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.

Hybrids and sperm thieves: amphibian kleptons

In biology a hybrid is the result of the reproduction of two parents of genetically different species, although in most cases hybrids are either unviable or sterile. Yet in some species of amphibians, sometimes hybrids are not only viable, but also become new species with special characteristics. In this entry we’ll show you two cases of amphibian hybrids that form what is known as a klepton and that make the definition of species a little less clear.

WHAT IS A KLEPTON?

A klepton (abbreviated kl.) is a species which requires another species to complete its reproductive cycle. The origin of the word klepton comes from the Greek word “kleptein” which means “to steal”, as the klepton “steals” from the other species to reproduce. In the case of amphibians, kleptons have originated from hybridation phenomena. The amphibian’s potent sexual pheromones and the multispecies choirs in the case of anurans, causes some males and females of different species to try to mate together. Yet hybrids are only viable between closely related species.

Among the different klepton species we can encounter two different methods depending on the type of conception: zygokleptons, in which there’s fusion between the egg and the sperm’s genetic material, and gynokleptons, in which the egg needs the stimulation from the sperm but doesn’t include its genetic material.

The different amphibian kleptons are usually constituted entirely by females (there are usually few or no males) that use the sperm of another species to perpetuate the klepton. As some kleptons depend on various related species, this can promote the creation of “species complexes” in which various similar species present hybridization areas and very complicated relationships among them. Below you’ll find two klepton examples, one in European anurans and the other in American urodeles.

HYBRIDOGENESIS IN WATER FROGS

The European water frogs (Pelophylax genus) form what is known as a “hybridogenetic complex” in which the hybrids from different species form kleptons which can’t reproduce among each other but, which must reproduce with a member of one of the parental species, “stealing” or “parasitizing” its sperm in order to survive.

Photo by Bartosz Cuber of two edible frogs (Pelophylax kl. esculentus) in amplexus. This is the best known hybrid both because of its wide distribution, and for being considered a delicacy in France.

In the hybridogenesis of water frogs the genetic material of both parents combines to form the resulting hybrid (zygoklepton). This hybrids (almost always females) will have half their genome from one species and half from the other. Yet, not being able to reproduce with a similar hybrid, during gametogenesis the hybrids eliminate the genetic material from one of the parent species. This way, when reproducing with an individual from the species whose genetic material has been deleted, they will form another hybrid.

Scheme of the genetic composition of the different Pelophylax kleptons. In this hybridogenetic complex four “natural” species intervene: the marsh frog (Pelophylax ridibundus, RR genome), the pool frog (Pelophylax lessonae, LL genome), the Iberian waterfrog (Pelophylax perezi, PP genome)  and the Italian pool frog (Pelophylax bergeri, BB genome).

The edible frog (Pelophylax kl. esculentus, RL genome) comes from the hybridization between the marsh frog and the pool frog. The Italian edible frog (Pelophylax kl. hispanicus, RB genome) stems from a hybrid between the marsh frog and the Italian pool frog. Finally, the Graf’s hybrid frog (Pelophylax kl. grafi, RP genome) originated from the hybridization between the edible frog (in which the DNA of the pool frog is eliminated from their gametes) and the Iberian waterfrog.

Schemes by Darekk2 of the hybridogenetic processes in the different European water frog’s kleptons. The bigger circles represent the individual’s genome and the smaller circles the gametes’ genetic material.

As we can see, the genetic information of the marsh frog is the only one present in all three kleptons. These kleptons delete the genetic material of the species with which they share their habitat from their gametes but keep the genetic material of the marsh frog (R). So for example, the edible frog (P. kl esculentus) deletes form its eggs the DNA of the pool frog (L) with which it encounters and breeds in its natural range, resulting in more edible frogs (RL). The marsh frog seldom reproduces with some of its hybrids and if it does, they produce normal marsh frogs.

SALAMANDERS WITH SEVERAL GENOMES

The salamanders of the Ambystoma genus, usually known as mole salamanders, are a genus endemic of North America and are the only living representatives of the Ambystomatidae family. Five of these species form what is known as the “Ambystoma complex”, in which these species contribute to the genetic composition of a unisexual lineage of salamanders which reproduce by gynogenesis (gynoklepton). Based on the mitochondrial DNA of the unisexual populations, it is thought that this complex originated from a hybridization event of about 2.4-3.9 million years ago.

This complex consists of the five following species: the blue-spotted salamander (Ambystoma laterale LL genome, photo by Fyn Kynd Photography), the Jefferson salamander (Ambystoma jeffersonianum JJ genome, photo by Vermont Biology), the small-mouthed salamander (Ambystoma texanum TT genome, photo by Greg Schechter), the streamside salamander (Ambystoma barbouri BB genome, photo by Michael Anderson) and the tiger salamander (Ambystoma tigrinum TiTi genome, photo by Carla Isabel Ribeiro).

In the gynogenesis of this all-female lineage, the egg needs activation by a sperm to start division and development but, it first has to duplicate its genetic material by endomitosis to avoid the formation of an unviable haploid (with half the genetic information) zygote. Yet, as in parthenogenetic reptiles, in the long term the lack of genetic recombination can take its toll on the individuals. That’s why this lineage of unisexual salamanders has the capacity of occasionally incorporating the whole genome from the males of four of the species which constitute the complex (currently the reproduction of streamside salamanders with members of the unisexual lineage hasn’t been documented).

Scheme from Bi, Bogart & Fu (2009) in which we can see the different paths that the gynogenetic mole salamanders can take while reproducing.

These individuals don’t mix the newly acquired genome, they add it. Therefore, among the members of this lineage we can find diploid, triploid, tetraploid and even pentaploid individuals (even if as the ploidy increases the individuals are less apt to survive) depending on how many different genomes the previous generations had incorporated.

Among the klepton, the most common genome combination is that of triploids based on the blue-spotted salamander and the Jefferson salamander, with the genomes LLJ (left, image by David Misfud) and JJL (right, image by Nick Scobel), even though the number of combinations is incredibly large. For this reason why scientists haven’t been able to decide a valid scientific name for this group of hybrid origins.

Unlike the water frogs, it is very difficult to define a scientific name for the klepton inside Ambystoma, as the genomes of the different species can be found in different combinations and proportions in different unisexual individuals.

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.
• Alain Dubois (2011). Species and “strange species” in zoology: Do we need a “unified concept of species”?. Comptes Rendus Palevol. Vol 10. Pp: 77-94.
• Bogart, Bi, Fu, Noble & Niedzwiecki (2007). Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome. Vol 50. Pp: 119-136.
• Bi, Bogart & Fu (2009). An examination of intergenomic exchanges in A. Laterale-dependent unisexual salamanders in the genus Ambystoma. Cytogenetic and Genome Research. Vol 124. Pp: 44-50.
• Cover photo by Dave Huth.

Open-air concerts: the call of frogs and toads

Well into mid-spring, when the nights get warmer, it’s in the more temperate latitudes where we can start hearing the songs of the frogs. If we get close to any humid area in summer we’ll hear the frog’s and toad’s choirs which sing to attract a mate and proclaim their territories. In this entry we’ll explain the functioning and secrets hidden behind the different calls and songs of the anuran world.

CALL ANATOMY

Anurans are the amphibian order with the greatest vocal abilities. Practically all species make different kinds of calls which they use to communicate and transmit information to their own kind. That’s why frogs and toads have developed a much more specialized vocal systems than the rest of lissamphibians to generate their famous calls.

New Granada cross-banded tree frog (Smilisca phaeota) in the midst of a call. Photo by Santiago Ron.

Anuran calls originate when the air passes from the lungs through the larynx where the vocal cords are found. Anurans are the only lissamphibians with true vocal cords, while urodeles and caecilians don’t have them. Lissamphibians must pump air to their lungs to breath (although they also breathe through their skin) and in most frogs the call is generated during exhalation.

The oriental fire-bellied toad (Bombina orientalis) differs from the rest of anurans in that it emits its call both during exhalation and inhalation. Photo by Flickpicpete.

Most frogs and toads also present vocal sacs that amplify the sound of their calls, some of which can be heard up to one kilometre away. Anurans may have one vocal sac in their throat, or two vocal sacs in the corners of their mouth. To emit their famous calls they must have their mouths and nasal openings closed, to direct the air to the vocal sacs. Even if some species do not have vocal sacs, most species emit calls in some form or another.

The marsh frog (Pelophylax ridibundus) is an example of a frog with two vocal sacs in the corner of its mouth. Photo by Xavier Robin.

THE REASON WHY THEY SING

Toads and frogs use their calls for one main reason: to mate. In anurans singing is a method to distinguish animals of their own species, to help males and females find each other and to detect receptive individuals. Normally the males are the ones who sing to attract females and that’s why there’s a sexual dimorphism in the vocal sacs, with males having more developed sacs than females and more elaborated calls.

Even if it’s hard to appreciate, here we can see how in oak toads (Anaxyrus quercicus) the males (left) present a bigger skin fold corresponding to a more developed vocal sac than the females (right). Image by Eric Shashoua.

It is thought that during the evolution of anurans a process of sexual selection has taken place with females selecting the males with the more adequate calls. As a general rule females prefer males with louder and deeper calls. Probably, this is due to the fact that the bigger males (which generally have the deeper voices) are usually the stronger and older ones, indicating that they have been able to survive for a longer time and that they have better genes to transmit to their offspring.

In this video by Pocketbattleship we can hear the song of the American bullfrog (Lithobates catesbeianus), which is deep and powerful.

Yet there are some species with very high-pitched calls in which the selection by females is focused on other factors. Most anuran females also prefer very frequent (with many repetitions of the sound) and longer calls (long-lasting sounds). This is because singing is a really intense activity that requires a lot of energy, indicating the males that have been able to store enough energy to carry out such an exhausting activity.

The call of the golden poison frog (Phyllobates terribilis) is really high-pitched and is characterized by its high frequency, as we can see in this video by Mavortium.

The mating season usually comes after some rainy weather in the more arid habitats and during the summer nights in the colder latitudes. Males usually form what we call “choirs” near bodies of water, as it’s in those where mating will take place. Anuran species can be separated into two groups based on their reproduction strategy: explosive breeders and continuous breeders.

Explosive breeders are usually found in dry habitats, where water availability is scarce most of the year. After some heavy rains, males congregate in the recently-formed water zones and form the choirs, singing for one or two nights. In these species females arrive simultaneously. This brings great numbers of males and females to congregate in one night and in the same area and, once the females arrive, the males quit singing and start competing energetically to make sure they mate.

Couch’s spadefoot toad (Scaphiopus couchii) is a desert living amphibian from the south of the United States, which is characterized by its explosive mating. Image by CaliforniaHerps.

The most complex behaviours occur in species which breed continuously (the majority of the anurans). In these species the breeding season can last for six months and, while males come first to the mating spots and start to form the choirs, females arrive sporadically, mate and then abandon the mating ponds. This implies that when a female arrives there are many males in the mating spot, creating a strong selection of males by the females.

Common toads (Bufo bufo) are one of the best examples of continuous breeders. Photo by Janek.

Instead of chasing the females like the explosive breeders, these use different calls both to stand out from the rest of the males and therefore be chosen by the females, and to warn male rivals not to approach their territory. Even if usually the males that are able to maintain their territories for the longest time are normally the ones that will have more offspring, there are also are the so-called “satellite males” which instead of singing, stay close to the males with the more powerful calls and intercept the females attracted by them.

A CALL FOR EACH SPECIES

Obviously, the calls also allow the females to differentiate the individuals of their own species from others. This can also help us, as anurans are usually secretive and nocturne animals and their calls allow us to identify which species we have around us, even if darkness covers it all.

Down below we share with you the calls and songs of some anurans from the Iberian Peninsula, in case you go on an evening out, to help you identify the most common toads and frogs you can find in humid zones.

The common midwife toad (Alytes obstetricans) normally sings at night and on land usually far from water, using underground shelters as echo chambers because, as the rest of midwife toads (Alytes genus), it has no vocal sacs. The call is a clear and flute-like note which is repeated regularly, as we can hear in this video by The Nature Box.

The call of the Iberian spadefoot toad (Pelobates cultripes) is similar to a hen’s cluck. The deep song of the spadefoot toad is usually hard to hear, because this anuran usually sings underwater, although in this video by Versicolora we can hear it pretty well.

The spiny toads (Bufo spinosus) usually sing alone, sporadically and without forming choirs, with their body half-submerged and their head out of the water. The call consists in a series of harsh and pretty high-pitched sounds as we can hear in this recording by Martiño Cabana Otero.

The natterjack toads (Bufo calamita) sing at night, in very shallow waters, with their body pretty upright and inflating their huge vocal sac. Their call is pulsatile, powerful and boomy, and is repeated without rest as we can see in this video by Florian Begou.

The Mediterranean tree frog (Hyla meridionalis) usually sings at dusk and at night, both in water, on land or, as we can see in this video by Pedroluna, perched in the vegetation. The call consists in a single intense, nasal and monotonous note, which is repeated in long and irregular intervals.

Perez’s frogs (Pelophylax perezi) present a wide range of sounds which go from the typical “croak” to a sonorous call similar to a cackle. The choirs of these frogs are usually numerous and really loud, as we can hear in this video by Martiño Cabana Otero.

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.
• H. C. Gerhardt (1994). The Evolution of Vocalization in Frogs and Toads. Annual Review of Ecology and Systematics. Vol 25. Pp: 293-324.
• Morgan J. McLean, Phillip J. Bishop, Shinichi Nakagawa (2012). Assesing the Patterns of Evolution in Anuran Vocal Sexual Signals. Evolutionary Biology. Vol 40 (1). Pp: 141-149.
• Sound Water Stewards. The Riveting Life of Tree Frogs.
• Museo Nacional de Ciencias Naturales (MNCN). Comunicación acústica en anuros ibéricos: Influencia del clima, hábitat y el ambiente sonoro.
• Cover photo by Brian Gratwicke.

The killer fungus: the nightmare of the amphibians

In recent years, the populations of amphibians around the world have suffered a major decline, to the point that many of them disappear completely. Many researchers are running that the loss of these populations is due to several factors: climate change, habitat loss and the presence of a parasitic fungus. In this article will announce the parasite known as killer fungus.

BATRACHOCYTRIUM DENDROBATIDIS 

This is the scientific name given to this fungus. It belongs to the class Chytridiomycetes, which gathers fungus parasites of plants and invertebrates. However, this is the only one of this kind affecting vertebrate organisms. It is related to the disappearance of more than 200 species of amphibians, including the golden toad of Costa Rica.

One of the latest images that we have of the golden toad (Almirante periglenes). (Photo: Richard K.)

It has a life cycle that consists of two phases: a stationary (sporangium) and one mobile (via zoospores). In the image below we can see an outline of the structure of this type of fungi. The sporangium has some fine extensions known as rhizoids or mycelium rizoidal that allows to anchor itself in the inner skin layer. The zoospore emerges from the sporangium when it matures and presents a single apical flagellum.

Diagram of the structure of the fungus Bd. (photo: trilobite glassworks)

Batrachocytrium dedrobatidis is a parasite and need a host that provide nutrients. In this case, the fungus feeds on keratin of skin of amphibians. Zoospores arrives to the skin of the host by water and encyst in the areas with greatest amount of keratin. They lose the flagel and become a sporangium. They develop the mycelium and again produce zoospores that emerge into the water. In the event that there are no hosts around, the parasite becomes a saprophyte (feeds on organic matter in decomposition) waiting for the arrival of new amphibians.

Life cycle of B. dendrobatidis. (Photo: Roseblum)

Why this process results in a disease for amphibians?

CHYTRIDIOMYCOSIS

In amphibians, the skin is one of the most important organs. It develops functions such as hydration, osmoregulation, the thermoregulation and breathing (for example, the lissamphibians breathe only through the skin. Discover them in this article). Fungus feeds on keratin of skin, destroys the upper layers and spread over all body surface, preventing this organ to perform ion exchange. Individuals die from cardiac arrest.

Image of microscopy of skin of an amphibian stricken with chytridiomycosis. The arrows indicate the sporangia. (Photo: Che Weldon)

The sporangia are attached to keratinized skin areas, which get their nutrients. Approximately between 4 and 6 days after infection, they begin to develop the zoospores (black areas in the interior of the sporangia of the image above).When these spores have matured, are released through a spout that is initially closed. Stopper (bottom image) dissolves shortly before the release of zoospores.

Image of the surface of the skin of a frog by electronic scanner. The papillae of the sporangium are identified with a triangle. The black arrow indicates a sporangium with the plug dissolved. (Photo: Berger).

This disease affects only adult specimens. Even so, tadpoles are reservoirs of the disease, so they can become infected but do not develop symptoms. The fungus infects the tadpole keratinized areas (normally the areas of the mouth) and when the metamorphosis takes place, the fungus expands to other areas.

GEOGRAPHIC EXPANSION: ARRIVAL TO SPAIN

The fungus is characteristic of South African populations of Xenopus laevis (African Toad of nails, used in research), but spread all over the world through the traffic from infected individuals. The situation is so serious and the world Organization for Animal Health (OiE) has classified chytridiomycosis as a notifiable disease. In addition B. dendrobatidis is included in the list of 100 most invasive exotic species by the IUCN (if you want to know that they are invasive species, please read the following article).

World regions which have been confirmed positive cases of chytridiomycosis. (Photo: Bd-maps).

Spain was the first European country to suffer an outbreak of chytridiomycosis, particularly in the Parque Natural de Peñalara in Madrid. The common midwife toad (Alytes obstetricans) was the most affected. Positive cases in other Spanish regions, as for example in the Balearic Islands have also been found. There are many investigations underway to solve this problem, like for example of Project Zero of the CSIC General Foundation.

Positive amphibians to chytridiomycosis in Spain (photo: Bd-maps)

THE CASE OF THE BALEARIC MIDWIFE TOAD

The Balearic midwife Toad  (Alytes muletensis) is endemic to the Balearic Islands. It is classified as a vulnerable species by the IUCN (in this article we talk about this organization and its red list of species). It lives in ponds and ravines of difficult access in the Serra de Tramuntana (Mallorca). Specimens can reach around 4 cm and are nocturnal. Generally, this species was threatened by the destruction of their habitat or predation, but the latest threat facing it is chytridiomycosis.

Balearic midwife Toad or ferreret (photo: Guillem Gutiérrez).

Researchers found that certain populations experienced a significant decrease in the number of specimens, and they appeared dead without apparent reason. Studies revealed that these deaths were due to the presence of the parasitic fungus B.dendrobatidis. The population that presented more problems was the belonging to the area known as Torrent dels Ferrets (in 2004 it was confirmed the first case of chytridiomycosis).

Evolution of the population of Alytes muletensis in the Torrent dels Ferrerets. There have been deaths by Bd since 2004 (photo: Joan Mayol)

Research to ending this fungus has been a success. At the end of 2015, researchers from the Balearic Islands confirmed the first successful treatment against chytridiomycosis. They carried out disinfection in the natural environment (to eliminate any presence of zoospore) and combined it with an anti-fungal treatment to tadpoles. They managed to completely eliminate the presence of the parasite, and thus save the population. Even so, efforts to put an end to this fungus should not cease.

·

Chytridiomycosis is still a serious problem for global amphibian populations, but there is still hope. 

REFERENCES

• World organisation for animal health (OiE)
• CSIC General Foundation: Lucha sin cuartel contra la quitridiomicosis (spanish), by Jaume Bosch.
• 100 of the most invasive alien species in the world, ISSG. PDF
• The Mallorcan midwife Toad, from discovery to conservation, Joan Mayol and Joan Oliver. (Spanish)
• Cover Photo: Vance Vredenburg.

 

How to breathe without lungs, lissamphibian style

Even though most terrestrial vertebrates depend on lungs for breathing, lissamphibians also present cutaneous respiration, they breathe through their skin. Even if this may seem a handicap, because they must always keep their skin moist enough, in this entry we’ll see the many benefits that cutaneous respiration gives them and how in some groups, it has completely replaced pulmonary respiration.

BREATHING AIR OR WATER

Terrestrial vertebrates use lungs to perform gas exchange. While our aquatic ancestors breathed using gills, these are of no use on land, as gravity would collapse them and cause them to lose their form. As lungs are found inside the body, they can keep their form in a habitat with much higher gravity. Both gills and lungs have highly branched structures to increase their diffusion surface, and this way facilitate gas exchange (in a larger surface there’s more exchange).

Specimen of giant mudskipper (Periophthalmodon schlosseri), a fish from southeast Asia which is able to get out of water due, in part, to cutaneous respiration. Photo by Bernard Dupont.

We can find a third form of gas exchange in vertebrates. Even if it’s not as widespread as gills or lungs, cutaneous respiration is found in several groups of animals, such as lunged fish and some marine reptiles (turtles and sea snakes). Yet the lissamphibians are the group that has brought their specialization in cutaneous respiration to the ultimate level.

HOW DO LISSAMPHIBIANS BREATHE?

Present day lissamphibians are the group of tetrapods with the highest diversity of breathing strategies. Apart from cutaneous respiration present in all species, most lissamphibians are born in an aquatic larval stage with gills. After metamorphosis they develop lungs to breathe on land.

The larvae of urodeles and apods present external, filamentous and highly branched gills which allow them to breathe underwater. These must be constantly moved for gas exchange to occur. Some neotenic salamanders maintain their gills during adulthood. On the other hand, anuran tadpoles present internal gills covered by gill pouches.

Portrait of a salamander larva in which the branched filamentous gills can be appreciated. Photo by Brian Gratwicke.

Most terrestrial lissamphibians present a pair of simple lungs with few ramifications and large alveoli. These have a low gas diffusion rate compared with amniote’s lungs. Also, while amniotes ventilate their lungs using the expansion of the thoracic cavity and the diaphragm, lissamphibians must force the air to their lungs using a buccal-pump system.

Scheme of the system of pulmonary respiration of lissamphibians. In the buccal-pump system, the buccal cavity is filled with air and then, elevating the mouth floor, this air is forced to the lungs. Image by Mokele.

Apart from gill and pulmonary breathing, lissamphibians take oxygen to their blood by cutaneous respiration. The skin of lissamphibians is very thin and has a high concentration of capillaries (it’s got a great number of blood vessels). As a result, it has a great capacity of diffusion of gas molecules, allowing cutaneous respiration using a countercurrent system.

Modified scheme of a countercurrent exchange system. In this, deoxygenated blood (with CO2) circulates in the opposite direction that air does (full of O2) and between both fluids the gas interchange happens, in an attempt to equalize the concentration of both gases. Modified image by Joe.

Lissamphibian skin is different from that of amniotes in that it doesn’t present scales, feathers or fur. This makes lissamphibian skin much more permeable to both gases and water (which makes them great bioindicators of the health of their environment, as their skin takes up many different kinds of soluble substances). That’s why lissamphibians must keep their skin relatively moist for the gas exchange to take place.

Male northern crested newt (Triturus cristatus) in its nuptial phase. Its wide tail crests increase the surface of skin also increasing gas diffusion. Photo by Rainer Theuer.

Lissamphibians live constantly in a delicate equilibrium in which the skin must be kept moist enough to allow gas exchange, but not too permeable as to lose water, dehydrate and die. They acheive this living in wet environments, or creating layers of moist skin to create an aqueous ambient around them.

Photo of a Bombay caecilian (Ichthyophis bombayensis) a lissamphibian which lives in swamps and other humid habitats. Photo by Uajith.

Many lissamphibians present a large quantity of skin, which increase the respiratory surface. Some examples are the vascular papillae of the hairy frog (Trichobatrachus robustus), the skin folds of the frogs of the Telmatobius genus or the wide caudal fins of many newts.

Drawing of the hairy frog (Trichobatrachus robustus) where the papillae which gives it its name can be seen. Image extracted from Proceedings of the Zoological Society of London (1901).

Even though most frogs get most of their oxygen from their lungs during summer, during the colder months (when their metabolism is slower) many species hibernate at the bottom of frozen lakes, conducting their gas exchange solely through their skin.

Many subarctic lissamphibians hibernate underwater, using their skin to extract oxygen from water and expel carbon dioxide from blood. Photo by Ano Lobb.

Adult urodeles present a much higher diversity of breathing strategies, and among them there is one family that is the only group of terrestrial vertebrates that has no trace of lungs.

LIVING WITHOUT LUNGS

Inside the suborder of the salamandroideans we find the Plethodontidae family. These animals are popularly called lungless salamanders because, as their name implies, they have no lungs and depend exclusively on their skin to conduct gas exchange.

California slender salamander (Batrachoseps attenuatus) photographed by Kaldari. This is a perfect example of the long and thin bodies of plethodontids which facilitate gas diffusion.

These urodeles are distributed mainly through the Americas, with some species in the island of Sardinia and the Korean Peninsula. The most surprising fact about plethodontids is that, like most salamandroids, they are mainly terrestrial animals and do not present an aquatic larval stage. Even though some species present gills during their embryonic development, these are lost before hatching and lungs are never developed.

Photo of a red salamander (Pseudotriton ruber) a plethodontid endemic from the Atlantic coast of the USA. Photo by Leif Van Laar.

It is believed that this family evolved in fast-flowing mountain streams. The presence of lungs would have made them float too much, and this would have made moving much more difficult in such habitats. The cold waters of alpine rivers are rich in oxygen, making cutaneous respiration more than enough for these small animals.

Video by Verticalground100 in which we can see some plethodontid species.

A thin and vascularized skin (facilitates diffusion) and the evolution of long and slender bodies (facilitates the transport of O₂ through all the body) made lungs useless for plethodontids. Currently, lungless salamander are the most numerous of all urodele families, and they represent more than half the animal biomass in many North American ecosystems. Also, they are much more active than most lissamphibians, with highly developed nervous and sensory systems, being voracious predators of arthropods and other invertebrates.

Ozark zigzag salamander (Plethodon angusticlavius) a curious lungless salamander common in the state of Missouri. Image by Marshal Hedin.

As you can see lissamphibian cutaneous respiration allows them to make things few tetrapods are able to do. Passing a whole winter underwater and living on land without lungs are some of the incredible feats reserved to a small group of animals. Maybe lissamphibians still depend on the aquatic medium to survive, but as we have seen, they are far from being slow or primitive, as they present some of the most impressive physiological adaptations found on the animal kingdom.

REFERENCES

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

• http://www.mhhe.com/biosci/genbio/raven6b/graphics/raven06b/other/raven06_53.pdf
• http://www.biol.unt.edu/~burggren/pdfs/1985/%2849%29Feder,Burggren1985BR.pdf
• http://tolweb.org/Plethodontidae/15441
• http://www.jstor.org/stable/2462624?seq=1#page_scan_tab_contents
• http://www.fs.fed.us/psw/topics/wildlife/herp/pleth.shtml
• Cover image by Michael Righi.

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/

 

The evolution of amphibians: the conquest of the land

Amphibians were the first group of vertebrates to develop limbs and to be able to leave the water to conquer the land. Even if they are seen as simple and primitive animals by most people, amphibians show a wide diversity of survival strategies which have allowed them to occupy most terrestrial and fresh-water habitats. On this entry we’ll explain some of the aspects related to their evolution, explaining how our ancestors managed to get out of the water.

ORIGIN OF THE AMPHIBIANS

Current amphibians, together with reptiles, birds and mammals are found within the superclass Tetrapoda (“four limbs”), the vertebrate group that abandoned the sea to conquer the land. These first tetrapods were amphibians and they evolved around 395 million years ago during the Devonian period from lobe-finned fish named sarcopterygians (class Sarcopterygii, “flesh fins”) within which we find the coelacanth and the current lungfish.

Specimen of coelacanth (Latimeria chalumnae) a sarcopterygian fish, photo by smerikal.

This group of fish is characterized by its fins which, instead of being formed by rays like in most bony fish, they have a bony base that allowed the subsequent evolution of the limbs of the first amphibians. Within the sarcopterygians, the nearest relatives of the tetrapods are the osteolepiformes (order Osteolepiformes) a group of tetrapodomorph fish that got extinct about 299 million years ago.

Restoration of Eusthenopteron, an extinct osteolepiform, by Nobu Tamura.

ADAPTATIONS TO LIVE ON LAND

The conquest of land was not done from one day to the other; it was possible with the combination of multiple adaptations. Some of the most important characteristics that allowed the first amphibians to leave the water were:

• Evolution of lungs, which are homologous to the gas bladder that allows fish to control its buoyancy. Lungs appeared as an additional way to get oxygen from the air. In fact, there is actually a sarcopterygian family the members of which have lungs to get oxygen from the air, for they live in waters poor on oxygen.

• Dissection of Protopterus dolloi a sarcopteryigian fish with lungs.

• Development of the choanaes, or internal nostrils. While fish present a pair of external nostrils at each side of its snout through which water passes on while swimming, the ancestors of the tetrapods only had one external nostril at each side connected to the internal nostrils, the choanae, which communicated with the mouth. This allowed them to get air through their noses using lung ventilation and this way to smell outside of water.
• Apparition of the quiridium-like limb. The quiridium is the tetrapod’s most basic characteristic. This limb is known for having the differentiated parts: the stylopodium (one bone, the humerus or the femur), the zeugopodium (two bones, the radius or tibia and ulna or fibula) and the autopodium (fingers, hands, toes and feet). While the stylopodium and zeugopodium derived from the sarcopterygian’s fins, the autopodium is a newly-evolved structure exclusive from tetrapods.

Simplified drawing of the structure of the quiridium, by Francisco Collantes.

In short, the relatives of the osteolepiformes developed the tetrapod’s typical characteristics before ever leaving water, because they probably lived in brackish, shallow waters, poor in oxygen and that dried out quickly and often.

THE FIRST AMPHIBIANS

Probably the creature known as Tiktaalik is the closest animal to the mid-point between the osteolepiformes and the amphibians. The first recorded amphibians were labyrinthodonts meaning that their teeth had layers of dentin and enamel forming a structure similar to a maze.

Cross-section of a labyrinthodont tooth, form "On the Genesis of Species", by St. George Mivart.

There were four main groups of primitive amphibians, each characterized by: a group that includes the first animals that were able to get out of water, a second group which contains the ancestors of the amniotes (reptiles, birds and mammals) and two more groups, both candidates to be the ancestors of modern amphibians.

Order Ichthyostegalia

Ichthyostegalians were the first tetrapods to be able to leave the water. They appeared at the late Devonian period and they were big animals with large wide heads, short legs and an aquatic or semi aquatic lifestyle (they probably were pretty clumsy on land). They moved around using mainly their muscular tail with rays similar to that of fish.

Fossil and restoration of Tiktaalik. Photo by Linden Tea.

Similarly to current amphibians, they presented a lateral line (sensory organ that allows fish to detect vibrations and movement underwater) and were able to breathe through their skin (they lost the cosmoid scales of their ancestors). Also, the eggs were laid in the water, from which the tadpoles emerged and later on, they suffered a metamorphosis process to become adults just like current amphibians. Subsequently ichthyostegalians gave rise to the rest of amphibian groups.

Skeletons of Ichthyostega and Acanthostega, two typical ichthyostegalians.

Clade Reptiliomorpha

Reptiliomorphs were the ancestors of amniotes and appeared about 340 million years ago. Most of them were usually large and heavy animals, which presented more advanced adaptations to live on land (laterally-placed eyes instead of dorsally-placed ones and a knobby more impervious skin). Even though, reptiliomorphs still laid their eggs in the water and had larval-stages with gills. It wouldn’t be until the late Carboniferous period when the first amniotes (animals that could lay their eggs on dry land) would emancipate completely from water.

Mounted skeleton of Diadectes a large herbivorous reptiliomorph from the American Museum of Natural History, photo by Ghedoghedo.

Order Temnospondyli

This group is one of the possible candidates to being the ancestors of modern amphibians. This is the most diverse group of primitive amphibians and it survived until the early Cretaceous period, about 120 million years ago. The temnospondyls varied greatly in shape, size and lifestyle.

Restoration of Eryops megacephalus a large temnospondylian predator, by Dmitry Bogdanov.

Most of them were meat-eaters, but some were terrestrial predators, some were semi aquatic and some had returned completely to water. Even though, all species had to return to water to breed for the fertilization was external; while the female was laying clutches of eggs in the water, the male released the sperm over them.

Mounted skeleton of Koskinonodon a 3 metres long temnospondyl, from the American Museum of Natural History, photo by Lawrence.

Within the temnospondyls we can find some of the biggest amphibians that ever lived, such as Prionosuchus, with an estimated length of 4,5 meters and about 300 kilograms of weight. Also, even though their skin was not covered with scales, it wasn’t completely smooth like in modern amphibians.

Restoration of Prionosuchus by Dmitry Bogdanov.

It is believed that this group could be the sister-taxon of modern amphibians, even though there’s one last group which could be a candidate to that post.

Order Lepospondyli

Lepospondyls were a small group of primitive animals which appeared at the early Carboniferous and disappeared at the late Permian period. Even though lepospondyls were not as numerous and smaller than the temnospondyls, they presented a wide range of body shapes and adaptations.

Restoration of Diplocaulus magnicornis, of about 1 metre long was the biggest of all lepospondyls, by Nobu Tamura.

The first lepospondyls looked superficially like small lizards, but subsequently lots of groups suffered processes of limb reduction or loss.

Restoration of Pelodosotis, an advanced lepospondyl, by Dmitry Bogdanov.

The relationship of the lepospondyls with the rest of tetrapods isn’t very clear. Different hypothesis go from some authors arguing that they are a group separated from the labyrinthodonts, some thinking that they are the ancestor of current amphibians and reptiles, and some even saying that they are the ancestors of only a portion of modern amphibians.

Restoration of Lysorophus, a Permian lepospondyl, by Smokeybjb.

As we can see, the classification of primitive amphibians can be an extremely complex thing. On this entry I tried to make a summary of the most important groups of ancient amphibians and, on the next one, we’ll center on the evolution of modern amphibians, the so-called “lissamphibians”, and we’ll look in more detail all the controversies surrounding these curious animals.

REFERENCES

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

• Cover photo: Tyler Keillor and Beth Rooney.
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1691537/pdf/14667343.pdf
• http://www.biology.ualberta.ca/courses.hp/biol606/papers/Ahlberg+1998.pdf
• http://usf.usfca.edu/fac_staff/dever/tetrapod_review.pdf
• http://icb.oxfordjournals.org/content/early/2007/08/13/icb.icm055.full.pdf+html
• http://www.usfca.edu/fac_staff/dever/tetropodevol.pdf
• http://icb.oxfordjournals.org.sci-hub.org/content/5/2/287