Functional anatomy of the buccal apparatus of Onchidoris bilamellata (Mollusca: Opisthobranchia)

Trans. zool. SOC. Lond. ( I 977) 34,45-86

Functional anatomy of the buccal apparatus of Onchidoris bilamellata (Mollusca: Opisthobranchia)

DENISE M. CRAMPTON* Dcpartment of Zoology, University of Reading

(Accepted 12 October 1976)

(With 17 figures in the text)

Published for

THE ZOOLOGICAL SOCIETY OF LONDON

ACADEMIC PRESS

*Now at the Medical Research Council, 20 Park Crescent, London.

COPYRIGHT 0 1911 BY THE ZOOLOGICAL SOCIETY OF LONDON, REGENT'S PARK, LONDON, NW1 4RY

Functional anatomy of the buccal apparatus of Onchidoris bilamellata (Mollusca : Opisthobranchia)

The ingestive cycle of Onchidoris is described based upon an anatomical investigation of the buccal apparatus together with observations of feeding activity and spontaneous and induced movements of the buccal apparatus. Feeding is accomplished by a complex series of movements of 25 buccal muscles operating the odontophore and the buccal pump. Protraction of the buccal apparatus is largely passive and is dependent upon increased blood pressure within the head whereby blood is isolated in a number of distinct haemocoels surrounding the buccal apparatus. The odontophore is everted through the mouth by the contraction of ventral and lateral odontophoral protractor muscles and the radular teeth are erected by a deformation of the odontophoral cartilage. The effective stroke of the radula results in the piercing of the barnacle mantle and the opercular plates are discarded by ciliary currents around the mouth of the dorid. Retraction of the buccal apparatus follows due to the contraction of buccal retractor and retractor of the buccal lip muscles and this is accompanied by the inhalant phase of the buccal pump. As a result of these last activities,all the soft parts of the barnacle, including the cirri, are taken into the buccal cavity. I t is suggested that Onchid~~ris represents a high degree of specialization in its feeding behaviour because, although many of the buccal muscles are homologous with those described in other opisthobranchs, their methods of operation, particularly in conjunction with a piercing, grasping radula and a buccal pump that can operate during both ingestion and swallowing, are unique. The buccal apparatus of O/zchidor.is is compared with that of a number of other opisthobranchs including Philine, Cylichrin and Archidoris. .

CONTENTS

Introduction . . Materials and methods

. . . . . . . . . . . . .

. . . . . . . . . . . .

Page . 49 . 49

External features of the head and observed feeding behaviour . . . . . . 50 Anatomy of the buccal apparatus . . . . . . . . . . . . . . 53 Musculature of the buccal apparatus . . . . . . . . . . . . . . 59 Blood supply of the anterior region of the body . . . . . . . . . . 12 Movement of blood through the buccal apparatus . . . . . . . . . . 14 Innervation of the buccal apparatus . . . . . . . . . . . . . . 15 The feeding cycle . . . . . . . . . . . . . . . . 15 Discussion . . . . . . . . . . . . . . . . . . . . . . 80 References . . . . . . . . . . . . . . . . . . 85

. . . .

. . . .

BUCCAL A N A T O M Y O F O N C H I D O R I S 49

INTRODUCTION

The method of operation of the gastropod buccal mass has intrigued malacologists ever since Ankel(l937, 1938) elucidated the mechanisms of radular action in a range of prosobranchs. Since that time, the buccal mass of prosobranchs, and to a lesser extent the pulnionates, has been extensively investigated, but detailed studies on opisthobranchs are few even though they have extremely varied diets and a wide range of radular structure.

Millott (1937) investigated the anatomy of Jorunna tomentosa (Cuvier) which feeds on sponges by rasping away large pieces and carrying these into the buccal cavity on recurved teeth. No description of buccal musculature was given so that the method of operation of the odontophore is not easily understood. The same applies to Morse’s (1968) description of the digestive system of Acanthodoris pilosa (Abildgaard) which rasps zooecia of Flus- trella hispida and sucks out the soft contents. Anatomical and functional aspects of the buccal mass have been carefully studied in bullomorphs by Lemche (1956) in Cylichna and Hurst (1 963) in Philine and Scaphander. These are representatives of the most primitive order of opisthobranchs and exemplify the numerous differences between the organization of the buccal mass in prosobranchs and the lower opisthobranchs. The higher opisthobranch orders have, however, been relatively neglected in respect of their buccal anatomy and function. Young (1969) investigated 48 Indo-West Pacific doridids and hexabran- chids, Forrest (1953) compared the feeding mechanisms of rasping and sucking dorids and Barnes & Powell (1954) described the damage to barnacles caused by Onchidoris. These accounts are generalized and give insufficient detail to provide either an understapding of the interrelationship between buccal anatomy and feeding behaviour in any one nudibranch or a comparison of the feeding mechanisms of primitive and more advanced opisthobranchs. The most comprehensive account of the structure and function of the doridacean buccal mass is that of Rose (1971) on Archidoris pseudoargus (Rapp), a dorid which has a rasping radula and feeds on encrusting sponges.

It was, therefore, considered opportune to carry out a detailed investigation of one of a group of higher opisthobranchs which have evolved a buccal pump-a muscular diverti- culum of the buccal cavity thought to assist in the ingestion of food. It would be surprising if the development of such a structure had not been accompanied by modifications to the remainder of the buccal apparatus from that found in grazing dorids such as Archidoris or an animal which grasps its prey with a strong, hooked radula like Philine. It was in order to explore these changes, and their significance, that this work was undertaken. An investigation of the buccal nerve and blood supply was an integral part of the study, both to further understanding of odontophoral activity and to trace homologies of muscles in Onchidoris, Archidoris and Philine.

MATERIALS AND METHODS

Animals were relaxed by placing them in either tap water or a solution of 7 % magnesium chloride in distilled water and details of musculature observed by adding a few drops of picric

50 D. M. C R A M P T O N

acid to the dissection. The topography of membranes was clarified by injecting aqueous methylene blue (Gurr) into haemocoels prior to dissection and ciliary tracts were studied by adding carmine particles to pieces of tissue in sea water. Injection of a carmine suspension into the ventricle illustrated the arterial system in the dissected animal, but for those arteries embedded in tissues, a hard setting injection fluid was used, either coloured rubber latex dissolved in 10% ammonia solution or a medium based upon acetone, plastic glue and coloured oil paint (Hian, 1971). Large nerves were traced by dissection in a saturated aqueous picric acid medium (Peacock, 1966) and finer nerves by Alexandrowicz’s method (1932). Radular preparations were stained in a 0.005 % solution of lignin pink (Gurr) in picric acid and histological information was obtained by sec- tioning material embedded in “paraplast” and stained in Heidenhein’s haematoxylin or Masson’s or Mallory’s trichrome stains (Pantin, 1969). The effects of muscle activity were investigated by observing the results of the electrical stimulation of individual muscles using conventional suction electrodes with a diameter of about 80 pm.

Spontaneous movements of the buccal apparatus were observed by making a median dorsal longitudinal incision through the anterior body wall and observing the buccal movements in response to barnacle extract injected through the mouth. Feeding was observed more easily by cutting away sections of the oral veil of starved animals which were then allowed to feed.

EXTERNAL FEATURES OF THE HEAD AND OBSERVED FEEDING BEHAVIOUR

When Oncliidoris is crawling, the mouth is obscured by the anterior dorsal and lateral portions of the mantle. The mouth is a flattened horizontal slit surrounded by greatly folded, white, fleshy, outer lips whose outer edge is confluent dorsally and laterally with the oral veil, a frilled extension of the head lying beneath the anterior portion of the mantle. The epithelium of the oral veil is ciliated, the tracts radiating outwards from the mouth so that particles accumulate on its dorsal surface and on the anterior edge of the foot.

Onchidoris is found associated with both Balanus balanoides and B. crenatus and tends to be gregarious, in groups of two to six clustered upon the under-surface of barnacle-covered rocks. Most feeding occurs at night although starved animals may feed at other times. When seeking food, Onchidoris crawls slowly over the barnacle-encrusted surface and eventually stops so that the head lies over the operculum of a barnacle. The dorid may stay in this position for a period of time ranging from 10 minutes to two hours, not all necessarily spent feeding. By removing animals at various stages it becomes obvious that the longest time is taken in opening the barnacle; ingestion of the contents is rapid (one individual was found to empty the exoskeleton in five seconds although others took up to 15). Examination of the barnacle afterwards shows that the scuta, terga and cirri have been removed with the whole of the soft parts, leaving only the hollow testa. The opercular valves are not ingested and are found where the animals have been feeding. The stomach contents are difficult to identify even immediately after feeding, but fractions of cirri are occasionally identified.

Feeding can be observed only by cutting away that portion of the mantle overhanging the mouth together with small areas of the oral veil. The first obvious phase is a dilatation of the outer lips (Fig. l(b)), with the oral veil pressed tightly against the vertical walls of the barnacle test. When the mouth is opened fully the expanded inner lips form a thick horseshoe-shaped ring, the cavity of which is filled by the buccal lips. These are then protracted rapidly and separate to reveal a pear-shaped aperture with the tapered end

(C)

oute

r

oral

vei

l

oral

vei

l

....

....

..

.. .:'...

odo

ntop

hore

\\

.....

...

//

....

. /

//

foot

oral

vei

l \\

......

......

. ...

......

\\

ca

vity

...

......

...

......

.....

._

...

lip

\ \

bu

cc

d /

cavi

ty

(d)

oral

vei

l

\'

rad

ula

r I

bucc

al

too

th

Imm

I ca

vity

FIG

. 1. O

nchi

dori

s: V

entr

al v

iew

of

head

dur

ing

feed

ing.

(a)

Res

ting

posi

tion;

(b)

at

the

begi

nnin

g of

odo

ntop

hora

l pr

otra

ctio

n; (

c) in

the

mid

dle

of

odon

toph

oral

pro

trac

tion;

(d)

the

effe

ctiv

e pha

se o

f th

e fe

edin

g cy

cle.

u

+

52 D. M . C R A M P T O N

FIG. 2. Onchidoris: Anterior haemocoels. (a) Sagittal section of the head: (b) Transverse section of the head.

B U C C A L A N A T O M Y O F O N C H I D O R I S 53

\-entral (Fig. l(c)). The odontophore is now visible between the buccal lips; the concavity af its cartilage may be seen but its teeth are closed. The next stage involves a dilatation of the buccal lips so that the inner lips are no longer visible. The odontophore is then fully protracted and changes shape with flattened lateral portions, spread radular membrane and erect teeth (Fig. l(d)).

A U-shaped gutter in the dorsal portions of the buccal lips leads to the aperture of the pedicel of the pump; sometimes the aperture itself may be visible. The next stage involves a dorsal movement of the dorsal edge of the odontophore and simultaneously, a flattening of the lateral edges of the cartilage, resulting in a medial and posterior rotation of the reeth so that those on each side of the midline come together. The odontophore then moves posteriorly into the buccal cavity and there is a gradual closing of the buccal lips. The dorsal gutter disappears and the lips retract. The next stages are the reverse of the opening stages of the feeding cycle, with the inner lips retracting and disappearing behind the closing outer lips.

The odontophore contacts the barnacle when fully protracted and executes a rapid anterior and dorsal movement. During this movement the radular teeth open and close in a "grabbing" action and this, repeated several times, results in the rupture of the barnacle mantle. How the scuta and terga are prevented from being ingested is not known, but ciliary currents on the dorid lips may be involved. Once the barnacle is opened the soft contents are ingested rapidly by the combined activity of the odontophore and the buccal pump described below.

ANATOMY OF THE BUCCAL APPARATUS

The mouth opens into a horizontally elongated tube about 0.8 mm long, which passes obliquely into the body cavity in a dorsoposterior direction (Figs 3,4, 8, 9, 11, 12,). It has a pronounced ventral furrow and greatly folded walls. The epithelium is not ciliated. The subepithelial layers contain unicellular glands (Fig. 4) discharging into the lumen. The rube is surrounded by a thick sheath of tissue containing oblique muscle fibres which, posteriorly, join the outer buccal membrane. The dilators of the oral tube insert on its oral edge (see below) while the inner boundary is marked by the inner lips (Figs 1, 3, 4, 9) (Alder & Hancock, 1855). These form a circular ring, bulkier ventrolaterally. Their edges extend anteriorly into the posterior portion of the oral tube in a relaxed animal, so that a transverse section through this region gives the appearance of a double wall. They contain a diffuse layer of circular muscle acting like a sphincter, blocking off the oral tube from the remainder of the tract. The epidermis is not ciliated and there are no gland cells.

Between the inner and buccal lips lies a small, thin-walled chamber- the buccal vestibule (Figs 3, 4, 9, 10). The buccal lips lie at the entrance to the buccal cavity and form a large cushion of tissue consisting of a strong band of circular muscle and loose connective tissue underlying a cuticularized epithelium. Their walls have a pair of ventrolateral and a pair of dorsolateral folds which continue posteriorly into the buccal cavity. The cuticle is thicker ventrally and forms a thickened ridge in the ventral midline, composed of a pair of longitudinal bars on either side of a central piece. Its extreme anterior edge projects over the ventral edge of the buccal lips. The ventral thickening merges with the rest of the buccai cuticle at the level of the odontophore.


Lying ventrally in the buccal cavity is the odontophore. Its supporting structure is a cushion of tissue, triangular in outline, resting on a broad base and tapering dorsoanteriorly. Its long axis is directed anteriorly at an angle of about 30" to that of the buccal mass. It is composed almost entirely of muscle fibres and lacks the collagenous layer of Helix and Arion (Crampton, 1973). Its homology with the prosobranch cartilage is doubtful, but the term odontophoral cartilage will still be applied here. The cartilage is of uniform thickness,

FIG. 3. Onchidoris: Sagittal section of the head. The buccal pump has been dorsally displaced, details of muscles, membrane nerves and arteries are omitted.

but its dorsal portions curve posteriorly to form a depression (Fig. 5(a)) housing the radula. The radula is about 2.5 mm long and uniformly 1 mm wide. The formula is 30x 2.1.2. The rachidian tooth is represented by a degenerate portion of basal plate and a small, posteriorly direct hook.

Anteriorly the subradular membrane is closely attached to the surface of the cartilage by the radular tensor muscles (see below). The buccal epithelium anterior to the radula is so closely applied to the anterior face of the cartilage as to prohibit independent movement over its surface. This contrasts with the condition found in most prosobranchs and pulmonates. The posterodorsal and dorsolateral walls of the buccal cavity are richly ciliated, the currents passing to the oesophagus. A pair of longitudinal folds passing into the oesophagus from the opening of the pedicel demarcate the dorsal food channel,

ss S I X O a I H 3 N O J O A N O L V N V 1V33n8

56 D. M . CRAMPTON

continued anteriorly to the buccal lips as a shallow gutter. The salivary duct opens posteriorly on the lateral buccal wall. Each is short and broad and their glands cover most of the posterior, ventral walls of the buccal mass (Figs 3, 6-10).

The oesophagus opens dorsally and posteriorly from the buccal cavity. Beneath its opening a posteriorly directed pouch, the floor of which is formed by the distal end of the

( 0 ) cort i loge l ip ( b ) I

lo te ro l , rodulor tensor cor t i loge

depressor

loterol odontopherol @wm protroctor &

anterior rodulor tensor

cortilooe o c 31 I I

too th

FIG. 5. O/zckidoris. (a) Odontophoral cartilage-posterior view. (b) Odontophoral cartilage-anterior view. (c) section of radula-dorsal view.

radular sac, is the equivalent of the pulmonate oesophageal pouch and the radular diverti- culum of prosobranchs (Graham, 1973). The oesophageal wall is folded and contains circular and longitudinal musculature although this is greatly reduced in comparison with the pulmonates. Around the oesophagus and expanding over the dorsal and dorsolateral posterior portions of the buccal mass is the oesophageal gland (Figs 4,6,8).

The most conspicuous structure associated with the buccal mass is the buccal pump

pr) 0 N

7 V 0

I I \

I - 0 u t :P 2F /

/

\

E E -

C 0

0, C 0 GI

._ -

per

iph

eral

mus

cle

of t

he

pum

p ou

ter

bucc

al m

embr

ane

late

ral

of t

he b

u

vent

rola

tera

l of

the

bu

ccal

r

FIG

. 7. O

nchi

dori

s. D

orsa

l dis

sect

ion

of th

e he

ad to

show

the

extr

insi

c bu

ccal

mus

cles

. The

bod

y ca

vity

has

bee

n op

ened

by

a m

edia

n do

rsal

long

itudi

nal

inci

sion

. The

repr

oduc

tive

syst

em, n

erve

rin

g an

d m

ajor

mem

bran

es h

ave

been

rem

oved

.

BUCCAL ANATOMY O F O N C H I D O R I S 59

(Fig. 6), termed the gizzard by Hancock & Embleton (1852), a rounded structure attached by a short stalk to the median, dorsal wall of the buccal cavity. The pump is about 1.5 mm in diameter and the pedicel 0.5 mm in length in a mature animal. The buccal pump always lies on the left side of the buccal mass, orientated so that the peripheral muscle band lies in a plane at right angles to the long axis of the buccal mass. The epithelium of the pump is strongly cuticularized (Fig. 4), the cuticular layer being about 1.7 pm thick. The underlying epithelium is columnar and the walls are made up of muscle blocks described below. The fibres of the deep radial muscles attach to an apparently collagenous layer (staining dark blue with Mallory’s stain) which lies beneath the epithelium. The pedicel opens into the buccal cavity through a slit-like aperture elongated in an anteroposterior direction.

MUSCULATURE OF THE BUCCAL APPARATUS

The anterior part of the gut is surrounded by a complex system of muscles : (a) extrinsic muscles linking the buccal apparatus to the body wall; (b) intrinsic muscles linking one area to another; (c) intrinsic muscles, limited to the walls of the buccal cavity and pump, the buccal

vestibule and oral tube.

Extrinsic rn uscles The extrinsic muscles lie within the outer buccal and cephalic membranes and form a

dense mass. There are three main sets.

1. Buccal retractors (Figs 6-9, 12, 14-17) Origin : lateral body wall posterior to the buccal mass. Insertion : the ring muscle anterior to the salivary gland on the posteroventral region of

the buccal mass. There are frequent muscular connections with the lateral and ventrolateral retractors of the buccal lip near its origin. Contraction of the retractors draws the posterior portion of the buccal mass backwards into the cephalic haemocoel at the end of the feeding cycle.

2. Retractors of the buccal lips. (Figs 6-9, 12, 14-17) Origin :

Insertion : These are three pairs of strong muscles all greatly divided at their origins which flare at their insertions piercing the inner buccal membrane near to their area of attachment on the lips. Upon contraction, the muscles draw the buccal lips posteriorly away from the outer lips. Their interconnections with the buccal retractors indicate that simultaneous contraction of both muscles would exert a strong pull on the whole buccal mass.

3. Dilutors o f the oral tube (Figs 7-9, 12, 14, 15, 17) Origin :

Insertion:

dorsolateral, lateral and ventrolateral body wall near the posterior region of the buccal mass. anterior dorsolateral, lateral and ventrolateral portions of the buccal lip.

dorsolateral, lateral and ventrolateral body wall opposite the posterior edge of the oral tube. the posterior region of the oral tube on all but the median dorsal and ventral regions.


FIG. 8. Onchidoris. Lateral view of the buccal apparatus. The buccal membranes have been cleared anteriorly and the buccal pump displaced dorsally. All extrinsic muscles have been cut at their insertions.

These comprise bands radiating from the oral tube to the body wall. The outer buccal membrane links the individual bands and forms a muscular sheath closely investing the oral tube and buccal vestibule. Contraction dilates the oral tube and, because of the proximity of the inner lips to the oral tube, also helps to part these. Their insertion is mainly lateral, but because the dorsal and ventral areas of the oral tube are held firmly in position by extensions of the outer buccal membrane passing from the body wall, this is prevented from flattening.

Intrinsic muscles Iiiiking different areas of the buccal apparatus These pass from the oral tube to the buccal mass. There are usually three well defined

sets, one pair dorsolateral and two ventrolateral pairs.

4. Buccal protractors Origin:

Insertion :

the dorsolateral and ventrolateral regions o f the proximal edge of the inner lips. the dorsolateral and ventrolateral portions of the ring muscle.


These muscles may be divided into one dorsal pair, the dorsolateral buccal protractors (Fig. 8), and one or two ventral pairs-the ventrolateral buccal protractors (Figs 8, 9). These muscles pass between the dorsolateral and ventrolateral retractors of the buccal lip. Their combined contraction draws the posterior portion of the buccal mass anteriorly. Because of their attachment to the inner lips there is necessarily some lateroposterior pull on these which aids in dilating the aperture between them.

( a ) mouth

oblique muscle of

p r o t r a c t o r

radular sac

I

o e s o p h a g u s

FIG. 9(a)

62 D. M. CRAMPTON

' Y

FIG. 9(b) FIG. 9. Ouchidoris. Progressiveventral dissectionof the buccal mass. (a). All buccal membranes havebeenremoved

and the oral tube has been cut around the base of the outer lips. The extrinsic muscles have been cut at their insertions and the radular sac is turned ventrally. (b) The ventral odontophoral protractors have been removed and the buccal sphincter cleared in the ventral midline exposing the buccal epithelium.

FIG

. 10.

Oiw

hido

vis.

Prog

ress

ive

vent

ral

diss

ectio

n of

the

buc

cal

mas

s (c

ontin

ued

from

Fig

. 9)

. (a)

The

buc

cal

wal

l has

bee

n cu

t ope

n m

idve

ntra

lly a

nd

the

bucc

al e

pith

eliu

m re

mov

ed o

n th

e le

ft si

de t

o ex

pose

the

late

ral

odon

toph

oral

pro

trac

tor.

(b)

The

who

le o

f th

e ve

ntra

l bu

ccal

wal

l ha

s be

en r

emov

ed,

expo

sing

the

car

tilag

e w

hich

has

bee

n cu

t in

half

long

itudi

nally

. The

left

late

ral o

dont

opho

ral p

rotr

acto

r ha

s be

en c

ut to

expo

se th

e sa

livar

y du

ct.

oI


5. Interbuccal tensors (Fig. 9(b)) Origin : Insertion :

These are fine strands around the inner and buccal lips closely applied to the walls of the buccal vestibule. They aid in approximating the lips and strengthen the wall of the vestibule.

anterior edge of the buccal lips. posterior edge of the inner lips

Intrinsic muscles of the buccal mass 6 . Buccal sphincter (Figs 4, 8-9, 11)

This forms a thick layer of muscle encircling the buccal cavity internal to the buccal protractor muscles and extending from the level of the buccal lips to an area behind the

ora l 'tube

tensor

FIG. 11. Onchidais. Lateral dissection of the buccal mass. The extrinsic muscles and part of the buccal sphincter have been renoved and the oral tube is stretched anteriorly. The buccal epithelium has been cut away around the right buccal pouch to show the odontophore and oesophageal pouch.

pedicel. Ventrally, it passes internal to the ventral odontophoral protractor muscles (No. 10). The continuity of the muscle is broken by the junction of pedicel and buccal cavity and here it inserts on the base of the pedicel.

Contraction of the sphincter constricts the buccal cavity and helps to push the odontophore backwards to its resting position at the end of the feeding cycle. The insertion of the muscle on the pedicel means that the entrance to the pedicel is dilated when the buccal sphincter contracts.


7. Ring muscle (Figs 9, 11, 14) This is probably a modified portion of the buccal sphincter. It lies around the posterior

edge of the buccal sphincter and follows a parallel course except ventrally where it passes external to the ventral odontophoral protractor muscle and attaches to the ventral edge of the cartilage. Midventrally it passes posterior to the entrance of the probuccal artery into the odontophoral sinus. The ring muscle appears to act like a tensor, forming a firm area of attachment for the buccal protractors, retractors and the posterior buccal tensor muscles.

8. Posterior buccal tensors (Figs 9, 11). Origin : Insertion : ring muscle.

These are a pair of thin sheets, each passing dorsally from its origin and curving around the posterior, ventral area of the buccal mass. Each then turns anterodorsally passing to

the posteroventral edge of the cartilage.

FIG. 13. Oilchidoris. Ventral view of the buccal mass to show arterial supply.

the salivary duct and inserts on the ring muscle along a line extending from the dorsal edge of the salivary duct to the lateral midpoint of the oesophagus. That part of the muscle lying towards the midline fuses with its partner of the other side and with the radular sheath. The muscle forms a continuous sheet across the posterior region of the buccal


mass extending from the distal portion of the radular sac dorsally to the base of the oesophagus, forming a sling around the whole of the posterior region of the buccal mass and strengthening this area when odontophoral movements occur. Its contraction draws the radular sac and oesophagus anteriorly into the buccal cavity. The buccal ganglia lie external to this.

9. Dorsolateral buccal tensor (Fig. 11) Origin : Insertion:

dorsal midline of the buccal mass posterior to the pedicel. the buccal epithelium and the internal fibres of the buccal sphincter on the lateral surface of the buccal wall.

This muscle is probably paired, but appears continuous about the median, dorsal region of the buccal mass. It helps to draw the posterior region of the buccal mass anteriorly during odontophoral protraction.

FIG. 14. Onchidoris. Lateral view of the buccal mass showing nerve supply. GOGI, 2: gastro-oesophageal nerves; C1-C3 : cerebral nerves.

10. Ventral odontophoral protractor (Figs 5(b), 8-9, 1 I , 15) Origin : ventral region of the buccal lips. Insertion : ventral, posterior edge of the cartilage.

These bulky muscles are broader at their insertion than their origin. They appear as a single unit near their point of insertion when the two halves separate to pass around the base of the probuccal artery. Contraction draws the cartilage anteriorly towards the buccal lips during the early stages of the feeding cycle. Attachment of the muscle to the buccal lips means that the ventral portion of the lip is drawn ventrally and posteriorly, therefore enlarging the entrance to the buccal cavity.

68 D . M . C R A M P T O N

11. Lateral odontophoral protractors (Figs 5, 11) Origin : Insertion:

These are a pair of flattened thick sheets which pass around the buccal cavity to their insertion. Although the greater part of the muscle lies internal to the buccal sphincter and abuts directly upon the buccal epithelium, some fibres are external to it. Its contraction lifts the cartilage and draws the odontophore anteriorly towards the buccal lips. Its action partly counteracts the activity of the ventral odontophoral protractor for, although both muscles effect an anterior pull on the cartilage, the ventral odontophoral protractor lifts

dorsolateral and lateral anterior edges of the buccal lips. lateral edges of the posterior half of the cartilage.

FIG. 15. Oizchidoris. Sagittal section of the head at the start of the feeding cycle. (In Figs 15-17 the buccal pump is not drawn and arrows indicate direction of blood flow.)

the cartilage lip whereas the anterodorsal pull on the lateral edges of the cartilage made by the lateral odontophoral protractors depresses it. The origin of the muscles on the buccal lips helps to dilate the entrance of the buccal cavity by exerting a posterolateral pull which complements the action of the ventral odontophoral protractors.

12. Radular retractors (Figs 4,5(a), 9, 11) Origin : posteroventral edge of the cartilage. Insertion : lateral surface of the subradular epithelium along a line reaching to the dorsal

third of the long axis of the cartilage.


The orientation of each muscle is such that those fibres which originate towards the ventrolateral edge of the cartilage insert the most dorsally on the subradular epithelium. For the greater part of their length the muscles lie within the concavity of the cartilage. The radular retractors are strong, thick muscles forming the posteroventral bulge of the buccal mass. Their contraction draws the radula posteriorly into the concavity of the cartilage and, simultaneously, causes it to close.

FIG. 16. Onchidoris. Sagittal section of the head during the effective phase of the feeding cycle.

13. Lateral radular tensors (Fig. 5(a)) Origin : Insertion :

dorsolateral area of the dorsal face of the cartilage. lateral surface of the subradular epithelium immediately opposite their insertion.

These are fine strands with a line of insertion extending from the radular retractor muscle to a point immediately behind the dorsal lip of the cartilage. The muscles keep this area of the radula pressed against the underlying cartilage.

14. Anterior radular tensor (Fig. 5(b)). Origin : Insertion :

dorsolateral edge of the ventral face of the cartilage. the subradular epithelium lying immediately over the point of origin.

These are a pair of thin bands closely associated with the cartilage depressors and

70 D. M . CRAMPTON

contracting with them. Like the lateral radular tensors, they keep this area of the radula appressed firmly against the anterior, dorsal region of the cartilage and also partially draw the free anterior edge of the subradular epithelium over the cartilage lip.

FIG. 17. Onchidoris. Sagittal section of the head at the start of odontophoral retraction.

Intrinsic muscles of the cartilage The odontophoral cartilage is a highly muscular structure and four sets of intrinsic

muscles can alter its shape, and so that of the radula.

15. Cartilage depressors (Figs 4, 5(b)) These are thin bands running from the posterior to the anterior edge of the ventral face

of the cartilage. Upon contraction they exert an anteroposterior pull on the ventral face of the cartilage and, since its lip is thinner than the remainder, this results in a ventropos- terior movement of the lip. Because the radula is closely applied to the dorsal surface of the cartilage through the activity of the radular tensors, the radula is drawn in a similar direction, resulting in a flattening of the subradular epithelium and a consequent erection of the teeth.

16. Ventral divaricator (Figs 4, 5(b), 9(b), lO(a)) This is a band of muscle passing around the posterior third of the ventral face of the

cartilage. It is attached to the lateral edges of the cartilage on either side and lies external

BUCCAL ANATOMY O F O N C H I D O R I S 71

to the cartilage depressors. The more superficial fibres are continuous with those of the lateral odontophoral protractor. Its contraction draws the lateral portions of the cartilage ventrally, flattening the dorsal face and stretching the radular ribbon laterally to open the teeth.

17. The cartilage approximator (Figs 4, 5(a)) This lies on the dorsal face of the cartilage and consists of fibres stretching between its

lateral margins. The fibres cover the cartilage as far forward as the lip, but are better developed posteriorly. They restore the cartilage shape and help to collapse the radula when deformation ceases. The muscle shows some continuity of its fibres with those of the radular retractor.

18. Intercartilage tensor (Fig. 4)

confer resilience when the cartilage is deformed by the odontophoral muscles. These fibres run through the substance of the cartilage from ventral to dorsal face. They

Buccal pump musculature There are three major systems responsible for efficient pumping.

19. Deep radial muscles of the pump (Fig. 4) The greater part of the pump wall consists of muscle fibres which run from the internal

to the external surface, orientated radially in respect of the lumen. None occur in the area of the peripheral muscle.

20. The peripheral muscle of the pump (Figs 3 , 4 , 7, 8, 11) This is a thick band of muscle which arises on the posterior, dorsal surface of the buccal

wall, passes around the pump and along the pedicel and then extends along the dorsal midline of the buccal mass to the dorsal area of the buccal lip. Its area of attachment to the buccal wall affords a strong anchor during contraction. Contraction of the peripheral muscle results in a bulging of the lateral walls of the pump, which in turn increases the volume and thus constitutes the “inhalant” phase.

21. Superficial radial muscle of the pump (Figs 4, 8 , 11 ) Like the peripheral muscles, the superficial radials are visible on the external surface of

the pump. The fibres lie between bundles of the deep radial musculature. For the most part they show a radial arrangement extending to the peripheral muscle band from the central point of the lateral pump walls. This arrangement is especially evident in the median area of the pump; in the pedicel the muscle strands adopt a more lateral course. Contraction of the superficial radial muscles results in a narrowing of the lateral walls of the pump, an action which antagonises that of the peripheral muscle.

Intrinsic muscles of the anterior portions of the buccal apparatus 22. Constrictor of the buccal lips (Figs 10(a), 11)

This is a thick, diffuse band of muscle encircling the buccal lips. Its contraction constricts the aperture to the buccal cavity and antagonises those muscles which retract the lips, the ventral and lateral odontophoral protractors.


23. Consfricfor of flie inner lip (Figs 9, 10, 11) This is a similar, but less bulky sphincter surrounding the anterior edge of the buccal

vestibule. Its contraction counteracts the activity of the buccal protractors, helping to occlude the entrance to the buccal vestibule and to push the buccal lips posteriorly during the final stages of the feeding cycle.

24. Oblique muscle of the oral tube (Fig. 9) The muscle fibres encompassing the oral tube are anterior extensions of the dilators of

the oral tube and are bound firmly within the outer buccal membrane closely affixed to the tube walls. The oblique muscle fibres pass around the tube obliquely; they confer some rigidity upon the walls of the tube for the efficient action of the dilators of the oral tube.

25. Labial retractors These consist of fine muscle fibres within the body wall which extend through the tissue

of the outer lips to insert upon their distal edges. Contraction of these fibres helps to open the mouth.

BLOOD SUPPLY OF THE ANTERIOR REGION OF THE BODY

The buccal apparatus is surrounded by a complex series of membranes which demarcate haemocoels. From the anterior dorsal and dorsolateral portions of the nerve ring, part of the heavily perforated cephalic membrane extends over the blood gland, encloses this, and passes to the dorsal body wall anterior to the rhinophores (Fig. 2). Laterally and ventrally, the cephalic membrane radiates from the ganglia to the body wall circumferentially behind the anterior border of the foot. The space thus enclosed is the cephalic haemocoel (Fig. 2(b)) containing the buccal apparatus. From the posterior edge of the oral tube the thick outer buccal membrane (Fig. 2(a)) radiates peripherally. This connects sections of the dilators of the oral tube and passes to the body wall. The dorsal and ventral portions of the outer buccal membrane pass to the body wall as thick elastic sheets marking the anterior boundary of the cephalic haemocoel and delimiting a space lying between the oral tube and the anterior body wall: the oral haemocoel (Fig. 2(a)).

The buccal apparatus is enclosed in the buccal haemocoel (Fig. 2(b)) formed by the inner buccal membrane originating on the posterior edge of the oral tube and inner lips and passing to the nerve ring. The membrane is intimately connected with the buccal walls, the radular sac and the posterior glandular areas. Anterodorsally the membrane evaginates to surround the buccal pump on the left side. Both buccal membranes are perforated with ostia ranging in size from 20 to 100 pm allowing intermixing of blood between cephalic and buccal haemocoels.

Arterial blood reaches the buccal apparatus through the cephalic artery (Fig. 12,) which arises from the anterior aorta. It plunges ventrally towards the nerve ring passing to the right of the midline and turns medially towards the lateral surface of the buccal mass (Fig. 12). The blood supply to the buccal apparatus is a much more open system than that of pulmonates and has no capillaries. The supply comes from two main sources, the probuccal artery (Figs 12, 13) and the anterior buccal artery, both arising from the cephalic artery at the origin of the right pedal artery (Fig. 12). The anterior buccal artery is a


large vessel which passes dorsally across the buccal mass, anterior to the salivary gland and within the tissue of the inner buccal membrane. At the level of the insertion of the buccal retractor muscle, it divides into two; the posterior branch is the posterolateral buccal artery. This passes dorsoposteriorly and divides into two branches which pass to the surface of the buccal mass. The ventral one goes to the salivary gland, while the dorsal branch supplies the oesophageal wall. Both divide greatly and some of the larger vessels curve around the posterior region of the buccal mass discharging blood into that region of the buccal haemocoel containing the buccal and gastro-oesophageal ganglia.

The anterior portion of the artery passes dorsoanteriorly within the inner buccal membrane and, at the level of the median point of the buccal cavity, a branch passes back over the lateral surface of the buccal mass. This is the lateral buccal artery, closely applied to the internal surface of the inner buccal membrane, and branching to cover nearly the whole lateral surface of the buccal mass. The finer branches discharge into the buccal haemocoel related to the muscles in this region, especially the dorsolateral and ventrolateral buccal protractors.

The main part of the artery continues over the dorsolateral surface of the buccal apparatus and produces a further branch which passes anteriorly towards the oral tube. Once it reaches the buccal vestibule, the artery divides into two branches which pass in opposite directions around its circumference, from which anteriorly directed branches pass into the glandular area of the oral tube and to the wall of the vestibule.

At the dorsolateral surface of the buccal mass, a buccal pump artery leaves the main arterial stem in a posterior direction, closely applied to the internal surface of the buccal membrane, branching to the underlying areas of the pump. The vessels do not enter the pump wall but open into the space between that and the outer buccal membrane. The anterolateral buccal artery arises at the same point as the buccal pump artery, runs along the dorsolateral surface of the oral tube (sometimes sending branches to the wall) and passes to the oral veil and outer lips.

The probuccal artery passes from the aorta to the posterior ventral midpoint of the buccal mass (Fig. 13) applied to the internal surface of the inner buccal membrane. At that point the artery opens into the buccal mass through an elliptical aperture about 100 pm long. From t h s point blood flows into three systems, the radular odontophoral, and buccal sinuses (Fig. 13). Surrounding the aperture, internal to the dorsal wall of the probuccal artery, a sheet of connective tissue is attached laterally to the cartilage on either side. It is continued anteriorly as a longitudinal strip (median strip) along the midventral surface of the buccal epithelium, to which it is closely connected, as far as the buccal lips (Fig. 9(b)). Posteriorly it expands into a triangular sheet attached ventrally and laterally to the subradular epithelium at the point where the radular sac joins the buccal mass. This is the radular septum (Figs 9(b), 13). Blood leaving the probuccal artery can therefore flow anteriorly along the median strip, posteriorly along the external surface of the radular septum or medially through the aperture into the buccal mass. Blood flow between the radular and buccal sinuses is reduced because the lateral portions of the sheet form a partial barrier. Blood passing posteriorly enters the radular sinus (Figs 2, 13.) which lies between the radular epithelium and the radular sheath. The anterior region of the radular sinus is delimited by the two radular retractor muscles. Blood therefore flows freely around the entire radular sac. The blood which is directed anteriorly along the median strip enters the buccal sinus, an extensive space lying between the buccal epithelium and the

14 D. M. CRAMPTON

intrinsic muscles of the buccal mass although the muscle layers themselves act as continua- tions of this sinus since blood has freedom of movement between individual muscle bundles, The blood which passes through the aperture in the connective tissue sheet enters the odontophoral sinus (Figs 4, 13) between the posterior face of the cartilage and the subradular epithelium and continued posteriorly amongst fibres of the radular retractor muscle. The buccal and odontophoral sinuses communicate to some extent as blood can flow through the lateral odontophoral protractor muscle and through the ventral portions of the cartilage in the region of the ventral edges of the ventral divaricator and cartilage approximator muscles.

MOVEMENT OF BLOOD THROUGH THE BUCCAL APPARATUS

The buccal muscles are supplied by means of sinus systems, two of which are important. The first lies around the external wall of the buccal mass and is distinct from the inner buccal sinuses which lie within the buccal mass.

Blood enters the first system through the anterior buccal artery and reaches the glandular areas of the posterior region and the lateral wall of the buccal mass before the buccal pump and oral tube. It lies between the walls of the buccal apparatus and the inner buccal membrane and eventually percolates through the ostia in the membrane into the cephalic haemocoel. Blood accumulates at the posterior region of the buccal mass around the salivary and oesophageal glands and the buccal ganglia. Since both sides of the buccal mass receive blood simultaneously the blood in the probuccal artery must be diverted around the aperture.

Blood leaving the probuccal artery enters the odontophoral and radular sinuses almost simultaneously, while the buccal sinus is filled a little later. Blood from the radular sinus passes through spaces in the radular sheath into the buccal haemocoel (Fig. 2), where it joins that from the anterior buccal artery. Blood in the odontophoral sinus either filters posteriorly into the radular sinus through the radular retractor muscle or anteriorly into the buccal sinus mainly through the lateral odontophoral protractor muscle. Blood flow within the buccal sinus is slow and dye must be injected under pressure before it passes through the wall of the buccal mass into the buccal haemocoel. The main areas for escape are the ventral and lateral walls. Blood probably leaves more rapidly when the buccal mass is active since contraction of various muscles blocks exerts pressure upon the sinus.

Although the aperture in the probuccal artery lacks the specialization of the similarly placed valve in pulmonates (Schmidt, 1916) it can be widened and occluded to some extent by movements of the odontophore. It is opened maximally when the cartilage is pulled anteriorly and its anterior face flattened, as occurs during protraction of the odontophore and contraction of the lateral and ventral odontophoral protractor muscles. The entrance is narrowed when these muscles relax and when the cartilage becomes concave (as in contraction of the cartilage approximator muscle).

The effect of varying aperture on the rate of flow into the odontophoral sinus is probably small but permits some re-direction of blood during odontophoral movements. When the aperture is smaller, more blood is diverted into the radular and buccal sinuses than when the odontophore is in its resting position.

The considerable mixing of blood between the two systems suggests that the method of vascularization is inferior to that of pulmonates and the separation between arterial and

B U C C A L A N A T O M Y O F O N C H I D O R I S 1 5

venous blood is less complete in Onchidoris. However, the small size of the buccal mass in the nudibranch probably makes an extensive capillary system unnecessary and since all buccal muscles are bathed in blood in the buccal haemocoel they probably receive an adequate supply. In addition, the rapid accumulation of blood in the buccal and cephalic haemocoels which is brought about by the lack of a capillary system is an important factor in the protraction of the buccal apparatus.

INNERVATION OF THE BUCCAL APPARATUS

Cerebral nerves The intrinsic muscles of the buccal mass, inner lips, buccal vestibule, oral tube and

outer lips are supplied by nerves from the cerebral ganglia (Figs 12, 14).

Buccal nerves The buccal ganglia are white, ovoid structures each about 400 pm long and 350 pm

across their greatest width joined to each other by a short, thick commissure and to the cerebral ganglia by the right and left cerebrobuccal connectives. The ganglia and commissure lie beneath the oesophageal gland. From the dorsolateral surface of each ganglion aconnective about 50 pm long passes to the gastro-oesophageal ganglion on each side. The gastro-oesophageal ganglia are white and spherical almost 200 pm in diameter.

The arrangement and areas of supply buccal nerves are as follows : 1. Dorsal buccal nerve-to the anterior, dorsolateral oesophagus and oesophageal gland and the ciliated region of the posterior dorsal and dorsolateral buccal epithelium. 2. Inner IaferaI buccal nerve-to the dorsal food channel and epithelium around the base of the pedicel and to the anterior region of the buccal cavity and lips. 3. Outer lateral buccal nerve-to the ring muscle, buccal sphincter, pedicel and muscles of the buccal pump. 4. Ventral buccal nerve-to the dorsolateral and ventrolateral buccal protractors, radular retractors, ring muscle, ventral odontophoral protractor and muscles of the cartilage. 5. Posterior buccal nerve-to the posterior buccal tensor (often), supra- and subradular epithelia within the radular sac. It also supplies part of the radular retractor muscle and salivary gland. Two nerves arise from each gastro-oesophageal ganglion, the gastric and the anterior

oesophageal. The oesophageal nerve arises ventrally from the ganglion and is smaller than the gastric nerve. It curves around the ventral regions of the oesophagus and divides several times over the ventral and ventrolateral surface supplying the anterior oesophageal wall and oesophageal gland. The gastric nerve passes along the lateral surface of the oesophagus posteriorly to the remainder of the gut. Small side branches supply the remainder of the anterior oesophagus anterior to the nerve ring.

THE FEEDING CYCLE

Protraction of the buccal apparatus appears to be largely passive. The complex arrangement of membranes around the buccal apparatus and their elastic nature allow for the


isolation of pockets of blood and varying pressures of haemolymph. For efficient protraction blood must accumulate within these sinuses to exert a forward pressure on the buccal mass providing that the body wall is immobilized. The way in which this occurs is specula- tive.

When the animal is feeding the dorsal surface of the body is convex and the foot less extended than during crawling. This indicates that the longitudinal muscles in body wall and foot are contracted, so as to shorten the long axis. The consequent dorsal displace- ment of the viscera means a corresponding dsplacement of haemolymph and an increased pressure within the sinuses. The nature of the membranes may also be important in increasing blood pressure within the head. The cephalic membrane, especially, has muscle fibres running within its matrix. A reduction in its area would reduce the volume of the sinus and displace fluid anteriorly. By one or both of these methods the pressure within the anterior sinuses probably reaches a level high enough to allow buccal protraction to occur.

For clarity I have divided the feeding cycle into four stages : (a) opening of the mouth and protraction of the odontophore; (b) piercing phase of the radula ; (c) retraction of the odontophore and closing of the mouth; (d) operation of the buccal pump.

These are not separate; the phases are continuous and overlap to some extent.

(a) Opening of the mouth mid protraction of the odontophore (Figs 1, 15) At the beginning of this phase the mouth lies over the operculum of the barnacle, the

oral veil presses tightly around the base of the test and surrounding rock. Shortly after this the dilators of the oral tube contract, resulting in its lumen enlarging. Because of the shortening of the oral tube which accompanies this the outer lips are pulled posteriorly. Simultaneously, the labial retractors retract them.

These activities enlarge the mouth. The oral tube is prevented from becoming dorso- ventrally flattened by the strong sheets of connective tissue which tie its dorsal and ventral portions to the body wall. Once the tube has enlarged and is in a fixed position the ventrolateral and dorsolateral buccal protractors contract. They now have a firm origin because the inner lips are secured by the continued contraction of the dilators of the oral tube, and their contraction draws the posterior region of the buccal mass anteriorly towards the inner lips.

The buccal mass cannot move without affecting adjacent structures. The intimate con- nection of the nerve ring with the anterior region of the oesophagus means that this, too, moves anteriorly in relation to the head. Because the nerve ring marks the posterior boundary of both cephalic and inner buccal membranes these are also drawn anteriorly, increasing pressure of blood around the buccal mass (Fig. 15). The buccal protractors cannot draw the buccal mass further forwards than their origin; at their maximum contraction the odontophore is level with the inner lips. Meanwhile, the forward movement of the buccal mass and the rise in pressure everts the inner lips through the mouth, a movement which may be observed externally (Fig. 1). The inner lips are followed closely by the buccal lips and once protracted they evert (Fig. l(b)) to overlie the inner lips. Towards the end of their protraction the odontophore itself is protracted by the combined contraction of the ventral and lateral odontophoral protractor muscles. Both muscles


have their origin on the anterior edge of the buccal lips and once these have reached the mouth they continue to move forwards because of the pressure of blood and so form a firm origin. The resulting anterior pull on both ventral and lateral edges of the odontophore result in the whole structure moving forwards in a straight line. Contraction of the odontophoral protractors also shortens the long axis of the buccal cavity so that the odontophore comes to lie within the buccal lips. At this stage these lips have been separated, partly by eversion, and partly by the pull exerted by the odontophoral protractor muscles, so that the entrance to the buccal cavity is enlarged and can accommodate the odontophore.

The movement of the odontophore has other effects: the radular sac is drawn dorsally and anteriorly into the buccal cavity, taking with it the posterior buccal wall and the oesophageal entrance, a movement aided by contraction of the posterior and dorsolateral buccal tensor muscles. The latter also pulls the buccal walls lateroposteriorly and gives the odontophore greater freedom of movement. At the end of this first phase, the buccal apparatus is fully protracted with the odontophore lying inside the buccal lips.

(b) The piercing phase of the radula (Figs l(c), 16) Towards the end of phase (a) marking the start of phase (b) the cartilage divaricator

muscle contracts, flattening the cartilage laterally. Shortly after this the cartilage depressor muscle contracts to shorten the long axis of the cartilage and draw the lip ventrally. Both actions protract and stretch the radular membrane, the anterior and lateral radular tensors ensuring meanwhile that it is pressed closely against the edges of the cartilage. The radula is now stretched tightly over the dorsal surface of the cartilage and its tension is increased by the pressure of blood within the odontophoral sinus. This is high for the following reasons. It has already been noted that contraction of the cartilage divaricator muscle enlarges the entrance of the probuccal artery and blood flows into both odontophoral and radular sinuses. When the cartilage depressor muscle contracts, however, the radula is pulled anteriorly so that the radular sinus is reduced. Blood within it can flow either through the radular sheath into the cephalic haemocoel or backwards to the odontophoral sinus. The forward flow means that pressure in the odontophoral sinus is high enough to keep the subradular epithelium tensed in its median regions.

The anterior movement of the radula together with the stretching of the subradular epithelium results in the teeth changing from a closed to an open position. In this process each rotates so that the tip, which was originally facing the posterior region of the buccal cavity, now points laterally. The movement is brought about by the anterior edge of the cartilage bending ventrally: this can be regarded as the bending plane (Ankel, 1936). While the radula is being protracted the whole odontophore has been pushed even further outside the mouth and the radular teeth are now in contact with the barnacle. The effective phase of the feeding process consists of a rapid retraction of the radula so that the hook- like teeth are pulled inwards and pierce the mantle. As the radula withdraws further and the teeth rotate to their resting position, the mantle is torn. Successive strokes in different places ensure that the mantle is completely ruptured and the scuta and terga together with bits of mantle are discarded, probably with the help of the ciliary tracts on the oral veil, but perhaps also with the help of the buccal pump. The thick cuticle over the ventral edges of the buccal lips prevents abrasion of the underlying epithelium (Fig. 3).

78 D . M . C R A M P T O N

Radular retraction is brought about by the simultaneous relaxation of the cartilage depressor, divaricator and radular tensor muscles and by the contraction of the radular retractor and cartilage approximator muscles. Contraction of the cartilage approximator muscle causes the cartilage to resume its concave shape, the radula is no longer stretched and the ventral pull exerted by the radular retractor muscle causes the radula to resume its position within the cartilage cavity. This movement allows the radular teeth to close and they execute a rotation the reverse of that during opening. It is not known whether the radular teeth are opened and closed repeatedly during one protraction of the odontophore. There seems to be no reason why successive opening and closing movements could not take place when the odontophore is protracted. Such activity is known to occur in Mono- donta (Nisbet, 1953) and Vivipnrus (Eigenbrodt, 1941) and is due to movements of the cartilage behind the radula. In Onchidoris the opening and closing of the radular teeth is also accomplished by cartilage movements and need not necessitate alteration in the position of other buccal structures. Workers investigating the feeding of related animals (Forrest, 1953 ; Morse, 1968) have not described radular activity.

(c) Retraction of the buccal apparatus and the closing of the mouth (Fig. 17) Retraction of the buccal apparatus follows the final retraction of the radula. This phase is not an exact reverse of protraction. Eversion of the odontophore has greatly altered the disposition of the various components of the buccal apparatus; the insertion of the buccal retractors now lies anterior to its position at rest and that of the retractors of the buccal lip lies anterior to, and internal to, that of the dilators of the oral tube. All these muscles have been stretched by protraction and so their contraction results in a rapid withdrawal of the whole buccal apparatus. The close interconnections of buccal and labial retractors at their origins indicates that maximum efficiency is obtained if both sets contract together. The interbuccal tensors ensure that the delicate wall of the buccal vestibule remains close to the buccal lip and is not ruptured by the backward pull of the latter.

The withdrawal of the odontophore from the mouth is followed rapidly by closure of all the lips. Contraction of the circular bands within the inner and buccal lips occurs as soon as the buccal apparatus has reached its resting place, and effectively closes the entrance to the buccal cavity and vestibule. The mouth probably closes passively because of the elas- ticity of the outer lip, but this is aided by relaxation of the labial retractors and the longitudinal muscle of the body wall. Contraction of the buccal sphincter occurs immediately after closure of the buccal lips and constricts the buccal cavity. Efficient contraction of the buccal sphincter can occur only when the odontophoral and buccal protractor muscles are relaxed during retraction of the buccal apparatus.

(d) The operation of the buccalpump Forrest (1953) and Morse (1968) referred to the operation of the buccal pump in Gonio-

doris and Acanthodoris as sucking. Forrest traced a series of evolutionary stages from a slight protuberance of the dorsal buccal wall in Palio nothus to the discrete organ present in Onchidoris and Adalariu, and correlated the degree of development with feeding habits. In Onchidoris this explanation may be too simple. Acunthodoris feeds on the bryozoan Flustrella hispida and Morse (1968) described how a hole is first rasped in the zooecium


and then the contents sucked out by the pump. In this mode of feeding an efficient sucking mechanism is desirable and one would expect a high degree of development of the pump, but the pump is not, in fact distinct from the buccal mass and has no pedicel. Onchidoris is equipped with a piercing and grabbing radula bearing strong teeth. If they can remove the scuta and terga of a barnacle they could, one would assume, equally well pull the barnacle into the buccal cavity leaving the hard test behind. Although a sucking mechanism would assist in this action it need not be so highly developed as it appears to be in an animal like Acanthodoris which depends entirely upon suction to draw prey into its mouth. However, the comparative degree of development of the buccal pump in the two animals appears to contradict this observation and is not, therefore, obviously linked with feeding habits.

The highly organized buccal pump of Onchidoris may have developed originally for feeding on animals other than barnacles-which seems unlikely-or it is correlated with some other process. Hancock & Embleton (1852) suggested that the primary function of the pump was trituration of food and perhaps also deglutition. The use of the organ for trituration is discounted by the fact that no food particles are found inside its cavity even in an animal killed while feeding, and also by a knowledge of the anatomy and method of contraction of the pump.

On the other hand, the anatomy of the buccal apparatus of Onchidoris seems adapted for swallowing. The oesophagus is a delicate structure with glandular walls, incapable of the peristalsis required to carry food away from the buccal cavity and commonly found in other gastropods. The food traverses the oesophagus rapidly and little food is present in it even when an animal is dissected immediately after feeding. A pumping action by some area in front of the oesophagus possibly accelerates the passage of food. The dorsal food channel, well developed in Onchidoris, leads directly from the pedicel to the oesophagus. Observation on dissected animals which displayed buccal activity showed that the action of the pump is always simultaneous with contraction of the buccal sphincter muscle. Since this contracts at the end of the visible feeding cycle the buccal pump is probably also most active at this stage. In addition, contraction of the sphincter widens the aperture of the pedicel and possibly augments the efficient operation of the pump. The degree of development of the pump may therefore be related not only to the ingestion of food, but also to the passage of food along the oesophagus. There is little doubt that the inhalant phase of the pump aids in drawing the soft parts of the barnacle into the buccal cavity. The fact that the buccal pump is in its exhalant phase during radular protraction suggests that the inhalant phase is linked with radular retraction when the aperture of the pedicel is close to the aperture of the test. The aperture at this stage is a slit elongated longitudinally by the anterior pull of the buccal wall. Contraction of the peripheral pump muscle tends to widen the aperture because the tension it creates is transferred along the anterior and posterior side of the pedicel and the dorsal wall of the buccal cavity. The result is a shortening of the longitudinal axis of the pedicel causing it to bulge laterally. This, together with an increase in internal volume of the pump, means that a strong negative pressure is produced within the buccal cavity, effecting a sucking action. During the exhalant phase an increase in pressure within the buccal cavity results in an outward force which could account for the rejection of the opercular valves of the barnacle.

During retraction of the odontophore and the buccal apparatus the buccal pump seems likely to aid swallowing. Contraction of the buccal sphincter muscle follows closure of the buccal lip and a constriction of the buccal lumen at this stage results in an increase in


pressure within the buccal cavity. The inhalant phase of the buccal pump occurs immediately before the contraction of the buccal sphincter muscle, but its exhalant phase is co- incidental with contraction of the latter. Because the buccal apparatus has now returned to its resting position the dorsal food channel (which was deformed during protraction of the posterior region of the buccal wall) has resumed its original position. Contraction of the buccal sphmcter opens the pedicel aperture to its greatest extent and simultaneously the superficial radial muscles of the pump contract to create a force directed both into the buccal cavity and posteriorly along the dorsal food channel. The increase in pressure within the buccal cavity caused by constriction of its lumen and the exhalant phase of the pump ensures that any food within it is directed rapidly into the oesophagus and so to the stomach.

DISCUSSION

A comparison of the buccal muscle systems of Onchidoris, Archidoris and Philine, in functional terms suggests a number of homologies (Table 1). The buccal retractors are similar in form and position in Archidoris (Rose, 1971) and Onchidoris, but in Philine (Hurst, 1963) their point of attachment is further forward on the buccal mass and they

TABLE I Table of comparison of the birccal tmrsciilatitre of Onchidoris bilamellata (present study), Archidoris psendoargas

(Rose, 1971a) atid Philine aperta (Hurst, 1963)

Function Oilchidoris Archidoris

(a) Extrinsic iiirtscles froin the body i v d l to the buccal t m s s Retracts buccal apparatus Buccal retractor Postero-lateral retractor

Retracts buccal lip Retractor of the buccal -

lip Dilates oral tube Dilators of the oral tube Oral dilator

Protracts buccal apparatus - -

(b) Extriiisic muscles litikiiig different regions of the biiccal apparatus Protracts buccal apparatus Dorsolateral buccal 7

protractor Ventrolateral buccal r Buccal protractor

- protractor j

Approximates buccal Interbuccal tensor and inner lips

(c) Ztitritisic inrrscles fiotti cartilage to birccrtl wall Protracts odontophore Ventral odontophoral

protractor - lateral odontophoral Inner buccal protractor protractor

Constricts the oesophagus - -

Philine -

Proboscis retractors prs. IV & V

Circum oral muscle. Proboscis retractors prs. I & VI. Proboscis retractor prs I, 11,111, VI

Ventral tensor

Posterior transverse muscle

B U C C A L A N A T O M Y O F O N C H I D O R I S

TABLE I-continued

81

Function Otichidoris Archidoris Philine ~~

(d) Intrinsic muscles from cartilage to si~bradirlar epitheliuni Retracts radula Radular retractor

Protracts radula Tenses radula

- Lateral radular tensor Anterior radular tensor

(e) Intrinsic muscles of the cartilage Protracts radula Cartilage depressors Spread radula Ventral divaricator

Re-curves radula Cartilage approximator Preserves the integrity Intracartilage tensors of the cartilage

(4) Intrinsic muscles of the buccal walls Constricts the buccal Buccal sphincter cavity Area for attachment of extrinsic muscles Preserving the integrity of buccal structures and aiding in odontophoral Dorsolateral buccal protraction tensor

Ring muscle

Posterior buccal tensor

Protraction of the radula Retracting the caecal fold Preserving the integrity of buccal structures

Constricts the oesophagus -

(9) Musculature of the buccal pump Constricts the buccal pump Dilates the buccal pump Support for the pump walls

Superficial radial muscles Peripheral pump muscle Deep radial musculature

Posterior radular Radular occlusor retractor Buccal tensor 3

- Outer oblique - -

- -

- - Anterior approximator Anterior transverse Median approximator muscle

Mentioned in the text - -

Fibres between st I and st 2

Outer buccal constrictor ?

Band muscle -

- Part of the superficial buccal musculature

Posterior buccal protractor Superficial dorsal protractor Radular sac protractor

- Radular elevator - Inner oblique - Buccal tensor 4 - Buccal tensor 1-4 - Median fibres of radular

occlusor - Intrinsic musculature

(h) Intrinsic mirscles of the remaiiider of the birccal apparatus Constricts the oral tube - ?

Constricts the buccal vesribule lip

Constrictor of the inner

Constrictor of the buccal lip

Maintaining the shape of Oblique muscle of the the oral tube oral tube Retracting the outer lip Labial retractors

Ventral circular muscle Intrinsic musculature of the oral tube Intrinsic musculature

Fibres in outer muscle coat

Columellar muscle

82 D. M . CRAMPTON

form part of a network of proboscis retractors which pull the extravert pack through the mouth. Buccal retractors similar to those of Onchidoris have been reported by Edmunds (1971) in Discodorisfiagilis (Alder & Hancock) and by Young (1969) in dorids which suck and rasp sponges. In Bullina roseana (Rudman, 1972a) there are four pairs which, as in Philine, are most effective when the buccal mass is protracted, but in Bullina they have an origin more anterior to their insertion. Retractors of the buccal lip are absent in Archidoris and Philine, although Rose's description suggests that the oral ddator muscles in the former resemble these more closely in form than they do the oral dilators of Onchidoris. The retractors of the buccal lip occur in other Doridacea including Dendrodoris (= Doriopsis) granulosa (Pease), Discodoris coerulescens Bergh, Platydoris scabra (Cuvier), Halgerda minor (Eliot) and Jorunna tomentosa (Cuvier), where they are called retractors (Edmunds, 1971).

The dilators of the oral tube found in Onchidoris have not been described in this form before. The equivalent muscles in Philine are proboscis retractors I and V and a number of strands of muscle (the circumoral muscles) linking the oral tube and outer lips. Extrinsic buccal protractors from the body wall are absent in Onchidoris and Archidoris but are represented in Philine by proboscis retractors I, 11, 111 and VI. These originate either laterally or anteriorly to their point of insertion and can act as retractors only when the buccal mass is everted. The buccal protractors in Onchidoris and Archidoris resemble one another and are not linked to the body wall. A similar series is present in Smaragdinella (Rudman, 1972b) but passes to the body wall at the side of the mouth; this is intermediate between the organization of Philine and Onchidoris. Gymnodoris (Young, 1969) has a set of muscles which closely resemble the buccal protractors of Onchidoris in having similar attachment points; Young calls them buccal retractors, and apparently they act as such when the odontophore is everted. However, as total eversion is not always necessary here, these muscles could also function as protractors. It is interesting to note that in those opisthobranchs where total eversion of the buccal apparatus occurs there are frequently muscles which act primarily as protractors and then become retractors (PR I in Philine; the extrinsic and intrinsic buccal retractors described by Young). Such muscles have also been described in some Stenoglossa where, instead of an extravert, a true proboscis is found (Burton, 1971).

Both Archidoris (Rose, 1971) and Onchidoris have muscles from cartilage to buccal wall assisting in the protraction of the odontophore. In Philine this function is served by the proboscis retractors already mentioned and the only muscle linking cartilage to body wall is the posterior transverse muscle which will be discussed later. Ventral odontophoral protractors, the bulkiest muscles in the buccal mass in Onchidoris, are not present in Archidoris. They are, however, represented in the longitudinal buccal musculature of Dendrodoris, Chromodoris and Gjimnodoris (Young, 1969) where they also cover the lateral buccal walls. Longitudinal muscles of this kind also occur in cephalaspids like Cylichna (Lemche, 1956). The lateral odontophoral protractor is similar in form to the inner buccal constrictor of Archidoris and serves the same function.

Muscles which retract the radula are identical throughout the Dorididae, but are more powerful in Archidoris because of the bulkier cartilage and wider radula. In Philine the radular occlusor muscle performs a comparable function and passes from the cartilage to the subradular epithelium, but inserts more medially than in Onchidoris. Lemche (1956) described two muscles in Cj~lichna, one like the radular retractor of Onchidoris (musculus


retractor radulae marginalis) and the other resembling the radular occlusor of PhiIine (musculus radulae medialis).

The fusion of the subradular epithelium with the cartilage in both Archidoris and Onchidoris means that the radula cannot be protracted independently of the cartilage and there must be a new means of opening the radula. This is achieved in Onchidoris by muscles fused with the ventral face of the cartilage (the cartilage depressors). These appear to be absent in Archidoris although Young (1969) described a radular protractor. However, his figure shows that the muscle is small and closely applied to the cartilage at its insertion. It is not difficult to imagine a muscle like this becoming increasingly more connected with the cartilage to produce the condition found in Onchidoris. Opening of the radular teeth in Philine occurs by the opposing forces of two muscles, the outer oblique (which exerts an anterior pull on the radula) and the inner oblique (which pulls the radula posteriorly). Only the outer oblique, however, originates on the cartilage. The radular tensor muscles of Onchidoris have not been described in other dorids and are a particular modification associated with the mode of operation of the odontophore.

Muscles passing around the anterior face of the cartilage are common in all dorids with more than one cartilage (Young, 1969) and are represented in Onchidoris by the ventral divaricator. In Archidoris a similar muscle is composed of an anterior and a posterior block, the former unknown except in this mollusc (Rose, 1971). The comparable muscle in Philine is the anterior transverse which is important in increasing the blood pressure beneath the radula and also acts as a pivot over which the odontophore turns. A muscle similar to the cartilage approximator in Onchidoris is described in Young’s account (1969) as the posterior transverse odontophoral muscle, and this is present in PhiIine (the posterior transverse muscle) which passes around the cartilage and then attaches to the buccal wall. Approximation of the two halves of the radula in Archidoris is effected by contraction of the outer buccal constrictor. Muscle fibres passing through the tissue of the cartilage are equivalent to the intracartilage tensors in Onchidoris. Strands having a similar function in Philine are represented by the ends of muscles which insert upon the cartilage where the fibres pass between the cartilage cells and interweave as they anchor themselves there. The additional intrinsic cartilage muscles in Philine link the two cartilages on each side and are unnecessary in Onchidoris.

Constriction of the buccal cavity in both Archidoris and Onchidoris is brought about by the activity of a buccal sphincter (termed the outer buccal constrictor by Rose). No comparable muscle is described in Philine (Hurst, 1963). However Rudman’s drawings (19724 of P. falklandica show a sphincter in this species which is also found in Cylichna (Lemche, 1956).

A number of tensor muscles have been described in all three opisthobranchs. In Archi- doris sheets of muscle help in the protraction of the buccal mass. Of these the posterior buccal protractor, although stronger and thicker, is identical to the dorsolateral buccal tensor of Onchidoris. Similar muscles are shown in Hurst’s drawings of Philine classified under the general term of superficial buccal musculature. The radular elevator muscle of Philine is not present in either Archidoris or Onchidoris, but may be present in the related Phanerophthalmus luteus (Quoy & Gaimard) (Rudman, 1972b).

A comparison of the buccal musculature of Onchidoris, Archidoris and Philine illustrates the essential similarity of the first two, the differences lying in the relative size and function of the various muscles. Philine, however, has a larger number of muscles, several of which


are not functionally homologous with those of the Dorididae. In order to understand the functional significance of these differences the feeding mechanism of each mollusc must be considered. Hydrostatic protraction of the odontophore occurs in both Philine and Onchidoris, but the method by which blood pressure is increased differs considerably. In Philine the anterior aorta and columellar muscle are closely associated, the artery being opened during the initial stages of feeding when the muscle relaxes and allows blood to enter the anterior sinuses. I n Onchidoris blood pressure is increased initially by a shortening of the body. In both animals protraction of the buccal mass reduces the volume of anterior sinuses, so aiding increase in pressure. Rose (1971) reported that blood pressure is not an important factor in this process in Archidoris even though extrinsic protractor muscles are absent.

Once the odontophore is protracted, Archidoris rasps by spreading the radula over the sponge and then withdrawing its two halves at different times so as to produce a cutting action of opposing rows of teeth. Philine everts the whole of its buccal apparatus as an extravert terminating in the opened radula. On retraction, the teeth interdigitate around the prey and the food is dragged back into the first part of the digestive tract. In Onchidoris the effective stroke of the radula is brought about solely by muscles contained within the cartilage and, unlike Archidoris, the teeth are not erected until the odontophore has been everted. The grabbing mechanism of the radular teeth in Philine results from the activity of muscles passing from the cartilage to the subradular membrane. The complex radular musculature of this mollusc appears to be associated with spreading the teeth as widely as possible and then effecting a powerful downward movement of the radula so that the teeth close together as they do in Archidoris. In Onchidoris the teeth are of less importance in grabbing and consequently do not open as much as in Philine nor do they interdigitate when closed.

The development of the buccal pump in Onchidoris has had a great influence on its feeding methods. Although suctorial feeding has been described for many opisthobranchs --Melibe and T e t h ~ ~ s (Kjerschow Agersborg, 1923) Retusa and Acteoiz (Hurst, 1963). Cymbulia (Howells, 1936), the Sacoglossa (Evans, 1953 ; Fretter, 1941), and Pleurobranchzis (Thompson & Slinn, 1959) and others such as pyramidellids (Fretter & Graham, 1949) -the development of a discrete pump is more limited. Forrest (1953) described a buccal pump in a number of the Doridacea, but it reaches its highest degree of development in Onchidoris where it is separated from the buccal cavity by a long pedicel.

The comparison of the anatomy and method of functioning of the buccal apparatus of Onchidoris with that of other opisthobranchs illustrates that, although built to the same basic pattern, Onchidoris has evolved a highly specialized food collecting apparatus.

The buccal mass permits food to be collected by a combination of suction and a radular action which differs from that of any other gastropod which has been described. When using a piercing implement it is necessary to ensure that the sharp edge of the tool is held firmly and that there is a strong force exerted behind it in order to produce a powerful thrust. In Onchidoris both requirements are supplied by the odontophoral apparatus. The fusion of the subradular epithelium with the ventral face of the cartilage, together with the presence of tensor muscles which hold the radula firmly against the cartilage edges, ensures that radula and cartilage act as a unit with little movement of one in relation to the other. The teeth cannot then be erected by a movement of the radula over the cartilage and so this is accomplished partly by an increase in blood pressure within the odontophoral sinus


And partly by deformation of the cartilage itself. The cartilage is an extremly mobile support far the radula since it is composed almost entirely of muscle fibres. Because many of the Cartilage movements are also extensions of directional forces applied to it through muscles passing to the buccal wall (especially the lateral odontophoral protractor), the muscle it hich flattens the cartilage (ventral divaricator) shows some degree of continuity with these. There is, therefore, no need for a well-developed cartilage sheath (indeed, its presence n ould seriously impede the interaction of intrinsic and extrinsic cartilage muscles) and instead, the cartilage becomes part of the intrinsic buccal musculature.

The strong force necessary to push the odontophore against the barnacle is supplied by the well developed odontophoral protractor muscles. Radular retraction is of less importance in Onchidoris than in many other gastropods because of the relative immobility of the radula and this has resulted in a reduction in size of these muscles. They are now more zoncerned with altering the shape of the cartilage, and consequently opening and closing the teeth, than pulling the radula posteriorly.

As the teeth close they form a series of backwardly directed hooks which are able to drag any material stuck on their tips through the mouth. However, taking food into the buccal cavity by this method is probably linked more with a general retraction of the whole buccal apparatus than with a posterior movement of the radula alone. In consequence, the buccal retractors, and the muscles of the buccal lips, are powerful. The teeth are similarly aided in this activity by the action of the buccal pump. The isolation of the pump from the buccal wall musculature means that if necessary it can function almost independently of odontophoral movements. This enables the pump mechanism to be used during both ingestion and swallowing. The interaction of the inhalant and exhalant activity of the pump tiith the buccal sphincter is instrumental in altering the pressure within the buccal cavity in order to push food into, and probably along the oesophagus. As a consequence the buccal sphincter is an important muscle and is well developed in Onchidoris. The well developed buccal nervous system undoubtedly accounts for the carefully controlled and synchronized activity of the buccal muscles and buccal pump and the open blood system around the buccal apparatus is a prerequisite for efficient odontophoral protraction and retraction.

The combination of piercing, grabbing and suctoral feeding methods developed by Onchidoris has therefore enabled this animal to exploit a rich food source which is used by few other animals but, at the same time the feeding mechanism is sufficiently flexible to allow other marine animals to be included in the dorid’s diet.

ACKNOWLEDGEMENTS This work was carried out under a University of Reading studentship and I should like to

thank Professor A. Graham for his invaluable advice during my period of research and for very kindly reading this manuscript. I should also like to express my thanks to Dr T. E. Thompson for reading the final draft.

I should like to record my thanks to the Director of the Marine Biological Laboratory at Citadel Hill, Plymouth, for providing laboratory and other facilities for this study.

REFERENCES ALDER, J . & HANCOCK, A. (1855). A inoiiograph of the British iiudibrorichiate Molluscn. London: Ray Society. .~LEXANDROW~CZ, J. S. (1932). The innervation of the heart of the Crustacea. I. Decapoda. Q. JI microsc. Sci. 75:

171-249.

86 D . M. C R A M P T O N

ANKEL, W. E. (1936). Die Frassparen von Helcioii und Littorim und die Funktion der Radula. Verh. dt. 2001. Ges.

ANKEL, W. E. (1937). Wie fresst Littoritin? 1. Radula-Bewegung und Fresspur. Senckenbergiarla 19: 317-333. ANKEL, W. E. (1938). Erwerb und Aufnahme der Nahrung bei den Gastropoden. Verh. dt. zool. Ges. 40: 223-295. BARNES, H. &POWELL, H. T. (1954). 0~ichidorisfirsca (Miiller) a predator of barnacles. J. nriim. Ecol. 23: 361-363. BURTON, D. J. F. (1971). The fitnctioiial anatomy of the feeding apparatus of some selected members of the Steno-

CRAMPTON, D. M. (1973). The firrictiorial anatomy of the buccal mass of one opisthobra~ich and three pulmonate

EDMUNDS, M. (1971). Opisthobranchiate mollusca from Tanzania (Suborder: Doridacea). Zool. J. Linn. Soc. 50:

EIGENBRODT, H. (1941). Untersuchungen iiber die Funktion der Radula einiger Schnecken. 2. 2. Morph. Okol.

EVANS, T. J. (1953). The alimentary and vascular systems of Alderia modesta (Lovtn) in relation to its ecology.

FORREST, J. E. (1953). On the feeding habits and the morphology and mode of functioning of the alimentary

FRETTER, V. (1941). On the structure of the gut of the Ascoglossan nudibranchs. Proc. 2001. Soc. Loiid. (B) 110: 185-

FRETTER, V. & GRAHAM, A. (1949). The structure and mode of life of the Pyramidellidae, parasitic opisthobranchs.

GRAHAM, A. (1973). The anatomical basis of function in the buccal mass of prosobranch and amphineuran molluscs.

HANCOCK, A. & EMBLETON, D. (1 852). On the anatomy of Doris. Phil. Trans. R. Soc. 142: 207-252. HIAN, KO BUN. (1971). A new injection fluid for malacologists. Proc. Unitas Malacologia Europaea Congres de

HOWELLS, H. H. (1936). The anatomy and histology of the gut of Cynibuliaperoiiii (Blainville). Proc. malac. Soc.

HURST,A. (1963). Studies on the stritetiire andfiirictiori of the feeding apparatus of Piiilirre apevta (L.) with a compara-

KJERSCHOW AGERSBORG, H. P. (1923). The morphology of the nudibranchiate mollusc Melibe (syn. Cllioraera)

LEMCHE. H. (1956). The anatomy and histology of Cylichiia (Gastropoda Tectibranchia). Spolia zool. Mus. Hauniens

MILLOTT, N. (1937). On the morphology of the alimentary canal, process of feeding, and physiology of digestion of

MORSE, M. P. (1968). Functional morphology of the digestive system of the nudibranch mollusc Acarzthodwis

NISBET, R. H. (1953). The structure mfdfiniction of the buccal mass in some gastropod molluscs. I. Monodonta lineata

PANTIN, C. F. A. (I 969). Notes oii microscopical techriique for zoologists. Cambridge: University Press. PEACOCK, A. H. (1966). Elememwy microtechnique. London: Edward Arnold Ltd. ROSE, R. M. (1971). Functional morphology of the buccal mass of the nudibranch Archidoris pseudoargus. J .

RUDMAN, W. B. (1972a) Studies on the primitive opisthobranch genera Bullinn Ftrussac and Micromelo Pilsbury.

RUDMAN, W. B. (19726). The herbivorous opisthobranch genera Phaiierophthalnius A. Adams and Smaragdinella

RUDMAN, W. B. (1972~). The genus Philine (Opisthobranchia Gastropoda). Proc. malac. SOC. Lotid. 40: 171-187. SCHMIDT, G. (1916). Blutgefasssytem und Mantelhohle der Weinbergschnecke (Helix pomatia). Z. wiss. Zool. 115:

THOMPSON, T. E. & SLINN, D. J. (1959). On the biology of the opisthobranch Pleurobraiichus membraiiaceus. J . mar.

YOUNG, D. K. (1969). The functional morphology of the feeding apparatus of some Indo-West-Pacific doiid nudi-

38: 17&186.

glossa (prosobranch gastropods). Ph.D. thesis, University of Reading.

gastropod molluscs. Ph.D. thesis, University of Reading.

339-396.

Tiere 37: 735-791.

Proc. malac. Soc. Loiid. 29: 249-258.

canal in some littoral dorid nudibranchiate Mollusca. Proc. Liiiii. Soc. Lorid. 164: 225-235.

198.

J. Mar. biol. Ass. U.K. 28: 493-532.

J.Zool., Lolid. 169: 317-348.

Malacologires Eitropeeris 4: 35.

Lolid. 22: 62-72.

tive corisideratioii of some other opisthobrarichs. Ph.D. thesis, University of Reading.

leoniria (Gould). 0. Jlmicrosc Sci. 67: 507-592.

16: 1-278.

the nudibranch mollusc Joriiiirin tonieritosa (Cuvier). Phil. Trans. R. Sor. (B.) 228: 173-217.

pilosa. Biol. Bull. mar. biol. Lab, Woods Hole 134: 305-319.

(da Costa). Ph.D. thesis, University of London.

ZOOI. Lolid. 165: 317-336.

Zool. J. Lirni. Soc. 51: 105-119.

A. Adams. Proc. malac. Soc. Lorid. 40: 189-210.

201-261.

biol. Ass. lJ.K. 38: 507-524.

branchs. Malacologia 9: 421-446.

Documents

Functional anatomy of the buccal apparatus of Onchidoris bilamellata (Mollusca: Opisthobranchia)