The problematical ancestral vertebrates, amphioxus and the tunicates, that are largely sedentary in habit, obtain their microscopic food through ciliary action by creating a current of water which flows into the mouth. Since the current of water also contains oxygen essential to respiration, it is obvious that respiratory organs placed in its pathway will be most favorably located for obtaining oxygen. Gills, lungs, and even more uncommon respiratory devices, such as swim bladders in fishes and pharyngoesophageal capillaries in lungless salamanders, therefore, are found colonizing at the anterior end of the alimentary canal. There is in fact an intimate relationship between the respiratory organs of vertebrates and the anterior end of the digestive tube.

Originally perhaps the entire digestive tube shared in the respiratory function, as suggested in the rectal breathing of certain fishes. Surely in amphioxus as much as the anterior half of the tube is concerned with respiration. In most vertebrates, however, the apparatus for breathing is more restricted, although still closely connected with the pharyngeal region.

Aquatic vertebrates like fishes have a series of paired lateral openings, the gill slits, in the sides of the pharynx, making possible a dual disposal of the water taken into the mouth. This can either pass straight on through the esophagus to the stomach and intestine, in which case its food content is utilized, or it can stream out through the porthole-like gill slits, when the oxygen that it contains is transferred to the delicate respiratory gills, or branchiae, hanging suspended within the space of the gill slits. In this way both respiration and alimentation are effected.

Between the gill slits, embedded in the walls of the pharynx, are skeletal parts of the splanchnocranium that form the gill arches, which furnish support for the vascular gills.

During the early embryonic development of all vertebrates, a series of internal pockets, or pharyngeal pouches (Fig. 318a), push outward from the sides of the pharynx. These are lined with the same sort of endodermal tissue found throughout the alimentary canal.

Meanwhile on the outside, corresponding indentations or depressions in the ectoderm, called visceral furrows (Fig. 318b), make an appearance. Later the pouches and the furrows meet, separated only by a thin sheet of tissue which in fishes breaks through to form the visceral clefts, or gill slits (Fig. 318c), thus completing the passage-way from the pharyngeal cavity to the outside.

In addition, along the margins of the clefts, delicate thin-walled evaginations containing capillaries develop as gill filaments, which are the essential organs of respiration. Each gill septum, or wall between successive visceral clefts, together with all of the filaments on both of its surfaces makes up a holobranch, or gill.

The number of pairs of gill slits varies from fourteen in the cyclostome Bdellostoma polytrema of the Pacific Coast, to only one pair, between the third and fourth gill arches, in certain salamanders.

Diagrams to illustrate the formation of the gill slits

The complicated branchial basketwork of tunicates forms a remarkable exception, as well as the sixty or more pairs of gill slits in the elongated pharynx of amphioxus.

Among reptiles, birds, and mammals gill slits do not normally break through, although both pouches and furrows occur in the embryo. Whenever a pharyngeal fistula, as occasionally reported in medical literature, turns up in a human being, the comparative anatomist, if not himself the possessor of the strange anomaly, is delighted with this reminder of past history.

Invertebrate Gills

The gills of invertebrates are not associated with pharyngeal gill slits, as in vertebrates, for there are no gill slits present. Gills may be located anywhere along the outside of the body within easy access of the water. For example, in free-swimming annelids, such as Nereis, large leaflike parapodial appendages extending along either side of the body function as “gills.” In mud-dwelling or tube-inhabiting annelids gills when present crowd together in beautiful feathery tufts at the exposed anterior end, since they would be at a disadvantage buried within the tube or the mud burrow.

The ciliary “gills” of lamellibranch mollusks are concerned primarily with directing a stream of microscopic food toward the mouth opening, and they are of doubtful respiratory service, this function being performed instead by the expanded surface of the “mantle.”

The thoracic gills of crustaceans and the abdominal gills of larval aquatic insects are simply thin feathery expansions of the chitinous exoskeleton, enclosing tracheal tubes which in this way extend outside of the body rather than being turned inside, as in land tracheates.

Primitive Gills of Amphioxus and Tunicates

The fact that tunicates are enveloped in a thick non-respiratory cellulose tunic makes necessary an enlarged pharyngeal basket, that forms a respiratory structure often exceeding in size all the other organs of the body. The tunicate Phallusia, for example, has a branchial basket perforated with several hundred gill slits, while the ghostly transparent Appendicularia, which are microscopic tunicates without a cellulose mantle and consequently with greater capacity for diffuse integumental breathing, possess only a single pair of gill slits.

Amphioxus is characterized by an exceptionally generous number of gill slits, and these are bordered by flat primitive vascular tissue that presents much less respiratory surface than is common to the more elaborate gills of fishes and amphibians. No expansive gill filaments, such as appear in higher aquatic vertebrates, are found hanging in the gill slits, so this ancestral animal is obliged to make up in number what it lacks in area of individual gills. The entire pharyngeal region is enclosed in an atrial cavity, so that the pharynx opens indirectly to the outside through a single ventral atrial pore, instead of directly through the gill slits. The walls of this atrial chamber protect the delicate gill surfaces from the sand in which amphioxus burrows, while allowing the unobstructed passage of water through the gill slits.

Diagrammatic cross section through the endostyle of Clavelina, showing glandular walls and ciliary bands in the groove

Since the numerous gill slits of both amphioxus and the tunicates increase the hazard of the escape of food through them, the development of a device for directing bits of food past these lateral openings to the esophagus is necessary. The apparatus accomplishing this end consists of two ciliated glandular grooves, the ventral endostyle (Fig. 319), and the dorsal epibranchial groove, in which food particles become collected together into a sort of mucous rope that spins along continuously into the gullet. Later in vertebrate evolution, when the endostyle is no longer needed for the purpose of collecting and steering food, this pharyngeal groove becomes transformed into the thyroid gland with an entirely different function.

The student of comparative anatomy often finds things like this in the morphological junk pile, that have become utilized for purposes entirely different from those to which they were originally put.

Cyclostome Gills

Diagram of the relation of the esophagus and respiratory tract

The arrangement of gills in cyclostomes is somewhat different from that in typical fishes. In Petromyzon a forward extension of the esophagus forms a partition between the alimentary and respiratory parts of the pharynx, leaving the branchial apparatus in a blind pocket ventral to the esophagus (Fig. 320). Water in its passage over the gills consequently may enter through the anterior gill slits instead of the mouth, which is frequently otherwise occupied on account of the suctorial habits of these animals. The gill slits are also modified by the narrowing of each end of the visceral cleft so that the filaments are enclosed in a rounded sac with a slender duct leading to it from the pharynx and another from it to the surface of the body (Fig. 321). Since the gills are located in these pockets, cyclostomes are frequently referred to as Marsipobranchs, meaning “pouched gills.” In this group different species of Bdellostoma have from ten to fourteen pairs of gill slits; Petromyzon, eight embryonic pairs but only seven in the adult; and Myxine, six pairs, with all the external passage-ways on each side of the body uniting into a common canal opening by a single pore to the outside (Fig. 321B).

Diagrams of the heads of Bdellostoma and Myxine

Elasmobranch and Holocephalan Gills

Gills of elasmobranch fishes are lateral in position in sharks and dogfishes but ventral in the flattened skates and rays. They open independently to the outside and are separated from each other not only by skeletal gill arches of cartilage, but also by primitive partitions attached to these arches, called branchial septa, on either side of which is located a set of filaments, or demibranch. A septum and its two demibranchs together make up a gill, or holobranch. Along the inner margins of the gill arches are fingerlike projections, the gill rakers, which not only keep food from entering the slits but also aid in directing it along the straight and narrow esophageal path in which it should go (Fig. 322A).

Relation of gills to branchial chamber

The most anterior pair of the pharyngeal portholes in elasmobranchs, between the mandibular and the hyoid arches, develops into the spiracles, not far posterior to the eyes in position. The walls of the spiracles are not provided with true gills, but in some cases may support, on one side at least, a “false gill,” or pseudobranch, so called because its blood supply is not derived directly like that of true gills from an afferent branchial artery bearing “impure” blood, but from the efferent branchial artery of the following gill arch which, having already given up its load of carbon dioxide and taken in oxygen, carries “pure” blood.

In bottom-feeding skates and rays the spiracles open dorsally instead of ventrally as the other pharyngeal gill slits do. They are useful, therefore, in taking the water of respiration into the branchial cavity when the mouth is otherwise occupied grubbing for food in the mud. No doubt sharks and dogfishes, which swim about freely and gracefully in water, likewise use the spiracles upon occasion, instead of the mouth, as an accessory port of entry for the water of respiration. The cub shark, Carcharias, and the mackerel shark, Lamna, are without spiracles.

The primitive shark, Heptanchus, has seven pairs of gill slits, and the frilled shark, Chlamydoselachus, as well as Hexanchus, six pairs, while for most elasmobranchs the typical number, aside from the spiracles, is five pairs. On each face of each gill slit, except the posterior side of the last slit, there is a demibranch, making a total of nine pairs of demibranchs in a fish with five pairs of slits.

Embryonic external gills of dogfish

Certain larval elasmobranchs which undergo considerable development within the eggshell before hatching have gill filaments so long that they hang out of the gill slits .as temporary “external gills” (Fig. 323). These unusual structures may serve not only for respiration but also as absorbing organs in connection with the enormous yolks present in these eggs.

A primitive shark, Chlamydoselachus, with an external flap for each separate gill slit

The holocephalans, or strange elephant fishes, which have much in common with elasmobranchs, possess only four pairs of gill slits and are further differentiated from them by an operculum. This is a flap of the integument developed on either side and extending backward from the margin of the hyoid arch, until it covers the external openings of the three anterior pairs of gill slits, leaving only the last pair open directly to the outside after the elasmobranch fashion. Possibly the forerunner of this opercular flap is seen in the elasmobranch, Chlamydoselachus, where the skin on the anterior margin of each gill slit extends backward as a small independent protective fold covering the opening of each gill slit separately (Fig. 324), a feature which gives Chlamydoselachus the common name of “frilled shark.”

Ganoid and Teleost Gills

The gill system of ganoids in some ways represents a connecting link between that of elasmobranchs and teleost fishes. Most Chondrostei still have nine pairs of demibranchs but nearly all Holostei lose the most anterior pair so that they are limited to eight pairs of demibranchs, i.e., four pairs of complete gills. In all bony fishes the gills are covered by an operculum that is stiffened by flat skeletal plates between the two surfaces of folded integument. Outside and anterior to the operculum on either side, there is a degenerate spiracle in some of the ganoids, while on the inner surface of the operculum there is attached a small opercular gill which is not homologous either with true gills or with the pseudobranchs of the hyoid arch.

The interbranchial septa in ganoids are reduced so that the demibranchs placed upon them back to back are no longer in separate individual chambers, but occupy a common branchial cavity (Fig. 325c). The reduction of the interbranchial septa becomes complete in teleost fishes, so that the gills all lie compacted closely together in a common chamber covered by the operculum (Figs. 322B and 325E).

The progressive reduction of gill septa in different fishes

The number of gill arches in both ganoids and teleosts is usually four or five pairs, although they may be reduced to three, or even two pairs in some of the bony fishes. Spiracles are not characteristic of teleosts.

The opercular opening becomes much diminished in such fishes as eels, which are thus enabled to retain water in the branchial chamber under unfavorable conditions. Probably the immediate reason why fishes suffocate when removed from a water environment is not because the gills dry up at once with a collapse of the capillaries in the gill filaments, but because when out of water the gills adhere to each other, leaving the exposable respiratory surface reduced beyond the danger point.

The structure of a typical teleost gill, with its relatively great expanse of respiratory surface within a small compass, and the arrangement of its capillaries are indicated in Fig. 326.

Structure of a typical gill, showing blood vessels

In ganoids and teleosts there are additional devices, besides the opercular lid, for protecting the delicate gills. Along the posterior and ventral margins of the operculum beyond the part stiffened by the flat opercular bones, a bordering fringelike flap is sometimes developed, which is supported by fanlike skeletal elements, the branehiostegal rays, that help in controlling the passage of water out of the branchial cavity.

On the inner pharyngeal side of the gill slits also there are present in varying degree, a series of stiff comblike projections along the inner margins of the gill arches, the gill rakers.

Dipnoan Gills

Of the three genera of living lungfishes that are found respectively in Australia, South America, and Africa, Aeoceratodus has four pairs of gills, Lepidosiren, three, and Protopterus, two. Spiracles are present in the embryos of these fishes, although not in the adults. In addition to the pharyngeal gills common to this group, four pairs of supplemental true external gills of the pinnate (pinna, feather) type are present in the larval stages of Lepidosiren and Protopterus (Fig. 327).

External gills in a larval stage of Lepidosiren

Amphibian Gills

The external gills of amphibians are attached as capillary detours upon the aortic loops in such a way that blood can go either directly around the vascular loops or roundabout through the gills (Fig. 328). This is quite different from the arrangement of the internal gills of fishes, which offers no alternative for the circulating blood except to pass through the gills themselves.

Section through branchial region of a 6 mm larva of Rana esculenta, showing vascular loop in external gills

As compared with internal gills, external gills are only weakly supported by a skeletal framework, and although always present during the tadpole stages of amphibians, they persist throughout life only in the perennibranchiate urodeles, as the name indicates. Such external gills occur in the larval forms of a few fishes, for example, in the dipnoans as already mentioned, in the cartilaginous ganoids, Polypterus and Calamoichthys, and in the teleosts, Gymnarchus and Heterotis.

The urodele amphibians have been separated into three groups according to the character of their gills, as follows: (1) Perennibranchiata, retaining both gills and gill slits throughout life; (2) Derotremata, losing gills and all the gill slits except one pair; and (3) Myctodera, or true salamanders, having neither gills nor gill slits when adult.

Although perennibranchiates preserve throughout life their tadpole-like external gills with two or three pairs of gill slits, these pharyngeal openings are no longer useful for their original purpose, since the water of respiration does not pass through the pharynx. Instead a fresh supply of dissolved oxygen is brought into contact with the gill filaments as the gills wave to and fro in the water, by means of muscles attached to the base of each gill. Five pairs of gill pouches form embryonically in the pharyngeal cavity, but the first and the fifth no longer break through. Necturus and Proteus belong in this group.

In derotremes only the gill slit between the third and the fourth gill arches becomes complete, while the external gills vanish during larval life. Amphiuma, Cryptobranchus, and Siren are derotremes.

The myctodere salamanders, as well as frogs and toads, have no gill slits, although embryonic pouches and furrows develop. The temporary external gills of these forms are sacrificed with the development of pulmonary and cutaneous respiration. The newts and true salamanders, including Amblystoma and Triton, are myctoderes.

The external gills of frog tadpoles become enclosed during metamorphosis by a fold of the skin without skeletal support, while the protective peribranchial chamber thus formed usually has a single opening to the outside, more rarely two, as in Pipa and Xenopus, corresponding physiologically to the atrial pore in the peribranchial chamber of amphioxus.

External leaflike gills of a larval caecilian

One of the tropical limbless amphibians, Caecilia, is exceptional, having larval external gills of peculiar crumpled leaflike structure, with a relatively large respiratory surface (Fig. 329).

Gill Structures in Land Vertebrates

The persistence of branchial remains in land forms, that have no use for gills even in embryonic life, is striking evidence of the common ancestry of all vertebrates.

Although gills are never present in reptiles, birds, or mammals, there are five pairs of embryonic visceral pouches and furrows in reptiles and mammals and four pairs in birds. Ordinarily these break through only briefly in reptiles and birds but not at all in most mammals. Only the anteriormost, or hyomandibular, pair remains well developed in adult mammals. The hyomandibular pouches become the Eustachian tubes and the middle ear cavity, which ordinarily remain separated by the ear drum from the external ear canal, derived from the ectodermal furrows.