prey during

eating. The number of teeth usually increases with age, probably allowing for the pursuit of

larger prey. The tongue itself is non-protrusible and of limited mobility, probably serving little

function in hunting. (Jared, Navas, & Toledo, 1999)

An interesting feature of caecilian skull morphology is the significant cranial kinesis

(streptosyly) in the quadrate-squamosal apparatus. This would appear to serve as a derived

mechanism for improving the magnitude of jaw closing force, and providing an alternative

closure mechanism in addition to the of the adductor muscles. The hypaxial muscle

(interhyoideus posterior) directs a ventro-posterior force on the retroarticular process of the

lower jaw. There are several probable advantages to such an adaptation. Research has shown that

this allows for the exertion of jaw closing force even when the mouth is nearly or entirely closed.

As tunnellers, caecilians must consider the extra effort required to burrow a tunnel wide enough

to allow for the passage of any protrusions, such as hypertrophied3 jaw muscles. This problem

has been effectively bypassed by the caecilians by investing in this interhyoideus

posterior/retroarticular system for strong jaw closing, then enclosing more limited adductor

muscles in bone, giving a streamlined profile favorable for digging. Additionally, as there is a

usually a tradeoff between bite speed and power, the caecilian, by possessing two separate

mechanisms, can specialize one (the IHP-RA) for strength, and the other (the adductors) for

speed. As a final bonus, the IHP-RA has been shown to be a very efficient leverage system,

being estimated at having a transmission efficiency of 90% or more. (Summers & Wake, 2005)

Respiration

3 Grown abnormally large.

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The respiration of Gymnophiona is complex and has been the subject of some research

interest. As befits an amphibian, most species utilize a combination of lungs, integument, and

gills in breathing, with the relative contributions of each varying by species, environment, and

life stage. (Jared, Navas, & Toledo, 1999) Although most have bilateral lungs, one is severely

reduced (no more than 10% of body length), leaving only one functional, usually, though not

always, the left4. (Jared, Navas, & Toledo, 1999; Smits & Flanagin, 1994) Terrestrial species

typically bear, “complex, clearly compartmentalized lungs and a highly vascularized

epithelium.” (Smits & Flanagin, 1994, p. 317) Breathing is like that in other amphibians, with

repeated buccal cycles used to inflate the elongated lung to a great pressure, followed by an

extended breath hold, and finally a single, passive exhalation. (Smits & Flanagin, 1994) This

breath cycle can be quite prolonged, with D. mexicanus being witnessed to breathe only once

every 5-15 minutes when at rest. (Bennett, Summers, & Brainerd, 1999) The inflation of this

rather long lung may be abetted by the series of cartilaginous rings reported in some species.

Observed caecilians do not ventilate and move simultaneously, perhaps being incapable of

concurrently using both trunk lucomatory muscles and those operating the elongate lung. (Smits

& Flanagin, 1994) Passive exhalation is currently thought to be universal in the order, loss of

active exhalation being a derived trait (similar to as seen in frogs) that is suspected to be resultant

of their unique locomotion. (Bennett, Summers, & Brainerd, 1999; Wells, 2007)

While CO2 release may occur mostly transcutaneously, consensus among researchers is

that most species rely primarily upon their lungs (used for up to 94% of oxygen uptake in T.

compressicaudus). Cutaneous exchange may be more substantial in water. (Jared, Navas, &

4 Examples from the aquatic family of Typhlonectidae show better development in the left lung, with lengths between 50-100% of the right lung. (Smits & Flanagin, 1994)

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Toledo, 1999) Caecilians have relatively thick skin for amphibians (a necessity in their tough

underground habitat), which is thought to be an impediment to efficient skin-breathing; however,

recent examination of skin thickness in terms of cell layers and epidermal thickness compares

favorably to those measured for eight North American urodeles, several of which are good skin-

breathers. (Smits & Flanagin, 1994) Study of the simultaneous contribution of lung and

cutaneous respiration both during rest and after exertion indicate that, while the two modes may

play nearly equal roles during rest, post exercise the rate of pulmonary uptake increases by many

times the rate of cutaneous respiration, perhaps an indication that caecilians are capable of

preferentially altering rates of blood perfusion between pulmonary and systemic (cutaneous)

arteries (which, like other amphibians, are connected in parallel to a single ventricle). In

Typhlonectes, during rest, 55% of O2 uptake was pulmonary, the rest presumably through

cutaneous respiration. The skin was the sight of most CO2 elimination (88%). Rates after

exercise changed little for cutaneous respiration (16 ±0.8 vs. 13.5 ±1.0 µL/g*hr) versus the

dramatic spike in pulmonary respiration (16 ±3.2 vs. 362 ±31 µL/g*hr). (Smits & Flanagin,

1994)

Adaptations to what are usually hypoxic and hypercampic5 underground and aquatic

habitats seem to have equipped caecilians with a relatively efficient respiration system. In terms

of blood properties, when measured (in T. compressicauda and B. taitanus), hematocrits6 and

hemoglobin concentration have been found to rank among the some of the highest known in

amphibians. This correlates with very high estimates of total blood volume (24-46% body mass

in Typhlonectes) to provide evidence for exceptional blood O2 storage capacity. Study of average

5 CO2 laden.6 Portion of blood volume occupied by erythrocytes.

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metabolic rates have shown a strikingly low resting rate7, doubtless an advantage in oxygen

deprived environments. This metabolic rate is remarkable within Amphibia: “…a 10g caecilian

consumes approximately 0.26 mL of O2 per hr, which is less than half that of an average anuran,

and substantially less than that of urodeles.” (Smits & Flanagin, 1994, p. 250) In the same study,

caecilians, defiant of their usual description as inactive, were found to be quite capable of

achieving high metabolic rates. For all species examined, recovery from exercise was quick , and

factorial increases in respiration rates over resting compare favorably with those observed in

salamanders and anurans of 5.0 (range 1.6-14.5) and 12 (range 4.2-35.2), respectively. Caecilians

were measured at an average of 12.1 (range 9.7-14.1) without including cutaneous VO2, the

researchers noting, “…the average aerobic capacity of caecilians probably exceeds that of

anurans.” (Smits & Flanagin, 1994, p. 253)

Reproduction and Development

While there has been only limited work done upon actual breeding behaviors, order

Gymnophiona encompasses species with diverse reproductive strategies and life cycles, running

the gamut from oviparous species with aquatic larvae to viviparous forms using direct

development. A few generalizations can be given by family. Rhinatrematidae, commonly

regarded as most basal of the caecilians, seem to be entirely oviparous with free-swimming

aquatic larvae. The similarly primitive Ichthyophiidae shares these characters, but lay their eggs

adjacent to, rather than in, water, with nests under vegetation or in burrows, probably attended by

the mother. The terrestrial and fossorial family Caeciliidae, fitting for being largest and most

derived in Gymnophiona, displays the widest variety of reproductive modes, with oviparous and

7 Authors of the study conjectured that the very low activity level observed in resting caecilian in comparison to other resting amphibians may contribute to this result. When not burrowing, caecilians largely remained motionless with the exception of occasional breathing.

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viviparous species, some beginning as free-swimming aquatic larvae, while others undergoing

direct development after hatching. Perhaps most notably, some species are known to be

viviparous, a trait shared with the aquatic Typhlonectes and the African, terrestrial

Scolecomorphiidae. (Wells, 2007) When studied, both oviparous and viviparous species come

out as achieving sexual maturity at approximately 2 years of age in males and 3 in females.

(Kupfer, Nabhitabhata, & Himstedt, 2005)

Reproductive structures of caecilians are in some ways quite distinct. All species of the

order utilize internal fertilization (Taylor, 1968), with all males possessing a unique intromittent

organ, the phallodeum, which itself is developed from the modified posterior end of the cloaca.

(Wells, 2007) Likewise novel is the manufacture of fluid necessary for sperm and sperm nutrient

transport within the Müllerian glands. Müllerian ducts are present up to a point in the

development of all vertebrates, becoming oviducts within the female while effectively

disappearing in males. Male caecilians are distinct in retaining this structure as functional

Müllerian glands. (Wake, 1977) Additionally, males of some aquatic forms seem to have

developed special structures for engaging and holding a female during copulation, including

Typhlonectidae which have a grasping organ below the body terminus, and others which have an

anal area modified into a sucker-like device. (Taylor, 1968) There has also been some evidence

that females in at least one species, I. cf. kohtaoensis, may be capable of some degree of sperm

retention. (Kupfer, Kramer, Himstedt, & Greven, 2006)

Oviparous, Ovoviviparous Species and Larval Development

The majority of oviparous caecilians have an annual reproductive cycle, with perhaps

dependency upon some external or internal factors. Certain species (i.e. T. compressicaudus and

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D. mexicanus) are known to depend upon rain to ensure the proper, moist environment for

reproduction. Research on I. cf. kohtaoensis provides strong evidence for a reproductive cycle

connected to the rainy season, mating probably occurring just prior to the onset of the rains and

hatching in the late portion of the season. (Kupfer, Nabhitabhata, & Himstedt, 2005) Clutch sizes

may vary quite a bit between species, from 6 (Idiocranium russelli) to 100 (Ichthyophts

malabarensis, S. annulatus), though 20-50 is average. Stored energy, both in the liver and in fat

deposits (between 8 and 30 are found on each side), play an important role in allowing for

vitellogenesis (and intra-uterine development of large embryos). (Jared, Navas, & Toledo, 1999;

Kupfer, Wilkinson, Gower, Muller, & Jehle, 2008)

Eggs may be retained within enlarged oviducts for the fetal life (ovoviviparity) of the

young or deposited in nests, which may be in burrows or under logs or other debris, bordering a

water source, as a stream or pond. (Kupfer, Kramer, Himstedt, & Greven, 2006; Taylor, 1968) It

is likely that in most species the females attend their eggs, though direct observations have been

limited to one Ichthyophiidae species (seen to guard its eggs for up to 3 months) and some

Caeciliidae. (Kupfer, Nabhitabhata, & Himstedt, 2004; Wells, 2007) After hatching, young may

proceed with direct development to the adult form, or make their way into water to continue as

an aquatic, free-swimming larva for up to 50 weeks before metamorphosis. (Jared, Navas, &

Toledo, 1999) Field studies of the Kenyan Boulengerula taitanus found the hatchlings of this

oviparous species to be fed initially by the outermost, hypertrophied flesh of the mother. Such an

extended and considerable parental investment is rarely seen outside of birds and mammals, and

further research on this phenomenon may be helpful in understanding the evolution of parental

care across disparate phylogenies. (Kupfer, Wilkinson, Gower, Muller, & Jehle, 2008)

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The larvae in Gymnophiona tend to bear a closer resemblance, morphologically and

trophicly, to their adult form. Usually they are hatched well along in development, already

bearing lungs, with the gills having degenerated or doing so rapidly after hatching, leaving one

or two gills slits. Normally, a tail is present to assist aquatic locomotion which is, in non-aquatic

forms, lost during metamorphosis, a period which sees changes such as the ossification of the

relatively fragile larval chondrocranium. (Wells, 2007) When observed, the larval stage has been

seen to be a generalist predator occupying the aquatic equivalent of the trophic role of the adult.

(Kupfer, Nabhitabhata, & Himstedt, 2005) Survival and hunting are doubtless improved greatly

by a highly evolved lateral line sensory system, having both mechano-receptive neuromasts and

ampullary organs which are sensitive to the weak electric fields of living organisms. (Wells,

2007; Jared, Navas, & Toledo, 1999) These are covered more in discussion on perception.

Viviparous Species

One of the most interesting features of order Gymnophiona is that fact that approximately

half of all species examined have been found to be viviparous, an expansion into bearing live

young not comparable in any other amphibian group. From an evolutionary standpoint, the

achievement of viviparity appears to the end of long line of adaptations developing towards

preservation of the undeveloped young, from nest guarding, to egg retention, loss of an aquatic

larval form, and finally live birth. (Wake, 1977) Following this line of thought, viviparity is not

found among the most basal families, Ichthyophiidae and Rhinatrematidae (as well as

Uraeotyphlidae), but rather in some Caeciliidae, Scolecomorphiidae, and perhaps all

Typhlonectidae. (Wells, 2007)

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Caecilians feature significant adaptations to facilitate viviparity: the posterior oviduct has

been differentiated into a uterus and a glandular system aids in egg production. (Wake, 1977)

Although maternal support of the embryo does not involve placentation, in all viviparous

species, initial embryonic development is fuelled by a yolk reserve which, soon being exhausted,

is replaced with lipid-rich secretions of the oviduct walls. These are scrapped up by quick-

growing fetal teeth and consumed directly, with the scraping of the epithelium possibly

stimulating further secretions. In T. compressicaudus, a good example of viviparity, the embryo

is also nourished by oophagy (of unfertilized and degenerated oocytes) and adelphophagy (of

dead embryos). Gestation lasts for around 6 months with an average of 2-4 embryos surviving to

the final stage of development. (Jared, Navas, & Toledo, 1999) The embryonic stage of

Typhlonectus grows well-developed, sac-like gills to facilitate gas exchange across the uterine

wall. (Wells, 2007)

Sensory Perception

The domination of sub-terranian and aquatic environments in the caecilian’s lifecycle

results in very specific evolutionary pressures upon their sensory systems. Being mostly deprived

of long lines of sight or the open air, vision and hearing have largely been discarded by

Gymnophiona. On the other hand, tactile and olfactory (chemical) sensations are crucial to

survival, feeding, and communication, and are commensurately well developed. Of great interest

as well is the use of adaptive or unique sensory systems, such as the larval lateral line and the

caecilian tentacle.

The caecilian ear does not possess its own opening, but rather must act by allowing

vibrations to penetrate through skin and muscle and cause reverberations in a continuous fluid

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circuit via a stapedial footplate, with the end organ being an amphibian papilla. There is neither a

tympanic membrane nor a cavity. The hearing of one species (Ichthyophis orthoplicatus), when

tested in air, was found to be quite poor. The researchers attribute this to inadequate transduction

from air to tissue, and proposed that performance may be significantly better in an aquatic

environ. (Wever & Gans, 1976)

The degree of vision and eye loss is fairly variable among the species of Gymnophiona,

with more basal families (Rhinatrematidae and Ichthyophiidae) and aquatic forms normally

displaying the least reduction. (Jared, Navas, & Toledo, 1999) In initial embryonic stages, eyes

are similar to those seen in fully-sighted amphibians, with a retina comprised solely of rod cells.

Later stages of development are retarded to degrees distinguished by species, though a number of

regressions are common, including the covering of eye with skin and/or bone, reduction or loss

of the lens, and loss of muscles for eye control. (Wells, 2007) Nevertheless, many species are

thought to still possess some degree of photoreceptive capabilities, with larval hatchlings

displaying immediate positive phototaxis (possibly to aid in escaping the burrow nest), later

changing to negative phototaxis (presumably seeking shelter from predators). (Jared, Navas, &

Toledo, 1999)

Seemingly subsuming many of the faculties of the eye is a fascinating, unique caecilian

organ, the chemosensitive tentacle. Being protrusible from the side of the head and connected to

the vomeronasal olfactory system, the tentacle is served mechanically by muscles originally used

for eye movement, lubricated by the Harderian gland (whose secretions are usually reserved for

the eyes), and innervated by the former oculomotor nerve. The association between the tentacle

and vomeronasal system leads to the hypothesis that it act as a conductor of chemicals from

substrate to the prominent olfactory system, which occupies approximately one-quarter of total

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caecilian head length. (Wells, 2007) Given that the tongue in caecilians is more or less non-

protrusible, the tentacle could also serve to supplement sensation in the same way the tongue

does in reptiles. Theorized uses are many-fold, including detection and tracking of prey,

identification of mates, and survey of soil conditions (e.g. consistency, temperature, and

moisture). (Jared, Navas, & Toledo, 1999; Taylor, 1968)

A second caecilian sensory feature of great interest is the advanced and highly evolved

lateral line system present in the larval stage of many species. This system is divided into two

areas of specialization. The neuromasts are sensitive to mechanical stimuli and consist of a

complex of sensory, mantle, and support cells. The electro-sensitive ampullary organs,

possessing a canal and lumen, are flask-shaped and located just beneath or at the base of the

epidermis. The ampullary organs are particularly useful in detection of both predators and prey,

being probably sensitive enough to detect the subtle electrical fields of muscular activity.

Additionally, the larvae of Ichthyophis may be able to use this electrosensing to judge the

distance between their heads and the water’s surface. (Wells, 2007; Jared, Navas, & Toledo,

1999)

Communication

Communication presents some unique problems for Gymnophiona, given their effective

lack of vision and very limited hearing capabilities. There is no direct evidence of any use of

sound in communication, although there have been some limited accounts of caecilian sound

production. (Wells, 2007) A specimen believed to be of Dermophis septentrionalis was

documented as making “soft yelps” (apparently when startled), “lip-smacking noises”, and, most

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interesting, a soft clicking when introduced to new areas. The reporters of this phenomenon

theorized that this clicking may have a use in orientation. (Thurow & Gould, 1977)

Such interesting digressions aside, tactile and chemical avenues seem to be the only ones

available for caecilians. A study on the aquatic Typhlonectes natans showed evidence of

chemically mediated communication. (Wells, 2007) Captive specimens were chemically

attracted to groups of their fellows, congregating at apparently marked rock shelters. Signals also

seemed to operate in mating: tests showed that, while non-reproductive females generally

preferred the chemical signals of females, reproductive females were attracted to males.

Likewise, males were more responsive to cues from receptive females than non-receptive ones,

though they did not appear to discriminate between related and unrelated females. Another

example of chemical communication may be found in S. annulatus. When alarmed, the young of

this species will withdraw from the nest on their own, returning at a later time. This is thought to

be evidence that mother and young maybe able to communicate their location via some form of

chemical signals. (Jared, Navas, & Toledo, 1999)

While researching an unusual case of head dimorphism in an African species, some

interesting information was found on possible use of tactile communication. (Teodecki, Brodie,

Formanowicz, & Nussbaum, 1998) Authors of the study noticed a multitude of bite marks on

their wild-collected specimens, which, on captive observation, were confirmed as being inflicted

by their fellows. The fact that these bites were predominantly shallow and directed towards the

rather sensitive head region indicated to the researchers that they were likely of a communicative

nature, possibly giving information about the biter’s sex, size, or even individual identity, or

maybe functioning as a type of inquiry.

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Behavior: Locomotion and Burrowing

In addition to using the lateral undulations likely ancestral to amphibians, caecilians have

evolved a unique morphology to support a locomotion particularly suited to their largely

fossorial habits. Caecilian trunk musculature occurs in a thick band that is closely attached to the

skin via a dense connective tissue while at the same time only loosely connected to the vertebral

muscle, which has the effect of allowing the vertebral column to move independent of both trunk

muscles and skin. This arrangement notably permits caecilians a so-called modified concertina

locomotion, or internal corkscrew mechanism. Of great use inside burrows, in this locomotion

the vertebral column is bent into curves without similar contortion of the trunk musculature, thus

forming an anchor for pushing the body forward in a way peculiar to caecilians and some snakes.

This movement style is further aided by hydrostatic pressure maintained with the aid of both a

helical array of tendons surrounding the body wall and vertical hypaxial muscles in the body

wall itself. (Wells, 2007; O'Reilly, Summers, & Ritter, 2000) Comparison of T. natans and D.

mexicanus locomotion showed that the aquatic T. natans was incapable of the same internal

concertina movement, something which the researchers connected with various phylogenetic

studies to postulate that this derived locomotion has been lost in some, more aquatic forms.

(Summers & O'Reilly, 1997)

The general caecilian method of burrowing is to make an angled insertion of the snout

into the ground and then, using the substrate as a brace, push the soil aside with the head,

continuing and enlarging hole by plowing and compacting the soil with the head and forcing

forwards with trunk and vertebral muscles, exhibiting cervical and anterior trunk arching as well

as posterior trunk bracing all reminiscent of other apodal, burrowing vertebrates. Burrowing

being one of the major occupations of a fossorial creature, it is no surprise that caecilians have

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become efficient diggers over time, both in terms of the musculature discussed in the preceding

paragraph, and the highly derived skull mentioned earlier, bones lost and fused into a compact

form well-covered in dermal bone and completed by a strengthened and pointed snout. Current

consensus places Rhinatrematids as the most basal family in Gymnophiona, and thus they are

thought to be the least effective burrowers, showing the fewest derived characters. Observation

of this group dwelling for some portion of their time on the surface among leaf litter would seem

to bear out this belief. Ichthyophiids as well are thought to be less adept at burrowing, with the

Caeciliaidae, Scolecomorphiidae, and Typhlonectidae ranked as the best diggers. (Ducey,

Formanowicz, Boyet, Mailloux, & Nussbaum, 1993)

A study carried out on four representatives of different Gymnophiona families obtained

some interesting data about caecilian burrowing habits. (Ducey, Formanowicz, Boyet, Mailloux,

& Nussbaum, 1993) Besides the somewhat predictable preference for less compact soil, the test

subjects were found to habitually delay before beginning a burrow, consistently seeking out and

identifying less compact soils and showing a great willingness to use existing holes, a clue that

caecilians in the wild may be apt to use burrows previously constructed either by themselves or

others. Also very suggestive was the comparative efficiency seen between the members of the

different families. While the study confirmed the caeciliid D. mexicanus as an enthusiastic and

capable burrower (consistent with its documented broad natural range), it nonetheless failed to

support the hypothesis that Ichthyophis was generally less adept at burrowing than other genera.

The authors acknowledge that the study was limited in its duration and soil types examined, but

offer that these results indicate previous field observations which placed Ichthyophis as a poor

digger could actually have been seeing behavioral adaptations rather than physical limitations of

the group.

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When swimming, caecilians are seen to create traveling waves through the length of their

body by means of undulations, in a process thought to be analogous to the anguilliform

swimming style of some salamanders and eels. Lateral undulations may be added when

navigating obstacles, as vegetation or detritus. (O'Reilly, Summers, & Ritter, 2000)

Behavior: Feeding

Limited direct observations of caecilians has placed them as being largely inactive

animals, yet one area in which they have been observed to be capable of dramatic and sustained

action is in predation and feeding. (Jared, Navas, & Toledo, 1999) While hard data is limited, all

caecilians are apparently generalist, opportunistic predators. With their tongues being non-

protrusible, caecilians catch prey solely with their mouths, clenching them with their strong IHP-

RA jaw closures and raking the protruding portions of their prey against the substrate or tunnel

walls. (Summers & Wake, 2005) D. mexicanus in particular has been observed to hold prey

within their jaws housing recurved, interlocking teeth well suited for holding on to prey. As a

group, caecilians tend to open their jaws more slowly than other amphibians, something which

has been suggested to be an adaptation to their near blindness, with a delayed jaw opening

allowing for the jaws to be used to gauge their prey better before attacking. (Wells, 2007)

The diets of most species have not been subjected to any systematic examination, but

known prey include beetles, snails, slugs, ants, termites, earthworms, crickets, instars

(orthoptera), and, rarely, snakes or lizards. (Jared, Navas, & Toledo, 1999; Wells, 2007;

Measey, Gower, Oommen, & Wilkinson, 2004) More unusual examples of prey are dead fish

and aquatic arthropods scavenged by T. compressicaudus and stomach samples of an I.

kohtaoensis containing remains of microhylid frogs. (Kupfer, Nabhitabhata, & Himstedt, 2005)

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An extensive survey of the feeding habits of the Indian species Gegeneophis ramaswamii

supported the classification of a generalist predator, but one which nonetheless seems to prey for

the most part upon ants, termites, and earthworms (so-called soil ecology engineers), as well as

beetles. (Measey, Gower, Oommen, & Wilkinson, 2004) Juvenile stages for this species, as in

others studied, showed little ontological distinction in diet, feeding for the most part on the same

prey, though in smaller amounts. It is notable that if many caecilians are likewise heavy

predators of these soil ecology engineers and occur in high densities, as some are known to do,

they could make a significant impact upon the overall soil ecosystem.

Behavior: Predation

In a recurrent theme, not a lot is known about the predation of caecilians or adaptations to

predation, though there are some suggestive features. Predators may include burrowing

mammals, ants, and reptiles, with snakes and carnivorous birds confirmed as active predators.

(Jared, Navas, & Toledo, 1999) Aquatic larval forms more likely than not must deal with such

pressures as fish, frogs, turtles, and aquatic mammals. The caecilian’s first line of defense is

simple enough: they remain in burrows during daylight hours, venturing out only under cover of

night. (Taylor, 1968) While active defense in the form of biting has not been documented,

defense by noxious chemicals is known to be used. Mucus secreted from the integument displays

antifungal and antibacterial effects, and the secretions of S. annuletus has been shown to cause

partial paralysis in Bufo tactertcus and Leptodactylus ocellatus, rats, in large quantities perhaps

even leading to death. (Jared, Navas, & Toledo, 1999)

Ecosystem Importance

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As mentioned previously, while there has been some number of quantitative studies upon

the morphology and phylogeny of caecilians, anything in the area of the behavior and ecology of

wild specimens has remained almost wholly unexplored. As such, it is difficult to do more than

roughly speculate about this order’s role within and significance to its environment. All data so

far collected affirms caecilians as generalist predators, and there is fair reason to guess that at

this lifestyle they are tolerably successful. They have managed to maintain populations for

millennia and across the globe, and certain species have been documented as being able to occur

in considerable density, even in agriculturally developed or otherwise disturbed areas. (Measey,

2004; Measey, Gower, Oommen, & Wilkinson, 2004; Measey, Mejissa, & Muller, 2006) If this

fact is coupled with the accounts of their heavy predation upon ants, earthworms, and termites-

termed sometimes as soil ecology engineers- it could point to a more crucial role in soil ecology

than previously suspected. Researchers working with African species have found a similar

propensity to consume soil ecology engineers, though dispute the assignment to caecilians of a

primary role in population control of these groups. (Jones, Loader, & Gower, 2006) Nonetheless,

the question of the extent to which caecilian predation upon soil ecology engineers may be either

a balancing pressure or destructive force, for these populations and, by extension, soil health in

general, is definitely worthy of further investigation.

Anthropogenic Importance

Given the great parsimony of human interaction with members of this order, which are

notoriously difficult for even experts to locate or isolate, it is difficult to speak of clear

anthropogenic importance. This is ignoring, of course, the intriguing biological questions which,

while being doubtless worthy of study, nonetheless are probably not directly connected to basic

human life. The ecological question discussed earlier, however, concerning possible impact upon

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soil health, may be of quite notable interest to human agriculture. If caecilians are found to be a

sufficiently efficacious predator of soil ecology engineers, enough to impoverish their own

environment to a measureable degree, than it is not inconceivable that certain species may grow

to be viewed as a new agricultural pest in their home regions, and be added to the list of causes

for the oft-lamented fragility of tropical soils vis-à-vis intensive agriculture. It is also interesting

to speculate as to whether integumental mucous secretions, which have been noted to have some

anti-fungal or otherwise noxious properties, may be investigated for possible medicinal use as

has been done with those of some frogs.

Conservation Status

At the risk of becoming monotonous, it again must be noted that research into caecilian

populations in general, let alone how they are impacted by modern human civilization, is

rudimentary at best. There have been a number of reports on caecilian species decline throughout

their worldwide tropical range, including in India, Sri Lanka, the Philippines, Southeast Asia,

China, Central America, Bolivia, Uruguay, and, to a lesser extent, in Africa (which has borne

little research in this area). David Gower and Mark Wilkinson undertook a survey of extant work

into the conservation of caecilians, their paper largely a testimony to the frustrations of making

such assessments on a group so little investigated. They give that, “Caecilians in general are

reported to be declining and facing extinctions…[H]owever, no quantitative data are given in

most reports, and causal hypotheses have not been tested.” (p. 47) Given that caecilian taxonomy

is, currently, sketchy at best and baseline population statistics, from which declines may be

measured, are almost non-existent, establishing the severity of declines and possible causal

factors, or even if such declines are occurring, begins to resemble guesswork. Gower and

Wilkinson plead for more and better data: “Anecdotal concerns merit consideration but, to be

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useful, reports should include details of taxa, dates, and localities. Future reports of caecilian

population trends need to be of higher scientific quality.” (p. 51) Additionally, where data are

available, it tend to point to a more complex, nuanced population status than previously assumed.

As noted earlier, significant populations of some species have been documented in agricultural or

otherwise human-disturbed habitats; thus, it may be taken that at least some species can tolerate

living within “man-made” environments, which may complicate the current view of habitat

destruction (especially of moist forests and streams presumed to be prime habitat) as one of the

largest conservation threats. Caecilians are a diverse, group, however, and, while some species

appear to even benefit from types of human settlement (e.g. the shade of plantation plants,

irrigation ditches), there is currently no knowledge of the possibility that other, less fortunate,

forms are driven out or to extinction under those same circumstances. Another important

consideration for caecilians is that their fossorial lifestyle combined with an integument not

impermeable to moisture (Jared, Navas, & Toledo, 1999), may well make them very susceptible

to the effects of pesticide or industrial runoff, or any seepage from sewage or dumping facilities,

although at least some specimens have been gathered from areas exposed to agrichemicals

(Gower & Wilkinson, 2005). Mostly aquatic forms and those dependent upon a larval stage

would need to contend with water pollution issues and the potential destruction of necessary

water habitat from dam construction, wetland drainage, and human development of water

resources. Chytridiomycosis, infection of chytrid fungi inhabiting aquatic and moist terrestrial

environs intersecting with caecilian ranges, has been a major threat to amphibian populations,

though so far infection has not been documented for a caecilian. Overall, the most important first

step in conserving caecilian diversity is likely to establish new protocols for and carry out field

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surveys of caecilian populations: without hard numbers to work with, everything else is mere

shot in the dark.

Conclusions

Being an exclusively tropical and mostly fossorial animal order which, at a vague

approximation, may be filed simply under “blind, snake-looking things”, Gymnophiona certainly

has all the right characters to be summarily dismissed by an average member of the public, or

even the common biology student. This would be a terrible error, however, as what research has

been carried out on them has yielded enough unique and fascinating properties to make one rue

the inherent frustrations of properly gathering and studying this group. Such highly derived

features as the interhyoideus posterior/retroarticular jaw closure mechanism, the chemi-sensitive

tentacle, and the modified concertina locomotion, to name a few, provide fertile new ground for

those interested in documenting and understanding animal diversity. Of particular anthropogenic

interest may be how, despite its great phylogenetic distance from more familiar groups such as

birds and mammals, Gymnophiona nonetheless shows independent development of such striking

traits as viviparity as well as evidence for some parental care and chemical-mediated

communication. It is especially compelling to consider how the presence of an entire spectrum of

reproduction strategies, from oviparity, through ovoviparity and viviparity, and from free-

swimming larvae to direct development, can be observed within this single order, providing a

ready opportunity for investigating the evolutionary development of reproduction strategies

through time. Similar work may also be done to shed light on how and under what circumstances

parental care arises. If this number of curious attributes has been found with the very modest

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amount of work done on this group, then one may only imagine what future, more intensive,

study may yield.

Works Cited

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Carroll, R. L. (2001). The Origin and Early Radiation of Terrestrial Vertebrates. Journal of Paleontology , 75 (6), 1202-1213.

Ducey, P. K., Formanowicz, D. R., Boyet, L., Mailloux, J., & Nussbaum, R. A. (1993). Experimental Examination of Burrowing Behavior in Caecilians (Amphibia: Gymnophiona): Effects of Soil Compaction on Burrowing Ability of Four Species. Herpetologica , 49 (4), 450-457.

Gower, D. J., & Wilkinson, M. (2005). Conservation Biology of Caecilian Amphibians. Conservation Biology , 19 (1), 45-55.

Jared, C., Navas, C. A., & Toledo, R. C. (1999). An appreciation of the physiology and morphology of the Caecilians (Amphibia: Gymnophiona). Comparative Biochemistry and Physiology , 123, 313-328.

Jones, D., Loader, S., & Gower, D. (2006). Trophic ecology of East African caecilians (Amphibia:Gymnophiona), and their impact on forest soil invertebrates. Journal of Zoology , 117-126.

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O'Reilly, J. C., Summers, A. P., & Ritter, D. A. (2000). The Evolution of the Functional Role of Trunk Muscles During Locomotion in Adult Amphibians. American Zoology , 40, 123-135.

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