From Wikipedia, the free encyclopedia
Jump to: navigation, search
This article is about four-limbed vertebrates. For the structure, see Tetrapod (structure).
Temporal range:
Late DevonianPresent,[1] 367.5–0 Ma
Extant tetrapoda.jpg
Representatives of extant tetrapod groups, (clockwise from upper left): a frog (an lissamphibian), a hoatzin and a skink (two Sauropsids), a mouse (a synapsid)
Scientific classification
Kingdom: Animalia
Phylum: Chordata
(unranked): Tetrapodomorpha
(unranked): Stegocephalia
Superclass: Tetrapoda
Goodrich, 1930

The superclass Tetrapoda (Ancient Greek τετραπόδηs tetrapodēs, "four-footed"), or the tetrapods /ˈtɛtrəpɒd/, comprises the first four-limbed vertebrates and their descendants, including the living and extinct amphibians, reptiles, mammals, birds, and some extinct fish. Tetrapods evolved from the lobe-finned fishes around 390 million years ago in the middle Devonian Period,[2] with modern tetrapod groups having appeared by the late Devonian, 367.5 million years ago.[1] The specific aquatic ancestors of the tetrapods, and the process by which land colonization occurred, remain unclear, and are areas of active research and debate among palaeontologists at present.

While most species today are terrestrial, the first tetrapods were fully aquatic. Amphibians today generally remain semiaquatic, living the first stage of their lives as fish-like tadpoles. Amniotes evolved about 340 million years ago (crown amniotes 318 mya), and their descendants drove most amphibians to extinction. One population of amniotes diverged into lizards, dinosaurs, birds and their relatives, while another diverged into mammals and their extinct relatives. Several groups of tetrapods, such as the caecilians, snakes, cetaceans, sirenians, and moas have lost some or all of their limbs. In addition, many tetrapods have returned to partially aquatic or fully aquatic lives throughout the history of the group (modern examples of fully aquatic tetrapods include cetaceans and sirenians). The first returns to an aquatic lifestyle may have occurred as early as the Carboniferous Period,[3] whereas other returns occurred as recently as the Cenozoic, as in cetaceans, pinnipeds,[4] and several modern amphibians.[5]

The change from a body plan for breathing and navigating in water to a body plan enabling the animal to move on land is one of the most profound evolutionary changes known.[6] It is also becoming increasingly well-understood as a result of more transitional fossil finds and improved phylogenetic analysis.[7]


Tetrapods can be defined in cladistics as the nearest common ancestor of all living amphibians (the lissamphibians) and all living amniotes (reptiles, birds, and mammals), along with all of the descendants of that ancestor. This is a node-based definition (the node being the nearest common ancestor). The group so defined is the crown group, or crown tetrapods. The term tetrapodomorph is used for the stem-based definition: any animal that is more closely related to living amphibians, reptiles, birds, and mammals than to living dipnoi (lungfishes). The group so defined is known as the tetrapod total group.[8]

Stegocephalia is a larger group equivalent to some broader uses of the word "tetrapod", used by scientists who prefer to reserve the word "tetrapod" for the crown group (based on the nearest common ancestor of living forms).[9] Such scientists use the term "stem-tetrapod" to refer to those tetrapod-like vertebrates that are not members of the crown group, including the tetrapodomorph fishes[10]

The two subclades of crown tetrapods are Batrachomorpha and Reptiliomorpha. Batrachomorphs are all animals sharing a more recent common ancestry with living amphibians than with living amniotes (reptiles, birds, and mammals). Reptiliomorphs are all animals sharing a more recent common ancestry with living amniotes than with living amphibians.[11]


Tetrapoda includes four classes: amphibians, reptiles, mammals, and birds. Overall, the biodiversity of lissamphibians,[12] as well as of tetrapods generally,[13] has grown exponentially over time; the more than 30,000 species living today are descended from a single amphibian group in the Early to Middle Devonian. However, that diversification process was interrupted at least a few times by major biological crises, such as the Permian–Triassic extinction event, which at least affected amniotes.[14] The overall composition of biodiversity was driven primarily by amphibians in the Palaeozoic, dominated by reptiles in the Mesozoic and expanded by the explosive growth of birds and mammals in the Cenozoic. As biodiversity has grown, so has the number of niches that tetrapods have occupied. The first tetrapods were aquatic and fed primarily on fish. Today, the Earth supports a great diversity of tetrapods that live in many habitats and subsist on a variety of diets.[13] The following table shows summary estimates for each tetrapod class from the IUCN Red List of Threatened Species, 2014.3, for the number of extant species that have been described in the literature, as well as the number of threatened species.[15]

IUCN global summary estimates for extant tetrapod species as of 2014[15]
Tetrapod group Image Class Estimated number of
described species[15]
Threatened species
in Red List[15]
Species evaluated
as percent of
described species[15]
Best estimate
of percent of
threatened species[15]
lay eggs in water
Lithobates pipiens.jpg Amphibians 7,302 1,957 88% 41%
adapted to lay eggs
on land
Florida Box Turtle Digon3.jpg Sauropsids(traditional reptilia+birds) 20,463 2,300 75% 13%
Squirrel (PSF).png Mammals 5,513 1,199 100% 26%
Overall 33,278 5,456 80%  ?



Devonian fishes, including an early shark Cladoselache, Eusthenopteron and other lobe-finned fishes, and the placoderm Bothriolepis (Joseph Smit, 1905).


Tetrapods evolved from early bony fishes (Osteichthyes), specifically from the tetrapodomorph branch of lobe-finned fishes (Sarcopterygii), living in the early to middle Devonian period.

Eusthenopteron, ~385 Ma
Tiktaalik, ~375 Ma
Acanthostega, ~365 Ma

The first tetrapods probably evolved in the Emsian stage of the Early Devonian from Tetrapodomorph fish living in shallow water environments.[16][17] The very earliest tetrapods would have been animals similar to Acanthostega, with legs and lungs as well as gills, but still primarily aquatic and unsuited to life on land.

The earliest tetrapods inhabited saltwater, brackish-water, and freshwater environments, as well as environments of highly variable salinity. These traits were shared with many early lobed-finned fishes. As early tetrapods are found on two Devonian continents, Laurussia (Euramerica) and Gondwana, as well as the island of North China, it is widely supposed that early tetrapods were capable of swimming across the shallow (and relatively narrow) continental-shelf seas that separated these landmasses.[18][19][20]

Since the early 20th century, several families of tetrapodomorph fishes have been proposed as the nearest relatives of tetrapods, among them the rhizodonts (notably Sauripterus),[21][22] the osteolepidids, the tristichopterids(notably Eusthenopteron), and more recently the elpistostegalians (also known as Panderichthyida) notably the genus Tiktaalik.[23]

Among the notable features of Tiktaalik are the absence of bones covering the gills. These bones would otherwise connect the shoulder girdle with skull, making the shoulder girdle part of the skull. With the loss of the gill-covering bones, the shoulder girdle is separated from the skull, connected to the torso by muscle and other soft-tissue connections. The result is the appearance of the neck. With the exception of Tiktaalik, this feature is found only in tetrapods, not in tetrapodomorph fishes. Tiktaalik also had a pattern of bones in the skull roof (upper half of the skul) that bears similarity to the end-Devonian tetrapod Ichthyostega. The two also shared a semi-rigid ribcage of overlapping ribs which could have served as a substitute for a rigid spine. In conjunction with robust forelimbs and shoulder girdle, both Tiktaalik and Ichthyostega may have had the ability to locomote on land in the manner of a seal, with the forward portion of the torso elevated, the hind part dragging behind. And finally, the fin bones of Tiktaalik are somewhat similar to the limb bones of tetrapods.[24][25]

There are, however, issues, among them Tiktaalik's long spine with far more vertebra than in any known tetrapod or any other known tetrapodomorph fish. Of even greater concern is the date: the oldest tetrapod trace fossils (tracks and trackways) predate Tiktaalik by a considerable margin. Several hypotheses have been proposed to explain the date discrepancy: 1) The nearest common ancestor of tetrapods and Tiktaalik dates to the Early Devonian. By this hypothesis, the Tiktaalik lineage is the closest to tetrapods, but Tiktaalik itself was late-surviving relict.[26] 2) Tiktaalik represents a case of parallel evolution. 3) Tetrapods evolved more than once.[27][28]

Euteleostomi (bony vertebrates)
Actinopterygii (ray-fined fishes)

Sarcopterygii (fleshy-limbed vertebrates)

(Actinistia) Coelacanth


Dipnoi (Lungfish)


†Tetrapodomorph fishes


Devonian fossils[edit]

The oldest evidence for the existence of tetrapods comes from trace fossils, tracks (footprints) and trackways found in Zachełmie, Poland, dated to the Eifelian stage of the Middle Devonian, 390-1 mya.[2] The adult tetrapods had an estimated length of 2.5 m (8 feet). They lived in a lagoon with an average depth of 1–2 m, although it is not known at what depth the underwater tracks were made. The lagoon was inhabited by a variety of marine organisms and was apparently salt water. The average water temperature was 30 degrees C (86 F).[29][30] The second oldest evidence for tetrapods, also tracks and trackways, date from 386 mya (Valentia Island, Ireland)[31]

The oldest partial fossils of tetrapods date from the Frasnian beginning ~380 mya. These include Elginerpeton and Obruchevichthys.[32] Some paleontologists dispute their status as true (digit-bearing) tetrapods.[33]

All known forms of Frasnian tetrapods became extinct in the Late Devonian extinction, also known as the end-Frasnian extinction.[34] This marked the beginning of a gap in the tetrapod fossil record known as the Famennian gap, occupying roughly the first half of the Famennian stage.[34]

The oldest near-complete tetrapod fossils, Acanthostega and Ichthyostega, date from the second half of the Fammennian.[35][36] Although both were essentially four-footed fish, Ichthyostega is the earliest known tetrapod that may have had the ability to pull itself onto land and drag itself forward with its forelimbs. There is no evidence that it did so, only that it may have been anatomically capable of doing so.[37][38]

The end-Fammenian marked another extinction, known as the end-Fammenian extinction or the Hangenberg event, which is followed by another gap in the tetrapod fossil record, Romer's gap, also known as the Tournaisian gap.[39] This gap, which was initially 30 million years, but has been gradually reduced over time, currently occupies much of the 13.9-million year Tournaisian, the first stage of the Carboniferous period.[40]

Palaeozoic tetrapods[edit]

Devonian stem-tetrapods[edit]

Ichthyostega, 374–359 Ma

Tetrapod-like vertebrates first appeared in the early Devonian period.[31] These early "stem-tetrapods" would have been animals similar to Ichthyostega,[29] with legs and lungs as well as gills, but still primarily aquatic and unsuited to life on land. The Devonian stem-tetrapods went through two major bottlenecks during what the Late Devonian extinctions, also known as the end-Frasnian and end-Fammenian extinctions. These extinction events led to the disappearance of stem-tetrapods with fish-like features.[41] When stem-tetrapods reappear in the fossil record in early Carboniferous deposits, some 10 million years later, the adult forms of some are somewhat adapted to a terrestrial existence.[40][42] Why they went to land in the first place is still debated.

Carboniferous tetrapods[edit]

Edops, 323-299 Ma

During the early Carboniferous, the number of digits on hands and feet of stem-tetrads became standardized at no more than five, as lineages with more digits died out. By mid-Carboniferous times, the stem-tetrapods had radiated into two branches of true ("crown group") tetrapods. Modern amphibians are derived from either the temnospondyls or the lepospondyls (or possibly both), whereas the anthracosaurs were the relatives and ancestors of the amniotes (reptiles, mammals, and kin). The first amniotes are known from the early part of the Late Carboniferous. Amphibians must return to water to lay eggs; in contrast, amniote eggs have a membrane ensuring gas exchange out of water and can therefore be laid on land.

Amphibians and amniotes were affected by the Carboniferous Rainforest Collapse (CRC), an extinction event that occurred ~300 million years ago. The sudden collapse of a vital ecosystem shifted the diversity and abundance of major groups. Amniotes were more suited to the new conditions. They invaded new ecological niches and began diversifying their diets to include plants and other tetrapods, previously having been limited to insects and fish.[43]

Permian tetrapods[edit]

Diadectes, 290–272 Ma

In the Permian period, in addition to temnospondyl and anthracosaur clades, there were two important clades of amniote tetrapods, the sauropsids and the synapsids. The latter were the most important and successful Permian animals.

The end of the Permian saw a major turnover in fauna during the Permian–Triassic extinction event. There was a protracted loss of species, due to multiple extinction pulses.[44] Many of the once large and diverse groups died out or were greatly reduced.

Mesozoic tetrapods[edit]

The diapsids (a subgroup of the sauropsids) began to diversify during the Triassic, giving rise to the turtles, crocodiles, and dinosaurs. In the Jurassic, lizards developed from other diapsids. In the Cretaceous, snakes developed from lizards and modern birds branched from a group of theropod dinosaurs. By the late Mesozoic, the groups of large, primitive tetrapod that first appeared during the Paleozoic such as temnospondyls and amniote-like tetrapods had gone extinct. Many groups of synapsids, such as anomodonts and therocephalians, that once comprised the dominant terrestrial fauna of the Permian, also became extinct during the Mesozoic; however, during the Jurassic, one synapsid group (Cynodontia) gave rise to the modern mammals, which survived through the Mesozoic to later diversify during the Cenozoic.

Cenozoic tetrapods[edit]

Following the great faunal turnover at the end of the Mesozoic, six major groups of tetrapods persisted into the Cenozoic era:


Linnaeus' 1735 classification of animals, with tetrapods occupying the first three classes

The classification of tetrapods has a long history. Traditionally, tetrapods are divided into four classes based on gross anatomical and physiological traits.[45] Snakes and other legless reptiles are considered tetrapods because they are sufficiently like other reptiles that have a full complement of limbs. Similar considerations apply to caecilians and aquatic mammals. Newer taxonomy is frequently based on cladistics instead, giving a variable number of major "branches" (clades) of the tetrapod family tree.

As is the case throughout evolutionary biology today, there is debate over how to properly classify the groups within Tetrapoda. Traditional biological classification sometimes failrs to recognize evolutionary transitions between older groups and descendant groups with markedly different characteristics. For example, the birds, which evolved from the dinosaurs, are defined as a separate group from them, because they represent a distinct new type of physical form and functionality. In phylogenetic nomenclature, in contrast, the newer group is always included in the old. For this school of taxonomy, dinosaurs and birds are not groups in contrast to each other, but rather birds are a sub-type of dinosaurs.

History of classification[edit]

The tetrapods, including all large- and medium-sized land animals, have been among the best understood animals since earliest times. By Aristotle's time, the basic division between mammals, birds and egg-laying tetrapods (the "herptiles") was well known, and the inclusion of the legless snakes into this group was likewise recognized.[46] With the birth of modern biological classification in the 18th century, Linnaeus used the same division, with the tetrapods occupying the first three of his six classes of animals.[47] While reptiles and amphibians can be quite similar externally, the French zoologist Pierre André Latreille recognized the large physiological differences at the beginning of the 19th century and split the herptiles into two classes, giving the four familiar classes of tetrapods: amphibians, reptiles, birds and mammals.[48]

Modern classification[edit]

With the basic classification of tetrapods settled, a half a century followed where the classification of living and fossil groups was predominately done by experts working within classes. In the early 1930s, American vertebrate palaeontologist Alfred Romer (1894–1973) produced an overview, drawing together taxonomic work from the various subfields to create an orderly taxonomy in his Vertebrate Paleontology.[49] This classical scheme with minor variations is still used in works where systematic overview is essential, e.g. Benton (1998) and Knobill and Neill (2006).[50][51] While mostly seen in general works, it is also still used in some specialist works like Fortuny & al. (2011).[52] The taxonomy down to subclass level shown here is from Hildebrand and Goslow (2001):[53]

  • Superclass Tetrapoda - four-limbed vertebrates
    • Class Amphibia - amphibians
    • Class Sauropsida - reptiles (includes birds)
      • Subclass Diapsida - diapsids, including crocodiles, dinosaurs (includes birds), lizards, snakes and turtles
    • Class Synapsida - mammals and their ancestors

This classification is the one most commonly encountered in school textbooks and popular works. While orderly and easy to use, it has come under critique from cladistics. The earliest tetrapods are grouped under Class Amphibia, although several of the groups are more closely related to amniotes than to modern day amphibians. Traditionally, birds are not considered a type of reptile, but crocodiles are more closely related to birds than they are to other reptiles, such as lizards. Birds themselves are thought to be descendents of theropod dinosaurs. Basal non-mammalian synapsids ("mammal-like reptiles") traditionally also sort under Class Reptilia as a separate subclass,[45] but they are more closely related to mammals than to living reptiles. Considerations like these have led some authors to argue for a new classification based purely on phylogeny, disregarding the anatomy and physiology.



Stem tetrapods are all animals more closely related to tetrapods than to lungfish, but excluding the tetrapod crown group. The cladogram bellow illustrates the relationships of stem-tetrapods, from Swartz, 2012:[54]


Dipnomorpha (lungfishes and relatives)










Gogonasus Gogonasus BW.jpg


Osteolepis Osteolepis BW.jpg






Eusthenopteron Eusthenopteron BW.jpg








Panderichthys Panderichthys BW.jpg


Tiktaalik Tiktaalik BW.jpg


Elginerpeton Elginerpeton BW.jpg


Acanthostega Acanthostega BW.jpg

Ichthyostega Ichthyostega BW.jpg

Whatcheeriidae Pederpes22small.jpg

Colosteidae Greererpeton BW.jpg

Crassigyrinus Crassigyrinus BW.jpg


Tetrapoda Seymouria BW.jpg

Crown group[edit]

Crown tetrapods are defined as the nearest common ancestor of all living tetrapods (amphibians, reptiles, birds, and mammals) along with all of the descendants of that ancestor.

The inclusion of certain extinct groups in the crown Tetrapoda depends on the relationships of modern amphibians, or lissamphibians. There are currently three major hypotheses on the origins of lissamphibians. In the temnospondyl hypothesis (TH), lissamphibians are most closely related to dissorophoid temnospondyls, which would make temnospondyls tetrapods. In the lepospondyl hypothesis (LH), lissamphibians are the sister taxon of lysorophian lepospondyls, making lepospondyls tetrapods and temnospondyls stem-tetrapods. In the polyphyletic hypothesis (PH), frogs and salamanders evolved from dissorophoid temnospondyls while caecilians come out of microsaur lepospondyls, making both lepospondyls and temnospondyls true tetrapods.[55][56][56]

Temnospondyl hypothesis (TH)[edit]

This hypothesis comes in a number of variants, most of which have lissamphibians coming out of the dissorophoid temnospondyls, usually with the focus on amphibamids and branchiosaurids.[57]

The Temnospondyl Hypothesis is the currently favored or majority view, supported by Ruta et al (2003a,b), Ruta and Coates (2007), Coates et al (2008), Sigurdsen and Green (2011), and Schoch (2013,2014).[56][58]

Cladogram modified after Coates, Ruta and Friedman (2008).[59]

Crown-group Tetrapoda 




 crown group Lissamphibia 





 Crown-group Amniota 






total group Lissamphibia
total group Amniota

Lepospondyl hypothesis (LH)[edit]

Cladogram modified after Laurin, How Vertebrates Left the Water (2010).[60]

Stegocephalia ("Tetrapoda") 















stem tetrapods
total group Amniota
total group Lissamphibia

Polyphyly hypothesis (PH)[edit]

This hypothesis has batrachians (frogs and salamander) coming out of dissorophoid temnospondyls, with caecilians out of microsaur lepospondyls. There are two variants, one developed by Carroll,[61] the other by Anderson.[62]

Cladogram modified after Schoch, Frobisch, (2009).[63]


stem tetrapods


basal temnospondyls













Anatomy and physiology of early tetrapods[edit]

The tetrapod's ancestral fish, tetrapodomorph, possessed similar traits to those inherited by the early tetrapods, including internal nostrils and a large fleshy fin built on bones that could give rise to the tetrapod limb. Their palatal and jaw structures were similar to those of early tetrapods, and their dentition was similar too, with labyrinthine teeth fitting in a pit-and-tooth arrangement on the palate.

A major difference between early tetrapodomorph fishes and early tetrapods was in the relative development of the front and back skull portions; the snout is much less developed than in most early tetrapods and the post-orbital skull is exceptionally longer than an amphibian's.

To propagate in the terrestrial environment, animals had to overcome certain challenges. Their bodies needed additional support, because buoyancy was no longer a factor. Water retention was now important, since it was no longer the living matrix, and could be lost easily to the environment. Finally, animals needed new sensory input systems to have any ability to function reasonably on land.


A notable characteristic that make a tetrapod's skull different from a fish's are the relative frontal and rear portion lengths. The fish had a long rear portion while the front was short; the orbital vacuities were thus located towards the anterior end. In the tetrapod, the front of the skull lengthened, positioning the orbits farther back on the skull.


In tetrapodomorph fishes such as Eusthenopteron, the part of the body that would later become the neck was covered by a number of gill-covering bones known as the opercular series. These bones functioned as part of pump mechanism for forcing water through the mouth and past the gills. When the mouth opened to take in water, the gill flaps closed (including the gill-covering bones), thus ensuring that water entered only through the mouth. When the mouth closed, the gill flaps opened and water was forced through the gills. In Acanthostega, a basal tetrapod, the gill-covering bones have disappeared, although the underlying gill arches are still present. Besides the opercular series, Acanthostega also lost the throat-covering bones (gular series). The opercular series and gular series combined are sometimes known as the operculo-gular or operculogular series. Other bones in the neck region lost in Acanthostega (and later tetrapods) include the extrascapular series and the supracleithral series. Both sets of bones connect the shoulder girdle to the skull. With the loss of these bones, tetrapods acquired a neck, allowing the head to rotate somewhat independently of the torso. This, in turn, required stronger soft-tissue connections between head and torso, including muscles and ligaments connecting the skull with the spine and shoulder girdle. Bones and groups of bones were also consolidated and strengthened.[64]

In Carboniferous tetrapods, the neck joint (occiput) provided a pivot point for the spine against the back of the skull. In tetrapodomorph fishes such as Eusthenopteron, no such neck joint existed. Instead, the notochord (a sort of spine made of cartilage) entered a hole in the back of the braincase and continued to the middle of the braincase. Acanthostega had the same arrangement as Eusthenopteron, and thus no neck joint. The neck joint evolved independently in different lineages of early tetrapods.[65]


Cross-section of a labyrinthodont tooth

Tetrapods had a tooth structure known as "plicidentine" characterized by infolding of the enamel as seen in cross-section. The more extreme version found in early tetrapods is known as "labyrinthodont" or "labyrinthodont plicidentine." This type of tooth structure has evolved independently in several types of bony fishes, both ray-finned and lobe finned, some modern lizards, and in a number of tetrapodomorph fishes. The infolding appears to evolve when a fang or large tooth grows in a small jaw, erupting when it still weak and immature. The infolding provides added strength to the young tooth, but offers little advantage when the tooth is mature. Such teeth are associated with feeding on soft prey in juveniles.[66][67]

Axial skeleton[edit]

With the move from water to land, the spine had to resist the bending caused by body weight and had to provide mobility where needed. Previously, it could bend along its entire length. Likewise, the paired appendages had not been formerly connected to the spine, but the slowly strengthening limbs now transmitted their support to the axis of the body.


The shoulder girdle was disconnected from the skull, resulting in improved terrestrial locomotion. The early sarcopterygians cleithrum was retained as the clavicle, and the interclavicle was well-developed, lying on the underside of the chest. In primitive forms, the two clavicles and the interclavical could have grown ventrally in such a way as to form a broad chest plate. The upper portion of the girdle had a flat, scapular blade, with the glenoid cavity situated below performing as the articulation surface for the humerus, while ventrally there was a large, flat coracoid plate turning in toward the midline.

The pelvic girdle also was much larger than the simple plate found in fishes, accommodating more muscles. It extended far dorsally and was joined to the backbone by one or more specialized sacral ribs. The hind legs were somewhat specialized in that they not only supported weight, but also provided propulsion. The dorsal extension of the pelvis was the ilium, while the broad ventral plate was composed of the pubis in front and the ischium in behind. The three bones met at a single point in the center of the pelvic triangle called the acetabulum, providing a surface of articulation for the femur.


Fleshy lobe-fins supported on bones seem to have been an ancestral trait of all bony fishes (Osteichthyes). The ancestors of the ray-finned fishes (Actinopterygii) evolved their fins in a different direction. The Tetrapodomorph ancestors of the Tetrapods further developed their lobe fins. The paired fins had bones distinctly homologous to the humerus, ulna, and radius in the fore-fins and to the femur, tibia, and fibula in the pelvic fins.[68]

The paired fins of the early sarcopterygians were smaller than tetrapod limbs, but the skeletal structure was very similar in that the early sarcopterygians had a single proximal bone (analogous to the humerus or femur), two bones in the next segment (forearm or lower leg), and an irregular subdivision of the fin, roughly comparable to the structure of the carpus / tarsus and phalanges of a hand.


In typical early tetrapod posture, the upper arm and upper leg extended nearly straight horizontal from its body, and the forearm and the lower leg extended downward from the upper segment at a near right angle. The body weight was not centered over the limbs, but was rather transferred 90 degrees outward and down through the lower limbs, which touched the ground. Most of the animal's strength was used to just lift its body off the ground for walking, which was probably slow and difficult. With this sort of posture, it could only make short broad strides. This has been confirmed by fossilized footprints found in Carboniferous rocks.


Early tetrapods had a wide gaping jaw with weak muscles to open and close it. In the jaw were moderate-sized palatal and vomerine (upper) and coronoid (lower) fangs, as well rows of smaller teeth. This was in contrast to the larger fangs and small marginal teeth of earlier tetrapodomorph fishes such as Eusthenopteron. Although this indicates a change in feeding habbits, the exact nature of the change in unknown. Some scholars have suggested a change to bottom-feeding or feeding in shallower waters (Ahlberg and Milner 1994). Others have suggesting a mode of feeding comparable to that of the Japanese giant salamander, which uses both suction feeding and direct biting to eat small crustaceans and fish. A study of these jaws shows that they were used for feeding underwater, not on land.[69]

In later terrestrial tetrapods, two methods of jaw closure emerge: static and kinetic inertial (also known as snapping). In the static system, the jaw muscles are arranged in such a way that the jaws have maximum force when shut or nearly shut. In the kinetic inertial system, maximum force is applied when the jaws are wide open, resulting in the jaws snapping shut with great velocity and momentum. Although the kinetic inertial system is occasionally found in fish, it requires special adaptations (such as very narrow jaws) to deal with the high viscosity and density of water, which would otherwide impede rapid jaw closure.

The tetrapod tongue is built from muscles that once controlled gill openings. The tongue is anchored to the hyoid bone, which was once the lower half of a pair of gill bars (the second pair after the ones that evolved into jaws).[70][71][72] The tongue did not evolve until the gills began to disappear. Acanthostega still had gills, so this would have been a later development. In an aquatically feeding animals, the food supported by water and can literally float (or get sucked in) to the mouth. On land, the tongue becomes important.


The evolution of early tetrapod respiration was influenced by an event known as the "charcoal gap," a period of more than 20 million years, in the middle and late Devonian, when atmospheric oxygen levels were too low to sustain wildfires.[73] During this time, fish inhabiting anoxic waters (very low in oxygen) would have been under evolutionary pressure to develop their air-breathing ability.[74][75][76]

Early tetrapods probably relied on four methods of respiration: with lungs, with gills, cutaneous respiration (skin breathing), and breathing through the lining of the digestive tract, especially the mouth.


The early tetrapod Acanthostega had at least three and probably four pairs of gill bars, each containing deep grooves in the place where one would expect to find the afferent branchial artery. This strongly suggests that functional gills were present.[77] Some aquatic temnospondyls retained internal gills at least into the early Jurassic.[78]


Lungs originated as an extra pair of pouches in the throat, behind the gill pouches.[79] They were probably present in the last common ancestor of bony fishes. In some fishes they evolved into swim bladders for maintaining buoyancy.[80][81] Lungs and swim bladders are homologous (descended from a common ancestral form) as is the case for the pulmonary artery (which delivers deoxygenated blood from the heart to the lungs) and the arteries that supply swim bladders.[82] Air was introduced into the lungs by a process known as buccal pumping.[83][84]

In the earliest tetrapods, exhalation was probably accomplished with the aid of the muscles of the torso (the thoracoabdominal region). Inhaling with the ribs was either primitive for amniotes, or evolved independently in at least two different lineages of amniotes. It is not found in amphibians.[85][86] The muscularized diaphragm is unique to mammals.[87]

Recoil aspiration[edit]

Although tetrapods are widely thought to have inhaled through buccal pumping (mouth pumping), according to an alternative hypothesis, aspiration (inhalation) occurred through passive recoil of the exoskeleton in a manner similar to the contemporary primitive ray-finned fish polypterus. This fish inhales through its spiracle (blowhole), an anatomical feature present in early tetrapods. Exhalation is powered by muscles in the torso. During exhalation, the bony scales in the upper chest region become indented. When the muscles are relaxed, the bony scales spring back into position, generating considerable negative pressure within the torso, resulting in a very rapid intake of air through the spiracle. [88] [89] [90]

Cutaneous respiration[edit]

Skin breathing, known as cutaneous respiration, is common in fish and amphibians, and occur both in and out of water. In some animals waterproof barriers impede the exchange of gasses through the skin. For example, and keratin in human skin, the scales of reptiles, and modern proteinaceous fish scales impede exchange of gasses. However, early tetrapods had scales made of highly vascularized bone covered with skin. For this reason, it is though that early tetrapods could engage some significant amount of skin breathing.[91]

Carbon dioxide metabolism[edit]

Although air-breathing fish can absorb oxygen through their lungs, the lungs tend to be ineffective for discharging carbon dioxide. In tetrapods, the ability of lungs to discharge CO2 came about gradually, and was not fully attained until the evolution of amniotes. The same limitation applies to gut air breathing (GUT), i.e., breathing with the lining of the digestive tract.[92] Tetrapod skin would have been effective for both absorbing oxygen and discharging CO2, but only up to a point. For this reason, early tetrapods may have experienced chronic hypercapnia (high levels of blood CO2). This is not uncommon in fish that inhabit waters high in CO2.[93] According to one hypothesis, the "sculpted" or "ornamented" dermal skull roof bones found in early tetrapods may have been related to a mechanism for relieving respiratory acidosis (acidic blood caused by excess CO2) through compensatory metabolic alkalosis.[94]


Early tetrapods probably had a three-chambered heart, as do modern amphibians and reptiles, in which oxygenated blood from the lungs and de-oxygenated blood from the respiring tissues enters by separate atria, and is directed via a spiral valve to the appropriate vessel — aorta for oxygenated blood and pulmonary vein for deoxygenated blood. The spiral valve is essential to keeping the mixing of the two types of blood to a minimum, enabling the animal to have higher metabolic rates, and be more active than otherwise.[95]



The difference in density between air and water causes smells (certain chemical compounds detectable by chemoreceptors) to behave differently. An animal first venturing out onto land would have difficulty in locating such chemical signals if its sensory apparatus was designed for aquatic detection.

Lateral line system[edit]

Fish have a lateral line system that detects pressure fluctuations in the water. Such pressure is non-detectable in air, but grooves for the lateral line sense organs were found on the skull of early tetrapods, suggesting either an aquatic or largely aquatic habitat. Modern amphibians, which are semi-aquatic, exhibit this feature whereas it has been retired by the higher vertebrates.


Changes in the eye came about because the refractive index of light differs between air and water, so the focal length of the lens altered to function in air. The eye was now exposed to a relatively dry environment rather than being bathed by water, so eyelids developed and tear ducts evolved to produce a liquid to moisten the eyeball.

Early tetrapods inherited a set of five rod and cone opsins known as the vertebrate opsins.[96][97][98]

Four cone opsins were present in the first vertebrate, inherited from invertebrate ancestors:

  • LWS/MWS (long- to medium-wave sensitive) - green, yellow, or red
  • SWS1 (short-wave sensitive) - ultraviolet or violet - lost in monotremes (platypus, echidna)
  • SWS2 (short-wave sensitive) - violet or blue - lost in therians (placental mammals and marsupials)
  • RH2 (rhodopsin-like cone opsin) - green - lost separately in amphibians and mammals, retained in reptiles and birds

A single rod opsin, rhodopsin, was present in the first jawed vertebrate, inherited from a jawless vertebrate ancestor:

  • RH1 (rhodposin) - blue-green - used night vision and color correction in low-light environments


Tetrapods retained the balancing function of the middle ear from fish ancestry.


Air vibrations could not set up pulsations through the skull as in a proper auditory organ. The spiracle was retained as the otic notch, eventually closed in by the tympanum, a thin, tight membrane.

The hyomandibula of fish migrated upwards from its jaw supporting position, and was reduced in size to form the stapes. Situated between the tympanum and braincase in an air-filled cavity, the stapes was now capable of transmitting vibrations from the exterior of the head to the interior. Thus the stapes became an important element in an impedance matching system, coupling airborne sound waves to the receptor system of the inner ear. This system had evolved independently within several different amphibian lineages.

The impedance matching ear had to meet certain conditions to work. The stapes had to be perpendicular to the tympanum, small and light enough to reduce its inertia, and suspended in an air-filled cavity. In modern species that are sensitive to over 1 kHz frequencies, the footplate of the stapes is 1/20th the area of the tympanum. However, in early amphibians the stapes was too large, making the footplate area oversized, preventing the hearing of high frequencies. So it appears they could only hear high intensity, low frequency sounds—and the stapes more probably just supported the brain case against the cheek.

See also[edit]


  1. ^ a b Alexander, Pyron R. (July 2011). "Divergence Time Estimation Using Fossils as Terminal Taxa and the Origins of Lissamphibia". Systematic Biology 60 (4): 466–481. doi:10.1093/sysbio/syr047. PMID 21540408. 
  2. ^ a b Narkiewicz, Katarzyna; Narkiewicz, Marek (January 2015). "The age of the oldest tetrapod tracks from Zachełmie, Poland". Lethaia 48 (1): 10–12. doi:10.1111/let.12083. ISSN 0024-1164. 
  3. ^ Laurin 2010, pp. 163
  4. ^ Canoville, Aurore; Laurin, Michel (June 2010). "Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on paleobiological inferences". Biological Journal of the Linnean Society 100 (2): 384–406. doi:10.1111/j.1095-8312.2010.01431.x. 
  5. ^ Laurin, Michel; Canoville, Aurore; Quilhac, Alexandra (August 2009). "Use of paleontological and molecular data in supertrees for comparative studies: the example of lissamphibian femoral microanatomy". Journal of Anatomy 215 (2): 110–123. doi:10.1111/j.1469-7580.2009.01104.x. PMC 2740958. PMID 19508493. 
  6. ^ Long JA, Gordon MS (Sep–Oct 2004). "The greatest step in vertebrate history: a paleobiological review of the fish-tetrapod transition". Physiol. Biochem. Zool. 77 (5): 700–19. doi:10.1086/425183. PMID 15547790.  as PDF
  7. ^ Shubin, N. (2008). Your Inner Fish: A Journey Into the 3.5-Billion-Year History of the Human Body. New York: Pantheon Books. ISBN 978-0-375-42447-2. 
  8. ^ Clack 2012, pp. 87–9
  9. ^ Laurin, Michel; Girondot, Marc; de Ricqlès, Armand (2000). "Early tetrapod evolution" (PDF). Trends in Ecology & Evolution 15 (3): 118–123. doi:10.1016/S0169-5347(99)01780-2. ISSN 0169-5347. 
  10. ^ Laurin 2010, p. 9
  11. ^ Benton 2009, p. 99
  12. ^ Marjanović D, Laurin M (2008). "Assessing confidence intervals for stratigraphic ranges of higher taxa: the case of Lissamphibia" (PDF). Acta Palaeontologica Polonica 53 (3): 413–432. doi:10.4202/app.2008.0305. 
  13. ^ a b Sahney, S., Benton, M.J. and Ferry, P.A. (August 2010). "Links between global taxonomic diversity, ecological diversity and the expansion of vertebrates on land" (PDF). Biology Letters 6 (4): 544–547. doi:10.1098/rsbl.2009.1024. PMC 2936204. PMID 20106856. 
  14. ^ Ward, P.D.; Botha, J.; Buick, R.; Kock, M.O.; Erwin, D.H.; Garrisson, G.H.; Kirschvink, J.L.; Smith, R. (4 February 2005). "Abrupt and gradual extinction among late Permian land vertebrates in the Karoo Basin, South Africa". Science 307 (5710): 709–714. Bibcode:2005Sci...307..709W. doi:10.1126/science.1107068. PMID 15661973. 
  15. ^ a b c d e f The World Conservation Union. 2014. IUCN Red List of Threatened Species, 2014.3. Summary Statistics for Globally Threatened Species. Table 1: Numbers of threatened species by major groups of organisms (1996–2014).
  16. ^ Clack 2012, pp. 125–6
  17. ^ McGhee 2013, p. 92
  18. ^ Clack 2012, p. 132
  19. ^ Laurin 2010, pp. 64–8
  20. ^ Steyer 2012, pp. 37–8
  21. ^ Clack 2012, p. 76
  22. ^ McGhee 2013, p. 75
  23. ^ McGhee 2013, pp. 74–75
  24. ^ Clack 2012, pp. 82–4
  25. ^ Steyer 2012, pp. 17–23
  26. ^ Janvier, Philippe; Clément, Gaël (7 January 2010). "Palaeontology: Muddy tetrapod origins". Nature 463 (7277): 40–41. doi:10.1038/463040a. ISSN 0028-0836. 
  27. ^ McGhee 2013, pp. 79–81
  28. ^ Clack 2012, p. 126
  29. ^ a b Niedźwiedzki, Grzegorz; Szrek, Piotr; Narkiewicz, Katarzyna; Narkiewicz, Marek; Ahlberg, Per E. (7 January 2010). "Tetrapod trackways from the early Middle Devonian period of Poland". Nature 463 (7277): 43–48. doi:10.1038/nature08623. ISSN 0028-0836. 
  30. ^ Narkiewicz, Marek; Grabowski, Jacek; Narkiewicz, Katarzyna; Niedźwiedzki, Grzegorz; Retallack, Gregory J.; Szrek, Piotr; De Vleeschouwer, David (15 February 2015). "Palaeoenvironments of the Eifelian dolomites with earliest tetrapod trackways (Holy Cross Mountains, Poland)". Palaeogeography, Palaeoclimatology, Palaeoecology 420: 173–192. doi:10.1016/j.palaeo.2014.12.013. ISSN 0031-0182. 
  31. ^ a b McGhee 2013, p. 78
  32. ^ Clack 2012, pp. 117–8
  33. ^ Laurin 2010, p. 85
  34. ^ a b McGhee 2013, pp. 103–4
  35. ^ Callier, V.; Clack, J. A.; Ahlberg, P. E. (2009). "Contrasting Developmental Trajectories in the Earliest Known Tetrapod Forelimbs". Science 324 (5925): 364–367. doi:10.1126/science.1167542. ISSN 0036-8075. 
  36. ^ Clack 2012, pp. 147
  37. ^ Clack 2012, pp. 159
  38. ^ Pierce, Stephanie E.; Clack, Jennifer A.; Hutchinson, John R. (2012). "Three-dimensional limb joint mobility in the early tetrapod Ichthyostega". Nature. doi:10.1038/nature11124. ISSN 0028-0836. 
  39. ^ McGhee 2013, pp. 214–5
  40. ^ a b Claessens, Leon; Anderson, Jason S.; Smithson, Tim; Mansky, Chris F.; Meyer, Taran; Clack, Jennifer (2015). "A Diverse Tetrapod Fauna at the Base of 'Romer's Gap'". PLOS ONE 10 (4): e0125446. doi:10.1371/journal.pone.0125446. ISSN 1932-6203. 
  41. ^ McGhee 2013, pp. 263–4
  42. ^ Research project: The Mid-Palaeozoic biotic crisis: Setting the trajectory of Tetrapod evolution
  43. ^ Sahney, S., Benton, M.J. & Falcon-Lang, H.J. (2010). "Rainforest collapse triggered Pennsylvanian tetrapod diversification in Euramerica" (PDF). Geology 38 (12): 1079–1082. doi:10.1130/G31182.1. 
  44. ^ Sahney, S., Benton, M.J. (2008). "Recovery from the most profound mass extinction of all time" (PDF). Proceedings of the Royal Society: Biological 275 (1636): 759–65. doi:10.1098/rspb.2007.1370. PMC 2596898. PMID 18198148. 
  45. ^ a b Romer, A.S. (1949). The Vertebrate Body. Philadelphia: W.B. Saunders.  (2nd ed. 1955; 3rd ed. 1962; 4th ed. 1970)
  46. ^ Lloyd, G.E.R. (1961). "The Development of Aristotle's Theory of the Classification of Animals". Phronesis 6 (1): 59–81. doi:10.1163/156852861X00080. JSTOR 4181685. 
  47. ^ Linnaeus, Carolus (1758). Systema naturae per regna tria naturae :secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis (in Latin) (10th edition ed.). Stockholm: Laurentius Salvius. 
  48. ^ Latreielle, P.A. (1804): Nouveau Dictionnaire à Histoire Naturelle, xxiv., cited in Latreille's Familles naturelles du règne animal, exposés succinctement et dans un ordre analytique, 1825
  49. ^ Smith, C.H. (2005): Romer, Alfred Sherwood (United States 1894-1973), homepage from Western Kentucky University
  50. ^ Benton, M. J. (1998) The quality of the fossil record of vertebrates. Pp. 269-303, in Donovan, S. K. and Paul, C. R. C. (eds), The adequacy of the fossil record, Fig. 2. Wiley, New York, 312 pp.
  51. ^ Neill, J.D. (ed.) (2006): Knobil and Neill’s Physiology of Reproduction, Vol 2, Academic Press, 3rd edition (p. 2177)
  52. ^ Fortuny, J.; Bolet, A.; Sellés, A.G.; Cartanyà, J.; Galobart, À. (2011). "New insights on the Permian and Triassic vertebrates from the Iberian Peninsula with emphasis on the Pyrenean and Catalonian basins" (PDF). Journal of Iberian Geology 37 (1): 65–86. doi:10.5209/rev_JIGE.2011.v37.n1.5. 
  53. ^ Hildebrand, M. & G. E. Goslow, Jr. Principal ill. Viola Hildebrand. (2001). Analysis of vertebrate structure. New York: Wiley. p. 429. ISBN 0-471-29505-1. 
  54. ^ Swartz, B. (2012). "A marine stem-tetrapod from the Devonian of Western North America". PLoS ONE 7 (3): e33683. doi:10.1371/journal.pone.0033683. PMC 3308997. PMID 22448265.  edit
  55. ^ Sigurdsen, Trond; Green, David M. (2011). "The origin of modern amphibians: a re-evaluation". Zoological Journal of the Linnean Society 162 (2): 457–469. doi:10.1111/j.1096-3642.2010.00683.x. ISSN 0024-4082. 
  56. ^ a b c Benton, Michael (4 August 2014). Vertebrate Palaeontology. Wiley. p. 398. ISBN 978-1-118-40764-6. Retrieved 2 July 2015. 
  57. ^ Narins, Peter M.; Feng, Albert S.; Fay, Richard R. (11 December 2006). Hearing and Sound Communication in Amphibians. Springer Science & Business Media. p. 16. ISBN 978-0-387-47796-1. Retrieved 2 July 2015. 
  58. ^ S. Blair Hedges; Sudhir Kumar (23 April 2009). The Timetree of Life. OUP Oxford. pp. 354–. ISBN 978-0-19-156015-6. 
  59. ^ Coates, Michael I.; Ruta, Marcello; Friedman, Matt (2008). "Ever Since Owen: Changing Perspectives on the Early Evolution of Tetrapods". Annual Review of Ecology, Evolution, and Systematics 39 (1): 571–592. doi:10.1146/annurev.ecolsys.38.091206.095546. ISSN 1543-592X. 
  60. ^ Laurin 2010, pp. 133
  61. ^ Carroll, Robert L. (2007). "The Palaeozoic Ancestry of Salamanders, Frogs and Caecilians". Zoological Journal of the Linnean Society 150 (s1): 1–140. doi:10.1111/j.1096-3642.2007.00246.x. ISSN 0024-4082. 
  62. ^ Anderson, Jason S. (December 2008). "Focal Review: The Origin(s) of Modern Amphibians". Evolutionary Biology 35 (4): 231–247. doi:10.1007/s11692-008-9044-5. ISSN 0071-3260. 
  63. ^ Frobisch, N. B.; Schoch, R. R. (2009). "Testing the Impact of Miniaturization on Phylogeny: Paleozoic Dissorophoid Amphibians". Systematic Biology 58 (3): 312–327. doi:10.1093/sysbio/syp029. ISSN 1063-5157. 
  64. ^ Clack 2012, pp. 29,45–6
  65. ^ Clack 2012, pp. 207,416
  66. ^ Clack 2012, pp. 373–4
  67. ^ Schmidt-Kittler, Norbert; Vogel, Klaus (6 December 2012). Constructional Morphology and Evolution. Springer Science & Business Media. pp. 151–172. ISBN 978-3-642-76156-0. Retrieved 15 July 2015. 
  68. ^ Meunier, François J.; Laurin, Michel (January 2012). "A microanatomical and histological study of the fin long bones of the Devonian sarcopterygian Eusthenopteron foordi". Acta Zoologica 93 (1): 88–97. doi:10.1111/j.1463-6395.2010.00489.x. 
  69. ^ Neenan, J. M.; Ruta, M.; Clack, J. A.; Rayfield, E. J. (22 April 2014). "Feeding biomechanics in Acanthostega and across the fish-tetrapod transition". Proceedings of the Royal Society B: Biological Sciences 281 (1781): 20132689–20132689. doi:10.1098/rspb.2013.2689. ISSN 0962-8452. 
  70. ^ Clack 2012, p. 49,212
  71. ^ Butler, Ann B.; Hodos, William (2 September 2005). Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. John Wiley & Sons. p. 38. ISBN 978-0-471-73383-6. Retrieved 11 July 2015. 
  72. ^ Cloudsley-Thompson, John L. (6 December 2012). The Diversity of Amphibians and Reptiles: An Introduction. Springer Science & Business Media. p. 117. ISBN 978-3-642-60005-0. Retrieved 11 July 2015. 
  73. ^ Clack, J. A. (2007). "Devonian climate change, breathing, and the origin of the tetrapod stem group" (PDF). Integrative and Comparative Biology 47 (4): 510–523. doi:10.1093/icb/icm055. ISSN 1540-7063. 
  74. ^ McGhee 2013, pp. 111,139–41
  75. ^ Scott, A. C.; Glasspool, I. J. (18 July 2006). "The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration". Proceedings of the National Academy of Sciences 103 (29): 10861–10865. doi:10.1073/pnas.0604090103. ISSN 0027-8424. 
  76. ^ Clack 2012, pp. 140
  77. ^ Clack 2012, pp. 166
  78. ^ Sues, Hans-Dieter; Fraser, Nicholas C. (13 August 2013). Triassic Life on Land: The Great Transition. Columbia University Press. p. 85. ISBN 978-0-231-50941-1. Retrieved 21 July 2015. 
  79. ^ Clack 2012, pp. 23
  80. ^ Laurin 2010, pp. 36–7
  81. ^ McGhee 2013, pp. 68–70
  82. ^ Webster, Douglas; Webster, Molly (22 October 2013). Comparative Vertebrate Morphology. Elsevier Science. pp. 372–5. ISBN 978-1-4832-7259-7. Retrieved 22 May 2015. 
  83. ^ Benton 2009, p. 78
  84. ^ Clack 2012, pp. 238
  85. ^ Clack 2012, pp. 73–4
  86. ^ Brainerd, Elizabeth L.; Owerkowicz, Tomasz (2006). "Functional morphology and evolution of aspiration breathing in tetrapods". Respiratory Physiology & Neurobiology 154 (1-2): 73–88. doi:10.1016/j.resp.2006.06.003. ISSN 1569-9048. 
  87. ^ Merrell, Allyson J.; Kardon, Gabrielle (2013). "Development of the diaphragm - a skeletal muscle essential for mammalian respiration". FEBS Journal 280 (17): 4026–4035. doi:10.1111/febs.12274. ISSN 1742-464X. 
  88. ^ Evans, David H.; Claiborne, James B. (15 December 2005). The Physiology of Fishes, Third Edition. CRC Press. p. 107. ISBN 978-0-8493-2022-4. Retrieved 28 July 2015. 
  89. ^ Graham, Jeffrey B.; Wegner, Nicholas C.; Miller, Lauren A.; Jew, Corey J.; Lai, N Chin; Berquist, Rachel M.; Frank, Lawrence R.; Long, John A. (January 2014). "Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods" (PDF). Nature Communications 5. doi:10.1038/ncomms4022. ISSN 2041-1723. 
  90. ^ Vickaryous, Matthew K.; Sire, Jean-Yves (April 2009). "The integumentary skeleton of tetrapods: origin, evolution, and development". Journal of Anatomy 214 (4): 441–464. doi:10.1111/j.1469-7580.2008.01043.x. ISSN 0021-8782. 
  91. ^ Clack 2012, pp. 233–7
  92. ^ Nelson, J. A. (March 2014). "Breaking wind to survive: fishes that breathe air with their gut". Journal of Fish Biology 84 (3): 554–576. doi:10.1111/jfb.12323. ISSN 0022-1112. 
  93. ^ Clack 2012, p. 235
  94. ^ Janis, C. M.; Devlin, K.; Warren, D. E.; Witzmann, F. (August 2012). "Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis". Proceedings of the Royal Society B: Biological Sciences 279 (1740): 3035–3040. doi:10.1098/rspb.2012.0558. ISSN 0962-8452. 
  95. ^ Clack 2012, pp. 235–7
  96. ^ David M. Hunt; Mark W. Hankins; Shaun P Collin; N. Justin Marshall (4 October 2014). Evolution of Visual and Non-visual Pigments. Springer. pp. 165–. ISBN 978-1-4614-4355-1. 
  97. ^ Stavenga, D.G.; de Grip, W.J.; Pugh, E.N. (30 November 2000). Molecular Mechanisms in Visual Transduction. Elsevier. p. 269. ISBN 978-0-08-053677-4. Retrieved 14 June 2015. 
  98. ^ Lazareva, Olga F.; Shimizu, Toru; Edward A. Wasserman (19 April 2012). How Animals See the World: Comparative Behavior, Biology, and Evolution of Vision. OUP USA. p. 459. ISBN 978-0-19-533465-4. Retrieved 14 June 2015. 


Further reading[edit]