CHAPTER VI

RESPIRATION AND CIRCULATION--THE MANTLE

The principle of respiration is the same in the Mollusca as in all other animals. The blood is purified by being brought, in successive instalments, into contact with pure air or pure water, the effect of which is to expel the carbonic acid produced by animal combustion, and to take up fresh supplies of oxygen. Whether the medium in which a mollusc lives be water or air, the effect of the respiratory action is practically the same.

Broadly speaking, Mollusca whose usual habitat is the water ‘breathe’ water, while those whose usual habitat is the land ‘breathe’ air. But this rule has its exceptions on both sides. The great majority of the fresh-water Mollusca which are not provided with an operculum (_e.g._ _Limnaea_, _Physa_, _Planorbis_), breathe air, in spite of living in the water. They make periodic visits to the surface, and take down a bubble of air, returning again for another when it is exhausted. On the other hand many marine Mollusca which live between tide-marks (_e.g._ _Patella_, _Littorina_, _Purpura_, many species of _Cerithium_, _Planaxis_, and _Nerita_) are left out of the water, through the bi-diurnal recess of the tide, for many hours together. Such species invariably retain several drops of water in their branchiae, and, aided by the moisture of the air, contrive to support life until the water returns to them. Some species of _Littorina_ (_e.g._ our own _L. rudis_ and many tropical species) live so near high-water mark that at neap-tides it must frequently happen that they are untouched by the sea for several weeks together, while they are frequently exposed to a burning sun, which beats upon the rocks to which they cling. In this case it appears that the respiratory organs will perform their functions if they can manage to retain an extremely small amount of moisture.[265]

The important part which the respiratory organs play in the economy of the Mollusca may be judged from the fact that the primary subdivision of the Cephalopoda into Dibranchiata and Tetrabranchiata is based upon the number of branchiae they possess. Further, the three great divisions of the Gasteropoda have been named from the position or character of the breathing apparatus, _viz_. Prosobranchiata, Opisthobranchiata and Pulmonata, while the name Pelecypoda has hardly yet dispossessed Lamellibranchiata, the more familiar name of the bivalves.

Respiration may be conducted by means of--(_a_) Branchiae or Gills, (_b_) a Lung or Lung-cavity, (_c_) the outer skin.

In the Pelecypoda, Cephalopoda, Scaphopoda, and the great majority of the Gasteropoda, respiration is by means of branchiae, also known as _ctenidia_[266], when they represent the primitive Molluscan gill and are not ‘secondary’ branchiae (pp. 156, 159).

In all non-operculate land and fresh-water Mollusca, in the Auriculidae, and in one aberrant operculate (_Amphibola_), respiration is conducted by means of a lung-cavity, or rarely by a true lung, whence the name _Pulmonata_. The land operculates (Cyclophoridae, Cyclostomatidae, Aciculidae, and Helicinidae) also breathe air, but are not classified as Pulmonata, since other points in their organisation relate them more closely to the marine Prosobranchiata. Both methods of respiration are united in _Ampullaria_, which breathes indifferently air through a long siphon which it can elevate above the surface of the water, and water through a branchia (see p. 158). _Siphonaria_ (Fig. 57) is also furnished with a lung-cavity as well as a branchia. Both these genera may be regarded as in process of change from an aqueous to a terrestrial life, and in _Siphonaria_ the branchia is to a great extent atrophied, since the animal is out of the water, on the average, twenty-two hours out of the twenty-four. In the allied genus _Gadinia_, where there is no trace of a branchia, but only a lung-cavity, and in _Cerithidea obtusa_, which has a pulmonary organisation exactly analogous to that of _Cyclophorus_,[267] this process may be regarded as practically completed.

[Illustration: FIG. 57.--=A=, _Siphonaria gigas_ Sowb., Panama, the animal contracted in spirit: _gr_, siphonal groove on right side. =B=, _Gadinia peruviana_, Sowb., Chili, shell only: _gr_, mark of siphonal groove to right of head.]

Respiration by means of the skin, without the development of any special organ, is the simplest method of breathing which occurs in the Mollusca. In certain cases, _e.g._ _Elysia_, _Limapontia_, and _Cenia_ among the Nudibranchs, and the parasitic _Entoconcha_ and _Entocolax_, none of which possess breathing organs of any kind, the whole outer surface of the body appears to perform respiratory functions. In others, the dorsal surface is covered with papillae of varied size and number, which communicate with the heart by an elaborate system of veins. This is the case with the greater number of the _Aeolididae_ (Fig. 58, compare Fig. 5, C), but it is curious that when the animal is entirely deprived of these papillae, respiration appears to be carried on without interruption through the skin.

[Illustration: FIG. 58.--_Aeolis despecta_ Johnst., British coasts. (After Alder and Hancock.)]

In the development of a distinct breathing organ, it would seem as if progress had been made along two definite lines, each resulting in the exposure of a larger length of veins, _i.e._ of a larger amount of blood, to the simultaneous operation of fresh air or fresh water. Either (_a_) the skin itself may have developed, at more or less regular intervals, elevations, or folds, which gradually took the form of papillae, or else (_b_) an inward folding, or ‘invagination,’ of the skin, or such a modification of the mantle-fold as is described below (p. 172) may have taken place, resulting in the formation of a cavity more or less surrounded by walls, within which the breathing organs were ultimately developed. Sometimes a combination of both processes seems to have occurred, and after a papilliform organ has been produced, an extension or prolongation of the skin has taken place, in order to afford a protection to it. Respiration by means of a lung-cavity is certainly subsequent, in point of time, to respiration by means of branchiae.

[Illustration: FIG. 59.--_Chiton squamosus_ L., Bermuda: =A=, anus; =Br=, branchiae; =M=, mouth.]

[Illustration: FIG. 60.--_Fissurella virescens_ Sowb., Panama, showing position of the branchiae: =Br=, branchiae: =E=, =E=, eyes; =F=, foot; =M=, mantle; =T=, =T=, tentacles.]

The branchiae seem to have been originally paired, and arranged symmetrically on opposite sides of the body. It is not easy to decide whether the multiple form of branchia which occurs in _Chiton_ (Fig. 59), or the simple form as in _Fissurella_ (Fig. 60), is the more primitive. Some authorities hold that the multiple branchia has gradually coalesced into the simple, others that the simple form has grown, by serial repetition, into the multiple. There appears to be no trace of any intermediate forms, and, as a matter of fact, the multiple branchia is found only in the _Amphineura_, while one or rarely two (never more) pairs of branchiae, occur, with various important modifications, in the vast majority of the Mollusca.

_Amphineura._--In _Chiton_ the branchiae are external, forming a long row of short plumes, placed symmetrically along each side of the foot. The number of plumes, at the base of each of which lies an osphradial patch, varies from about 70 to as few as 6 or 7. When the plumes are few, they are confined to the posterior end, and thus approximate to the form and position of the branchiae in the other Amphineura. In _Chaetoderma_, the branchiae consist of two small feather-shaped bodies, placed symmetrically on either side of the anus, which opens into a sort of cloaca within which the branchiae are situated. In _Neomenia_ the branchiae are still further degraded, consisting of a single bunch of filaments lying within the cloaca, while in _Proneomenia_ there is no more than a few irregular folds on the cloaca-wall (Fig. 61).

[Illustration: FIG. 61.--Terminal portions of the Amphineura, illustrating the gradual degradation of the branchiae, and their grouping round the anus in that class. =A=, _Chiton_ (_Hemiarthrum_) _setulosus_ Carp., Torres Str.; =B=, _Chiton_ (_Leptochiton_) _benthus_ Hadd., Torres Str.; =C=, _Chaetoderma_; =D=, _Neomenia_; _a_, anus; _br_, _br_, branchiae; _k_, _k_, kidneys; _p_, pericardium. (=A= and =B= after Haddon, =C= and =D= after Hubrecht.)]

In the _Prosobranchiata_, symmetrically paired branchiae occur only in the Fissurellidae, Haliotidae, and Pleurotomariidae, in the former of which two perfectly equal branchiae are situated on either side of the back of the neck. These three families taken together form the group known as _Zygobranchiata_.[268] In all other families the asymmetry of the body has probably caused one of the branchiae, the right (originally left), to become aborted, and consequently there is only one branchia, the left, in the vast majority of marine Prosobranchiata, which have been accordingly grouped as _Azygobranchiata_. Even in _Haliotis_ the right branchia is rather smaller than the left, while the great size of the attachment muscle causes the whole branchial cavity to become pushed over towards the left side. In those forms which in other respects most nearly approach the Zygobranchiata, namely, the Trochidae, Neritidae, and Turbinidae, the branchia has two rows of filaments, one on each side of the long axis, while in all other Prosobranchiata there is but one row (see Fig. 79, p. 169).

[Illustration: FIG. 62.--_Bullia laevissima_ Gmel., showing branchial siphon =S=; =F=, =F=, =F=, foot; =OP=, operculum; =P=, penis; =Pr=, proboscis; =T=, =T=, tentacles. (After Quoy and Gaimard.)]

In the great majority of marine Prosobranchiata the branchia is securely concealed within a chamber or pouch (the respiratory cavity), which is placed on the left dorsal side of the animal, generally near the back of the neck. For breathing purposes, water has to be conveyed into this chamber, and again expelled after it has passed over the branchia. In the majority of the vegetable-feeding molluscs (_e.g._ _Littorina_, _Cerithium_, _Trochus_) water is carried into the chamber by a simple prolongation of one of the lobes or lappets of the mantle, and makes its exit by the same way, the incoming and outgoing currents being separated by a valve-like fringe depending from the lobe. In the carnivorous molluscs, on the other hand, a regular tube, the _branchial siphon_, which is more or less closed, has been developed from a fold of the mantle surface, for the special purpose of conducting water to the branchia. After performing its purpose there, the spent water does not return through the siphon, but is conducted towards the anus by vibratile cilia situated on the branchiae themselves. In a large number of cases, this siphon is protected throughout its entire length by a special prolongation of the shell called the canal. Sometimes, as in _Buccinum_ and _Purpura_, this canal is little more than a mere notch in the ‘mouth’ of the shell, but in many of the Muricidae (_e.g._ _M. haustellum_, _tenuispina_, _tribulus_) the canal becomes several inches long, and is set with formidable spines (see Fig. 164, p. 256). In _Dolium_ and _Cassis_ the canal is very short, but the siphon is very long, and is reflected back over the shell.

The presence or absence of this siphonal notch or canal forms a fairly accurate indication of the carnivorous or vegetarian tendencies of most marine Prosobranchiata, which have been, on this basis, subdivided into _Siphonostomata_ and _Holostomata_. But this classification is of no particular value, and is seriously weakened by the fact that _Natica_, which is markedly ‘holostomatous,’ is very carnivorous, while _Cerithium_, which has a distinct siphonal notch, is of vegetarian tendencies.

In the Zygobranchiata the water, after having aerated the blood in the branchiae, usually escapes by a special hole or holes in the shell, situated either at the apex (_Fissurella_) or along the side of the last whorl (_Haliotis_). In _Pleurotomaria_ the slit answers a similar purpose, serving as a sluice for the ejection of the spent water, and thus preventing the inward current from becoming polluted before it reaches the branchiae (see Fig. 179, p. 266).

In _Patella_ the breathing arrangements are very remarkable. In spite of their apparent external similarity, this genus possesses no such symmetrically paired plume-shaped branchiae as _Fissurella_, but we notice a circlet of gill-lamellae, which extends completely round the edge of the mantle. It has been shown by various authorities that these lamellae are in no sense morphologically related to the paired branchiae in other Mollusca, but only correspond to them functionally. The typical paired branchiae, as has been shown by Spengel, exist in _Patella_ in a most rudimentary form, being reduced to a pair of minute yellow bodies on the right and left sides of the back of the ‘neck.’ A precisely similar abortion of the true branchiae, and special development of a new organ to perform their work, is shown in _Phyllidia_ and _Pleurophyllidia_ (see below under Opisthobranchiata). This circlet of functional gills in _Patella_ has therefore little systematic value, being only developed in an unusual position, like the eyes on the mantle in certain _Pelecypoda_, to supply the place of the true organs which have fallen into disuse. Accordingly Cuvier’s class of _Cyclobranchiata_, which included _Patella_ and _Chiton_, has no value, and has indeed long been discarded. In _Chiton_ the gills never extend completely round the animal, but are always more or less interrupted at the head and anus. They are the true gills, the plumes being serially repeated in the same way as the shell plates.

[Illustration: FIG. 63.--_Patella vulgata_ L., seen from the ventral side: _f_, foot; _g.l_, circlet of gill lamellae; _m.e_, edge of the mantle; _mu_, attachment muscle; _sl_, slits in the same; _sh_, shell; _v_, vessel carrying aerated blood to the heart; _v´_, vessel carrying blood from the heart; _ve_, small accessory vessels.]

[Illustration: FIG. 64.--_Patella vulgata_ L., seen from the dorsal side after the removal of the shell and the black pigment covering the integument; the anterior portion of the mantle is cut away or turned back: _a_, anus; _br_, _br_, remains of the true branchiae (ctenidia); _i_, intestine; _k_, _k´_, kidneys; _k.ap_, their apertures on each side of the anus; _l_, liver; _m_, _m_, mantle; _mu_, attachment muscles, severed in removal of shell; _t_, _t_, tentacles.]

In the land Prosobranchiata (Cyclostomatidae, Cyclophoridae, Aciculidae, Helicinidae) which, having exchanged a marine for an aerial life, breathe air instead of water, the branchia has completely disappeared, and breathing is conducted, as in the Pulmonata, by a lung-cavity. In certain genera of land operculates, _e.g._ _Pupina_, _Cataulus_, _Pterocyclus_, a slight fissure or tube in the last whorl (see Fig. 180, p. 266) serves to introduce air into the shell, which is perhaps otherwise closed to air by the operculum. In _Aulopoma_, which has no tube, the operculum admits free circulation of air. In certain other Cyclostomatidae the apex is truncated, and air can enter there. De Folin closed with wax the aperture of _Cycl. elegans_, and found that on placing it in a pneumatic machine, the shell gave off air through its whole surface. On the other hand, _Cylindrella_ and _Stenogyra decollata_, on being submitted to the same test, showed that the truncated part alone was permeable by air.

Fischer and Bouvier have made some interesting observations on the breathing of a species of _Ampullaria_ (_insularum_ Orb.). The species has, in common with all _Ampullaria_, two siphons, but while the right siphon is but slightly developed, the left is very long, almost twice as long as the shell (see Fig. 65). The animal, when under the water, lengthens its siphon, brings the orifice to the surface, and by alternately raising and depressing its head produces in the pulmonary sac movements of ex- and inspiration; these are repeated about ten or fifteen times at regular intervals of from six to eight seconds, a method of respiration strongly resembling that of the Cetacea. At the same time, branchial respiration takes place. If powdered carmine is added to water, the particles are seen to enter the branchial cavity by the siphon and pass out by the short right siphon. Sometimes the animal remains under water for hours without rising to the surface to inspire air. In _Valvata_ (Fig. 66) the branchia is very large, and projects like a leaf or fan above the shell on the left side; on the corresponding position on the right side is a long filiform appendage, which some have regarded as representing the other branchia.

[Illustration: FIG. 65.--_Ampullaria insularum_ Orb.: =A=, breathing water; =B=, breathing air; =Si=, siphon; =T=, upper; _t_, lower tentacles; =X=, pallial expansion, performing the part of excurrent siphon. (After Fischer and Bouvier, x ⅓.)]

_Opisthobranchiata._--A true branchia occurs only in the Tectibranchiata and the Ascoglossa. It lies on the right side, and is usually more or less external, being partly covered sometimes by the shell (as in _Umbrella_, Fig. 5), sometimes by a fold of the mantle. In the Pteropoda (which are probably derived from the Tectibranchiata), all the Thecosomata, with the exception of _Cavolinia_, have no specialised branchia, but probably respire through portions or the whole of the integument. In the Gymnosomata an accessory branchia has in many cases been developed at the posterior end of the body. _Pneumodermon_ alone has both lateral and posterior branchiae well developed, _Clione_ and _Halopsyche_ are destitute of either, while the four remaining families have one branchia, sometimes lateral, sometimes posterior.[269]

[Illustration: FIG. 66.--_Valvata piscinalis_ Müll.: _br_, branchia; _fi_, filament; _f.l_, foot lobes. (After Boutan.)]

[Illustration: FIG. 67.--_Doris_ (_Archidoris_) _tuberculata_ L., Britain: _a_, anus; _br_, branchiae, surrounding the anus; _m_, male organ; _rh_, _rh_, rhinophores. × ⅔.]

[Illustration: FIG. 68.--_Pleurophyllidia lineata_ Otto, Mediterranean: _a_, anus; _br_, secondary branchiae; _m_, mouth; _s.o_, sexual orifice.]

Certain of the Nudibranchiata possess no special breathing organs, and probably respire through the skin (_Elysia_, _Limapontia_, _Cenia_, _Phyllirrhoë_). The majority, however, have developed secondary branchiae, in the form of prominent lobes or leaf-like processes (the _cerata_), which are carried upon the back, without any means of protection. These cerata are, as a rule, of extreme beauty and variety of form, consisting sometimes of long whip-like tentaculae, in other cases of arborescent plumes of fern-like leafage, in others of curious bead-like appendages of every imaginable shape and colour. In _Doris_ they lie at the posterior end of the body, in a sort of rosette, which is generally capable of retraction into a chamber. In _Phyllidia_ and _Pleurophyllidia_ these secondary branchiae lie, as in _Patella_, on the lateral portions of the mantle.

The Scaphopoda in all probability possess neither true nor secondary branchiae.

_Pulmonata._--When we use the term ‘lung,’ it must be remembered that this organ in the Mollusca does not correspond, morphologically, with the spongy, cellular lung of vertebrates; it simply performs the same functions. The ‘lung,’ in the Mollusca, is a pouch or cavity, lined with blood-vessels which are disposed over its vaulted surface in various patterns of network. The pulmonary sac or cavity is therefore a better name by which to denote this organ.

[Illustration: FIG. 69.--_Geomalacus maculosus_ Allm., S. Ireland: =P.O=, pulmonary orifice.]

It seems probable, as has been already shown (pp. 18–22), that all Pulmonata are ultimately derived from marine forms which breathed water by means of branchiae. Thus we find intermediate forms, such as _Siphonaria_, possessed of both a branchia and a pulmonary sac, the former being evanescent, while in _Gadinia_ and _Amphibola_ it has quite disappeared. In the vast majority of _Pulmonata_ no trace of a branchia remains; its function is performed by a chamber, always situated at the right side of the animal, and generally more or less anterior, admitting air by a narrow aperture which is rhythmically opened and closed. In _Arion_ and _Geomalacus_ (Fig. 69) this aperture is in the front of the right side of the ‘shield,’ in _Limax_ (Fig. 71) in the hinder part, in _Testacella_ (Fig. 20) it is near the extremity of the tail, under the spire of the shell; in _Janella_ it is on the middle of the right edge of the shield (Fig. 70). If a specimen of _Helix aspersa_, or better, of _H. pomatia_, is held up to the light, the beautiful arborescent vessels, with which the upper part of the pulmonary chamber is furnished, can be clearly seen by looking through the aperture as it dilates. It is only in the Auriculidae that an actual spongy mass of lung material appears to exist. When in motion, a _Helix_ inspires air much more frequently than when at rest. Temperature, too, seems to affect the number of inspirations; it appears doubtful whether, during hibernation, a snail breathes at all. In any case, the amount of air required to sustain life must be small.

[Illustration: FIG. 70.--_Janella hirudo_ Fisch., N. Caledonia: =G=, generative orifice; =P=, pulmonary orifice; =T=, =T=, tentacles. (After Fischer.)]

[Illustration: FIG. 71.--_Limax maximus_ L.: =PO=, pulmonary orifice. × ⅔.]

With regard to the respiration of fresh-water Pulmonata there appears to be some difference of opinion. It is held, on the one hand, that the Limnaeidae only respire air, making periodic visits to the surface to procure it, and that they perish, if prevented from doing so, by asphyxiation. If, we are told,[270] as a _Limnaea_ is floating on the surface of the water in a glass jar, a morsel of common salt be dropped upon its outstretched foot, it will sink heavily to the bottom, emitting a stream of air from its pulmonary orifice. On recovering from the shock, it will anxiously endeavour to regain the surface, but will have some difficulty in doing so, owing to its now much greater specific gravity. When it succeeds, it creeps almost out of the water, and exposes its respiratory orifice freely to the air. If the experiment is repeated several times on the same individual, it becomes so much weakened that it has to be taken out of the water to save its life. Moquin-Tandon, on the other hand, is strongly of opinion[271] that there is no absolute necessity for _Limnaea_ to obtain air by rising to the surface, and that, if prevented from emerging, it can obtain air from the water. When covered in by a roof of ice, _Limnaea_ has not been observed to suffer any inconvenience. Moquin-Tandon kept _L. glabra_ and _Planorbis rotundatus_ in good health under 20 mm. of water for eighteen and nineteen days, and relates a case in which _Physa_ was kept alive under water for four days, and _Planorbis_ for twelve. Young specimens, both of _Limnaea_ and _Planorbis_, do not rise to the surface for a supply of air; they are hatched with the pulmonary cavity full of water.

It is probable, therefore, that Limnaeidae are capable, on occasion, of respiration through the skin. Some authorities are of opinion that certain long and narrow lamellae, situated within the pulmonary sac, are employed for the purpose of aqueous respiration. _Ancylus_, which never makes periodic excursions to the surface, perhaps respires by receiving into its pulmonary chamber the minute quantities of oxygen given off by the vegetation on which it feeds.

Limnaeidae taken from a great depth of water, _e.g._ from 130 fathoms in the lake of Geneva, have been examined by Forel.[272] The pulmonary sac is full of water, but there is no transformation of organs, no appearance of a branchia, to meet the changed circumstances of their environment. Doubtless a good deal of respiration is done by the skin; being soft and vascular, it respires the air dissolved in the water. Forel cites cases of _Limnaea_ living at much shallower depths, which come to the surface once, and then remain below for months. The oxygen of this supply must soon have become exhausted, and the animals, discontinuing for a time the use of the pulmonary chamber, must have respired through the skin. Shallow-water _Limnaea_, according to the same authority, remain beneath the surface during cold weather; when warm weather returns they rise to the surface to take in a supply of air. Since the water at great depths is always very cold, there is no need for the _Limnaea_ living there to rise to the surface at all.

It is a curious fact that _Limnaea_, which have been respiring by the skin for the whole winter, should suddenly, on the first warm days of summer, take to rising to the surface and breathing air. But exactly the same phenomenon is shown in the case of _Limnaea_ from great depths. Placed in an aquarium, they _immediately_ begin rising to the surface and inspiring air; in other words, they experience instantaneously a complete transformation of their respiratory system.

In _Onchidium_, a land pulmonate which has retrogressed to an amphibious or quasi-marine mode of life, there is no organ which represents the pulmonary or branchial cavity, the so-called lung being only a cavity of the kidney. Respiration is, however, conducted by the skin as well, and by the dorsal papillae.[273]

Land Mollusca can sustain, for a considerable time, complete deprivation of atmospheric air. Helices placed in an exhausted receiver show no signs of being inconvenienced for about 20 hours, and are able to survive for about two or three days. If detained under water, they are very active for about 6 hours, then become motionless, the body swells, owing to the water absorbed, and death ensues in about 36 hours. Immersion for only 24 hours is generally followed by recovery. In the latter case, the cause of death is not so much deprivation of air as compulsory absorption of water by the skin. The amount of water thus taken up is surprising. Spallanzani found that a _Helix_ which weighed 18 grammes increased in weight by 13½ grammes after a prolonged immersion. Even slugs enclosed in moist paper gained more than 2 grammes in the course of half an hour. Experiment has shown that the amount of carbonic acid gas produced by respiration stands in direct relation to the amount of food consumed. Four pairs of snails were taken which had recently awakened from their winter sleep and had eaten heartily, and an equal number, under the same circumstances, which had been prevented from eating. It was found that the first four pairs produced, in consuming a given amount of oxygen, 11, 9, 10, and 13 parts respectively of carbonic acid, while the second set produced, in consuming the same amount of oxygen, only 4, 8, 7, and 9 parts of carbonic acid.[274] Hibernating Helices, if weighed in December and again in April, will be found to have lost weight, due to the expiration of carbonic acid. Owing to the difficulty of experiment, opinions vary as to the absolute temperature of snails. It appears to be established that several snails, if placed together in a tube, raise the temperature one or two degrees C., but as a rule, the temperature of a solitary _Helix_ differs very slightly from that of the surrounding air. Increased activity, whether in respiration or feeding, is found to raise the temperature.

[Illustration: FIG. 72.--_Cardium edule_ L.: =A=, anal; =B=, branchial siphon; =F=, foot. (After Möbius.)]

W. H. Dall, writing of the branchia in _Pelecypoda_, remarks[275] that there can be no doubt that its original form was a simple pinched-up lamella or fold of the skin or mantle. This, elongated, becomes a filament. Filaments united by suitable tissue, trussed, propped, and stayed by a chitinous skeleton, result in the forms, wonderful in number and complexity, which puzzle the student to describe, much more to classify.

[Illustration: FIG. 73.--_Scrobicularia piperata_ Gmel., in its natural position in the sand: =A=, efferent or anal siphon; =B=, afferent or branchial siphon. (After Möbius.)]

In Pelecypoda the branchiae are placed on each side of the body, between the mantle and the visceral mass. They lie in a chamber known as the _branchial cavity_. Leading into this cavity, and behind it, are, as a rule, two tubes or siphons, one of which conducts water to the branchiae, while the other carries it away after it has passed over them. The lower is known as the _branchial_ or _afferent_ siphon, the upper as the _anal_ or _efferent_ siphon (see Figs. 72 and 73). The

## action of these siphons can readily be observed by placing a little

carmine in water, near to the siphonal apertures of an _Anodonta_ or _Unio_. In many cases (_e.g._ _Psammobia_, _Tellina_, _Mya_, genera which burrow deeply in sand) both the siphons are exceedingly long, sometimes considerably longer than the whole shell. In some cases the two tubes are free throughout their entire length, in others they become fused together before their entrance within the shell (Fig. 74). In other genera, which do not burrow (_e.g._ _Ostrea_, _Pecten_, _Arca_, _Mytilus_), the siphons are rudimentary or altogether absent (Fig. 75).

[Illustration: FIG. 74.--_Solecurtus strigillatus_ L., Naples: _s.af_, afferent siphon; _s.ef_, efferent siphon, the two uniting in _SS_ externally to the shell, × ½.]

[Illustration: FIG. 75.--_Mytilus edulis_ L., attached by its byssus (=By=) to a piece of wood: =F=, foot; =S=, anal siphon, the branchial siphon being below it and not closed. (After Möbius.)]

The number and arrangement of the branchiae varies considerably. It appears probable that the different degrees of complication of the gill indicate degrees of specialisation in the different groups of Pelecypoda, in other words, assuming that a simpler form of gill precedes, in point of development, a more complicated form, the nature of the gill may be taken as indicating different degrees of removal from the primitive form of bivalve.

1. The simplest form of gill (_Nucula_, _Leda_, _Solenomya_, etc.) is that which consists (Fig. 76, A, compare Fig. 100, p. 201) of two rows of very short, broad, not reflected filaments, the rows being placed in such a way that they incline at right angles to one another from a common longitudinal axis. The filaments are not connected with one another, nor are the two leaves of each gill united at any point. (_Protobranchiata._)

[Illustration: FIG. 76.--Morphology of the branchiae of Pelecypoda, seen diagrammatically in section: =A=, _Protobranchiata_; =B=, _Filibranchiata_; =C=, _Eulamellibranchiata_; =D=, _Septibranchiata_; _e_, _e_, external row of filaments; _i_, _i_, internal row of filaments; _e´_, external row or plate folded back; _i´_, internal row folded back; _f_, foot; _m_, mantle; _s_, septum; _v_, visceral mass. (From A. Lang.)]

[Illustration: FIG. 77.--Four gill filaments of _Mytilus_, highly magnified; _cj_, ciliary junctions; _f_, filament. (After Peck.)]

2. In the _Anomiidae_, _Arcadae_, _Trigoniidae_, and _Mytilidae_ each gill consists of two plates or rows of much longer filaments, which consequently occupy a much larger space in the mantle cavity (Fig. 76, B). Unable to extend beyond the limits of the mantle, filaments are reflected or doubled back upon one another, those of the external plate being reflected towards the outside, those of the internal plate towards the inside. Each separate filament is not connected with the filament next adjacent, except by surface cilia situated on small projections on the sides of the filaments, and interlocking with the cilia of the adjacent filament. The two superposed plates or leaves of the gill may or may not be united by cords running between the two parts of a filament. (_Filibranchiata._)

3. In the _Pectinidae_, _Aviculidae_, and _Ostreidae_ a further development takes place. The filaments of each gill are reflected in the same way as in the _Filibranchiata_, but the part thus reflected may become completely united or ‘concresce’ with the mantle on the exterior and with the base of the foot on the interior side. The leaves of each gill plate, which have thus become doubled (the gills being apparently two instead of one on each side), are folded or crumpled, and the filaments are modified at the re-entrant angles of the fold. (_Pseudolamellibranchiata._)

4. In all the remaining _Pelecypoda_, except class 5, in other words, in the very large majority of families, the filaments are either reflected, as in (3), or simple; but the process of concrescence is so far advanced that the adjacent filaments are always intimately connected with one another in such a way as to admit the passage of the blood; and the leaves of each gill-plate (Fig. 76, C) are united by cross channels in a similar way. (_Eulamellibranchiata._)

5. In certain of the _Anatinacea_ alone (_Cuspidaria_, _Lyonsiella_, _Poromya_, _Silenia_) the gills are transformed into a more or less muscular partition, extending from one adductor muscle to the other (Fig. 76, D), and separating off the pallial chamber into two distinct divisions, which communicate by means of narrow slits in the partition. (_Septibranchiata._)

[Illustration: FIG. 78.--Transverse section of portion of an outer gill plate of _Anodonta_, highly magnified: _il_, inner lamella; _il´_, outer lamella; _ilj_, interlamellar junctions; _v_, large vertical vessels. (After Peck.)]

Thus the process of gill development in the Pelecypoda appears to lead up from a simple to a very complex type. In its original form, at all events in the most primitive form known to us, the gill is a series of short filaments, quite independent of one another, strung in two rows; then the filaments become longer and double back, while at the same time they begin to show signs of adhesion, as yet only superficial, to one another. In a further stage, the reflected portions become fused to the adjacent surfaces of the foot and mantle, while the interlamellar junctions serve to lock the two gill-plates together; finally, the mere ciliary junction of adjacent filaments is exchanged for intimate vascular connection, while the gill-plates as a whole become closely fused together in a similar manner.

This theory of origin is strengthened by closer observation of the phenomena of a single group. Taking the Septibranchiata as an instance, we find that in _Lyonsiella_ the branchiae unite with the mantle in such a way as to form two large pallial chambers, the structure of the branchiae being preserved, and their lamellae covering the

## partition. A further stage is observed in _Poromya_. There, a similar

## partition exists, but it has become muscular, preserving, however, on

each side two groups of branchial lamellae, separated one from the other by a series of slits, which form a communication between the two pallial chambers. A further stage still is seen in _Silenia_. There the same muscular partition exists, but the branchial lamellae on either side have disappeared, the slits between the two chambers, which occur in _Poromya_, still persisting, but separated into three groups. _Cuspidaria_ represents the last stage in the development. In the ventral chamber there appears nothing at all corresponding to a branchia; the surface of the partition appears perfectly uniform, but on careful examination three little separate orifices, remains of the three groups of orifices in _Silenia_, are observed.[276]

_Relation between Branchiae and Heart._--The object of the branchiae being, as has been already stated, to aerate the blood on its way to the heart, we find that the heart and the branchiae stand in very important structural relations to one another. When the branchiae are in pairs, we find that the auricles of the heart are also paired, the auricle on the right and left sides being supplied by the right and left branchiae respectively. This is the case with the Dibranchiate Cephalopods (_Argonauta_, _Octopus_, _Loligo_, etc.), the Zygobranchiate Prosobranchs (_Fissurella_, _Haliotis_), and all _Pelecypoda_. In the _Amphineura_ (_Chiton_, etc.) there are two auricles corresponding to the two sets of multiple branchiae. In the case of the Tetrabranchiate Cephalopods (_Nautilus_) there are four auricles corresponding to each of the four branchiae. Compare Fig. 79, A, B, C, D, E.

On the other hand, when the branchia is single, or when both branchiae are on the same side, and one is aborted and functionless, the auricle is single too, and on the same side as the branchia. This is the case with the Tectibranchiate Opisthobranchs (_Philine_, _Scaphander_, etc.), all the Pectinibranchiate Prosobranchs (Rachiglossa, Taenioglossa, and Ptenoglossa), and the other Azygobranchiate Prosobranchs (Trochidae, Neritidae, etc.). In the last case the right auricle exists, as well as the left, but is simply a closed sac, the coalescing of the two gills on the left side having thrown all the work upon the left auricle. Compare Fig. 79, F, G, H.

[Illustration: FIG. 79.--Diagram illustrating the relations between branchiae, heart, and aorta in the Mollusca: =A=, In Chiton; =B=, Pelecypoda; =C=, Dibranchiate Cephalopoda; =D=, Tetrabranchiate Cephalopoda; =E=, Prosobranchiata Zygobranchiata; =F=, Prosobranchiata Azygobranchiata; =G=, Prosobranchiata Monotocardia; =H=, Opisthobranchiata Tectibranchiata: 1, Ventricle; 2, Auricle; 3, Aorta; 3_a_, Cephalic aorta; 3_b_, Visceral aorta; 3_c_, Posterior aorta. (From A. Lang.)]

=Circulatory System=

All Mollusca, without exception, possess a circulatory system of more or less complexity. The centre of the system is the heart, which receives the aerated blood from the breathing organs, and propels it to every part of the body. In the Scaphopoda alone there appears to be no distinct heart.

The heart may consist simply of a single auricle and ventricle, and an aorta opening out of the ventricle. From the aorta the blood is conveyed to the various parts of the body by arteries. Veins convey the blood back to the breathing organs, after passing over which it returns by the branchial or pulmonary vein to the heart, thus completing the circuit.

As regards position, the heart is situated within the pericardium, a separate chamber which in the Pelecypoda, Cephalopoda, and the bilaterally symmetrical Gasteropoda lies on the median line, while in the asymmetrical Gasteropoda it is on one or other of the sides of the body, usually the right. The veins connected with the branchiae, and consequently the auricle into which they open, are situated _behind_ the ventricle in the Opisthobranchiata (whence their name), while in the Prosobranchiata they are situated _in front of_ the ventricle.

The number of auricles corresponds to the number of branchiae. Thus there is only one auricle in the great majority of Prosobranchiata (which are accordingly classified as _Monotocardia_), and also in the Opisthobranchiata, while the Pulmonata have a single auricle corresponding to the pulmonary chamber. There are two auricles in the Amphineura, in a small group of Gasteropoda, hence known as _Diotocardia_, in all Pelecypoda, and in the Dibranchiate Cephalopoda. In the Tetrabranchiate Cephalopoda alone there are four auricles corresponding to the four branchiae.

A single aorta occurs only in the Amphineura and in the Tetrabranchiate Cephalopoda. In all the other groups there are two aortae, leading out of the anterior and posterior ends of the ventricle in Pelecypoda and Dibranchiate Cephalopoda, while a single aorta leads out of the posterior end alone, and subsequently bifurcates, in most of the Gasteropoda. One aorta, the cephalic, supplies the front part of the body, the oesophagus, stomach, mantle, etc.; the other, the visceral aorta, supplies the posterior part, the liver and sexual organs.

The general circulatory system in the Mollusca has not yet been thoroughly investigated. As a general rule, the blood driven from the ventricle through the aorta into the arteries, passes, on reaching the alimentary canal and other adjacent organs, into a number of irregular spaces called _lacunae_. These in their turn branch into _sinuses_, or narrow tubes covered with muscular tissue, which penetrate the body in every direction. In the Dibranchiate Cephalopoda true capillaries are said to occur, which in some cases form a direct communication between the arteries and veins. According to some authorities[277] capillaries and veins exist in certain Pelecypoda in connexion with the intestinal lacunae, but this again is regarded by others as not established. A similar difference of opinion occurs with regard to the precise function of the foot-pore which occurs in many Mollusca, some holding that it serves as a means for the introduction of water into the blood-vascular system, while others regard it as a form of secretion gland, the original purpose of which has perhaps become lost.

=Blood.=--As a rule, the blood of the Mollusca--_i.e._ not the corpuscles but the liquor sanguinis--is colourless, or slightly tinged with blue on exposure to the air. This is due to the presence of a pigment termed _haemocyanin_, in which are found traces of copper and iron, the former predominating. _Haemoglobin_, the colouring matter of the blood in Vertebrates, is, according to Lankester,[278] of very restricted occurrence. It is found--(1) in special corpuscles in the blood of _Solen legumen_ (and _Arca Noae_); (2) in the general blood system of _Planorbis_; (3) in the muscles of the pharynx and jaws of certain Gasteropoda, _e.g._ _Limnaea_, _Paludina_, _Littorina_, _Chiton_, _Aplysia_. This distribution of haemoglobin is explained by Lankester in reference to its chemical activity; whenever increased facilities for oxidisation are required, then it may be present to do the work. The Mollusca, being as a rule otiose, do not possess it generally diffused in the blood, as do the Vertebrata. The actively burrowing _Solen_ possesses it, and perhaps its presence in _Planorbis_ is to be explained from its respiring the air of stagnant marshes. Its occurrence in the pharyngeal muscles and jaws of other genera may be due to the constant state of activity in which these organs are kept.[279]

According to Tenison-Woods[280] a species of _Arca_ (_trapezia_ Desh.) and two species of _Solen_, all Australian, have red blood. It is suggested that in these cases the habits of the animal (the _Solen_ burrowing deeply in sand, the _Arca_ in mud) require some highly oxidising element, surrounded as the creature is by ooze. In _Arca pexata_ (N. America) the blood is red, the animal being familiarly known as the ‘bloody clam.’ Burrowing species, however, are not all distinguished by this peculiarity. Tenison-Woods finds red fluids in the buccal mass of many Gasteropoda, _e.g._ in species of _Patella_, _Acmaea_, _Littorina_, _Trochus_, _Turbo_, giving the parts the appearance of raw meat.

=The Mantle=

On the dorsal side of the typical molluscan body, between the visceral sac and the shell, lies a duplicature of the integument, generally known as the _mantle_. The depending sides of the mantle, which are usually somewhat thickened, enclose between themselves and the body mass a chamber of varying size and shape, called the _mantle cavity_, which communicates freely with the external air or water, and encloses and furnishes a protection for the organ or organs of respiration. On its upper or dorsal surface the mantle is closely applied to the shell throughout its whole extent, the cells with which it is furnished secreting the materials from which the shell is formed (see p. 255). The whole mantle is capable, to some degree, of secreting shelly matter, but the most active agent in its production is the mantle edge or margin.

In the Prosobranchiata the mantle cavity, for reasons which have already been explained, is found on the left side of the animal, its front portion being in many cases produced into a tubular siphon. Within the mantle cavity are found, besides the branchia, the anus, the apertures of the kidneys, and the osphradium. In the pulmonata the mantle fold encloses a so-called lung-cavity. The front edge of the mantle coalesces with the integument of the neck in such a way as to enclose the cavity very completely, the only communication with the outer air being by means of the contractile breathing or pulmonary aperture on the right side. In the Tectibranchiate Opisthobranchs the mantle fold is inconsiderable, and is usually not of sufficient extent to cover the branchia, while in the Nudibranchs, which have no true branchiae, it disappears altogether.

In the Pelecypoda the mantle cavity is equally developed on each side, enclosing the two sets of branchiae. The mantle may thus be regarded as consisting of two equal portions, which form a sort of lining to the two valves. The lower or ventral portion of the mantle edges may be simple, or provided with ocelli (_Pecten_, _Arca_), tentacles, cilia (_Lima_, _Lepton_), or doubled folds. The two portions of the mantle touch one another along the whole line of the edge of the two valves, and, although thus in contact, may remain completely separate from one another, or else become permanently united at one or more points. This fusion of the mantle edges corresponds to important changes in the organisation of the animal as a whole. The anal and branchial siphons are no more than prolongations of the mantle edges on the posterior side into a tubular form. These ‘siphons’ exhibit the siphonal form more distinctly according as the adjacent portions of the mantle become more definitely fused together.

[Illustration: FIG. 80.--Diagram illustrating the various stages in the closing of the mantle in Pelecypoda: =A=, mantle completely open; =B=, rudiments of siphons, mantle still completely open; =C=, mantle closed at one point; =D=, mantle closed at two points, with complete formation of siphonal apertures; =E=, development of siphons, ventral closure more extended; =F=, mantle closed at three points, with fourth orifice: _f_, foot; _s.a_, _s.b_, anal and branchial siphons; 1, 2, 3, first, second, and third points of closure of mantle. (After A. Lang.)]

This progressive fusion of the mantle edges may be taken as indicating definite stages in the development of the Pelecypoda. A perfectly free mantle edge, joined at no point with the edge of the adjacent mantle, occurs in _Nucula_, _Arca_, _Anomia_, and _Trigonia_ (see Fig. 80, A, B). Here there is nothing in the nature of a siphon, either anal or branchial; in other words, no contrivance exists to prevent the spent water which has passed over the branchiae from becoming mixed with the fresh water which is to reach them. When the mantle edges are fused at _one point only_, this is invariably on the middle part of the posterior side, thus separating off an anal opening which may become prolonged into a tube-like form. At the same time the adjacent underlying portions of the mantle edges draw together, without actually coalescing, to form an opening for the incurrent stream of water, the rudiments of the ‘branchial siphon’ (Fig. 80, C). This is the case with most _Mytilidae_ (see Fig. 75) with _Cardita_, _Astarte_, and _Pisidium_. In the next stage the branchial opening is separated off by the concrescence of the mantle edges beneath it, and we have the mantle united _in two places_, thus forming three openings, the ventral of which is the opening for the protrusion of the foot (Fig. 80, D). This is the case in _Yoldia_, _Leda_, the majority of the Eulamellibranchiata (_e.g._ _Lucina_, _Cyrena_, _Donax_, _Psammobia_, _Tellina_, _Venus_, _Cardium_, _Mactra_), and all Septibranchiata. In _Chama_ and _Tridacna_ the fused portions of the mantle become more extended, and in _Pholas_, _Xylophaga_, _Teredo_, _Pandora_, and _Lyonsia_ this concrescence takes place over the greater length of the whole mantle edge, so that the mantle may be regarded as closed, with the exception of the three apertures for the foot and the two siphons (Fig. 80, E).

In certain genera there occurs, besides these three apertures, a fourth, in the line of junction between the pedal and branchial orifices. It appears probable that this fourth orifice (which has been regarded by some as an inlet for water when the siphons are retracted), stands in relation to the byssal apparatus (Fig. 80, F). In _Lyonsia_, for instance, a thick byssus protrudes through the orifice, which is large and open. In _Solen_, _Lutraria_, _Glycimeris_, _Cochlodesma_, _Thracia_, _Aspergillum_, and a few more genera, which have no byssus, the orifice is very small and narrow. It is possible that in these latter cases, the byssal apparatus having become atrophied, the orifice has been correspondingly reduced in size.[281]

=Mantle Reflected over the Shell.=--It is sometimes the case that the mantle edges tend to double back over the external surface of the shell, and to enclose it to a greater or less extent. When this process is carried to an extreme, the edges of the reflected mantle unite, and the shell becomes completely internal. We see an incipient stage of this process in _Cypraea_ and _Marginella_, where the bright polish on the surface of the shell is due to the protection afforded by the lobes of the mantle. A considerable portion of the shell of _Scutus_ is concealed in a similar way, while in _Cryptochiton_, _Lamellaria_, and _Aplysia_ the shell is more or less completely enclosed. Among Pulmonata, it is possible that in forms like _Vitrina_, _Parmacella_, _Limax_, and _Arion_, we have successive stages in a process which starts with a shell completely external, as in _Helix_, and ends, not merely by enveloping the shell in the mantle, but by effecting its disappearance altogether. In _Vitrina_ and some allied genera we have a type in which the mantle lobes are partly reflected over the shell, which at the same time exhibits rather less of a spiral form than in _Helix_. In the stage represented by _Parmacella_, the mantle edges have coalesced over the whole of the shell, except for a small aperture immediately over the spire; the nucleus alone of the shell is spiral, the rest considerably flattened. In _Limax_ the shell has become completely internal, and is simply a flat and very thin plate, the spiral form being entirely lost, and the nucleus represented by a simple thickening at one end of the plate. In _Arion_, the final stage, we find that the shell, being no longer needed as a protection to the vital organs, has either become resolved into a number of independent granules, or else has entirely disappeared.

Some indications of a similar series of changes occur in the Pelecypoda. The mantle edge of _Lepton_ is prolonged beyond the area of the valves, terminating in some cases in a number of filaments. In _Galeomma_ and _Scintilla_ the valves are partially concealed by the reflected mantle lobes, and in a remarkable form recently discovered by Dall[282] (_Chlamydoconcha_) the shell is completely imbedded in the mantle, which is perforated at the anterior end by an orifice for the mouth, and at the posterior end by a similar orifice for the anus. In all these cases, except _Lepton_, it is interesting to notice that the hinge teeth have completely disappeared, the additional closing power gained by the external mantle rendering the work done by a hinge unnecessary. It is quite possible, on the analogy of the Gasteropoda mentioned above, and also, it may be added, of the Cephalopoda and other groups, that we have here indicated the eventual occurrence of a type of Pelecypoda altogether deprived of valves, a greatly thickened mantle performing the part of a shell.[283]

* * * * *

The following works will be found useful for further study of this portion of the subject:--

=F. Bernard=, Recherches sur les organes palléaux des Gastéropodes prosobranches: Ann. Sc. Nat. Zool. (7) ix. (1890), pp. 89–404.

=G. Cuvier=, Le Régne animal (ed. V. Masson); Mollusca, Text and Atlas.

=C. Grobben=, Beiträge zur Kenntniss des Baues von Cuspidaria (Neaera) cuspidata Olivi, nebst Betrachtungen über das System der Lamellibranchiaten: Arb. Zool. Inst. Wien, x. (1893), pp. 101–146.

=E. Ray Lankester=, Encyclopaedia Britannica, 9th ed., vol. xvi. (1883), Art. ‘Mollusca.’

=A. Ménégaux=, Recherches sur la circulation des Lamellibranches marins: Besançon, 1890.

=K. Mitsukuri=, On the structure and significance of some aberrant forms of Lamellibranchiate gills: Q. Journ. Micr. Sc., N.S. xxi. (1881), pp. 595–608.

=H. L. Osborn=, On the gill in some forms of Prosobranchiate Mollusca: Stud. Biol. Lab. Johns Hopk. Univ. iii. (1884), pp. 37–48.

=R. Holman Peck=, The structure of the Lamellibranchiate gill: Q. Journ. Micr. Sc., N.S. xvii. (1877), pp. 43–66.

=P. Pelseneer=, Contributions à l’étude des lamellibranches: Arch. Biol. xi. (1891), pp. 147–312.

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