BREATHING FISH

     At first, it may seem as if the ability to breathe atmospheric oxygen in the ancestors of the amphibians was an almost insurmountable challenge.  Upon closer consideration, however, the evolution of air-breathing seems well within the capabilities of aquatic organisms.  The ability of aquatic animals to breath oxygen from the air is thought to have evolved at least 67 times (Maina, 1998).   A number of crustaceans can breathe air.  There are lung-like structures in some snails.  Some oligochaete and polychaete worms perform gas exchange through their anus (Maina, 1998). The sea cucumber Holothuria tubulosa can breathe in stagnant water by rising through the surface and performing gas exchange through its cloaca (Hoar, 1983, p. 505).  Some fish perform gas exchange with water moved through their highly vascularized rectum.  Some aquatic turtles possess 2 sacs opening into the cloaca which can function in gas exchange (Weichert, 1970, p. 244).  A considerable number of fish can breathe oxygen from air.  The majority do so as a supplement to the oxygen supplied by their gills but some are actually obligate air breathers that would drown in water without access to air. 

     Different groups of fish have evolved different mechanisms for air breathing.  Increased vascularization of caudal and pelvic fins function in respiration in the walking goby (Periopthalmus) and the South American lungfish, respectively (Weichert, 1970, p. 244).  Some fish perform gas exchange with the air through their buccopharyngeal apparatus (mouth and throat) such as Electrophorus electricus of the family Electrophoridae.  Some do so through using an opercular structures, such as Hypopomus brevicostris of the family Sternarchidae, Symbranchus marmotatus and Monopterus javanesis of the family Symbranchidae, Pseudapocryptes lanceolatus of the family Gobiidae, Heteropneustes fossilis of the family Saccobranchidae, Clarias lazera, Clarias magur, and Clarias mossambicus of the family Clariidae, and Macropodus cupanus, Colisa fasciata, Betta, Osphronemus gorami, and Anabas testudineus from the family Anabantidae (Maina, 1998).  While the fine filaments of  most fish gills collapse in air, a few fish, such as Symbranchus and Hypopomus, possess modified gills which do not collapse in air in addition to vascularized mouth and pharyngeal cavities which permit gas exchange.  Gill breathing in air occurs in eels and Periopthalmus.  In electric eels, the folding of the oral cavity increases the respiratory surface to about 15% of the total body surface.  This area apparently performs sufficient gas exchange since the gills in adults are almost nonfunctional (Johansen, Kjell from Hoar, 1970).

     Some fish perform gas exhange in their intestine, such as Misgurnus fossilis and Lepidocephalichthys guntea from the family Cobitidae and Doras of the family Doridae.  Some members of the family Ophicephalidae possess pharyngeal lungs such as Opicephalus (Channa) puntatus, O. marulius, O. striatus, O. gachua, and Amphipnous cuchia.  Anguilla anguilla, A. bengalensis, and A. japonicus of the family Anguillidae can perform gas exchange through their skin.    Eels which are removed from water can absorb about 60% of their oxygen uptake in water.  While most of this oxygen exchange in air occurs through the skin, a significant portion occurs across the gills, indicating that their gills have also been adapted for air-breathing (Hoar, 1970; Maina, 1998).   Some members of the families Loricaridae and Callichthyidae possess modifications of their gastrointestinal tract which allow gas exchange using swallowed air.  Some of these fish are obligate air breathers and may travel for short distances over land (Maina, 1998).  An air-breathing species of the family Loricaridae is pictured in the following photos.

     Bony fish possess a sac which opens into the esophagus.  While it is called a swim bladder and the buoyancy it generates is an adaptation for swimming, this structure can also be used for respiration and seems to be homologous to tetrapod lungs.  Some actinopterygian fish perform gas exchange using their swim bladder, such as Arapaima gigas of the family Arapaimidae, Gymnarchus of the family Gymnarchidae, Erythrinus unitaeniatus of the family Characinidae, Umbra from the family Umbridae, and Notopterus notopterus and Notopterus chitala of the family Notopteridae.  Maina, 1998).  This sac is used for the respiration of oxygen from air in dipnoan sarcopterygians and in the most primitive actinopterygians, suggesting that this was its primitive function in the ancestral bony fish.  In other words, swim bladders seem to have evolved from lungs rather than lungs from swim bladders.  (Perry, 2001).

      Basal actinopterygians even possess blood vessels which correspond to the pulmonary circuit of lungfish and tetrapods, although there is no separation of this blood from that of the systemic circuit in the heart (Johansen, Kjell from Hoar, 1970).  The blood hematocrit (the percentage of the blood composed of red blood cells) of some air-breathing fishes even reaches that observed in humans (such as that of Symbranchus, 47%, and of Electrophorus, 41%) (Johansen, Kjell from Hoar, 1970).  (Perry, 2001).  The brainstem activity in swallowing is similar in the gar (which possesses a swim bladder) and tetrapods (which have lungs) (Perry, 2001).  The first fish to breathe oxygen from air may have taken advantage of muscular mechanisms of gulping food which are similar to those used in breathing (Dutta, p. 138).    

GAR

BOWFIN

Note that there are capillaries in the swim bladder of fish which bring the blood close enough to the epithelial lining of the bladder to perform gas exchange with the air contained within.

LUNGS

     If a lung is defined as a vascularized sac which performs gas exchange with the air, then lungs are known in some spiders, decapods, chilopods, isopods, and snails (and in all scorpions).  In invertebrates, gas exchange occurs through diffusion only, in contrast to vertebrate lungs which require muscle contractions to transport air through respiratory surfaces. (Hoar, 1983, p. 508)

     The ancestors of bony fish evolved lungs as an endodermal outpocket of the esophagus (Romer, p. 363).  Although advanced actinopterygians (teleosts) converted this outpocket to a swim bladder to control buoyancy, the earliest actinopterygians possess lungs (such as Polypterus) whose texture is similar to amniote lungs.  The gar pike and Amia will suffocate without atmospheric air; as will sarcopterygian lungfish (Romer, p. 360, 364).  The placoderm Bothriolepis possessed a pair of pharyngeal pouches which extended posteriorly and probably functioned as simple lungs.  Some sharks possess a vestigial structure which may be related to this (Weichert, 1970; Kardong). 

      Among vertebrates, lungs are not unique to tetrpods, they actually evolved in fish before the adaptation to life on land.  Some fish alive today, appropriately called lungfish, possess true lungs, the homologs of tetrapod lungs.  The Australian lungfish, the most primitive of the three lungfish, possesses a single lung while the African and South American lungfish possess paired lungs.  Once African lungfish (Protopterus) reach more than 100g in size, more than 85% of their oxygen is obtained through gas exchange in the lung (Orgeig, 1995).  While the Australian lungfish is a facultative air breather, African and South American lungfish are primary air breathers during several months of the year which they spend on land (Hoar, 1970).  The African lungfish secretes a mucus cocoon where it waits in the mud for the next rainy season.  During this time, it depends on oxygen from the air which is breathed through its lungs.  Experimentally, these lungfish have been able to survive 5 years in this state.(Webster, 1974, p. 372)  The lungs of lungfish actually function better than those of many amphibians. (Weichert, 1970, p. 221).

          In some lungfishes, the lungs possess adaptations such as internal divisions and alveoli-like chambers which resemble the lungs of amphibians.  Electron microscopic examination has demonstrated that lungfish and amniote lungs share the same basic structure. (Johansen, Kjell from Hoar, 1970; Romer, p. 364-6).    

    Amphibian lungs are similar to the lungs of lungfish and empty into the esophagus, as do those of lungfish.  Many amphibian lungs have alveoli, at least in the basal areas.  In reptiles, there is an increased internal complexity in the lungs as septa further divide them (Romer, p. 363; 366   Amphibian and reptilian lungs are located in the pleuroperitoneal cavity (Weichert, 1970).  Mammalian ancestors evolved separate pleural cavities (also present in some reptiles) (Romer, p. 320).  Reptiles possess both type I and type II cells in their lungs (Maina, 1998).

      Birds possess the most efficient respiratory system among tetrapods. Air sacs in bones also help lower specific gravity— a preadaptation for flight which was achieved by some feathered dinosaurs. The majority of the air in the avian respiratory system is outside the lungs (Webster, 1974, p. 384).  Most snakes a vestigial left lung. (Torrey, p. 334). 

FROG

TURTLE

ALLIGATOR

OPOSSUM

SHEEP

PIG

CAT

     The number of lobes of the lungs varies in primates.  The rhesus monkey possesses an accessory lobe (lobus azygos) on the posterior side of the right lung.  Tarsiers have additional lobes and orangutan lungs usually lack lobes. (Hartman)

MONKEY

HUMAN MODEL

SURFACTANT

     Human lungs depend on surfactant proteins to decrease water tension in air sacs.  The epithelia of an air sac is pictured below.