Arxiu d'etiquetes: lissamphibian

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.

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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.

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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.

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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.

th-graph-min
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.

new-species-burrowing-caecilian-egg-closeup_48946_600x450-min
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.

urodela-min
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.

litoria_ewingii_tadpole-min
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.

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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.

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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:

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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.

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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.

Fire Bellied Toad
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.

Pelophylax_ridibundus_call
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.

Oak_toad,_sexual_dimorphism,_eshashoua_pd
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.

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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.

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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:

Difusió-anglès

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).

Giant_Mudskipper_(Periophthalmodon_schlosseri)_(15184970133)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.

Salamander_larva_closeupPortrait 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.

Four_stroke_buccal_pumpingScheme 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.

600px-ExchangerflowModified 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.

KammolchmaennchenMale 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.

Bombay_caecilianPhoto 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.

TrichobatrachusGreenDrawing 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.

6887057816_d68fccf4f4_oMany 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.

Kaldari_Batrachoseps_attenuatus_02California 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.

Northern_red_salamander_(Pseudotriton_ruber)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.

3679651745_d678454a1b_oOzark 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:

Difusió-anglès

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.
FrogSkinSection 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.
teethPhoto 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.
10050622254_8cffbfb0e4_oSkeleton 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).
Two_stroke_buccal_pumpingExplicative 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.

Batrachia proceraTwo 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.

temnospondyliDrawings 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.

 Lissamphibian_phylogenyModified 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.

TriadobatrachusInterpretation 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).
3888291918_f779053a0a_oPhoto 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.

Litoria_chloris_callingRed 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.

Paratype_of_Paedophryne_amauensis_(LSUMZ_95004)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.

BufoBufoTadpolesTadpoles 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.

Salamandra_TigrePhoto 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.

Joung_and_very_large_larva_of_Salamandra_infraimmaculata,_Ein_Kamon,_IsraelYoung 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.

20090924201238!P_striatus_USGSPhoto 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.

Eocaecilia_BWRestoration 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.

Ichthyophis kohtaoensis, ca 12Yellow-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).

KONICA MINOLTA DIGITAL CAMERAPhoto of Gymnopis multiplicata an american caecilian. Photo by Teague O'Mara.

REFERENCES

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

 Difusió-anglès

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.

6227540478_88c4b03cd2_o
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.

Eusthenopteron_BWRestoration 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.
  • Lungs_of_Protopterus_dolloiDissection 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.
Quiridio
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.

Labyrinthodon_MivartCross-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.

5212816060_da1a11e94e_oFossil 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.

ichthyostega(1)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.

Diadectes_phaseolinusMounted 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.

Eryops1DBRestoration 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.

Buettneria
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.

Prionosuchus_DBRestoration 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.

Diplocaulus_BWRestoration 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.

Pelodosotis1DBRestoration 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.

LysorophusRestoration 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:

Difusió-anglès