Metamorphosis and amphibian larvae

The word amphibian comes from ancient Greek words “amphi”, which means “both” and “bios”, which means “life”. Even if the word amphibious is an adjective used to describe animals that can live both on land and water, in the case of amphibians it also refers to both life stages through which these animals go through, as amphibians are born in an aquatic larval stage and become adults via a process of metamorphosis. In this new entry we’ll explain how metamorphosis works at a hormonal level, which anatomical changes occur during this period and the differences of this process among the different lissamphibian orders.

LISSAMPHIBIAN METAMORPHOSIS

Metamorphosis is present in the three lissamphibian orders. This process was already present in the first terrestrial tetrapods, which had to lay their eggs in water. Yet not all extant species present external metamorphosis, as some of them hatch as diminutive adults (as 20% of anuran species). In these species metamorphosis happens equally inside the egg before hatching, what’s called internal metamorphosis.

Red-eyed tree frog eggs (Agalychnis callydryas) just before hatching, by Geoff Gallice.

As a general rule, lissamphibians lay their eggs in water. In most species, aquatic larvae will hatch from gelatinous eggs, even if their morphology varies a lot between different species. Yet larvae of all lissamphibians present a set of common characteristics:

• External gills, thanks to which they can breathe underwater.
• Absence of eyelids and retinal pigments associated with sight outside of water.
• Presence of a lateral line (or equivalent), sensorial organ characteristic of fish which allow them to sense vibrations underwater.
• Thinner skin.
• Subaquatic anatomic adaptations.

Photo of a fire salamander (Salamandra salamandra) in which the external gills and the pisciform looks of the larva can be appreciated, by David López.

During metamorphosis, most structures useful during the larval stage are reabsorbed through apoptosis, a controlled cell death process. In many cases this process is highly conditioned by various environmental factors such as population density, food availability and the presence of certain chemical substances in water.

HORMONAL CHANGES

At the hormonal level, metamorphosis is characterized by the interaction between two kinds of hormones: thyroid hormones and prolactin. While the thyroid hormones as thyroxin (secreted by the thyroid gland) stimulate the metamorphosis process, prolactin (secreted by the pituitary gland or hypophysis) inhibits it. The concentration of these two hormones (regulated by the Hypothalamus→Hyphophysis→Thyroid) is what controls the different stages of metamorphosis.

Scheme by Mikael Häggström of the hypothalamus (green), hypophysis or pituitary (red), thyroid (blue) axis in human beings and the release of thyroid hormones.

PREMETAMORPHOSIS

This is the larval growth stage, and it lasts around the first 20 days of life (depending on the species). This stage is characterized by a low secretion of thyroidal hormones and by a high concentration of prolactin that inhibits the metamorphosis process. This is due to the fact that the hypothalamus→hypophysis system is still not mature.

PROMETAMORPHOSIS

It’s a period of reduced growth with slow morphological changes, due to the rise of thyroxin concentration in blood caused by the growth of the thyroid gland. Also, the hypothalamus→hypophysis axis starts developing, which will trigger even more the rise of the thyroxin concentration and will lower the prolactin, giving way to great morphological changes.

METAMORPHOSIS CLIMAX

It’s the point in which the hyothalamus→hypophysis→thyroid axis is at its maximum capacity and it is when great morphological changes happen in the larva, which will end up becoming a miniature adult. Finally, thyroxin levels will start to be restored by a negative feedback system of the thyroxin over the hypothalamus and the hypophysis.

Scheme from Brown & Cai 2007, about the general levels of thyroid hormones during the different metamorphosis’ stages.

MORPHOLOGICAL CHANGES

During the metamorphosis process, larvae will go through a set of anatomical changes that will allow them to acquire their adult form. Some changes common to most species are the acquisition of eyelids and new retinal pigments, the reabsorption of the gills and the loss of the lateral line. Other morphological changes vary among the different orders. For example in caecilians (order Apoda) larvae already look like miniature adults but with external gills. Also, most caecilians present internal metamorphosis and the hatchlings have no trace of gills.

Photo from Blog do Nurof-UFC of a caecilian egg, inside which we can see the larva with gills.

In urodeles (order Urodela), the external metamorphic changes aren’t that spectacular either. Larvae are pretty similar to adults, as their limbs develop quickly, although they present external filamentous gills, have no eyelids and present a largely-developed caudal fin. Even their carnivorous diet is similar to that of the adult’s. Yet the great diversity of salamanders and newts gives as a result a great variety of life cycles; from viviparous species that give live birth, to neotenic species that keep larval characteristics through their adult stage.

Photo by David Alvarez of the viviparous birth of a fire salamander (Salamandra salamandra), and photo by Faldrian of an axolotl (Ambystoma mexicanum) a neotenic species.

Frogs and toads (order Anura) are the group in which metamorphic changes are more dramatic. The anuran larva is so different that it’s called a tadpole, which differentiates from the adult both by its looks and its physiology and behaviour. Even if tadpoles are born with external gills, these are soon covered by skin folds that form a gill chamber. Also, tadpoles have a round, limbless body and a long, vertically-flattened tail, which allows them to swim swiftly in water.

Photo by J. J. Harrison of a southern brown tree frog tadpole (Litoria ewingii).

One of the main differences between adult and larval anurans is their diet. While adult frogs and toads are predators, tadpoles are herbivorous larvae, feeding by filtering suspended vegetal particles or by scraping off algae from rocks using a series of keratinous “teeth” present in some species. This is reflected in their spirally-shaped and extremely long digestive system in order to allow them to digest large quantities of vegetal matter. Tadpoles are tireless eating machines, with some filter-feeding species being able to filter eight times their body volume of water per minute.

Photo by Denise Stanley of a tadpole, in which we can see both the keratinous “teeth”, and the spiral-shaped intestine.

After metamorphosis, tadpoles will reabsorb their gills and tail, their digestive system will shorten, and will develop limbs and lungs, becoming small amphibians prepared for a life on land.

Recently metamorphosed spiny toad (Bufo spinosus) by David López.

As we have seen, the metamorphosis process varies greatly among the different species of each order. This process results in the fact that that most lissamphibians spend a part of their lives in water and the other on land, a representative fact of the transition of the first tetrapods from the aquatic to the terrestrial medium. Also, the great diversity of ecological niches occupied by both the adults and the larvae of the different species and the wide array of environmental factors that affect the metamorphosis process, make lissamphibians great bioindicators of an ecosystem’s health.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Masó & Pijoan (2011). Anfibios y Reptiles de la Península Ibérica, Baleares y Canarias. Ediciones Omega.
• Brown & Cai (2007). Amphibian metamorphosis. Developmental Biology. Vol. 306. Pp: 20-33.
• Your Article Library. Process of Metamorphosis in Amphibians and it’s Hormonal Control.
• Metamorfosis de anfibios.
• Cover image by Brian Gratwicke.

Limb regeneration, from the axolotl to human beings

The regeneration of lost or damaged body parts in animals is known from many centuries ago. In 1740 the naturalist Abraham Trembley observed a small cnidarian that could regenerate its head if it was cut off, so he called it Hydra, in reference to the monster from Greek mythology that could grow back its multiple heads if they were cut off. Afterwards, it was discovered that there were many other species of animals with regenerative abilities. In this entry we’ll talk about these animals.

Regeneration in the animal kingdom

Regeneration of body parts is more widespread between the different groups of invertebrates than it is between the vertebrates. This process can be bidirectional, in which both parts of the animal regenerate their missing parts to form two animals (just like the hydra, planarians, earthworms and starfishes) or unidirectional, in which the animal loses an extremity but it just regenerates, without forming two animals (arthropods, molluscs and vertebrates). In vertebrates, fishes and amphibians are the ones that present the greatest regenerative capacities, although many lizards and some mammals are able to regrow their tails.

Image by Matthew McClements about bidirectional regeneration in planarians, hydras and seastars. Extracted from Wolbert's Principles of Development.

Regeneration can be done by two different ways:

• Regeneration without active cellular proliferation or “morphallaxis”. In this type, the absent body part is regrown through remodelling of pre-existing cells. This is what happens in the Hydra, in which lost body parts are regenerated without the creation of new material. So, if a hydra is cut in half, we’ll obtain two smaller versions of the original hydra.

Video about an experiment in which an Hydra has been cut in different pieces. Video by Apnea.

• Regeneration with cellular proliferation or “epimorphosis”. In this type, the lost part is regenerated via cellular proliferation, it is “newly created”. In most cases, it happens through the formation of a specialized structure called blastema, a mass of undifferentiated cells which appears during phenomena of cellular regeneration.

Almost all groups of animals with regenerative capacities present regeneration with blastema formation. Yet the origin of the blastemal stem cells varies between groups. While planarians present pluripotent (that can differentiate to any kind of cell type) stem cells all along their bodies, vertebrates have specific cells in each type of tissue (cartilage, muscle, skin…) that only regenerate cells of the tissue they come from.

In land vertebrates, lizards and urodeles are the ones that present the most powerful regenerative abilities. Down below we’ll see how they regenerate and the applications it has in modern human medicine.

Expendable tails

When you are a small animal that is being chased by a cat or any other predator, it probably is better for you to lose your precious tail than to lose your life. Some terrestrial vertebrates have evolved following this philosophy, and they are able to shed off their tails voluntarily through a process called caudal autotomy. This allows them to escape from their predators, which are entertained with the still moving lost tail.

 Video in which we can see how some lizards like this red-tailed vanzosaur (Vanzosaura rubricauda) have brightly coloured tails to attract the attention of predators. Video by Jonnytropics.

Autotomy or self-amputation, is defined as a behaviour in which the animal can shed off one or more body parts. Caudal autotomy is found in many species of reptiles and in two species of spiny mouse of the genus Acomys. In reptiles we can find caudal autotomy in lacertids, geckos, skinks and tuataras.

Foto of a Cairo spiny mouse (Acomys cahirinus), a mammal which is able to shed and regrow its tail. Photo by Olaf Leillinger.

In reptiles, the fracture of the tail happens in specific areas of the caudal vertebras which are naturally weakened. The autotomy may happen in two different ways: intravertebral autotomy, in which the vertebra at the centre of the tail have transversal fracture planes prepared to break if they are pressed hard enough, and intervertebral autotomy, where the tail breaks between vertebras by muscular constriction.

Tridimensional model of the fracture planes on the tail of a lizard and the regeneration post-autotomy of a cartilaginous tube. Image extracted from Joana D. C. G. de Amorim et al.

Caudal autotomy allows the animal to escape, but it isn’t without cost. Many reptiles use their tails as a reserve of fat and losing this energy store is usually detrimental for the animal. That’s why many lizards, once the threat has disappeared, look for their lost tail and eat it, to at least regain the energy it had as fat. In addition, regenerating a new tail requires a great expenditure of energy.

Photo of a Catalonian wall lizard (Podarcis liolepis) that has shed its tail. Photo by David López Bosch.

The regeneration of the tail in reptiles differs from that of amphibians and fishes in that it happens without the formation of a blastema and instead of an actual regeneration of the caudal vertebras, it forms a cartilaginous tube along it. The new tail is stiffer and shorter than the original one, and it usually regenerates whole some weeks after the amputation. Most lizards can regenerate their tails multiple times, but some species like the slow worm (Anguis fragilis) can only do it once. Sometimes, the original tail isn’t completely broken but the regeneration mechanisms are activated, which can lead to lizards and geckos with more than one tail.

Detail of the tail of a common wall gecko (Tarentola mauritanica) which has regenerated the tail without losing its original tail. Photo by Rafael Rodríguez.

Urodeles, the kings of regeneration

Of all tetrapods, amphibians are the ones that present the more astonishing regenerative capacities. During the larval stage of most species, both the tail and the limbs (if they have them) can be regenerated after its loss. The scientific community thinks that this is due to the fact that in amphibians the development of limbs and other organs is delayed until the moment of metamorphosis. Yet, frogs and toads (anurans) only maintain their regenerative powers during their tadpole stage, losing them when reaching adulthood.

Wood frog tadpole (Rana sylvatica) which, like all amphibians, delays the development of its legs up to the moment of metamorphosis. Photo by Brian Gratwicke.

Instead, many salamanders and newts (urodeles) conserve their regenerative powers their whole life. Even if many species present caudal autotomy, unlike lizards urodeles are able to completely regenerate, not only their tails, but practically any kind of lost body tissue. Of all known species, the axolotl (Ambystoma mexicanum), a neotenic amphibian which reaches adulthood without undergoing metamorphosis, has served as a model organism for the study of the formation of the blastema that precedes regeneration.

 Video about the axolotl, this curious amphibian which is greatly endangered. Video by Zoomin.TV Animals.

Regeneration as it happens in salamanders has stages genetically similar to the ones that occur during the development of the different body tissues and organs during the embryonic development of the rest of vertebrates. In the axolotl (and in the rest of urodeles) regeneration of a limb after amputation goes through three different stages:

• Wound healing: During the first hour after the amputation, epidermal cells migrate to the wound. The closing of the wound usually completes two hours later with the same mechanisms as in the rest of vertebrates. Yet, the complete regeneration of the skin is delayed up until the end of the regeneration.
• Dedifferentiation: This second phase, in which the blastema is formed, starts 24 hours after amputation. This is composed both of cells from the specialized tissues of the amputated zone which lose their characteristics (they obtain the capacity to proliferate and differentiate again) and cells derived from the connective tissue that migrate to the amputation zone. When these cells of different origins accumulate and form the blastema, the cellular proliferation starts.
• Remodelling: For the third stage to start, the formation of the blastema is required. Once the blastema is formed by different dedifferentiated cells, the formation of the new limb follows the same pattern as any kind of vertebrate follows during embryonic development (it even has de same genes intervening).

Diagram about the formation of the blastema in a zebrafish (Danio rerio) another model organism. Image from Kyle A. Gurley i Alejandro Sánchez Alvarado.

Recently fossils have been found from many different groups of primitive tetrapods which present signs of regeneration. Proof has also been found of limb regeneration in temnospondyl (Apateon, Micromelerpeton and Sclerocephalus) and lepospondyl (Microbrachis and Hyloplesion) fossils. This wide variety of basal tetrapod genera presenting regeneration and the fact that many fish also present it, has led many scientists to consider if the different groups of primitive tetrapods had the ability to regenerate, and if it was lost in the ancestors of amniotes (reptiles, birds and mammals).

Photo of an axolotl, by LoKiLeCh.

However, it is believed that the genetic information that forms the blastema could still be found in the DNA of amniotes but in a latent state. Of the three stages of the regeneration process, the only one exclusive to urodeles is the dedifferentiation stage, as the healing stage is the same as in the rest of vertebrates and the remodelling stage is like the one during embryogenesis. Currently many studies are being carried out on the way to reactivate the latent genes that promote the formation of the blastema in other vertebrates, such as humans.

Some human organs like the kidneys and the liver already have some degree of regenerative capacities, but thanks to investigation with stem cells in animals like salamanders and lizards currently it is able to regenerate fingers, toes, genitals and parts of the bladder, the heart and the lungs. As we have seen, the different animals able to regenerate amputated limbs hold the secret that could save thousands of people. Remember this the next time you hear that hundreds of species of amphibians and reptiles are endangered because of human beings.

References

During the writing of this entry the following sources have been consulted:

• Cover photo by Peter Halasz.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.eurostemcell.org/de/node/19896
• https://www.ncbi.nlm.nih.gov/pubmed/12455626
• https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3480082/
• http://ftp.eebweb.arizona.edu/courses/Ecol483_583/Bateman%20and%20Fleming%202009.pdf
• http://www.sciencemag.org/content/276/5309/81.short
• http://www.ambystoma.org/
• http://www.nature.com/nature/journal/v527/n7577/full/nature15397.html

Frogs, toads and newts: the last amphibians

With about 7000 living species, amphibians currently occupy almost all the habitats on Earth. While in the last entry we explained the origin of the first tetrapods and how those gave rise to the different groups of primitive amphibians, in this entry we will explain in more detail the characteristics of current amphibians, the so-called lissamphibians.

AMPHIBIANS AND LISSAMPHIBIANS

The term “Lissamphibia” (“smooth amphibian”) is used to name current amphibians and it’s useful to tell them apart from the rest of fossil amphibians, while the term Amphibia (“double life” referring to the aquatic larval stage of most species), is used to name all tetrapods except the amniotes (reptiles, birds and mammals).

Most authors consider lissamphibians a monophyletic group (a group which includes all the descendants of a common ancestor) which includes the different groups of modern amphibians. The main characteristics of this group are:

Dermal characteristics

• Smooth, scaleless, permeable skin that allows gas exchange (both pulmonary and cutaneous respiration) and the absorption of water (most amphibians usually do not need to drink water). This makes them susceptible to skin infections like the one from the Batrachocytrium dendrobatidis fungus.

Section through frog skin by Jon Houseman. A: Mucous gland, B: Chromophore, C: Granular poison gland, D: Connective tissue, E: Stratum corneum, F: Transition zone, G: Epidermis, and H: Dermis.

• Two types of skin glands: mucous (the majority, to maintain humidity) and granular (less numerous, secrete toxins of different intensity).

Skeletal characteristics

• Pedicellate and bicuspid teeth.

Photo of pedicellate teeth, in which the crown and base are made of dentine and are separated by a narrow layer of uncalcified dentine.

• A pair of occipital condyles.
• Short, stiff ribs not encircling the body.
• Four digits on the front limbs and five digits on the hind limbs.

Skeleton of giant salamander in which we can see some of the characteristics of lissamphibians. Photo by Graham Smith.

Auditory characteristics

• Papilla amphibiorum, a group of specialized cells in the inner ear which allow them to hear low frequency sounds.
• Stapes-operculum complex which are in contact with the auditory capsule, improve reception of aerial and seismic waves.

Other characteristics

• Fat bodies associated with gonads.
• Presence of green rods in the visual cells (these allow the perception of more colours).
• Presence of a muscle elevator of the eye (called levator bulbi).
• Forced-pump ventilation system (their short ribs do not allow pulmonary ventilation, so they pump the air through their mouth).

Explicative diagram about buccal ventilation in lissamphibians, by Mokele.

TAXONOMY AND EVOLUTIONARY THEORIES

Nowadays only three living amphibian orders persist: the order Salientia or Anura (which includes frogs and toads), the order Caudata or Urodela (salamanders and newts) and the order Gymnophiona or Apoda (caecilians). The second name of each order refers to the current species and their recent ancestors, while the first name refers to the whole order since the separation of each order.

There are two hypotheses regarding the relationships between the three orders. The most accepted both by anatomic and molecular analyses is that Salientia and Caudata are grouped together into the clade Batrachia, while the other one is that Caudata and Gymnophiona together form the clade Procera.

Two hypothetical evolutionary trees by Marcello Ruta & Michael I. Coates (2007), showing the Batrachia and Procera hypotheses on the relationships between Salientia (S), Caudata (C) and Gymnophiona (G).

Currently there are three groups of hypotheses of the origin of lissamphibians: the temnospondyl hypotheses, the lepospondyl hypotheses and the polyphyletic hypotheses.

Temnospondyls are the main candidates to be the ancestors of lissamphibians, as they share many characteristics, such as the presence of pedicellated, bicuspid teeth, and short, stiff ribs. Authors defending these theories say that lissamphibians suffered during their evolution a process known as paedomorphosis (retention during the development of juvenile characteristics), this way explaining why temnospondyls reached such large sizes while lissamphibians are much smaller and usually have lighter and less ossified cranial structures.

Drawings from Marcello Ruta & Michael I. Coates (2007) of skeletons belonging to Celteden ibericus (left, a lissamphibian) and Apateon pedestris (right, a temnospondyl) to show similitudes in skeletal structure.

Hypotheses regarding a lepospondyl origin for lissamphibians do not have such a strong support as the temnospondyl hypotheses. However, recently some statistical studies combining anatomic and molecular data have given some support to these hypotheses.

Nevertheless, there is a third group of hypotheses we must consider, the ones that say that lissamphibians are a polyphyletic group (with different origins for the different orders). According to one of these theories, frogs and salamanders (clade Batrachia) would have a temnospondyl origin, while caecilians (order Gymnophiona or Apoda) would have originated from lepospondyl ancestors, many of which had already suffered a limb reduction process.

 Modified outline of the three different hypotheses regarding the origins of the lissamphibians; 1. Lepospondyl origin, 2. Temnospondyl origin, 3. Polyphyletic origin.

Still, most authors support a monophyletic and temnospondyl origin for lissamphibians, but alternative hypotheses shouldn’t be discarded.

SALIENTIA OR ANURA

With up to 4750 species, frogs and toads form the most diverse lissamphibian order. The first known Salientia is Triadobatrachus, which, despite having a tail, already presented some typical characteristics of modern frogs, such as a short spine with few vertebras and the hind limbs longer than the front limbs.

Interpretation by Pavel Riha, of the ancient Salientia, Triadobatrachus massinoti.

The anatomy of modern anurans is unique among the animal kingdom. Their skeleton seems totally dedicated to allow these animals to jump (even though many species move simply by walking). Some of their characteristics are:

• A short and stiff trunk (less than 12 vertebras), an especially long pelvic girdle and the vertebras of their posterior end (that in other amphibians form the tail) are reduced and fused forming the urostyle.
• Long hind limbs, with the tibia and fibula fused together (to aid in impulse during jumping) and short and strong front limbs (to resist the impact on the landing).

Photo of a pig frog (Rana grylio), a typical american anuran.

Also, of all current amphibians frogs are the ones with the most developed hearing apparatus and vocal organ. Males, usually present specialized structures to amplify sound during the mating season.

Red eyed tree frog (Litoria chloris) showing the vocal sac, used to amplify the sound of its calls.

Size in anurans varies from 3 kg in weight and 35 centimetres in length of the goliath frog (Conraua goliath) to the 7, 7 millimeters long recently discovered Paedophryne amanuensis, currently the smallest known vertebrate.

Photo from Rittmeyer EN, Allison A, Gründler MC, Thompson DK, Austin CC (2012)  of Paedophryne amanuensis, the smallest known vertebrate in the world on a US dime.

With such a diversity, vital strategies of anurans vary greatly and it’s difficult to generalize on their reproductive biology, even though most show indirect development (born as tadpoles and passing through a metamorphosis process) and they mate and lay their eggs in an aquatic medium.

Tadpoles of common toad (Bufo bufo) from northern Germany by Christian Fischer.

URODELA OR CAUDATA

The urodeles or caudates are the order of lissamphibians which externally most resemble primitive amphibians. This group includes salamanders and newts, most of which have a long body, a well-developed tail and four relatively short legs. Most urodeles are terrestrial and are distributed mainly in the northern hemisphere, with a few species inhabiting the tropics.

Photo of an eastern tiger salamander (Ambystoma tigrinum) from the House of Sciences, Corunna - Spain. Taken by Carla Isabel Ribeiro.

Most species present internal fertilization and are oviparous. Most also present indirect development (larvae, metamorphosis, adult), and the larvae usually resemble miniaturized adults with external, ramified gills. Various groups of salamanders suffer neoteny phenomenon, in which individuals, even though sexually developing into adults, externally keep larval characteristics.

Young and very large larvae of near eastern fire salamander (Salamandra infraimmaculata), Ein Kamon, Israel. Photo by Ab-Schetui.

Currently, urodeles are classified into three suborders: the Sirenoidea, the Cryptobranchoidea and the Salamandroidea. Sirenoideans are urodeles with both specialized and primitive characteristics, such as the loss of hind limbs and the presence of external gills. Cryptobranchoideans are large primitive salamanders (up to 160 centimetres) which present external fertilization, while salamandroideans are the most numerous group of urodeles (with more than 500 species) and the most diverse, with most species being terrestrial and having internal fertilization using packs of sperm called spermatophores.

Photo of a northern dwarf siren (Pseudobranchus striatus) a sirenoidean from the United States.

GYMNOPHIONA OR APODA

The most ancient known member of the order Gymnophiona is Eocaecilia micropodia, an amphibian about 15 centimetres long with a considerably long body, a short tail and really small limbs.

Restoration by Nobu Tamura of Eocaecilia micropodia an ancient Gymnophiona from the early Jurassic.

Current caecilians (order Apoda) have completely lost any trace of limbs, girdles or tail, due to their adaptation to a subterranean lifestyle. That’s why they also suffered a process of cranial hardening and their eyes are extremely reduced. They also present a series of segmentary rings all along their bodies, which make them look somewhat like earthworms.

Yellow-striped caecilian (Ichthyophis kohtaoensis) from Thailand, by Kerry Matz.

There are currently about 200 species of caecilians divided into 10 families. Their size varies from about 7 centimetres in the species Idiocranium russelli from Cameroon, to up to 1,5 meters of Caecilia thompsoni from Colombia. They present a pantropical distribution, internal fertilization and a great variation in their development (there are viviparous and oviparous species and some which endure metamorphosis while some have direct development).

Photo of Gymnopis multiplicata an american caecilian. Photo by Teague O'Mara.

REFERENCES

The following sources have been consulted in the elaboration of this entry:

• Cover photo: Hagerty Ryan.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.livescience.com/5529-land-creatures-wild-appearances.html
• http://www.tandfonline.com.sci-hub.org/doi/abs/10.1017/S1477201906002008
• http://www.nature.com.sci-hub.org/nature/journal/v453/n7194/abs/nature06865.html
• https://quizlet.com/7138074/amphibian-natural-history-flash-cards/
• http://vertebrates.voices.wooster.edu/sample-page/
• http://www.usfca.edu/fac-staff/dever/tetra_evo12.pdf
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3350690/