Caecilian Amphibians

Researchers Find Snake-Like Venom Glands in Caecilian Amphibians

A team of scientists from Brazil and the United States has found the specialized oral glands in the jaws of the ringed caecilian (Siphonops annulatus), a snake-shaped amphibian related to frogs and salamanders.

The ringed caecilian (Siphonops annulatus). Image credit: Carlos Jared.

The ringed caecilian (Siphonops annulatus). Image credit: Carlos Jared.

Neither snakes nor worms, caecilians (order Gymnophiona) are limbless amphibians found in tropical climates of Africa, Asian and the Americas.

These creatures are aquatic or live in burrows of their own making. They are nearly blind and use a combination of facial tentacles and slime to navigate their underground tunnels.

Owing to their distribution and burrowing habits, caecilians consist in one of the least known vertebrate groups.

“We think of amphibians — frogs, toads and the like — as basically harmless,” said Utah State University’s Professor Edmund ‘Butch’ Brodie, Jr., co-author of the study.

“We know a number of amphibians store nasty, poisonous secretions in their skin to deter predators. But to learn at least one can inflict injury from its mouth is extraordinary.”

“These animals produce two types of secretions — one is found mostly in the tail that is poisonous, while the head produces mucus to help with crawling through the earth,” added senior author Dr. Carlos Jared, Director of the Structural Biology Lab at the Butantan Institute in São Paulo.

“Because caecilians are one of the least-studied vertebrates, their biology is a black box full of surprises.”

“It is while examining the mucous glands of the ringed caecilian that I stumbled upon a never before described set of glands closer to the teeth,” said first author Dr. Pedro Luiz Mailho-Fontana, a postdoctoral researcher in the Structural Biology Lab at the Butantan Institute.

In the study, the researchers analyzed the morphology of the ringed caecilian’s head and found a series of small fluid-filled glands in the upper and lower jaw, with long ducts that opened at the base of each tooth.

Using embryonic analysis, they found that these oral glands originated from a different tissue than the slime and poison glands found in the caecilian’s skin.

“The poisonous skin glands of the ringed caecilian form from the epidermis, but these oral glands develop from the dental tissue, and this is the same developmental origin we find in the venom glands of reptiles,” Dr. Mailho-Fontana said.

“This marks the first time glands of this kind have been found in an amphibian.”

Structure of the upper jaw and lower jaw of the ringed caecilian (Siphonops annulatus): (A) the ringed caecilian; (B) upper jaw; (C) lower jaw; (D) head after partial skin corrosion showing the tooth-related glands digitally enhanced in green; (E) section of the upper labial region showing the glands and glandular ducts. Black arrows (outer tooth row); white arrow (inner tooth row); arrowheads (cavities that accommodate the teeth when the mouth is closed). Abbreviations: To - tongue, S - skin, E - eye, Te - tentacle, Oe - oral epithelium. Image credit: Mailho-Fontana et al, doi: 10.1016/j.isci.2020.101234.

Structure of the upper jaw and lower jaw of the ringed caecilian (Siphonops annulatus): (A) the ringed caecilian; (B) upper jaw; (C) lower jaw; (D) head after partial skin corrosion showing the tooth-related glands digitally enhanced in green; (E) section of the upper labial region showing the glands and glandular ducts. Black arrows (outer tooth row); white arrow (inner tooth row); arrowheads (cavities that accommodate the teeth when the mouth is closed). Abbreviations: To – tongue, S – skin, E – eye, Te – tentacle, Oe – oral epithelium. Image credit: Mailho-Fontana et al, doi: 10.1016/j.isci.2020.101234.

The scientists think that the ringed caecilian may use the secretions from these snake-like oral glands to incapacitate its prey.

“Since caecilians have no arms or legs, the mouth is the only tool they have to hunt,” said co-author Dr. Marta Maria Antoniazzi, an evolutionary biologist at the Butantan Institute.

“We believe they activate their oral glands the moment they bite down, and specialized biomolecules are incorporated into their secretions.”

In a preliminary chemical analysis of the ringed caecilian’s oral gland secretions, the authors found high activity of phospholipase A2, a common protein found in the toxins of venomous animals.

“The phospholipase A2 protein is uncommon in non-venomous species, but we do find it in the venom of bees, wasps, and many kinds of reptiles,” Dr. Mailho-Fontana said.

In fact, the biological activity of phospholipase A2 found in this species was higher than what is found in some rattlesnakes. Still, more biochemical analysis is needed to confirm whether the glandular secretions are toxic.

If future work can verify the secretions are toxic, caecilian oral glands could indicate an early evolutionary design of oral venom organs.

“If we can verify the secretions are toxic, these glands could indicate an early evolutionary design of oral venom organs,” Professor Brodie said.

“They may have evolved in caecilians earlier than in snakes.”

“Unlike snakes which have few glands with a large bank of venom, the ringed caecilian has many small glands with minor amounts of fluid,” Dr. Jared said.

“Perhaps caecilians represent a more primitive form of venom gland evolution. Snakes appeared in the Cretaceous probably 100 million years ago, but caecilians are far older, being roughly 250 million years old.”

The discovery is reported in a paper in the journal iScience.

_____

Pedro Luiz Mailho-Fontana et al. Morphological Evidence for an Oral Venom System in Caecilian Amphibians. iScience, published online July 3, 2020; doi: 10.1016/j.isci.2020.101234

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