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THE PHARYNX AND ITS GILLS
CUTANEOUS GAS EXCHANGE AND GILLS
BACTERIABACTERIA       The first cells evolved in a world with little atmospheric oxygen.  Oxygen was probably toxic to them, as it is to many bacteria today which can only survive in anaerobic environments.  Thus, the ability to exchange and utilize oxygen was not essential to early life.  As oxygen slowly accumulated in the Precambrian atmosphere, life evolved the ability to tolerate oxygen and ultimately eukaryotic cells required it.  Some eukaryotic organisms evolved into multicellular animals, which utilized oxygen but lacked specific respiratory structures. All animals perform gas exchange through their superficial cells (e.g. the skin), which is the only site of gas exchange with the environment in the most primitive animals.   Many primitive animals are very flat to increase the surface area for cutaneous gas exchange.
     Many of the Precambrian animals in the Ediacaran fauna were also very flat.  Annelid worms such as Dickinsonia could reach lengths of more than a meter but were only a few millimeters thick.

dICKINSONIA

PLANARIA

PLANARIA

     Cutaneous respiration continues to play a significant role in some vertebrates, especially eels, amphibians, and bats.  The amount of respiration performed through the skin in amphibians varies.  In dry-skinned toads, 20% of the total gas exchange occurs through the skin while cutaneous respiration reaches 76% of total gas exchange in the salamander Triturus.  Salamanders of the family Plethodontidae lack lungs and perform all of their gas exchange through the skin. The giant aquatic salamander Cryptobranchus (which can reach about 2 feet and 2 pounds) performs more than 90% of its respiration through its skin. (Hoar, 1983, p. 497).  A lizard may take up 2% of its oxygen and lose 4% of its carbon dioxide through its skin.  In mammals, the oxygen which is absorbed through the skin is primarily used by skin cells.  In bats, 12% of carbon dioxide may be lost through the skin (primarily the wings)(Prosser, 1973, p.168).  Even vertebrates that depend on gills or lungs as their primary organs of gas exchange (including humans) perform cutaneous respiration (Kardong, p.403).

    Early in the history of life, invertebrates evolved additional anatomical structures to supplement the gas exchange performed by the skin.  Gills exist in many invertebrates such as worms, mollusks, arthropods.  Many polychaete worms possess parapodia which can contribute to respiration and some even possess true gills (Barrington, p. 212).  In primitive arthropods (such as copepods and most ostracopods), parapodia assist in cutaneous respiration similar to their function in worms (Barrington, p. 226).  Many aquatic animals, such as arthropods, can also perform gas exchange in air.  The horseshoe crab Limulus can survive several days out of water (Barrington, p. 228).

     In humans, the respiratory tract is lined by ciliated cells which can sweep mucus away from the lungs to the mouth, where it can be swallowed.  This mucociliary mechanism was originally a feature of the digestive system, rather than the respiratory system.  All animals with a digestive cavity, ranging from simple coelenterates through vertebrates possess cilia move particles which are caught in mucus toward the digestive cavity (Fretter).  Although this is a feeding mechanism in lower animals (especially filter feeders), higher vertebrates utilize this same mechanism to remove microbes and debris from the respiratory tract and take it to the stomach to be destroyed.   Early bilateran animals (such as flatworms), evolved a pharynx which was ciliated, and possessed longitudinal and circular muscle layers (Dougherty, p. 197, Beklemishev 2, p. 196).  The pharynx of a flatworm is depicted below.

PHARYNX

Ciliated pseudostratified epithelia (which lines the human trachea) exists in the pharynx of hemichordates.  (Benito, form Harrison 1997, p. 72.)

          Many aquatic animals draw water into their bodies and later expel it.  Although this may primarily be a filter-feeding mechanism, it offers the organism an opportunity to perform gas exchange as well.  The filter feeding of sponges not only allows nutrient exchange, but also an exchange of oxygen and carbon dioxide (Barrington).  Sponge cells are depicted below.

SPONGE

Deuterostomes originally seem to have used their pharyngeal slits for filter feeding.  These structures cannot be considered gills in hemichordates given that they possess too few blood vessels servicing the pharyngeal slits to perform much gas exchange  (Harris; Benito, form Harrison 1997, p. 59).  In hemichordates (acorn worms) the pharynx includes pouches which open to the exterior through slits and solid endoskeletal bars, just as in the gill-bearing pharynx of fish (Benito, form Harrison 1997, p. 20).

       In urochordates, the pharyngeal slits are essential for gas exchange and can thus be considered gills (Harris).  The pharyngeal slits of an adult tunicate are evident in the following image.

TUNICATE

  The blood vessels to pharyngeal slits are more extensive in urochordates than hemichordates (Harris).  These structures function as part of the internal gills around the pharynx (unlike the external gills observed in other groups of invertebrates; Romer, p. 348).  In cephalochordates, aortic arches carry deoxygenated blood to the gills from which oxygenated blood travels to the dorsal aorta (Willey, 49).   Cephalochordates use gelatinous rods in walls around gill clefts for support.  Fish possess cartilaginous rods in their gill arches.  After the loss of gills following the adaptation to terrestrial environments in tetrapods, the cartilage of the vertebrate pharyngeal arches was modified to form structures such as the hyoid, trachea, and larynx (Willey, 28).  

    In Amphioxus, the pharynx stretches for half the length of the body and contains 100-200 gill slits (depending on the species).  Each gill bar contains a skeletal rod for support composed of collagen and glycosaminoglycans. (Ruppert, from Harrison, 1997, p. 434).  A few of the anterior bars may open onto the external environment for part of their lives.  Amphioxus performs significant gas exchange through skin in addition the gas exchange performed with the water which enters the mouth, passes over these gill clefts, and departs the body through a single atriopore opening on the ventral side of its posterior  (Weichert, 1970, p. 211).

AMPHIOXUS
     Hagfish may have from 6 (Myxine) to 14 (Bdellostoma) pharyngeal pouches (Weichert, 1970, p. 209).  Jawless have a cartilaginous branchial basket around pharyngeal arches. (Weichert, 1970, p. 214).  Hagfish are depicted below.
HAGFISH HAGFISH
HAGFISH HAGFISH

lamprey

LAMPREY

     In gnathostomes, gills are no longer involved in feeding (as in lower chordates, lamprey larvae, and fossil ostracoderms) (Romer, p. 357).  While the cleft between the first and second arch either closes or is modified to form a spiracle, a normal gill slit was located here in the most primitive jawed vertebrates, placoderms (Weichert, 1970, p. 214).  Some lungfish have capillaries in all their gill arches while others lack capillaries in the first two arches (Hoar, 1970).  Chick and turtle embryos may have some outgrowths from the pharyngeal arches which are vestigial homologs of gills (Weichert, 1970, p. 221)

SHARK

SHARK

SHARK

PERCH

PERCH

Cross section of fish gill:

GILL

GAR
Some fish evolved additional respiratory structures.  Note that the gar possesses a swim bladder and the lungfish possesses lungs which supplement the gas exchange of the gills.  In sarcopterygians and tetrapods, the lungs develop from the ventral portion of the respiratory pharynx while the swim bladder develops from the dorsal side (Perry, 2004). 

Like fish, amphibian larvae regulate respiration through the detection of oxygen by gill neuroepithelial cells (Jonz, 2006). Features of the neural control of respiration and the response to hypoxia are shared between mammals and amphibians (Hedrick, 2005).

LUNGFISH

LUNGFISH

LUNGFISH

     Even though land vertebrates no longer use gills for respiration, tetrapod embryos develop pharyngeal pouches with slits, cartilaginous bars, aortic arches, and their own cranial nerves as occurs in fish.  These tissues are subsequently remodeled in tetrapod embryos.

The following images are of the pharyngeal arches in a chick embryo.

PHARYNGEAL ARCHES PHARYNGEAL ARCHES
PHARYNGEAL ARCHES

PIG EMBRYO

PHARYNGEAL ARCHES

PHARYNGEAL ARCHES
PHARYNGEAL ARCHES PHARYNGEAL ARCHES

Human embryos develop these pharyngeal pouches, slits, bars, and aortic arches as do all chordate embryos.  Despite the adaptation to terrestrial environments, tetrapod embryos still bear vestiges of the aquatic ancestral condition.

 

EMBRYO