On the Ciliary Mechanism and s Interrelationships of ... · nidae) which ar oef special interes antd hav e been dealt with in separate papers (see Atkins I an, Partd II), thse majority

On the Ciliary Mechanisms andInterrelationships of Lamellibranchs.

PAET III: Types of Lamellibranch Gills andtheir Food Currents.

By

Daphne Atkins, B.Sc.Marine Biological Laboratory, Plymouth.

With 18 Text-figures.

CONTENTS.PAGE

INTRODUCTION . . . . . . . . . . 375

TYPES OF GILLS AND THEIE CILIATION 379

T Y P E A. Protobranchia 380

T Y P E B. Filibranehia and Pseudolamellibranohia . . . 382T Y P E C. Many Eulamellibranohia 388T Y P E D. Unionidae 408

T Y P E E. Tellinidae, Semelidae, and Anatinaeea . . . . 409T Y P E F . Lasaea rubra 412T Y P E G. Luoinidae, Montaoutidae, and Teredinidae . . . 413

DISCUSSION 415

SUMMAKY 419

I N T R O D U C T I O N .

IN the course of work on living gills, those of some ninetyodd species of Lamellibranchia, belonging to sixty genera andforty-one families, have been investigated. The great majoritywere marine, three only, Dre i s sens i a p o l y m o r p h a(Pallas), S p h a e r i u m oorneum (L.), and A n o d o n t aa n a t i n a (L.), being from fresh water. Separate accounts ofthe gills and their currents of all the species would entail muchneedless repetition, and, except for some forms (Nuculanidae,Arcidae, Anomiidae, Pteriidae, Solenidae, Ostreidae, Pecti-nidae) which are of special interest and have been dealt within separate papers (see Atkins, Parts I and II), the majority

376 D. ATKINS

can be grouped under more or less clearly defined types. Addi-tional notes on certain of those possessing specialized sortingdevices are given in Part II. In the following notes it is quitepossible that instances of frontal currents in opposite directionson the same gill filament, as in Ba rnea Candida (L.),P e t r i c o l a pho lad i fo rmis Lamarck, Spisu la sub-t r u n c a t a (da Costa), and Spisu la e l l ip t i ca (Brown),have been overlooked and only the obvious currents recorded.

A fact that has emerged from the work is the stability ofform and of the direction of the currents on the inner demi-branch, and the variability of the outer one.

The inner demibranch has:1. With apparently few known exceptions, both descending

(direct) and ascending (reflected) lamellae, though the depthof the ascending relative to the descending varies. The fewexceptions are all found in the Filibranchia. In two of them,H e t e r a n o m i a s q u a m u l a (L.), and Dimya a r g e n t e a(see Ridewood, pp. 193-5), both demibranchs consist of descend-ing lamellae only. Variation of the inner demibranch whilethe outer consists of both lamellae is found according toPelseneer (1903, p. 41, PL vii, fig. 86; 1906, fig. 207, p. 227,and p. 228) in Adacna rca n i t e n s Pels., a member of theArcidae, and in P l i c a t u l a a u s t r a l i s (1911, p. 96, PL xii,fig. 11) where the inner demibranch consists of a descendinglamella only. Eidewood (1903, p. 208), however, found bothdemibranchs of P l i c a t u l a aus t ra l i s^ to have descendingand ascending lamellae, as did also Watson (1930, p. 26, PI. v,fig. 3).̂

2. On the inner demibranch there is always a longitudinalcurrent along the free edge which is oral in direction, except inthe Arcidae and Anomiidae where it is aboral in direction (seePart I). There is generally a more or less marked groove at the

1 Pelseneer (1911, p. 32) suggested that Ridewood had wrongly deter-mined the species, but after the confirmative work of Watson some otherexplanation of the differing accounts would seem to be necessary. Ciliateddisks are present only at the ventral edges of the demibranchs and the upperedges of the ascending lamellae in this species, so that possibly the ascendinglamellae are apt to fall down if material is not well preserved.

THE CILIARY MECHANISMS OF LAMELLIBRANCHS 377

free edge,1 but in some bivalves, such as members of theArcidae, Anomiidae, Pectinacea, Tellinidae, and Semelidae, itis extremely shallow or absent.

3. On the inner demibranch the frontal currents are towardthe free edge on both lamellae. However, in Arcidae andAnomiidae, and in Cu l t e l lu s p e l l u c i d u s , there is a varia-tion, in that independent or separate dorsal and ventral currentsoccur on all gill filaments of this demibranch (see Part I); whilein certain Pseudolamellibranchia and Solenidae, which haveplicate gills, not only does this occur on certain of the ordinaryand apical filaments, but in the troughs of the plical groovesthe current is entirely dorsalward on both lamellae. In manybivalves for a short distance over the proximal ends of thedescending filaments there may be a current axial in direction(e.g. in certain Mactridae, S p h a e r i u m co rneum (L.), &c).This is indicated by Orton (1912, fig. 14, p. 462) in his diagramof the general mode of feeding in Lamellibranchs.

The outer demibranch on the other hand shows considerablevariation both in structure and currents. Pelseneer (1911,pp. 95-6) has noted its reduction in length (extends not as faranteriorly as the inner) and in depth (dorso-ventrally) in anumber of forms. The chief structural variations are as follows:

1. The outer demibraneh may be about the same depth asthe inner (e.g. in M y t i l u s , Ga leomma, P i n n a , Lima):where such gills are plicate the plications are as deep in theouter as in the inner demibranch. But in most forms it isconsiderably, though not evenly, narrower (e.g. S p h a e r i u m ,Cardium), and, where such gills are plicate, the plicationsare often less marked than on the inner demibranch, with fewerfilaments to a plica.

2. The outer demibranch, with few exceptions, was found tobe without a supra-axial extension in the Filibranchia andPseudolamellibranchia (as constituted by Pelseneer, 1911),

1 The free edge of the demibranohs may be regarded as normally morpho-logically ventral, but is by no means topographically ventral in relationto the shell in all bivalves. In those in which the gill axes run obliquelydorso-ventral, the free edges of the demibranchs may be actually almostanterior.

878 D. ATKINS

though in some species the ascending lamellae of both demi-branchs were as deep, or nearly as deep, as the descending. InO s t r e a they may be somewhat deeper than the descending,and this is especially noticeable of the outer demibranch ofOs t r ea a n g u l a t a . A supra-axial extension was found inmost of those Eulamellibranchs which have an outer demibranchconsisting of both lamellae; its degree of development variesgreatly, however, from narrow, L e p t o n s q u a m o s u m , todeep, with oblique filaments and frequently smooth when therest of the demibranch is plicate as in certain of the Veneridae;and it may not be present throughout the length of the demi-branch. Graham (1934a, p. 184) gave as characteristic of theSolenidae the absence of a supra-axial extension to the outerdemibranch. In members of this family it appears very narrowin the living animal, but is nevertheless obvious in sections(see Atkins, 1936, Part I, p. 299, fig. 42).

3. The outer demibranch may be upturned and consist ofboth lamellae, as in the posterior third of the gill of Te l l ina(see Eidewood, 1903, p. 151). In the Semelidae (= Scrobi-culariidae) (Sc rob icu la r i a p l a n a , Abra a l b a , Abran i t ida ) there also appears to be a recurved portion to theouter demibranch, but it is difficult to judge how far this is dueto contraction: Eidewood (1903, p. 235) stated that it is com-posed of the direct lamella only in S c r o b i c u l a r i a p i p e r a t a(= S c r o b i c u l a r i a plana) . In all these forms the junctionof the two lamellae of the outer demibranch is made on a gentlecurve, not at an acute angle as between those of the inner demi-branch. A much rounded lower edge to the inner demibranchis known only in some Verticordiidae (Anatinacea) (Eidewood,1903, p. 266).

4. The outer demibranch may be upturned and consist ofthe direct lamella only, as in the middle third of the gill ofTe l l ina and throughout the gill of the Anatinacea (Eidewood,1903, p. 151).

Pelseneer (1911, p. 96) considered that dorsal orientationof the outer demibranch is not due to upward bending, butthat what remains of this demibranch is nothing but thesupra-axial extension in the Anatinacea, and the supra-axial


extension with a mere trifle of the demibranch itself in theTellinidae.

5. The outer demibranch may consist of the direct lamellaonly but normal in direction as in Lasaea r u b r a (Pelseneer,1889, fig. 2, p. 40). In H e t e r a n o m i a s q u a m u l a andDimya a r g e n t e a both demibranchs consist of descendinglamellae alone.

6. The outer demibranch may be entirely wanting, as inLucinidae and Montacutidae. In the Teredinidae it is but avestige (see Eidewood, 1903, p. 260). It is wanting in the an-terior third of the gill of Te l l ina d o n a c i n a , Te l l inafabu la , and of A b r a . There is some variation in theTellinidae as to the length (antero-posterior) of the outer demi-branch: in Te l l ina donac ina and Te l l ina fabu la itis considerably shorter than the inner, as Eidewood (1903,p. 234) found in Te l l ina n i t i d a and Te l l ina (Arcopagia)capso ides , but in Te l l ina c rassa and Tel l ina t e n u i sit extends as far forward as the inner, though anteriorly it isvery narrow.

It is tempting to connect the variability of form of the outerdemibranchs in different Lamellibranchs with their later forma-tion embryologically. Unfortunately there is not a great dealof detailed information on the development of gills. Eice (1908)found in Myt i lus edulis—in which the outer and innerdemibranchs are very similar—that though the filaments ofthe outer demibranch do not begin to appear till about twentyfilaments of the inner demibranch have been formed, there isa change in the method of formation of the filaments when thespat is about 1 -6 mm. in length, and the inner and outer demi-branchs then develop pa r i p a s s u .

TYPES OF GILLS AND THEIR CILIATION.

In the Lamellibranchia a number of different types of gillstructure are found, most of which Eidewood (1903, fig. 2,p. 152) has shown in diagrammatic sections taken transverselyto the axes. In the present work the basis of classification is ongill structure and ciliary currents. The various types of gillsand their ciliation is as follows, see also Text-fig. 18.

380 D. ATKINS

TYPE A (Protobranchia: Text-fig. 1).

In the Protobranchia the gill consists of two rows of leaflets,attached to a branchial axis. The leaflets are dependent, exceptin the Solenomyidae, in which those of the outer demibranch areupturned.

The frontal currents are from the outer edge of the gill acrossthe axis to the inner edge, along which there is an oralwardcurrent, restricted, at least in N u c u l a , to that part of thegill behind the posterior edge of the foot (Text-fig. 1, I—II).Material collecting at the end of this route may either fall onthe mantle and be rejected, or may be removed by the palpsand palp appendages and conveyed to the mouth. Materialcollecting along the inner edge anteriorly, where there is nolongitudinal current, is also removed by the palps. There areno currents along the gill axes.Nuculidae: Nucu la nuc l eus (L.), (2)1; Nucu la r a d i a t a

Hanley, (2) (see also Orton, 1912). Orton (1913, pp. 38-40) has described So lenomya t o g a t a with similardirection of currents.

At least one ciliary variation is known:A (a), Text-fig. 1, III.—The frontal currents are rather

complicated, being in three tracts on each leaflet. On thefrontal edges of the leaflets the current (due to coarse cilia) isas in A, that is from the outer edge of the gill toward theinner edge, but interrupted along the axis by a longitudinalcurrent. Material may either pass across the axial groove, orinto it, according apparently to the type of material. Thereis no current along the inner edges of the gills, and materialcollecting here either falls on the mantle and is rejected, or isremoved by the palps and palp appendages and conveyed tothe mouth.

On each side of the frontal surfaces of the leaflets fine frontalcilia beat toward the axial groove on both demibranchs. Anoralward current is present in the axial groove to about thetwelfth pair of leaflets from the anterior end, but in front of

1 The numbers in brackets after names of species refer to the number ofspecimens examined.

THE CILIARY MECHANISMS OF LAMBLLIBRANCHS 881

this point the current is posterior. Material arriving from bothdirections is carried along the frontal surface of the twelfthinner leaflet to its inner edge, whence it is removed by the palpsand palp appendages and conveyed to the mouth.

inLEGENDS FOR TEXT-FIGURES.

In all figures # indicates the position of orahvard longitudinalcurrents; © the position of weak or incipient oralward longitu-dinal currents; X the position of posteriorly directed longitudinalcurrents. I.D., and O.D., inner and outer demibranchs; d.,dorsal edge of ascending lamella. Arrows indicate the directionof frontal currents.

TEXT-FIG. 1.

I. Type A: Nucu la . Modified after Orton, 1912.II. Type A: Solenomya t o g a t a . Modified after Orton, 1913.III. Type A (a): Nueu lana m i n u t a . Diagrammatic transverse

sections showing the form of the gill and the direction of thefrontal currents.

382 D. ATKINS

Nuculanidae: N u c u l a n a m i n u t a (Miiller) from Millport.Full account in Part I (Atkins, 1936).

In Yold ia l ima tu l a , according to Kellogg (1915, pp. 691-9), the frontal currents on both demibranchs are toward theaxial groove, along the whole length of which the currentis oralward, but in addition with a posterior current alongthe anterior part of it. Frontal currents toward the inneredges of the gills are apparently absent in Yo ld i a , orKellogg failed to observe them.

TYPE B (Filibranchia and Pseudolamellibranchia:Text-figs. 2-5).

In all the Filibranchia and Pseudolamellibranchia examinedthe outer demibranch differs little from the inner, and is with-out a supra-axial extension, except in Ostreidae, in which theascending lamellae of both demibranchs are frequently slightlydeeper than the descending. Two main sub-types occur basedon structure.

B (1), Text-fig. 2.—The demibranchs consist of both descend-ing and ascending lamellae, and the gill has the form of theletter W, though the outer demibranch may be less deep thanthe inner. There is a deep groove at the free edge of both innerand outer demibranchs, termed marginal groove (see Rice,1900, p. 72).

All frontal currents are ventralward, except for narrow zonesbordering the dorsal food grooves. Oralward longitudinalcurrents are found: in the marginal grooves; between the basesof the two demibranchs of each side of the body; and along thedorsal edges of all ascending lamellae.Mytilidae: Myt i l u s edul i s L., (many); Modiolus

modio lus (L.), (6); Modiolus phaseo l i nus (Philip-pi), (1); Modiolus a d r i a t i c u s Lamarck, (2);Musculus (=Modio la r i a ) m a r m o r a t u s (Forbes),(2); Musculus (=Crene l l a ) d iscors (L.) from Mill-port, (2); gills filibranchiate, flat, and homorhabdic.

Pinnidae: P i n n a f ragi l i s Pennant, (3): gills eulamelli-branchiate, plicate, and heterorhabdic.


Two ciliary variations of B (1) occur, due to the presence oftwo kinds of frontal cilia on the filaments.

B (la), Text-fig. 3.—The gills are filibranchiate, flat, andhomorhabdic. The free edges of all demibranchs are ungrooved.

TEXT-FIG. 2.

Type B (1): Mytilidae and Pinnidae. Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

Adjacent antagonistic frontal currents occur on all filaments:coarse cilia active only on stimulation, beat ventrally; fine,continuously active, cilia, beat dorsally. These may be inthree tracts, a median one of coarse cilia, with one of fine cilia

384 D. ATKINS

on each side (Arcidae); or in two tracts, one of coarse cilia onthe posterior side of the frontal surface, and one of fine cilia onthe anterior side (Anomiidae). Oralward longitudinal currents

TEXT-FIG. 3.

Type B (la): Arcidae and Anomiidae. Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

are found: between the bases of the two demibranchs of eachside of the body and along the dorsal edges of all ascendinglamellae. Posteriorly directed currents occur along the un-grooved free ventral edges of the demibranchs.

Although tracts of oppositely beating frontal cilia occur in


the Anomiidae, no general dorsal movement of material has beenobserved under experimental conditions, and the animals wouldseem to subsist largely on such material as is brought directlyto the broad dorsal food grooves by the main water current.Arcidae: Glycymeris g lycymer is (L.), (12); Area

t e t r a g o n a Poli, (6); Area lac tea L., (2). Detailedaccount given in Part I (Atkins, 1936).

Anomiidae: Monia squama (Gmelin), (7); Monia patel l i -formis (L.), (4). Detailed account given in Part I(Atkins, 1936) (for He te ranomia , see p. 387).

B (1 b), Text-fig. 4.—The lamellae are plicate and hetero-rhabdic; the gills may be either filibranchiate or eulamelli-branchiate. The free edges of the demibranchs may be grooved(Ostreidae); flattened or slightly grooved (Pectinidae, Limidae);or with the inner grooved and the outer slightly flattened(Pteriidae).

The frontal currents are dorsalward in the plical grooves(i.e. on the principal and adjacent ordinary filaments), andmainly ventralward on the crests (i.e. ordinary and apicalfilaments). At least in some species (e.g. P t e r i a h i r u n d o ,Chlamys ope rcu l a r i s , Chlamys t i g e r i n a , Ostreaedul i s , Ostrea v i rg in ica , Ostrea angula ta) , onsome, or all, of the ordinary and apical filaments, adjacentantagonistic frontal currents occur; coarse cilia beating ventrallyand fine ones dorsally: Lima was not examined for this. Asin B (la) these cilia are either in two tracts (e.g. P t e r i ahirundo), or in three tracts (e.g. Ostrea). Oralward cur-rents are found: along the free ventral edges of the demibranchs;between the bases of the two demibranchs of each side of thebody; and along the dorsal edges of all ascending lamellae.Pteriidae: P t e r i a h i rundo (L.), (1): gills filibranchiate.

Full account in Part I (Atkins, 1936).Pectinidae: Pec ten maximus (L.), (3); Chlamys dis-

t o r t a (da Costa), (2); Chlamys t i ge r ina (Miiller),(3); Chlamys ope rcu la r i s (L.), (2): gills filibranchiate.

Limidae: Lima hians (Gmelin), (2); Lima loscombiSowerby, (2); gills eulamellibranchiate (see also Studnitz,1931).

386

ORDINARY FILAMENT

PRINCIPAL FILAMENTTEXT-FIG. 4.

Type B(16): P t e r i a h i r u n d o . Diagrammatic transverse sectionshowing the form of the gill and the direction of the frontalcurrents. It would represent most Pseudolamellibranchia, exceptthat in Ostrea the ascending lamellae are slightly deeper thanthe descending.


Ostreidae: Ostrea edulis L., (3); Ostrea virginicaGmelin, (3); Ostrea angulata (Lamarck), (2): gillseulamellibranchiate (see also Yonge, 1926; Nelson, 1923;Atkins, 1937, Part II, p. 342).

TEXT-FIG. 5.

Type B (2): H e t e r a n o m i a . Diagrammatic transverse sectionshowing the form of the gill and the direction of the frontalcurrents.

B (2), Text-fig. 5.—The demibranchs consist of descendinglamellae only.

The obvious frontal currents (due to coarse cilia) are ventral-ward on all filaments. A posteriorly directed rejection current

is found along the adherent ventral edges of the two innerdemibranchs. A longitudinal current is absent along the ventraledges of the outer demibranchs, the recurrent paths on the mantleserving as rejection tracts for these. Broad oralward longitu-dinal currents occur between the bases of adjacent demibranchsof each side of the body. Though tracts of fine dorsally beatingcilia occur on all filaments, no general dorsalward movement ofmaterial has been observed under experimental conditions, andit seems as though the animal subsists largely on materialbrought directly to the broad dorsal food grooves by the mainwater current.

It may be considered that this type of gill should have beenplaced before the W-shaped type, as it is an actual example ofthe hypothetical type of gill which Pelseneer (1889, p. 43)conceived to be the link between the protobranchiate andfilibranchiate types. However, as the frontal currents are com-plicated, and it is doubtful whether the simplicity of the gill ofH e t e r a n o m i a is primitive—lack of a lamella (Lasaearubra) , and even of a demibranch (Lucinidae, Montacutidae,Teredinidae) is found among Eulamellibranchs—it has beenplaced second.Anomiidae: H e t e r a n o m i a squamula (L.), (12): gill fili-

branchiate, flat, and homorhabdic. Full account in Part I(Atkins, 1936).

TYPE C (many Eulamellibranchia: Text-figs. 6-13).Most of those Eulamellibranchs in which the outer demibranch

consists of both lamellae have a more or less distinct supra-axialextension, though it may not be present throughout the lengthof the demibranch: it is very narrow in some species, e.g.Kel l ia s u b o r b i c u l a r i s , L e p t o n s q u a m o s u m , andthe Pholadidae. In the great majority the outer demibranchis, in varying degree, less deep than the inner. The inner demi-branch in some bivalves is almost as deep (dorso-ventrally) asit is long (antero-posteriorly), as in Veneridae and in Sphaer -ium co rneum; in others long and narrow, as in Pholadidae.

Frontal currents on both lamellae of the inner demibranch passto the free-grooved edge, along which is an oralward current,

THE CILIAKY MECHANISMS OF LAMELLIBRANCHS 389

as also between the bases of the two demibranchs of each sideof the body. In the majority of species longitudinal currentsalong the dorsal edges of the ascending lamellae of the inner andouter demibranchs were not found (see also Kellogg, 1915),but such are present in Dre i s sens ia p o l y m o r p h a ,A s t a r t e s u l c a t a , and the Solenidae. In Lamellibranchsgenerally, with some few exceptions (e.g. Mytilidae, P i n n af rag i l i s , Dre i s sens ia p o l y m o r p h a , A s t a r t e sul-cata) longitudinal currents are found along the dorsal edgesof the ascending lamellae only when the frontal cilia beatdorsally on these lamellae. This mostly occurs only when thefrontal currents are complicated, adjacent antagonistic tractsof cilia being present on the same filament (e.g. G1 y c y m e r i s,Monia, Cultel lus) , with, in addition, a difference in thedirection of the frontal currents in the grooves and on the crestsof certain bivalves having plicate and heterorhabdic gills (e.g.P e c t e n , Solen).

Two main sub-types of C occur based on the absence or pre-sence of a groove at the free edge of the outer demibranch, andcorrelated differences in the direction of the frontal currentson the descending lamella of that demibranch.

C (1), Text-fig. 6.—In many Eulamellibranchs a groove ispresent at the free edge of the inner but not of the outer demi-branch. The outer demibranch is generally less deep than theinner, especially anteriorly, the most notable exception beingGaleomma. The absence of a marginal groove on the outerdemibranch of many Lamellibranchs was noted by Eice (1900,P- 72).

There is no interruption of the latero-frontal or lateral ciliaat the free edge, the appearance is that of a simple bendingof the filaments, with, in some forms, slight flattening of theedge.

The frontal currents on the outer demibranch are ventralwardon the ascending lamella, round the bend at the free edge, anddorsalward on the descending lamella, there being no modifica-tion of the frontal cilia and no longitudinal current at the freeedge. There appears to be a distinct tendency for particles,especially large ones or masses of particles, conveyed by the

390 D. ATKINS

•frontal cilia of the ascending lamella to pass off the demibranchat the free edge. A proportion of such material is drawn upbetween the outer and inner demibranchs and on to the de-

TEXT-FIG. 6.

Type C (1): Many Eulamellibranchia. Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

scending lamellae of these by the current produced by thelateral cilia.

Oralward longitudinal currents are found: along the marginalgroove of the inner demibranch, and between the bases of the

THE CILIARY MECHANISMS OP LAMELLIBRANCHS 391

two demibranchs of each side of the body. In Dre i s sens i ap o l y m o r p h a and A s t a r t e s u l c a t a longitudinal currentsare also found along the dorsal edges of all ascending lamellae.Dreissensiidae: Dre i s sens i a p o l y m o r p h a (Pallas),1 (2):

lamellae flat and homorhabdic. The inner demibranchhangs somewhat lower than the outer. In Dre i s sens i ap o l y m o r p h a though the food currents are as describedfor the type, yet on the descending lamella of the outerdemibranch on rare filaments the frontal cilia beat in theopposite direction to the normal, that is they beat ventrally.Particles transported by these cilia, however, pass on tofilaments with dorsally beating cilia, either before reachingthe free edge, or at the edge.

Astartidae: A s t a r t e s u l c a t a (da Costa), (2): lamellae flatand homorhabdic. In the narrow posterior halves of the gillsthe junction of the dorsal edges of the ascending lamellaeof the inner demibranchs i n t e r se is ciliary, as is alsothat of the outer demibranchs with the mantle. In theanterior region, however, the junctions appear to beorganic. Owing to the easily dissolved nature of the ciliaryjunction it may be clearly seen that the gill axes are freefor a considerable distance posteriorly, being attached againonly at the extreme tips.

Thyasiridae: T h y a s i r a f lexuosa (Montagu), (2): lamellaeflat and homorhabdic. Dark pigment granules present inthe sub-filamentar tissue.

Erycinidae: Ke l l i a s u b o r b i c u l a r i s (Montagu), (2): lamel-lae flat and homorhabdic. Outer demibranch about halfthe depth of the inner. For Lasaea r u b r a see p. 412.

Leptonidae: L e p t o n s q u a m o s u m (Montagu), (2): lamellaeflat and homorhabdic. Outer demibranch rather less thanhalf the depth of the inner.

Galeommatidae: Galeornma t u r t o n i Sowerby, (2):lamellae flat and homorhabdic. Demibranchs deep: accord-ing to Eidewood (1903, p. 228) the outer hangs lower than

1 I am indebted to Mr. C. Oldham for living specimens of Dre issens iapo lymorpha , from the Shropshire Union Canal, near Maeabury Marsh,Shropshire.

392 D. ATKINS

the inner, but in the two specimens examined at Plymouththere seemed little difference in the depth of the two demi-branchs, the outer being perhaps slightly less deep thanthe inner.

Sphaeriidae: S p h a e r i u m corneum (L.), (2): lamellae flatand homorhabdic. The inner demibranch is almost as deepas long: the outer is about a quarter the depth of the inner.An account of the gill currents, agreeing with the presentone, is given by Stenta (1903, p. 225).

Cardiidae: Card ium edule L., (2), (also see Orton, 1912);Card ium ovale Sowerby, (1): lamellae deeply plicateand heterorhabdic. The outer demibranch is only abouta quarter the depth of the inner.

Kellogg (1915, p. 667) described Card ium corb is withsimilar direction of currents and no groove at the free edgeof the outer demibranch.

Erodonidae: Aloid is g ibba (Olivi) (= Corbula nucleus) ,(2): lamellae flat and homorhabdic.

Solecurtidae: S o l e c u r t u s scopula (Turton) (= cand i -dus), (2); S o l e c u r t u s chamaso len (da Costa)(= a n t i q u a t u s), (2): lamellae plicate and heterorhabdic.The gills extend into the basal conjoined portion of thesiphons.

Kellogg (1915, p. 666) stated that in Tage lus Califor-nia n u s ' currents on all gill faces are to the margins andforwards'.

It was observed in a small specimen of S o l e c u r t u sscopula 1^ inches long, living in fine sand in the Labora-tory, that when well extended the inhalent siphon reacheda length of 4 | inches, and the exhalent 3£ inches. Theregion where the two siphons were conjoined was 1J incheslong. On rapid removal of the animals from the water andrough handling, portions of the siphons distal to the con-joined basal region are frequently thrown off by suddenviolent muscular contraction. Fragmentation of the siphonsof both S o l e c u r t u s scopula and S o l e c u r t u sc h a m a s o l e n is frequently seen when specimens arebrought in from S. S. Salpa. If autonomy has recently

THE CILIARY MECHANISMS OF LAMELLIBRANCHS 3 9 3

occurred the free portions of the siphons will be short. Inthe contracted state the siphons show annular constrictions,and it is at these places that they are thrown off. Promthe structure of the moderately long corrugated siphons ofSolen m a r g i n a t u s Montagu (= vagina) (Solenidae)it seemed probable that they also are capable of autonomy.Mr. A. J. Smith of the Plymouth Marine Station has in-formed me that whilst collecting on the sand bank up theEiver Yealm he saw a medium-sized plaice peck at thesiphon of a Solen m a r g i n a t u s , just showing abovethe sand. The Solen at once burrowed below thesurface leaving a section of the siphon on the sand. Afew minutes later when the tide went down he dug upthe Solen m a r g i n a t u s , thus making sure of itsidentity: also that he has seen many sections of Solensiphons in dredgings, and some in bowls under circulation.

Hiatellidae: H i a t e l l a ( = S a x i c a v a ) a r c t i c a (L.), (2);H i a t e l l a g a l l i c a n a (Lamarck) (= rugosa ) , (4):lamellae flat and homorhabdic. The gills are long andnarrow; the outer demibranch is about half the depth of theinner; they extend a considerable way into the basalportion of the siphons. The gills are sensitive and contractboth antero-posteriorly and dorso-ventrally on stimulation.

Gastrochaenidae: G a s t r o c h a e n a dub ia (Pennant), (1):lamellae flat and homorhabdic. On stimulation the gillscontract both antero-posteriorly and dorso-ventrally.

Several ciliary variations of C (1) occur. Two of these, C (1 a)and C (1&), show a progressive development of an oral wardcurrent along the free edge of the outer demibranch and lead onnaturally to C (2); the other two, C (1 c) and C (Id), are ciliaryvariations probably correlated with habitat, and show complica-tions of frontal currents due to the presence of two kinds offrontal cilia on all filaments of certain of the lamellae.

C (1 a), Text-fig. 7.—In a few bivalves an incipient oralwardcurrent is present along the ungrooved free edge of the outerdemibranch. This is due to the presence at the margin of coarsecilia on the posterior half of the frontal surface of each filament(Text-fig. 8). These beat toward the edge and forward, creating

394 D. ATKINS

a slight longitudinal current, but frequently sending particlesoff the demibranch. In fact, in these species there is a slightdevelopment of the cirrus-like cilia characteristically found along

TEXT-PIG. 7.

Type C (la): e.g. Pho l ad idea loscombiana . Diagrammatictransverse section showing the form of the gill and the directionof the frontal currents.

the grooved margins of demibranchs (see Wallengren, 1905,I and II), and which may be called terminal cilia.

On the anterior half of the frontal surface of each filamentunmodified frontal cilia are continuous round the bend, and

THE CILIARY MECHANISMS OF LAMBLLIBRANCHS 395

particles are transported by these from the ascending to thedescending lamella.

The terminal cilia are fewer in P h o l a d i d e a loscom-b iana than in the other bivalves of this type: they aresomewhat less coarse in Gari t e l l i n e l l a than in Gari fer-

POST

TEXT-FIG. 8.

Gari fervensis (= ferroensis). Sketch to show the appear-ance of the living filaments at the free edge of the outer demi-branch (descending lamella). The frontal surface is shown insurface view; the large latero-frontal cilia (eu.-l.-f.c.) and lateral(I.e.) cilia as they appear in optical section. Arrows indicate thedirection of beat of the frontal cilia (/.c.) and of the coarse terminalcilia (i.e.). The latter beat toward the free edge and anteriorly.Ant., anterior; Post., posterior; pro-l.-f.c, pro-latero-frontal cilia;s.c, sensory cilium. x 506J.

vens i s (= ferroensis) . In all except Donax v i t t a t u sthey are confined to the margins of the demibranchs, but insome individuals of that species they are continued dorsally as asingle row on the posterior side of the filament for a quarter toa third of the depth of the demibranch. They are also presentfor a varying distance on the inner demibranch and appear tobe a specialization for removing sand grains (see Atkins, Part II).These cilia beat ventrally, and therefore in individuals in which

396 D. ATKINS

they extend for a considerable distance on the descending lamellaof the outer demibranch the obvious frontal currents over thisdistance is ventral when they are active, though the fine ciliaare beating dorsally from the free edge.Donacidae: Donax v i t t a t u s (da Costa), (4): lamellae flat

and homorhabdic.Asaphidae (= Psammobi idae) : Gari t e l l i ne l l a (La-

marck), (3); Gari fervens is (Gmelin) (= ferroensis),(3): lamellae broadly plicate and heterorhabdic. Garit e l l i ne l l a is a deposit feeder, as is also probablyGari f e rvens i s .

Pholadidae: P h o l a d i d e a loscombiana Turton, (3):lamellae flat, or slightly plicate, and homorhabdic. Thegills are sensitive and contract dorso-ventrally on stimula-tion. They extend into the siphons, and are here narrow(see p. 407 for Barnea p a r v a , and p. 398 for Ba rneaCandida).

C (1 b), Text-fig. 9.—The difference between this group andthe previous one is in the degree of development of thecoarse cilia at the free edge of the outer demibranch. In thisgroup they occupy most of the frontal surface at the demibranchmargin. They beat ventrally on both lamellae, and anteriorly,creating a distinct oralward longitudinal current; but even herethere is a tendency for particles travelling over the ascendinglamella to pass off the demibranch. The terminal cilia extendbut a slight distance dorsally from the edge, although thedistance varies in different species, e.g. it is greater in P a p h i arhomboides than in Gafrar ium min imum. Even atthe free margin there is an exceedingly narrow tract of finefrontal cilia beating round the bend, but this is overshadowedby the coarse cilia, though to a less extent in My si a andGafrar ium than in the others.

In Venus ve r rucosa and Venus casina there appearsto be some tendency for grooving of the free edge of the outerdemibranch to occur. In one of two Venus ve r rucosa thefree edge was distinctly grooved, though in places a few un-grooved filaments intervened: the longitudinal current was dis-tinct. The frontal current, however, on the descending lamella

THE CILIARY MECHANISMS OF LAMELLIBEANCHS 397

was dorsal in direction, except along the free margin for a depthof one or two millimeters, where it was ventralward. Fourspecimens of Venus cas ina were examined. In three the

TEXT-FIG. 9.

Type C (16): e.g. Venus f a sc i a t a . Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents

free edge of the outer demibranch was ungrooved, the filamentsbeing merely slightly flattened at the bend. On the descendinglamella the frontal currents were dorsal in direction except over

S98 D. ATKINS

a narrow ventral zone of one or two millimeters over whichparticles passed ventrally into the longitudinal current alongthe free edge. In one specimen the free edge of the outer demi-branch was distinctly grooved and on some filaments a ventral-ward current was present for a considerable distance from the

Veneridae: Dos in ia e x o l e t a (L.), (3): lamellae broadlyplicate, with little differentiation of principal filaments. Inone specimen particles were seen clearly to pass round thefree edge of the outer demibranch, while in two others therewas a distinct longitudinal current.

Dos in ia l u p i n u s (L.) ( = A r t e m i s l i nc t a ) , (8):lamellae broadly plicate. A somewhat weak anterior cur-rent along the free edge of the outer demibranch.

Gaf ra r ium (Circe) min imum (Montagu), (2): lamellaeof outer demibranch practically flat, those of inner broadlyplicate and heterorhabdic.

Venus v e r r u c o s a L., (2); Venus cas ina L., (4):lamellae broadly plicate and slightly heterorhabdic.Venus (=Chione) o v a t a Pennant, (2): lamellaebroadly plicate and heterorhabdic. The current along thefree edge of the outer demibranch is somewhat slight andparticles have been seen to pass round the edge. Venus(=Chione) f a s c i a t a (da Costa), (3); Venus(=Chione) s t r i a t u l a (da Costa), (4); lamellae broadlyplicate and heterorhabdic.

P a p h i a r h o m b o i d e s (Pennant) (= Tapes v i rg ineus) ,(2): lamellae broadly plicate. For P a p h i a p u l l a s t r aand P a p h i a d e c u s s a t a see p. 405.

Petricolidae: Mysia (=Luc inops i s ) u n d a t a (Pennant),(4): lamellae broadly plicate. The siphons are free andflexible, and the inhalent very long; this bivalve is probablya deposit feeder. For P e t r i c o l a pho l ad i fo rmi s seep. 398.

C (lc), Text-fig. 10.—A small group of Eulamellibranchs,B a r n e a Candida (L.), P e t r i c o l a pho lad i f ormisLamarck, Sp isu la s u b t r u n c a t a (da Costa), andSpisu la e l l i p t i c a (Brown), show what are with little doubt


adaptative ciliary structures (see Atkins, Part II), namely, thepresence on all or certain of the lamellae of coarse ventrallybeating frontal cilia, in addition to the normal frontal cilia.

TEXT-FIG. 10.

Type C (lc): e.g. Barnea Candida. Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

On the descending lamella of the outer demibranch the twokinds of cilia create frontal currents in opposite directions, andso these four species have to be considered separately. In allthese forms oralward currents are present between the bases

400 D. ATKINS

of the two demibranchs of each side of the body, and along thefree edge of both inner and outer demibranchs.

B a r n e a Candida1 (Pholadidae), (2), has flat and homo-rhabdic lamellae. The marginal groove of the inner demibranchis shallow, that of the outer extremely shallow, there beinglittle more than a flattening of the edge. In addition to the finefrontal cilia, there is a tract of stout, cirrus-like cilia on theposterior side of the frontal surfaces of the filaments of alllamellae; these beat ventrally. On both lamellae of the innerdemibranchs and the ascending one of the outer, the fine frontalcilia also beat ventrally, but on the descending lamella of theouter demibranchs, except for a narrow ventral marginal region,they beat dorsally, that is in the opposite direction to the coarsecilia, as may be seen by direct observations of their beat, and bythe movement of particles. The distance from the free edge ofthe descending lamella of the outer demibranch at which thefine cilia beat in opposite directions varies somewhat on differentfilaments. When small quantities of fine carborundum (3P) aredropped on this lamella, some particles travel dorsally and someventrally. Large quantities dropped on the lamella are removedrapidly to the free edge, except over a narrow dorsal region,where large frontal cilia are few or absent, and particles in con-sequence are conveyed dorsally by the fine frontal cilia.

P e t r i c o l a pho lad i fo rmis 2 (Petricolidae), (2), hasbroadly plicate, but—so far as can be seen without sections—homorhabdic lamellae. The marginal groove of the inner demi-branch is well formed, that of the outer distinct, but shallow:the current along them is oralward. The ciliation of the fila-ments and the frontal currents on them are similar to those ofB a r n e a Candida: the cirri, however, are considerably largerthan those of that species.

Sp isu la s u b t r u n c a t a and Spisu la e l l i p t i c a3 (Mac-tridae) have flat and homorhabdic lamellae. In Sp isu las u b t r u n c a t a , (3), in addition to the normal frontal cilia asingle row of very long and coarse cilia is present on the

1 For other Pholadidae see p. 396 and p. 407.2 For Mysia u n d a t a see p. 398.

For other Mactridae see p. 405.


posterior sides of the frontal surfaces of the filaments of thedescending lamellae of the outer and inner demibranchs. Theyare closely placed ventrally, but tend to space out dorsally,being few and far between in the dorsal region. In Sp i su lae 11 i p t i c a, (5), such cilia generally extend only a short distancefrom the free edges, though the distance is subject to variation,and in some individuals they extend nearly a quarter to a thirdthe depth on the descending lamella of the outer demibranch,though widely spaced dorsally. In both species the coarse cilia,except for those bordering the margin, appear to be active onlywhen stimulated. On the descending lamella of the inner demi-branch the beat of the coarse cilia is in the same direction asthat of the fine ones, that is toward the ventral edge.

In Spisu la s u b t r u n c a t a the fine cilia on the descendinglamella of the outer demibranch beat toward the free edge fora very short distance only: over most of the depth of the lamellathey beat dorsally. This is obvious from the direction of move-ment of particles, and from observations of the direction of beatof the cilia. The relative distances probably vary in differentspecimens. The row of coarse cilia on the other hand beatventrally, and when the lamella is flooded with carborundumquickly transport it to the free edge. On the ventral half ofthe lamella this is the obvious current. Over the dorsal region,where the coarse cilia are few, the movement of particles isalmost entirely dorsalward. In Sp isu la s u b t r u n c a t athere is a good oralward current along the edge of the outerdemibranch, but there appears to be some variation in the formof the free edge. In some specimens the filaments were rounded,or but slightly flattened in this position, in others slightlygrooved. The flattened and grooved conditions are sometimesfound in the same demibranch.

In two out of five specimens of Spisu la e l l i p t i c a thefrontal currents and the condition of the free edge of the outerdemibranch were similar to those described for Sp isu las u b t r u n c a t a . In three, however, the free edge of the outerdemibranch was distinctly grooved, and the fine frontal ciliabeat ventrally toward it over the lower two-thirds of thedescending lamella of this demibranch, the direction of the beat

402 D. ATKINS

being seen in side view of the filaments: no dorsal movement ofparticles over this region of the lamella was observable. Theshells of these three animals differed slightly from those of theother two; the connexion of the shell differences with those ofthe gill, however, may be entirely fortuitous, and Mr. R.Winckworth has courteously identified them all as membersof the same species. But it is probable that they are fromdifferent habitats. It is to be expected from the relationshipsof types C (1, 1 a, 1 b, 1 c, and 2) that some species will be foundin which a certain amount of variation occurs; in which perhapsa change from ungrooved to grooved condition of the outerdemibranch is taking place, with consequent change in directionof beat of the normal fine frontal cilia on the descending lamellaof this demibranch (see Atkins, 1930).

C (Id), Text-fig. 11.—A most interesting ciliary variationof the type C (1) is that found in Cul te l lus p e l l u c i d u s ,which has flat and homorhabdic gills.

The obvious frontal currents are as in C (1), that is ventral-ward on both lamellae of the inner demibranch, but ventralwardon the ascending and dorsalward on the descending lamellaof the outer demibranch, with no longitudinal current at theungrooved free edge of the latter. On both lamellae of the innerdemibranch and also the ascending one of the outer, these cur-rents are due to coarse cilia. On these three lamellae there are inaddition tracts of fine frontal cilia, which beat dorsally, judgingfrom the movement of particles. Oralward currents are foundnot only along the shallow marginal groove of the inner demi-branch and between the bases of adjacent demibranchs of eachside of the body, but also along the dorsal edges of all ascendinglamellae.Solenidae: Cu l t e l lu s pe l l uc idus (Pennant), (4). Pull

account in Part I (Atkins, 1936). For Solen and Ens i ssee p. 407.

C (2), Text-fig. 12.—In certain Eulamellibranchs a groove ispresent at the free edge of the outer as well as of the inner demi-branch, and distinct oralward currents are present in thesegrooves. In some species the outer demibranch is only slightlyless deep than the inner (Barnea parva) , in others consider-


ably less deep (Mya truncata), while in others the depthvaries greatly in different regions (Mactra corallina). Themarginal groove of both demibranchs is deep in Lutraria

TEXT-FIG. 11.

Type C (Id): Cul te l lus pe l luo idus . Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

lutraria and Mya t runcata; moderately deep in Barneaparva, Mactra corallina, and Paphia decussata;rather shallow in Spisula solida; and that of the outerextremely shallow in Paphia pullastra. The groove insome species is not at the exact ventral edge, but slightly on

NO. 315 D d

404 D. ATKINS

the inner side, e.g. in Spisula solida and Mya truncata;an orientation probably due to the demibranchs curving inwardover the visceral mass.

TEXT-FIG. 12.

Type C (2): e.g. L u t r a r i a l u t r a r i a . Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

In all these species the frontal currents on all lamellae aretoward the free margins of the demibranchs, except over thedorsal region of the descending lamella of the outer demibranchof some forms, where for a certain distance the cilia beat dorsally

THE CILIARY MECHANISMS OF LAMEIiLIBRANCHS 405

into the oralward tract between the two demibranchs of eachside of the body. In some (Paphia p u l l a s t r a , Mya t r u n -cata) the current is dorsal for as much as a third to a halfthe depth of this lamella, but the distance appears to vary indifferent individuals. In P a p h i a d e c u s s a t a , with deeplyplicate lamellae, the current in the plical grooves of the descend-ing lamella of the outer demibranch passes dorsally over aboutthe upper two-thirds of the lamella, while on the crests it passesventrally for about the lower two-thirds, so that in the middlethird of the lamella currents pass in opposite directions in thegrooves and on the crests, but everywhere particles tend to passfrom the crests into the grooves.

In Sp i su la sol ida the dorsalward current in the dorsalregion is present on the descending lamellae of both demibranchs,but over a greater distance on the outer than on the inner. Thedividing line between dorsal and ventral currents is not clearcut, but is at different levels on adjacent filaments.

In Mac t r a c o r a l l i n a and B a r n e a p a r v a a tract ofcoarse, cirrus-like cilia is present in addition to the normal finecilia on the frontal surfaces of the filaments (see Atkins, PartII). There is, however, no difference in the direction of beat ofthe two kinds of cilia.

Oralward longitudinal currents are found in the marginalgrooves, and between the bases of adjacent demibranchs of eachside of the body, but were not observed along the dorsal edges ofthe ascending lamellae.Veneridae: P a p h i a (= Tapes) p u l l a s t r a (Montagu), (4);

P a p h i a d e c u s s a t a (L.), (2): lamellae plicate and hetero-rhabdic (for other Veneridae see p. 398). Kellogg (1915)found frontal currents to be ventralward on all lamellaeof Venus m e r c e n a r i a (p. 641), Chione f l uc t i -fraga (p. 644), Chione s u c c i n c t a (p. 644), T ive lac r a s s a t e l l o i d e a (p. 644), and S a x i d o m u s g igan-t iu s (p. 648).

Mactridae: Mac t r a c o r a l l i n a (L.) (= Mac t r a s t u l -torum), (3); Sp i su la so l ida (L.), (2): lamellae flatand homorhabdic. Kellogg (1915) described M a c t r aso l id i s s ima (p. 645), Sp isu la p o l y n y m a (p. 647),

406 D. ATKINS

and Spisu la p l a n u l a t a (p. 648) with similar type offrontal currents (for other Mactridae see p. 400).

ORDINARY FILAMENT PRINCIPAL FILAMENT

TEXT-FIG. 13.

Type C (2 a): Solen and En sis . Diagrammatic transversesection showing the form of the gill and the direction of thefrontal currents.

Lutrariidae: L u t r a r i a l u t r a r i a (L.), (4): lamellae broadlyplicate and homorhabdic. Kellogg (1915) described the


same direction of frontal currents for S c h i z o t h e r u sn u t t a l l i i , var. c a p a x (p. 632).

Myidae: Mya t r u n c a t a L., (1): lamellae flat and homo-rhabdic: the filaments with interlamellar septa are moreopaque than those without them, and this tends to givethe lamellae a slightly plicate appearance. All frontalcurrents are ventralward in Mya a r e n a r i a (Kellogg,1915, p. 649; Yonge, 1923, p. 24); and also i n P l a t y o d o nc a n c e l l a t u s (Kellogg, p. 651).

Pholadidae: B a r n e a p a r v a (Pennant), (5): lamellae flat andhomorhabdic. According to Eidewood (1903, p. 259) thereare very feebly marked and unequal plicae.

Kellogg (1915) described P h o l a d i d e a p e n i t a (p. 679),P h o l a d i d e a ovo idea (p. 681), Z i r faea g a b b i(p. 682), and B a r n e a pac i f ica (p. 685) with the sametype of frontal currents (see p. 396 for P h o l a d i d e al o s c o m b i a n a , p. 400 for B a r n e a Candida).

C (2 a), Text-fig. 13.—A complicated ciliary variation of thetype C (2) is found in Solenidae with plicate and heterorhabdicgills. The frontal currents on the crests (ordinary and apicalfilaments) are mainly ventralward, but dorsalward in thegrooves between them (principal, and in Ens i s adjacentordinary filaments). On most of the ordinary and apical fila-ments are adjacent antagonistic currents; coarse cilia beatingventrally and active only on stimulation, and fine cilia beatingdorsally and continuously active. Orahvard currents are foundnot only at the free grooved edges of the demibranchs, and be-tween the bases of the two demibranchs of each side of the body,but also along the dorsal edges of all ascending lamellae. Thistype is similar to that found in a number of Pseudolamelli-branchs, B (lb) (Text-fig. 4), except for the presence of a supra-axial extension to the outer demibranch. The ciliary mechan-isms of the gills of Solen and Ens i s have been treated indetail in Part I (Atkins, 1936).Solenidae: Solen m a r g i n a t u s Montagu ( = v a g i n a ) ,

(3); Ens i s s i l iqua (L.), (many); Ens i s a r c u a t u s(Jeffreys), (many); Ens i s ensis (L.), (1). For Cu te l l u sp e l l u c i d u s see p. 402.

408 D. ATKINS

TYPE D (Unionidae: Text-fig. 14).

The outer demibranch of the gill is ungrooved, in this resemb-ling type C (1). The frontal currents, however, differ from those

TEXT-PIG. 14.

Type D: Unionidae. Diagrammatic transverse section showing theform of the gill and the direction of the frontal currents.

described for that type, in fact no marine bivalve has beenfound with frontal currents similar to those of the fresh-waterUnionidae. The gill currents of A n o d o n t a have been in-vestigated by several authors (Stenta, 1903, p. 224; Wallengren,


1905, II, pp. 6-10, figs, A-E; Siebert, 1913; Allen, 1914), mostthoroughly by Wallengren; those of Unio by Kellogg (1915,pp. 687-91) and Allen (1914); those of Q u a d r u l a andL a m p s i l i s by Allen (1914). A n o d o n t a a n a t i n a (L.),(1), was investigated for the present work.

On the inner demibranch the frontal currents are toward themarginal groove on both lamellae: along this groove is an oral-ward current.

On the outer demibranch the frontal cilia beat dorsally overmost of the depth of both lamellae, but for a very short distanceat the ventral margin on both lamellae the unmodified frontalcilia beat ventrally, that is toward the free edge (see alsoWallengren, 1905, ii, fig. D, p. 8 and p. 9), though slightlyanteriorly, and send particles off the demibranch: there areno large terminal cilia at the free edge, and a longitudinalcurrent is absent in this position. Particles travelling up theascending lamella pass into an oralward current along its dorsaledge; while those travelling up the descending lamella pass intothe wide anterior current between the bases of the two demi-branchs of each side of the body (see also Wallengren, 1905,ii, figs, A, B, p. 7).

TYPE E (Tellinidae, Semelidae, Anatinacea: Text-fig. 15).

A number of Eulamellibranchs are remarkable in having theouter demibranch upturned, consisting of the direct lamellaonly in the Anatinacea, but with a recurved lamella in theposterior part of the gill in the Tellinidae (see Eidewood, 1903,pp. 151-3, figs. 1 B - E ; 2 H, J) and apparently also in theSemelidae (see p. 378). As previously mentioned Pelseneer(1911, pp. 95-6) considered that it is nothing but the supra-axial extension in the Anatinacea, with a mere trifle of thedemibranch itself in the Tellinidae.

On the inner demibranch frontal currents are to the free edgewith its oralward current. The free edge of the inner demibranchis either very slightly grooved or else flattened in Tellinidaeand Semelidae, which are deposit feeders; and deeply groovedin the Anatinacea, which are most probably suspension feeders.

On the outer demibranch the frontal currents are axial in

410 D. ATKINS

direction and continuous across the axis with those of thedescending lamella of the inner demibranch, particles beingconveyed to the oralward current along the free edge of thelatter. In those species in which the outer demibranch possessesa recurved lamella, the current passes around the bend and downthe direct lamella (Text-fig. 15, I). In Abra n i t i d a thereis an oralward current along the axis in the anterior region ofthe gill.Tellinidae: T e l l i n a t e n u i s da Costa, (2); Te l l ina

fabu la Gmelin, (1); Te l l ina d o n a c i n a L., (2):lamellae flat and homorhabdic. In Te l l ina fabu la andTe l l ina d o n a c i n a the gill is about the size of the palp;in Te l l ina t e n u i s the gill is considerably larger thanthe palp: in all the palps are large.

Macoma b a l t h i c a (L.), (1): lamellae flat and homo-rhabdic. Gill about the size of the palp: palps large.Kellogg (1915, p. 661, fig. 33) gave the same direction forthe currents of M a c o m a s e c t a .

Semelidae (= Scrobiculariidae): Abra a lba (S. Wood), (2);Abra n i t i d a (Miiller), (2): lamellae flat and homo-rhabdic. Gill about the same size, or rather smaller than,the palp: palps large. Kellogg (1915, p. 660, fig. 32)described similar direction of frontal currents in S e m e 1 edec i sa .

Periplomatidae: Cochlodesma p r a e t e n u e (Montagu),(1): lamellae deeply plicate and heterorhabdic.

Thraciidae: T h r a c i a v i l l o s i u s e u l a (Macgillivray), (2);T h r a c i a d i s t o r t a (Montagu), (1): lamellae deeplyplicate and heterorhabdic.

Lyonsiidae: Lyons i a no rweg ica (Gmelin), (3): lamellaedeeply plicate and heterorhabdic. Kellogg (1915) describedthe same direction of currents in M y t i l i m e r i a n u t -t a l l i i (p. 656, fig. 22) and Lyons i a sax ico la (p. 659,fig. 27).

Pandoridae: P a n d o r a p i n n a (Montagu), (1): lamellaebroadly plicate and heterorhabdic, with nine filaments toa plica. Outer demibranch very narrow.

E (a), Text-fig. 15, II.—A variation in the ciliary currents


TEXT-FIG. 15.

I. Type E: Most Tellinidae, Semelidae, and Anatinacea; except thatin the Anatinacea the reflected lamella of the outer demibranchis wanting.

II. Type E (a): Tellina crassa and Scrobicularia plana.Diagrammatic transverse sections showing the form of the gilland the direction of the frontal currents.

occurs in certain species in that an oralward current is presentalong the axis, i.e. between the two demibranchs of each sideof the body, and particles carried by the frontal cilia of the outerdemibranch pass into this. Species with such an axial current

412 D. ATKINS

seem generally larger than those without. Except for the dorsalorientation of the outer demibranch, the gill currents are similarto those of the C (1) type.Tellinidae: Tel l ina c rassa Pennant, (3): lamellae broadly

plicate and homorhabdic; inner demibranch large.Semelidae (= Scrobiculariidae): Sc rob icu la r i a p lana (da

Costa), (1): lamellae flat and homorhabdic; inner demi-branch large. No groove is present at the edge of the innerdemibranch, which is but slightly flattened; an anteriorcurrent is nevertheless present.

A detailed examination of the feeding mechanism of thedeposit-feeding Lamellibranchs, which suck up bottom detritusand contained organisms, by means of their long, free, flexiblesiphons, would be of interest. While some of these, e.g. Te l l inac ra s sa , Te l l ina t e n u i s , and Sc rob icu l a r i a p l a n a ,have large gills, others, Tel l ina fabu la , Tel l ina dona-c ina , Abra a lba , Abra n i t i d a , have them considerablyreduced, in fact about the same size or rather smaller than thepalps. From a somewhat cursory examination of these latterspecies it seemed as though much of the material entering themantle chamber by the extremely long inhalent siphon wascarried directly toward the large palps (see also Atkins, Part II,pp. 367-870). The correlation of small gills and large palpsis also met with in the deposit feeding Protobranchs, Nuculidae,and Nuculanidae, in which the gills are small and the chieffeeding organs are the palp appendages, which are extrusiblebeyond the shell and convey material directly to the large palps(Atkins, 1936, Part I, p. 186).

TYPE P (Lasaea r u b r a : Text-fig. 16).The outer demibranch consists of the descending lamella

only, but normal in direction. The frontal currents on thislamella are dorsalward into an orally directed current betweenthe two demibranchs of each side of the body. On the innerdemibranch the frontal currents are normal in direction, thatis they are toward the free edge, with its oralward current,on both lamellae. Lasaea r u b r a is a minute bivalve and thecurrents are therefore difficult to discern.


Erycinidae: Lasaea (=Kellia) rubra (Montagu), (2):gills flat and homorhabdic. For Kellia suborbicu-laris see p. 391.

TEXT-FIG. 16. TEXT-FIG. 17.

FlO. 16.—Type F: Lasaea r u b r a . Diagrammatic transverse sectionshowing the form of the gill and the direction of the frontal currents.

FIG. 17.—Type G: Lucinidae, Montacutidae, and Teredinidae. Dia-grammatic transverse section showing the form of the gill and thedirection of the frontal currents.

TYPE G (Lucinidae, Montacutidae, Teredinidae: Text-fig. 17).

The outer demibranch is entirely wanting in the Lucinidaeand Montacutidae, and vestigial in Teredo n a v a l i s (see

414 D. ATKINS

Eidewood, 1903, p. 260). The formation of the inner demibranchin Teredo is peculiar in that while the direct lamella descends,the reflected lamella passes horizontally inwards (see Eidewood).

The frontal currents of the inner demibranch are normal,passing toward the grooved free edge on both lamellae. Theonly longitudinal current is an oralward one in the marginalgroove.Lucinidae: Myr t ea ( = L u c i n a ) sp in i fe ra (Montagu),

(1), P h a c o i d e s (=L.) bo rea l i s (L.), (2); lamellaeflat and homorhabdic. The single demibranch is deep; inM y r t e a sp in i f e ra the ascending lamella is only abouthalf the depth of the descending, but in P h a c o i d e sb o r e a l i s it is almost as deep as the descending. Thefrontal currents appear to be slow. The palps are tiny.In both species the gills are dark brown—except the lobesof the marginal groove—the colour being due to granulesin the sub-filamentar tissue, and not in the epithelium ofthe filaments proper. Prom a habitat of silty sand.

Montacutidae: M o n t a c u t a ( = T e l l i m y a ) f e r rug inosa(Montagu), (1): lamellae flat and homorhabdic. The singledemibranch is deep; it is sensitive to stimulation. The gillaxes run almost dorso-ventrally. The palps are of a goodsize. Commensal with E c h i n o c a r d i u m c o r d a t u m inclean or silty sand (Marine Biol. Assoc., 1931, pp. 243, 298).

Mysel la (= Mon tacu t a ) b i d e n t a t a (Montagu), (2):lamellae flat and homorhabdic. The ascending lamella isabout half the depth of the descending. The palps arelarge. Found associated with O p h i o c n i d a b r a c h i a t a ,in numbers just below or above the disk, and i n P h a s c o l o -soma and other burrows in silty sand (Orton, 1923,p. 861; Marine Biol. Assoc, 1931, p. 243).

E n t o v a l v a p e r r i e r i (Malard), (2): lamellae flat andhomorhabdic. Occurring attached to L e p t o s y n a p t ai n h a e r e n s in coarse, loose sand (Marine Biol. Assoc,1931, pp. 242, 300).

Teredinidae: Teredo n a v a l i s L., (1): lamellae flat. Forthe structure of the gill see Eidewood (1903, p. 260). Boresin wood.


DISCUSSION.

Ridewood (1903, p. 150; fig. 2 D, p. 152) gave the gill W-shaped in transverse section—such as found in most Filibranchiaand Pseudolamellibranchia—as occurring in the majority ofLamellibranchia. In most of the British Eulamellibranchsinvestigated, possessing an outer demibranch consisting of twolamellae, there was a supra-axial extension, slight in some, deepin others, and in the majority the outer demibranch was notonly considerably less deep than the inner, but was withouta marginal groove.

Kellogg's work on the ' Ciliary Mechanisms of Lamellibranchs'(1915) in which he described those of thirty-two species, apartfrom the Protobranch Yold ia , gives the impression that it isusual for the frontal currents on both lamellae of both demi-branchs to pass toward the free edge, but in many BritishEulamellibranchs though the current is toward the free edgeon the ascending lamella of the outer demibranch, it is towardthe axis on the descending lamella. Where this occurs there isvery rarely a marginal groove on the outer demibranch, as foundin one specimen each of Venus ve r rucosa and Venusc a s i n a, though there may be a distinct longitudinal currentat the free edge. Kellogg (1915) in several American species ofVeneridae (Venus m e r c e n a r i a , p. 641; Chione f luc t i -f raga, p. 644; Chione succ inc t a , p. 644; Tivelac r a s s a t e l l o i d e a , p. 644; and Sax idomus g i g a n t i u s ,p. 648) found the frontal currents passed to the free edge on alldemibranchs; he does not state, however, whether a marginalgroove was present on the outer demibranch. Ventral directionof all frontal currents was found in P a p h i a p u l l a s t r a andP a p h i a decussata—though not in P a p h i a rhom-boid es—among the eleven British species of Veneridaeinvestigated.

Although some ninety odd species have been examined thesebelong to a large number of families, so that in many familiesbut one or two species have been seen; the greatest number,eleven, being in the Veneridae. It is therefore not knownwhether the members of a family usually have the same type

B[2J

Bfa)

TEXT-FIG. 18.

Diagrammatic transverse sections of types of Lamellibranch gillawith their food currents. The inner demibranch is on the right inall sections.

A. Protobranchia; e.g. Nucula: A (a), Nuculana minuta .B. Filibranchia and Pseudolamellibranchia: B (1), Mytilidae,

Pinnidae; B (la), Arcidae, Anomiidae; B (16), most Pseudo-lamellibranchia: I, ordinary and II, principal filaments; B (2),Heteranomia.

0. Many Eulamellibranchia: C (1), many Eulamellibranehia; C (1 a),e.g. Pholadidea loacombiana; C (16), e.g. Venus fas-ciata; C (lc), e.g. Barnea Candida; C {Id), Cultelluspellucidus; C (2), e.g. Lut ra r ia lu t r a r i a ; C (2 a), Solenand Bnsis: I, ordinary and II, principal filaments.

D. Unionidae.E. Tellinidae, Semelidae, Anatinacea: E (a), Tellina crassa,

Scrobicularia plana.F. Lasaea rubra .G. Lucinidae, Montacutidae, Teredinidae.

418 D. ATKINS

of gill and frontal currents. In nine of the forty-one familiesdifferent sub-types or types were found within the family. Inseven they denote chiefly an increasing efficiency in food con-veyance on the outer demibranch, and occasionally some specialciliary mechanism correlated with habitat; in two, Anomiidaeand Erycinidae, marked structural differences in the gills. Inthe Pholadidae three variations were found, namely C (la),Pholadidea loscombiana; C (lc), Barnea Candida;and C(2), Barnea parva (see Text-fig. 18). Two variationswere found in each of the following eight families: in Anomiidae,B (lft), Monia squama and Monia patelliformis;and B (2), Heteranomia squamula: in Erycinidae,C (1), Kellia suborbicularis; and F, Lasaea rubra:in Veneridae, C (lb), most species; and C (2), Paphia pul-lastra and Paphia decussata: in Petricolidae, C (1 b),Mysia undata; andC(lc), Petricola pholadiformis:in Mactridae, C (lc), Spisula subtruneata , Spisulaelliptica; and C (2), Spisula solida, Mactra coral-lina: in Solenidae, C (Id), Cultellus pellucidus; andC (2a), Solen marginatus, Ensis siliqua, Ensisarcuatus, Ensis ensis: in Tellinidae, E, Tellinatenuis, Tellina fabula, Tellina donacina.Macomabalthica; and E (a), Tellina crassa: in Semelidae, E,Abra alba, Abra nit ida; and E (a), Scrobiculariaplana.

It is an interesting possibility that C (1), C (1 a), C (1 b), andC (2) form a natural series with increasing efficiency in foodconveyance on the outer demibranch (see Text-fig. 18). In thesimplest forms, C (1), the frontal currents on the ascendingand descending lamellae of that demibranch are continuous,uninterrupted by any longitudinal current at the free edge.Particles are carried into an oralward tract along the gill axes(i.e. between contiguous demibranchs of each side of the body),which is frequently broad, with a strong current. In C (1 a) atthe free edge there is modification of some of the frontal cilia(terminal cilia), with a slight oralward current. In C (1 b) thereis a definite oralward current, which, however, has had littleeffect on the direction of beat of the unmodified frontal cilia.


In one specimen each of Venus v e r r u c o s a and Venusc a sin a at the free edge there was a slight groove with a goodcurrent, but even this had little affected the direction of beatof the frontal cilia. In C (2) there is a distinct groove with astrong oralward current at the free edge of the outer demibranch,toward which beat the frontal cilia on both descending andascending lamellae. This last type is rather similar to thatfound in the Mytilidae and Pinnidae (Type B (1)) except forthe general absence of a current along the dorsal edges of theascending lamellae, the presence in certain species of dorsalwardcurrents over a considerable dorsal region of the descendinglamella of the outer demibranch, and the presence of a supra-axial extension. It is found among the higher Eulamellibranehfamilies.

It is generally difficult to see a connexion between the typeof gill and frontal currents, and the habitat and mode of life—though it must be confessed that little is known of details ofthese. Certain bivalves, however, have additional tracts ofcoarse ventrally beating frontal cilia, which are clearly corre-lated with habitat (see Atkins, Part II). Such cilia beat in theopposite direction to the normal frontal cilia in some types ofgill, and are necessarily included in the present study.

SUMMARY.

Seven main types of Lamellibranch gills and their foodcurrents, together with a number of varieties, have been de-scribed. These are shown summarily and comprehensively inthe composite diagram in Text-fig. 18.

LITERATURE.

Allen, W. R. (1914).—"The Food and Feeding Habits of FreshwaterMussels", 'Biol. Bull. Woods Hole', vol. xxvii.

Atkins, D. (1930).—"On Abnormal Conditions of the Gills in Mytilusedulis. Part I. On Permanent Natural Reversal of the Frontal Ciliaon the Gill Filaments of Mytilus edulis", 'Journ. Mar. Biol. Assoc.',vol. xvi, N.S.

(1936-7).—"On the Ciliary Mechanisms and Interrelationships ofLamellibranohs, Parts I and II" , 'Quart. Journ. Micr. Soi.', vol. lxxix.

Esohrioh, H. (1931).—"Cultellus pellucidus", 'Zool. Jahr.', Bd. liii.NO. 315 B e

420 D. ATKINS

Ghosh, E. (1920).—"Taxonomic Studies on the soft parts of the Solenidae",'Rec. Ind. Mus.', vol. xix.

Graham, A. (1934).—"The Cruciform Muscle of Lamellibranchs", 'Proc.Roy. Soc. Bdin.', vol. liv, pt. 1.

(1934a).—"The Structure and Relationships of Lamellibranchspossessing a Cruciform Muscle", ibid., pt. 2.

Kellogg, J. L. (1915).—"Ciliary Mechanisms of Lamellibranchs, withdescriptions of anatomy", ' Journ. Morph.', vol. xxvi.

Marine Biological Association, 1931.—'Plymouth Marine Fauna', 2nd ed.Nelson, T. C. (1923).—"The Mechanism of Feeding in the Oyster", 'Proc.

Soc. Exp. Biol. and Med.', vol. xxi.Orton, J. H. (1912).—"The Mode of Feeding of Crepidula, &e.", 'Journ.

Mar. Biol. Assoc.', vol. ix, N.S., 1910-13.(1913).—" The Ciliary Mechanism on the gill, and the Blode of Feeding

in Amphioxus, Ascidians, and Solenomya togata", ibid., vol. x, N.S.,1913-15.

(1923).—"Some new Commensals in the Plymouth District",'Nature', vol. cxii.

Pelseneer, P. (1889).—"Sur la classification phylogenetique des Pelecy-podes", 'Bull. Sci. France et Belg.', torn, xx, ser. 3, vol. 2.

(1903).—'Mollusques. Rfeultats du Voyage du S.Y. Belgica en 1897-1898-1899.'

(1906). "Mollusca", 'A Treatise on Zoology', edited by E. RayLankester. Adam and Charles Black, London.

(1911).—'Les Lamellibranches de l'Expedition du Siboga', PartieAnatomique, Monographie liii a, Siboga-Expeditie.

Rice, E. L. (1900).—"Fusion of Filaments in the Lamellibranch Gill",'Biol. Bull. Woods Hole', vol. ii, 1900-1.

(1908).—"Gill Development in Mytilus", ibid., vol. xiv, 1907-8.Ridewood, W. G. (1903).—"On the Structure of the Gills of the Lamelli-

branchia", 'Phil. Trans. Roy. Soc, Lond.', B, vol. cxcv.Siebert, W. (1913).—"Das Korperepithel von Anodonta cellensis", 'Zeit.

f. wiss. Zool.', Bd. cvi.Stenta, M. (1903).—"Zur Kenntniss der Stromungen im Mantelraume

der Lamellibranchiaten", 'Arb. Zool. Inst. Univ. Wien.', torn, xiv,heft 2.

Studnitz, G. (1931).—"Die Morphologie und Anatomie von Lima inflata,der Feilenmuschel, nebst biologisohen Untersuchungen an Lima hiansGmel", 'Zool. Jahr.', Bd. liii.

Wallengren, H. (1905, I).—"Zur Biologie der Muscheln. I. Die Wasser-stromungen", 'Lunds Univ. Arsskrift', N.F., Afd. 2, Bd. i, nr. 2.

(1905, II).—"II. Die Nahrungsaufnahme", ibid., N.F., Afd. 2, Bd. i,nr. 3.

Watson, H. (1930).—"On the Anatomy and Affinities of Plioatula",'Proc. Malac. Soc. Lond.', vol. xix, pt. 1.


Winckworth, R. (1932).—"The British Marine Mollusca", ' Journ. Conch.',vol. xix, no. 7.

(1934).—"Names of British Mollusca. I I " , ibid., vol. xx, no. 1.(1934a).—"Names of British Mollusca. I l l " , ibid., vol. xx, no. 2.

Yonge, C. M. (1923).—"The Mechanism of Feeding, Digestion and Assimila-tion in the Lamellibranch Mya", 'Brit. Journ. Exp. Biol.', vol. i, 1923-4.

(1926).—"Structure and Physiology of the Organs of Feeding andDigestion in Ostrea edulis", 'Journ. Mar. Biol. Assoc.', vol. xiv, N.S.,1926-7.

Documents

On the Ciliary Mechanism and s Interrelationships of ... · nidae) which ar oef special interes antd hav e been dealt with in separate papers (see Atkins I an, Partd II), thse majority