Comparative buccal anatomy in Helisoma (mollusca, pulmonata, basommatophora)

JOURNAL OF MORPHOLOGY 203107-116 (1990)

Comparative Buccal Anatomy in Helisoma (Mollusca, Pulmonata, Basommatophora)

DAVID A. SMITH Department of Biology, Wabash College, Crawfordsoille, Indiana 47933

ABSTRACT Dissections were performed to document buccal anatomy in three species of the pulmonate genus Helisoma Swainson, 1840. The 28 muscles which are responsible for radular feeding in these animals are organized in three concentric and integrated envelopes. The deepest of these includes muscles which manipulate the radula about the odontophoral cartilage. Elements of the middle envelope direct movements of the cartilage within the buccal cavity, and muscles of the outer envelope control movements of the buccal mass within the cephalic haemocoel. Motion analysis by videomicrography showed that muscles of the middle and outer envelopes contribute to the action of radular feeding by acting as antagonists to other muscles and to hydrostatic elements of the buccal apparatus. Observations of radular dentition showed that although each of the three species examined has a unique radula, especially with regard to the specific details of tooth shape, all resemble a radula characteristic of the Planorbidae with regard to other, more general, aspects of ribbon architecture.

The radula, odontophoral cartilage, and muscles of the molluscan buccal mass work together to provide food material to the esophagus. Al- though buccal architectures may vary among cephalate molluscs, the fundamental elements of feeding are similar throughout members of this group. During grazing the radula is pro- truded through the mouth, accelerated across the substrate, and withdrawn. Food particles carried on the toothed surface of the radula are then passed to the esophagus and to the posterior alimentary canal.

Most early study of the mechanism of radular feeding had been based upon "naked eye" observations of individuals grazing the inside walls of aquaria (Woodward, '06; Longstaff, '13). More recent studies (Kater, '74; Morris and Hickman, '81; Hickman and Morris, '85) have used micro- cinematography. The present investigation is a synthetic one which incorporated detailed anatomical reconstructions of the buccal mass of Helisoma triuoluis (Say), and of two allied species, into an analysis of radular mechanics based on microvideomicrography. Results parallel previous functional and anatomical studies of other Basommatophora (Carriker, '46a,b; Demian, '62; Walter, '69; Hembrow, '73; Goldschmeding and DeVlieger, '75) and provide specific anatomical description to complement recent neurophysio- logical study of these animals (Kater, '74; Rose and Benjamin, '79; Brace and Quicke, '81; Bul- loch, '87).

MATERIALS AND METHODS

Materials for dissection were collected in May 1988, from three sites. In central New York Heli- soma triuoluis was taken from Richfield Springs (75'01.78'W, 42'51.85") and Helisoma campanulata (Say) was sampled from Dutcher Pond (75'57.60'W, 43'17.55"). In Indiana Helisoma anceps (Menke) was collected from Vanbibber Lake (3g043.25", 86'53.64'W).

Adults (10-20 mm shell height) used for anatomical reconstruction were relaxed in a solution of Nembutal in tap water (250 mgL) and fixed in 7% formalin. Because it was not possible to view all muscles from a single type of intact preparation, two dissection strategies were used. To view external musculature, a midline incision was made from the dorsal rim of the mouth to the mantle edge. Skin flaps were cut to the foot and pinned. If care was taken during this proce- dure, the sheet of transverse muscle which sepa- rates the haemocoelic space of the head from that of the visceral mass remained intact allow- ing investigation of these fine structures. The buccal retractors, esophagus, and the circumesophageal nerve ring were then cut to facilitate access to ventral muscle groups and to those muscles which join the buccal mass to the mouth. To facilitate observation of intrinsic musculature, the entire buccal mass was removed through a midline incision similar to the one described above. The tissue was then pinned to a clean

o 1990 WILEY-LISS, INC.

108 D.A. SMITH

dissecting dish to allow access to any muscle group of particular interest. All illustrations were drawn freehand from dissected material. Ana- tomical authorities included Carriker ('46a), Demian ('62), and Hembrow ('73). Specific no- menclature and numbering of buccal components follow Demian ('62). Numbers appearing in parentheses throughout the text identlfy particular muscles in Figures 1-3.

Preparations used to observe radular dentition were made by first sacrificing animals in boiling water and removing them from their shells. The entire buccal mass of each individual was dissected from the head, softened in satu- rated KOH for 2-5 sec, and transferred to distilled water. Radulae were then removed with fine forceps, placed onto clean glass slides, ar- ranged, and covered with coverglasses. Prepara- tions were held in distilled water for 24 hr, dehy- drated in 70% EtOH, and air-dried. New coverglasses and mounting fluid were then ap- plied. Preparations were examined under oil im- mersion using phase-contrast illumination.

No electromyographic recordings were made; however, video images of semitransparent Heli- soma trivolvis embryos assisted in the analysis of muscle function and in the identification of sets of muscle antagonists. Although other au- thors (Thomas et al., '85) have shown that there are differences between the adult and juvenile feeding niches of snails like Biomphalaria, the mechanism of radular feeding, in Helisoma at least, is the same for both juveniles and for adults. Video images were produced with an RCA CKCO2l camera. Filming utilized an egg capsule attached to a glass plate which was in- verted to permit viewing through its transparent underside. Of more than 250 recorded sequences of radular feeding, five were selected for detailed motion analysis.

RESULTS Buccal morphology in Hetisoma

There are 28 muscles which control the buccal mass in the three species of Helisoma documented here (Figs. 1-3). These muscles are ar- ranged in three concentric and integrated envelopes. One muscle group includes fibers which pass from the inside of the body wall to the exterior walls of the buccal mass. These assist in protraction and in retraction of the mass. The second system includes muscles which pass from the interior walls of the buccal mass to the odontophoral cartilage. These assist in rotation, pro- trusion, and in retraction of the odontophore. The third muscle system consists of fibers which originate from the cartilage and insert on the radular ribbon. These elements generate the re-

ciprocating movements of the radula which occur during feeding. There are other smaller sys- tems which open and close the mouth, control the dorsal and lateral mandibles, stiffen the cartilage, and suspend the radula sac from the exterior walls of the buccal mass.

Below follow descriptions of the 28 muscles which comprise the buccal apparatus of the three species of Helisoma studied here. Muscle descriptions were determined from detailed examination of at least 50 adult individuals of each species.

1. Dorsolateral protractors Dorsolateral protractors originate on either

side of the mouth at the body wall. These are thick bands, broad, and flared at their origins. They pass dorsally to insert on the exterior wall of the buccal mass near the esophagus in associa- tion with the posterior jugalis (14).

2. Preventral protractors Preventral protractors are a series of thin fi-

bers which originate on the ventral body wall below and about the mouth. Origins are adjacent to those of the suboral dialators (8). Preventral protractors pass posteriorly to insert along the midline of the ventral wall of the buccal mass in front of the postventral levators (7).

3. Postventral protractors Postventral protractors originate along the

ventral walls of the cephalic haemocoel directly behind and below the mouth. They pass posteriorly to insert on the ventral edges of the cartilage near the buccal artery. In H. trivolvis the insertion of the postventral protractors occurs at the meeting of the infraventral odontophoral protractors (19) and the supramedian radular tensors (20). In H. anceps and especially in H. campan- d a t a the insertion of the postventral protractors is mostly to the conspicuous knobs of the supramedian radular tensors (20).

4. Dorsolateral retractors Dorsolateral retractors originate on the ceiling

of the cephalic haemocoel. These long, thin muscles pass ventrally to insert on the exterior w& of the buccal mass, about the mouth, below the insertion of the dorsomandibular dialators (9).

5. Buccal retractors Buccal retractors originate on the columnar

muscle of the foot at the posterior limit of the cephalic haemocoel. They pass anteriorly through the circumesophageal nerve ring. Near the buccal mass the muscles divide so that each inserts

COMPARATIVE ANATOMY IN HELISOMA 109

at two locations on the external wall of the mass, ventrally to the posterior surface of the cartilage, and dorsally to the posterior surface of the cartilage at or just above the midline of the mass. In each of the three species of Helisoma dissected here the positions of these muscles are asymmet- rical with regard to their relationship with the circumesophageal nerve ring. The right retractor passes through the ring formed by the cerebral, pleural, and pedal ganglia, while the left passes through the ring formed by the cerebral, pleural, parietal, and visceral ganglia.

6. Preventral levators Preventral levators originate on the ceiling of

the cephalic haemocoel behind fibers of the postventral levators (7). These long, slender muscles descend to insert on the external surface of the mass near the lower edges of the mouth, and on the mandibular approximator (16).

7. Postventral levators. Postventral levators originate on the ceiling of

the cephalic haemocoel, anterior to and above the origins of the preventral levators (6). This series of thick fibers runs ventrally, passing closely about the walls of the buccal mass, to insert along the ventral midline of the mass behind the preventral protractors (2).

8. Suboral dialators Suboral dialators comprise a series of thin

fibers which originate along a broad region of the ventral body wall from within the snout. These pass posteriorly to insert broadly on the ventral wall of the buccal mass about the mouth. To- gether with the dorsomandibular dialators (9) the suboral dialators form a ring of fibers about the mouth. This muscular ring conneds the mouth to the snout of the animal.

9. Dorsomandibular dialators Dorsomandibular dialators are a ring of short

fibers which originate on the dorsal body wall from within the snout. They pass ventrally to insert on the dorsal wall of the buccal mass, broadly about the mouth.

10. Suspensor of the radula sac Carriker (’46a) has documented this muscle in

Lymnaea stagnalis appressa. Demian (’62) showed that the suspensor of the radula sac “hardly exists” in Lymnaea, Physa, Bi- omphalaria, Bulinus, Ancylus, and Acroloxus. Hembrow (’73) showed this muscle in Planorbar- ius. If the suspensor is present in Helisoma, it exists as a narrow band of short, diffuse, fibers

running between the buccal ganglia and the distal end of the radda sac.

11. Labial retractors Labial retractors comprise an extensive series

of small fibers within the snout of the animal. These radiate from the body wall and attach to the buccal mass broadly, forming a ring about the mouth.

12. Labial sphincters Labial sphincters are a diffuse band of fibers

of the body wail and snout. These are difficult to distinguish from fibers of the labial retractors (11). 13. Anterior jugalis

The unpaired anterior jugalis originates dorsally on the buccal mass below the fibers of the buccal sphincter (15). The muscle passes ventrally as a wide band to insert on the ventral face of the cartilage.

14. Posterior jugalis Compared to the anterior jugalis (13), the pos-

terior jugalis is a very thin muscle sheet covering the posterior walls of the buccal mass. The muscle originates anteriorly on the dorsal mandible and runs under the buccal sphincter (15) and the anterior jugalis (13) to insert on the ventral edge of the cartilage. The posterior jugalis covers portions of the esophagus, the supramedian radula tensors (20), and the supralateral radula tensors (21), as well as the distal end of the radula sac. Together with the anterior jugalis (13) this muscle forms most of the roof of the buccal mass. Where the posterior jugalis passes below the dorsolateral protractors (1) it is translucent and the radula sac may be seen descending to the cartilage. 15. Buccal sphincter

The buccal sphincter is a heavy band of muscle which circles the anterior portion of the buccal mass. It runs posteriorly from the mouth to the anterior limit of the resting cartilage.

16. Mandibular approximator The mandibular approximator is a thick mus-

cle band at the anterior extreme of the buccal mass. The muscle is most easily seen on the ventral wall of the mass where it passes about the lower parts of the mouth. It mingles exten- sively with the buccal sphincter (15).

17. Dorsal odontophoral flexor Dorsal odontophoral flexors are small muscle

bands which originate on the dorsolateral ceiling

110

b.

D.A. SMITH

2 0

m

1 rnm I r s

Figure 1


of the buccal cavity adjacent to where the subradular membrane and the supralateral radula tensors (21) meet. The thin fibers of the dorsal odontophoral flexors insert on the dorsal edges of the cartilage.

18. Ventral odontophoral protractors Ventral odontophoral protractors run above

the infraventral odontophoral protractor (19) and below the basal epithelium of the buccal cavity. These thin muscle bands originate near the mouth at the anterior limit of the ventral wall of the buccal cavity. The bands pass posteriorly and insert broadly on the ventral edges of the cartilage. These are less robust then the underlying infraventral odontophoral protractors (19).

19. Infraventral odontophoral protractors Together with the ventral odontophoral pro-

tractors (18) the infraventral odontophoral protractors compose the ventral wall of the buccal mass. These muscles originate from the ventral wall of the buccal cavity where fibers mingle with the buccal sphincter (15) and mandibular approximator (16). Insertions occur along the ventral edges of the cartilage. From the central midline of the buccal mass these bands wrap dorsally about the mass to merge with the descending arms of the anterior jugalis (13).

20. Supramedian radula tensors Supramedian radula tensors originate from

the extreme ventral edges of the odontophoral cartilage. They pass posteriorly for a short length to wrap about the ventral edges of the cartilage and then pass dorsally and anteriorly to lie within the posterior median concavity of the cartilage, between the cartilage and the overlying radula sac. The posterior portions of the muscles are

Fig. 1. Right-lateral a: and ventral b views of the buccal mass of Helisoma triuoluis. Left-side, extrinsic, musculature (on the right as viewed from below) has been removed in panel h. be, buccal epithelium; c, odontophoral Cartilage; e, esophagus; m, mouth; rs, radula sac; sg, salivary gland; 1, dorsolateral protractors; 2, preventral protractors; 3, postventral protractors; 4, dorsolateral retractors; 5, buccal retractors; 6, preventral levators; 7, postventral levators; 8, suboral d d a - tors; 9, dorsomandibular dialators; 11, labial retractors; 12, labial sphincters; 3, anterior jugalis; 14, posterior jugah; 15, buccal sphincter; 16, mandibular approximator; 17, dorsal odontophoral flexor; 18, ventral odontophoral protractors; 19, infraventral odontophoral protractors; 20, supramedian radula tensors; 21, supralateral radula tensors; 22, i n f r a m d i radula tensors; 23, infracartilage tensor, 24, intercartilage tensors; 25, lateral suspensors of the radula sac; 26, inferior suspensor of the radula sac 27, superior suspensor of the radula sac; 28, tensor of the hood.

conspicuous and form two knobs about the ventral edges of the cartilage. The tensors insert on the ventral edges of the radula sac directly beneath the point where the radula is reflected over the dorsal lip of the cartilage.

21. Supralateral radula tensors The supralateral radula tensors comprise the

lateral walls of the buccal mass and are by far the largest of the muscles of this organ. The supralateral radula tensors originate ventrally on the lateral edges of the cartilage. From here they pass ventrally for a short space and then turn dorsally to wrap about the margins of the cartilage. The tensors then turn in about the dorsal edges of the cartilage and insert along a broad area, which includes the edges of the radula sac adjacent to where the radula emerges from beneath the collostylar hood, the underside of the subradular epithelium in front of the region where the radular reflects about the dorsal tip of the cartilage, and the epithelium of the buccal cavity in front of, behind, and to the sides of the odontophoral cartilage.

22. Inframedian radula tensors Inframedian radula tensors originate on the

anterior face of the cartilage at its extreme ventral edge. These are thin muscles which run between the cartilage and the epithelium of the buccal cavity. The inframedian radula tensors insert anteriorly on the subradular epithelium.

23. Infracartilage tensor The infracartilage tensor is an unpaired mus-

cle band that spans the posterior ventral face of the cartilage. Anteriorly, the infracartilage tensor meets the buccal sphincter (15).

24. Intercartilage tensors The odontophoral cartilage has many associ-

ated muscle fibers which are collectively termed the intercartilage tensors. Some pass laterally across the anterior face and are visible as silvery streaks in intact preparations. Others run at right angles to the long axis of the cartilage.

25. Lateral suspensors of the radula sac Lateral suspensors of the radula sac originate

on the supralateral radula tensor (21), where the supramedian radula tensors (20) pass about the ventral tips of the cartilage. These small fibers pass laterally to insert on the faces of the distal end of the radula sac. The lateral suspensors of the radula sac run deeply within the buccal anatomy and may not usually be seen with superficial dissection.

112 D.A. SMITH

a.

e -

5

i 20

rn

I mm

b.

I I rnrn r s

Fig. 2. Right-lateral a: and ventral b views of the buccal mass of Helisomo campanulata. Left-side, extrinsic, musculature (on the right as viewed from below) has been removed in panel b. Abbreviations and numbers as for Figure 1.


a.

e-

5

m.

b.

. 2

2c

Fig. 3. Right-lateral a: and ventral b views of the buccal mass of Hel i som anceps. Left-side, extrinsic, musculature (on the right as viewed from below) has been removed in panel b. Abbreviations and numbers as for Figure 1.

114 D.A. SMITH

26. Inferior suspensor of the radula sac This muscle originates ventrally on the poste-

rior median face of the cartilage. It inserts to the ventral face of the distal end of the radula sac. This muscle may be seen most clearly in H. campanulata. In H. trivolvis and in H. anceps the inferior suspensors are smaller and may not be seen with superficial dissection.

27. Superior suspensor of the radula sac The superior suspensor of the radula sac origi-

nates on the dorsal wall of the buccal mass below the esophagus. The unpaired suspensor passes ventrally to insert on the dorsal surface of the distal end of the radula sac.

28. Tensor of the hood The tensor of the hood originates within the

anterior portion of the radula sac. This muscle inserts on the underside of the collostylar hood.

Although each of the buccal masses examined differs with regard to absolute dimension, interspecific comparisons of each component muscle indicated that all muscles are approximately pro- portional with regard to size. When looking at the dissected masses however, one can discern minor differences in overall appearance. The mass of H. trivolvis is larger than that of either H. campanulata or of H. anceps. Because the posterior edge of the cartilage of H. trivolvis falls well below the ventral edge of the mouth, the infraventral odontophoral protractors (19) are long and form one side of an almost triangular mass. The masses of H. campanulata and of H. anceps are more square, with the infraventral odontophoral protractor (19) running almost parallel to the dorsal surface of the mass. The buccal mass of H. anceps is compact and in ventral view is shortened anteriorly in the region of the buccal sphincter (15) and posteriorly about the lateral and posterior limits of the supralateral radular tensors (21). The radula sac in H. trivolvis is always sheathed below the posterior jugalis (14). The distal limit of the radula sac in H. anceps often projects from beneath the posterior jugalis (14). The radula sac of H. campanulata projects noticeably from beneath the covering of the posterior jugalis (14). This effect is enhanced by some shortening of the anterior jugalis (13) and allows examination of the inferior suspensor of the radula sac (26).

Buccal function in Helisoma Radular feeding in Helisoma may be divided

into six stages (Smith, '87, '88) (Table 1). During the first of these (Rest) the long axis of the buccal mass lies parallel to the floor of the ce-

TABLE 1. Muscles responsible for primary control of b~lccal uctiuity in Helisoma'

Buccal region Activity Muscles

Inner Envelope Radula protraction 21,22 Radula retraction 20,21

Middle envelope Cartilage protraction 13,14,17 Cartilage retraction 17,18,19

Outer envelope Mass protraction 1,2,3,4,7 Mass retraction 3,W

'See Smith ('87, '83). and G o l & c h e d i and DeVlieger ('75).

phalic haemocoel and the cartilage rests within the lumen of the buccal mass. During the second phase of activity (Radular protraction) feeding is initiated by activity of the inframedian radular tensors (22) which draw the radula over the tip and down the anterior face of the cartilage. Dur- ing the third phase (Buccal protraction) the buccal mass is rotated, within the cephalic haemocoel, anteroventrally through an arc of approximately 65'. The dorsolateral protractors (l), preventral protractors (2), and anterior jugalis (13) pull the buccal mass forward and down, while the postventral levators (7) lift the posterior. Odontophoral rotation is then initiated by activity of the dorsal odontophoral flexors (17), anterior jugalis (13) and the posterior jugalis (14). During the fourth and fifth phases (Radu- lar retraction and Buccal retraction) the rasp stroke is characterized initially by retraction of the radular ribbon, and later by acceleration of the odontophore across the substrate. The first of these movements is brought about by activity of the supramedian radula tensors (20). Acceler- ation of the cartilage is brought about by contractions of the infraventral(l9) and ventral odontophoral protractors (18). Because radular retraction is in progress before withdrawal of the odontophore has been initiated, odontophoral retraction constitutes the cutting motion of rad- uiar feeding. Once in contact with the substrate, the odontophore travels at a velocity of approximately 1.5 cm/sec. At the end of the rasp the long axis of the cartilage lies perpendicular to the floor of the buccal cavity. During the sixth and final phase of feeding (Buccal hyperretraction), the leading edge of the cartilage is brought back toward the opening of the esophagus. This move- ment is facilitated by pressures generated from collapse of the cephalic haemocoel, collapse of the buccal mass, and by contractions of the anterior jugalis muscle (13). Furthermore, motion analysis suggests that pressure within the buccal mass may be increased during radular feeding by blood volumes supplied by the buccal artery. When hyperretraction is complete, the buccal mass is returned to its resting position by contrac-


tions of the buccal retractors (5), postventral levators (7), and the preventral levators (6). The total elapsed time for a complete rasp cycle is approximately 1.0-1.5 sec. Muscles involved in buccal activity are listed in Table 1.

Radular dentition The radula of Helisoma is a matrix of tooth

rows and columns. In H. triuoluis examined here the dimensions of this matrix ranged from 114 to 142 rows (3.0-3.5 mm in length) by 33-57 columns with a radula formula of 11-20 (marginal) + 5-8 (lateral) + 1 (rachidian). Matrix dimensions for H. campanulata ranged from 106 to 125 rows (2.0-2.5 mm) by 43-55 columns with a radular formula of 1&20 + 5-7 + 1. In H. anceps dimensions of the tooth matrix ranged from 132 to 150 rows (1.5-2.0 mm) by 43-47 columns with a radula formula of 17-19 + 4-5 + 1. With regard to the specific details of radula tooth shape H. triuoluis, H. campanulata, and H. anceps are unique species; however, each resembles other Planorbids in more general aspects of radular architecture (Burch and Jeong, '84).

DISCUSSION

Results from the present study concur with recent ideas concerning the mechanism of gastropod feeding (Brace and Quicke, '81; Hawkins et al., '89) and have shown that the radula of Heli- soma triuoluis slides over the underlying cartilage while the cartilage accelerates across the substrate during each feeding stroke. Smith ('88) has discussed the details of this mechanism and has suggested that, in contrast to other possible programs, the one described here is more effi- cient because feeding involves the application of a dynamic radula to ungrazed substrate by a dynamic cartilage. Losses in food gathering effi- ciency, characteristic of other proposed mechanisms, result from either a static cartilage (Cu- vier, 1817; Geddes, 1879) or a static radula (Huxley, 1853; Herrick, '06). For more detailed and fully documented descriptions of feeding kinetics in Helisoma, see Smith ('87, '88). The present synthesis of dynamic functional analysis and anatomy extends earlier work of Gold- schmeding and DeVlieger ('75) by increasing the resolution of anatomical detail and by incorporat- ing the functional significance of haemocoelic spaces into a more complete consideration of the mechanism of radular action. Results from vid- eomicrographic analysis showed that muscle elements of three concentric envelopes control the

movements of the buccal mass (8 elements), odontophoral cartilage (6 elements), and radula (4 elements). In addition to the contractile and antagonistic action of these elements, results also indicated that interactions between blood volumes and the haemocoelic spaces of the head play significant roles in generating motive forces important to the program of radular feeding in Helisoma.

Although buccal architectures differ slightly among the species studied, each maintains 28 muscles in approximately the same position and orientation. Furthermore, although the absolute dimensions of the individual muscle elements differ in mature adults of the three species, the proportionate sizes of the muscles in different individuals appeared to be approximately equal. The anatomical descriptions provided here most closely resemble reconstructions of Lymnaea and Biomphalaria provided by Demian ('62) (Figs. 9,15,11,17). Buccal anatomy would appear to be somewhat conservative in the Basommato- phora.

Observations showed that although certain features of radular architecture, such as total number of tooth rows and the proportions of lateral and marginal teeth, are relatively conservative, the specific shapes of rachidian, lateral and marginal teeth are unique for each of three species examined. It is because of this specific uniqueness that the molluscan radula continues to play a central and important role in studies of molluscan taxonomy. Because previous work (Calow, '70) and more recent study (Smith, '89) has shown that Helisoma and other members of the Basommatophora are generalized feeders, showing no feeding selectivity among Aufwuchs components, it is unlikely that any interspecific differences in tooth dentition could result in significant interspecific differences in the neu- rally and mechanically conservative mechanism of radular feeding.

ACKNOWLEDGMENTS

This research was supported by funds from the Senate Research Committee of Syracuse Uni- versity, the Theodore Roosevelt Memorial Fund, the Treves and Carscallen Funds of Wabash College, and by a grant from the Howard Hughes Medical Institute to Wabash College. I thank Drs. W.D. Russell-Hunter and Ruth D. Turner for stimulating an appreciation for how small things work. I also thank Joseph Trumpey for many long hours dedicated to creating the draw- ings which illustrate this manuscript and for dealing, always diplomatically, with a perfection- ist.

116 D.A. SMITH

LITERATURE CITED Brace, R.C., and D.L.J. Quicke (1981) Activity patterns in

radular retractor motoneurones of the snail, Planorbanus. J. Camp. Physiol. 142t259-270.

Burch, J.B., and K.H. Jeong (1984) The radular teeth of selected Planorbidae. Malacol. Rev. 17.6784.

Bulloch, A.G.M. (1987) Somaimtatin enhances neurite out- growth and electrical coupling of regenerating neurons in Helisoma. Brain Res. 412.6-17.

Calow, P. (1970) Studies on the natural diet of Lymnaea pereger obtusa (Kobelt) and its possible ecological implica- tions. Proc. Malac. Sac. Land. 39;20%215.

Carriker, M.R. (1946a) Morphology of the alimentary system of the snail Lymnaea stagnalis appressa Say. Trans. Wi. Acad. Sci. Arts Lett. 38: la .

Carriker, M.R. (1946b) Observations on the functioning of the alimentary system of the snail Lymnaea stagnalis appressa Say. Biol. Bull. 91:&111.

Cuvier, G. (1817) MBmoire pour servir a l’histoire et B l’anatomie des mollusques. Deterville: Paris.

Demian, E.S. (1962) Comparative morphological studies on the buccal mass of the Lymnaeacea Goteborgs. K. Vet- ensk. -Vitterh. -Samh. Handl. Ser. B 9tl-30.

Geddes, P. (1879) On the mechanism of the odontophore in certain molluscs. Trans. 2001. Sac. Land. 10t485-491.

Goldschmeding, J.T., and T.A. DeVlieger (1975) Functional anatomy and innervation of the buccal complex of the freshwater snail Lymnaea stagnalis. Proc. K. Ned. Akad. Wet. 78C.468476.

Hawkins, S.J., D.C. Watson, AS. Hill, S.P. Hardmg, M.A. Kyriakides, S. Hutchinson, and T.A. Norton (1989) A com- parison of feeding mechanisms in microphagous herbivo- rous intertidal prosobranch in relation to resource parti- tioning. J. Moll. Stud. 55:151-165.

Hembrow, D. (1973) Observations on the structure and function of the buccal mass of Planorbarius corneus (L.). Prw. Malac. Sac. Land. 40505521.

Herrick, J.C. (1906) Mechanism of the odontophoral apparatus in Sycotypus canaliculatus. Am. Nat. 40:707-737.

Hickman, C.S., and T.E. Morris (1985) Gastropod feeding tracks as a source of data in analysis of the functional morphology of radulae. Veliger 27t357-365.

Huxley, T.H. (1853) On the morphology of the cephalous Mollusca. Philce. Trans. R. Sac. Land. 143:2%65.

Kater, S.B. (1974) Feeding in Helisoma triuoluis: the morphological and physiological bases of a fixed action pattern. Am. Zool. 14t1017-1036.

Longstaff, J. (1913) Feeding-tracks of gastropods. Proc. Linn. Soc. Land. 125.1CL72.

Morris, T.E., and C.S. Hickman (1981) A method for artifi- cially protracting gastropod radulae and a new method of radula function. Veliger 24t8590.

Rose, R.M., and P.R. Benjamin (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J. Exp. Biol. 80:137-163.

Smith, D.A. (1987). Functional Adaptation and Intrinsic Bi- ometry in the Radula of Helisoma triuolui. Ph.D. Disserta- tion, Syracuse University, Syracuse, New York.

Smith, D.A. (1988) Radular kinetics during grazing in Heli- soma triuoluis (Gastropoda: Pulmonata). J. Exp. Biol. 136: 89-102.

Smith, D.A. (1989) A test of feeding selectivity in Helisoma triuoluis (Gastropoda, Basommatophora). Trans. Amer. Mi- crmc. Soc. 108:394402..

Thomas, J.D., D.I. Nwanko, and P.R. Sterry (1985) The feedimg strategies of juvenile and adult Biomphalaria gla- brata (Say) under simulated natural conditions and their relevance to ecological theory and snail control. Proc. R. Soc. Land. B 226t177-209.

Walter, H.J. (1969) Illustrated biomorphology of the “angulata” lake form of the basommatopharan snail Lym- naea catascopium Say. Malacol. Rev. 2tl-102.

Woodward, B.B. (1906) On some “feeding tracks” of gastropods. Proc. Malacol. Soc. Land. 7t31-33.

Documents

Comparative buccal anatomy in Helisoma (mollusca, pulmonata, basommatophora)