The
Ecology and Digestive System of the Struthiolariidae
(Gastropoda)
By J. E. MORTON
{From the Department of Zoology, Auckland University College)
SUMMARY
The two neozelanic species Struthiolaria papulosa and Pelicaria vermis have been
studied as regards ecology, feeding mechanism, and structure and function of the
digestive system. They are dwellers on sand or sand-mud-flat, with a feeding position
just below the surface, where they construct paired siphonal tubes with the rostrum.
A ciliary mode of feeding has been acquired by the modification of the gill filaments
and the pallial rejection system. The alimentary canal is adapted for deposit feeding
and has developed a crystalline style. Food particles are conducted to the stomach by
a functionally reduced mucus-secreting oesophagus, where they are subjected to the
action of the rotating style, and a complex system of ciliary currents. Digestible particles are passed into paired diverticula, where absorption and intracellular digestion,
takes place, while faecal material is surrounded with mucus and formed into firm
pellets by the ciliary and muscular action of the intestine. The relationships of the
Struthiolariidae are discussed, and their origin from the Aporrhaidae is postulated.
CONTENTS
INTRODUCTION .
M A T E R I A L
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A N D M E T H O D S
L I F E RELATIONS
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The Habitat
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External Characters and Movements
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T h e Feeding Position: Formation o fSiphonal Tubes
T h e Mechanism o fFeeding
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T h e Buccal and Oesophageal Regions
S Y S T E M
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DIGESTIVE
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T h e Stomach and Crystalline Style C a e c u m
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T h e Digestive Diverticula
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T h e M e c h a n i s m o fD i g e s t i o n
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T h e Intestinal Region
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C O M P A R A T I V E
REFERENCES
DISCUSSION
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INTRODUCTION
'
I "*HE family Struthiolariidae Fischer comprises a small group of prosoX branch molluscs, with an extensive time range and geographical distribution in Tertiary seas, but including only four recent genera, all in the
southern hemisphere, of which three have but one surviving species. Perissodonta Martens 1878 is represented by one species at Kerguelen Land and
[Quarterly Journal Microscopical Science, Vol. 92, p a r t 1, March, 1951.]
2421.1
B
2
Morton—Ecology and Digestive System of.
another at South Georgia, and Tylospira Harris 1897 by a single species in
New South Wales. The present paper deals with the representatives of the
two New Zealand genera—Siruthiolaria Lamarck 1818, as now restricted,
and Pelicaria Finlay 1928. The two species Struthiolaria papulosa (Martyn
1784) and Pelicaria vermis (Martyn 1784) have long been known to conchology, being accurately figured in Thomas Martyn's The New Conchologist
from shells collected on Cook's first voyage, probably by Sir Joseph Banks in
Queen Charlotte Sound. Our anatomical knowledge of the Struthiolariidae
is, however, extremely fragmentaiy. Quoy and Gaimard (1833) give fairly
accurate figures of the external characters of the New Zealand species. Hutton
(1882) contributed a note on the anatomy of Struthiolaria papulosa; his
description and drawings are rough and inaccurate, though the dentition and
operculum were for the first time correctly figured. As regards the biology
of the New Zealand forms, Powell (1937) has briefly concluded that Struthiolaria and Pelicaria are deposit feeders. A detailed examination of the structure
and feeding mechanism of Struthiolaria papulosa has brought to light features
of special biological interest. Pelicaria vermis has been compared with
Struthiolaria throughout and found to agree in all essential characters.
MATERIAL AND METHODS
Specimens of both Struthiolaria papulosa and Pelicaria vermis used in the
present work were collected in New Zealand at Cheltenham and Takapuna
beaches on the shore of Rangitoto Channel near Auckland. The mode of life
was studied in the field, while material was dissected, with the help of a
Zeiss binocular, both alive for the study of ciliary and digestive action, and
after fixation with Bouin's Fluid. This fixative was found excellent for general
histological work, while Carnoy's without chloroform was used for the quick
fixation of ciliated tissues. Paraffin sections were cut at 8 microns and doublestained with Delafield's haematoxylin and van Gieson's picrofuchsin.
LIFE RELATIONS
The habitat. Struthiolaria papulosa (Text-fig. 2) is found widely throughout
New Zealand and extends to the Kermadec Islands. It occurs characteristically on the lowermost littoral fringe of clean sand-mud-flats, of which
Cheltenham Beach is a typical example, with a wide expanse of shore some
three-quarters of a mile long and 300 yards between tides. Wave action is
relatively subdued and an area of fine shell sand has become covered with a
thin mantle of organic sediment, plant detritus, and benthic diatoms. Water
movement is nevertheless sufficient to ensure a well-aerated substratum, the
more stable conditions of mud-fiat being undeveloped and Zostera present
only in isolated tufts. There is a comparatively rich fauna, including selective
deposit feeders such as Struthiolaria, and at least six pelecypods; detritus
eaters (Echiuris, Amphiura, the synaptid Trochodota, and a hitherto unrecorded
enteropneust, Ptychodera) as well as carnivorous gastropods (Alcithoe and
Ancilla) and polychaetes (Glycera, Nephthys, and a maldanid).
Struthiolariidae {Gastropoda)
3
Pelicaria vermis (Text-fig. 1) is confined to the North Island—accompanying in general the rather more common Struthiolaria papulosa. It is also more
tolerant of muddy conditions, being well represented at Waikowhai in the
Manukau Harbour, where Struthiolaria does not extend. In addition, both
species probably occur fairly widely in the soft benthic sub-littoral, being
TEXT-FIGS, I-Z
Fig. 1. Pelicaria vermis, shell x j . Takapuna, Auckland. Fig. 2. Struthiolaria papulosa,
shell x | . Cheltenham, Auckland.
recorded by Powell (1937) in the Maoricolpus-\-Dosinula and Taioera-\Venericardia formations.
External characters and movements. Struthiolaria has the general appearance
of a typical mesogastropod prosobranch; the most conspicuous external feature is the highly extensible foot and head region, for the Struthiolariidae—
though sedentary feeders—have, like most sand-flat inhabitants, retained
active powers of locomotion. Struthiolaria papulosa measures two or three
times the length of Pelicaria vermis and is further distinguished by its somewhat handsome appearance—translucent milk-white in colour, with the exposed parts of the head, trunk, and foot marked with fine close-set lines of
orange-red. Pelicaria vermis, on the other hand, is yellowish or clay-coloured,
with rather less conspicuous lineations of rust-red. The cephalic tentacles in
Struthiolaria are tapering and sharply pointed, in Pelicaria less slender and
more bluntly tipped.
The foot is very labile and possesses a broad oval creeping surface attached
to the trunk by a short, cylindrical 'waist' region capable of great elongation.
The operculum is reduced to a small chitinous plate with the distal end produced into a strong, sharp claw which is at times employed as an accessory
locomotor organ (Text-fig. 3). The Struthiolariidae exhibit two types of
4
Morton—Ecology and Digestive System of
movement, the first by using the plantar surface of the foot, the other by
the levering action of the operculum. The normal creeping movement on the
surface of the sand is performed by the widely expanded sole, the operculum remaining out of use on the dorsal surface of the foot. There is also a
second mode of progression by the use
of the sole which is observed to best
advantage upon a hard surface as at
the bottom of a glass dish. The sole is
placed firmly upon the substratum and
the body-whorl of the shell raised clear
of the ground by the elongation of the
muscular 'waist' region; the heavy shell
is then allowed to fall some distance
forward in the direction of movement,
B
and the sole is again moved forward in
TEXT-FIG. 3. S. papulosa, diagrams advance of the shell for the repetition
showing the position of the foot, in of this rather clumsy lunging movement
normal creeping movement (A) and oper(cf. Yonge (1937), on Aporrhais).
cular movement (B).
When the operculum is employed in movement, the extent of the sole is
greatly reduced by withdrawal of blood from the pedal sinus, and the foot
and trunk elongate to form a narrow muscular column. The sole—now small
and oval—is displaced dorsally, and the muscular lobe carrying the operculum
is thrust forward so that the sharp claw projects from the tip of the foot.
The opercular claw is used mainly in the characteristic movement of 'righting'
the shell when the animal is overturned; it is thrust round forcibly beneath
the left side of the shell and dug deeply into the substratum, when the considerable leverage of the foot serves to heave the shell over to its normal
position. The claw of the operculum may also be used as a defensive weapon
when a specimen is taken up on the hand, the sharp-tipped foot being
extended for 2 to 3 in. and moved about vigorously seeking a point of purchase. The opercular movements of Struihiolaria are chiefly of interest in
showing how the normal mode of locomotion in the related highly specialized
Strombidae may have arisen. In this group the sole is vestigial and the
animal progresses by a series of convulsive leaps by the flexion of the foot as
the opercular blade is thrust into the substratum.
The feeding position: formation of siphonal tubes. During feeding Struthiolaria lies buried immediately beneath the surface of the sand and constructs
a pair of mucus-lined siphonal tubes. It is not in the strictest sense adapted
for burrowing; despite Oliver's statement (1923) that it ploughs along below
the surface, it is quite clear that progression does not take place while the
animal is buried, although the feeding position is abandoned at frequent
intervals and the animal crawls about freely upon the surface. The nodulose
turreted shell is characteristically that of a surface-dwelling gastropod, in
contrast with burrowing forms at Cheltenham such as Andlla and Pervicada.
Struthiolariidae (Gastropoda)
5
The animal submerges itself by a continuation of the normal crawling
movement, and anterior canal being depressed slightly and pushed below the
sand, while the labile anterior margin of the foot is thrust downward, obtaining purchase in the sand and drawing the shell behind it. Gradually, the
inhalant siphonal
aperture
exhalent siphonal
apert • —
TEXT-FIGS.
4-7
Fig. 4. S. papulosa buried below the surface, showing the mode of formation of the siphonal
tubes. Fig. 5. Surface view of the substratum, showing the inhalant siphonal aperture (right)
and the exhalant aperture (left). Figs. 6 and 7. Diagrams showing the action of the proboscis in forming siphonal tubes.
pallial current and the entrenching movements of the foot clear a space into
which the whole shell subsides. The buried animal may usually be located
by a small raised mound of sand as well as by the two openings of the siphonal
tubes (Text-fig. 5), approximately i£ in. apart and about one-sixth of an
inch in diameter. These tubes, described originally in the related Aporrhais
(Yonge, 1937), are unique among molluscs in being paired and widely
separated—an inhalant tube directly above the left side of the animal
and an exhalant tube on the right. The side-walls are very regular, being
compacted with a thin secretion of mucus as in burrowing polychaetes and
Enteropneusta.
6
Morton—Ecology and Digestive System of
The siphonal tubes of Struthiolaria are constructed by the action of the
proboscis (Text-fig. 4), which exhibits a high degree of adaptation for its role.
The retracted organ forms a short dorso-ventrally flattened tube, some threequarters of an inch long, with its integument thrown into very regular, closeset annular rugae. By a copious inflow of blood from the body haemocoele
into the rhynchocoele, the proboscis may be extended to form a cylindrical
siphon-like organ, almost 3 in. in length, terminated by a circular oral disk
bearing the vertical slit-like mouth at its centre. The oral disk is radially
streaked with yellowish and grey, and may be flat, depressed to form a shallow
funnel, or when fully expanded, somewhat convex. The integument of the
proboscis is beset with numerous mucous cells, which are especially dense
round the marginal rim of the oral disk. There are also large numbers of
fusiform sensory receptor cells, of the same type as occur in the integument
of the cephalic tentacles; it appears that the proboscis serves also as a sensory
organ for maintaining contact with the surface while the animal is buried.
In the formation of the siphonal tubes the proboscis is at short intervals
pushed up through the sand to establish a pair of holes. It is first narrowly
compressed by the contraction of the circular muscles passing round the
rugae, and at the same time greatly elongated and pointed at the tip by partial
inflow of blood and the relaxation of its longitudinal muscles (Text-fig. 6).
Except for the oral disk, the wall is not everted as in the pleurecbolic introvert
type of proboscis. When the oral disk reaches the surface, the circular muscles
are relaxed, and the rhynchocoele tensely engorged by the increased bloodsupply, the dilation of the rostral artery being assisted by the contraction of
extrinsic muscle slips inserted on its wall. The oral disk is now widely expanded with its marginal rim extending slightly beyond the edge of the
siphonal tube (Text-fig. 4). The organ is then quickly withdrawn, and firmly
moulds the wall of the tube in its downward passage, expressing a coat of
mucus, especially from the periphery of the oral disk (Text-fig. 7). From time
to time during feeding the proboscis is extended through one or other tube
like a pelecypod siphon, removing obstructions, and maintaining sensory
contact with the surface. A specimen removed from sand in a laboratory dish
well exhibits the stereotyped tube-forming movements of this organ, with
periodical erection, engorgement, and rapid withdrawal.
The pallial cavity in Struthiolaria (Text-fig. 8) is extremely spacious, and
a continuous current of water enters from the inhalant tube and leaves by the
exhalant, serving respiratory, cleansing, and food-collecting functions. On
taking up a specimen in the hand, a strong jet of water is expelled from the
exhalant side by the sudden retraction of the head and foot, which serves
to close the cavity in front. The aperture is otherwise unprotected and the
free margin of the mantle forms a continuous skirt covering the wide callused
peristome of the shell. It is liberally supplied with blood, and as the gill is
primarily specialized as a current-producing organ, apparently serves an
accessory respiratory function. Just behind the right mantle margin and a
short distance in front of the anus^ lies a single pallial tentacle (Text-fig. 8)
Struthiolariidae {Gastropoda)
7
resembling in appearance one of the cephalic tentacles. It is extended in life
through the exhalant siphonal tube, while the left cephalic tentacle passes
through the inhalant tube. The pallial tentacle is densely coated with cilia,
which maintain a' strong outward current through the siphonal tube serving
hypobranchial gland
exhalant chamber
of pallial cavity
rectum
inha!=nt chamber
of pallial cavity
ctenidium
ctenidial axis
food groove
operculum
pharynx with
salivary glands
siphonal lappet
ctenidium
hypobranchial gland
TEXT-FIGS.
8-9
Fig. 8. S. papulosa. The entire animal, showing the pallial cavity opened along the right
side, and the course of the alimentary canal; natural size. Fig. 9. 5. papulosa. Diagram. matic transverse section of the pallial cavity.
to carry away waste products from the pallial cavity. Aporrhais and the
burrowing Strombidae have a similar pallial tentacle which presumably
serves the same function, and Yonge (1947) has described a similar mechanism
in the unrelated genus Valvata.
The mechanism of feeding. Struthiolaria obtains its food by ciliary means,
the inhalant current carrying into the pallial cavity a stream of roughly selected
detritus and micro-organisms including diatoms and Foraminifera, as well as
a good deal of non-nutritive material such as shell fragments, spicules, and
sand grains. Of prime importance in the collecting of food particles for ingestion is the ctenidium, which in Struthiolaria reaches a length of z\ to 3 in.
8
Morton—Ecology and Digestive System of
It is immediately apparent on opening the pallial cavity (Text-fig. 8), extending back from the margin of the mantle (across which the anterior filaments
may protrude) to the narrow posterior end of the cavity, thus completely
encircling the body-whorl. The ctenidial axis (Text-fig. 13) lies along the
left side of the mantle, and the monopectinate lamina arches to the right
across the whole-width of the mantle cavity. It is composed of some 300-400
tubular filaments, each a narrow, laterally compressed rod, attached proximally to the mantle wall on the left side, along the first half of its dorsal edge,
while its distal half is entirely free. The great development of the ctenidium
divides the pallial cavity (Text-fig. 9) obliquely into two longitudinal compartments each roughly triangular in section. The left compartment or inhalant chamber is the more venttfally placed, being floored by the dorsal surface
of the trunk and bounded above by the curved ctenidial septum, extending
from the roof of the pallial cavity on the left to near the floor on the right.
The right, or exhalant, chamber lies somewhat dorsally to the inhalant, its
floor being the gill septum while it is roofed by the hypobranchial, or pallial,
mucous gland (Text-fig. 9). The pallial epithelium is here extremely thickened
and thrown into wide, yellowish-brown transverse rugae, secreting much
colourless viscid mucus.
The individual gill filaments are highly adapted to the mode of life. Like
the triangular leaflet of the generalized prosobranch gill (Yonge, 1938), each
is formed of a membranous fold of integument enclosing a narrow respiratory
blood space, and basally attached to the mantle. In Struthiolaria the filament
apex is carried across to the right side of the pallial cavity, to form a long,
free distal portion, strengthened by the well-developed, paired, chitinous
skeletal rods. In histological structure (Text-figs. 10, 11) the filament is noteworthy for the relatively increased area occupied by the very long lateral
cilia (Text-fig. 10). They maintain a strong flexual beat across the filament
from ventral to dorsal sides, creating a continuous water current from inha. lant to exhalant chambers. In addition to the lateral field there are two principal tracts of shorter cilia; the ventral edge of the filament is clad with short,
fast-beating frontal cilia, which direct a current towards the apex, while
along the dorsal edge runs a tract of abfrontal cilia, smaller and with a weaker
beat than the frontals. The original function of the frontal and abfrontal cilia
was no doubt to collect particles for transport to the free edge of the gill
and rejection from the pallial cavity (Yonge, 1947). In Struthiolaria, as in
other ciliary feeding Prosobranchia (Yonge, 1938), it was only a short step
to establish a feeding mechanism by which nutritive particles were collected
by the frontal and abfrontal currents.
The inhalant current bearing food and detritus is drawn into the pallial
cavity on the left across the small triangular siphonal lappet (Text-fig. 8),
passing inwards along the osphradium (Text-fig. 13) which may be regarded
as an organ for the detection of entering sediment (Hulbert and Yonge,
1937). In Struthiolaria, the osphradium forms a simple linear sensory tract
which runs across the siphonal lappet, and passes backwards parallel to the
Strutkiolariidae {Gastropoda)
9
anterior third of the gill axis. It is edged on either side by a narrow darkpigmented ridge bearing a tall ciliary fringe whose beat serves to divide the
entering stream of particles. Some of these seem to be directed across the
trunk to the right, but by far the greater number are drawn by the strong
ctenidial current to the left, where—before reaching the gill—they pass across
frontal cilia
skeletal rod
skeietal rod
frontal cilia
ateral cilia
lateral cilia
blood sinus
respiratory epithelium
muscle
anfrontal cilia
TEXT-FIGS, IO-IZ
Fig. 10. Transverse section through the middle portion of a ctenidial filament. Fig. 11.
Transverse section through the apex of a ctenidial filament. Fig. 12. Diagrammatic lateral
view of the apical portion of a ctenidial filament.
a special mucus-secreting region or 'endostyle'. This is a narrow tract of tall
(40 fi) ciliated and glandular epithelium of very uniform structure (Text-figs.
13, 14) overlying the efferent branchial vessel along the entire gill axis. Narrow
wedge-shaped ciliated cells, with ciliary coat 6-7 /x in height, alternate regularly with the long cigar-shaped gland cells, filled with dark-staining secretion.
The fusiform nuclei of the ciliated cells are displaced upward to the free surface; those of the gland cells are rounded and basal. Following Orton (1912)
and subsequently Yonge (1938) and Graham (1938) this region is referred
to as an endostyle; it is not, however, homologous with the similarly named
structure in ascidians and Cephalochordata, which is located within the gut
along the floor of the pharynx.
io
Morton—Ecology and Digestive System of
The secretion of the endostyle entangles food and particles of detritus while
at the same time the ciliary field maintains a rapid transverse beat, carrying
a continuous sheet of mucus with entrapped particles across the ctenidial axis
to the frontal surface of the gill. The frontal cilia at once carry the particles
across the ventral aspect to the right margin of the gill. The lateral cilia beating inwards between the filaments serve as a sieve mechanism for straining off
solid particles from the respiratory current. Such smaller particles as may
pass through the sieve between the filaments receive a small accretion of
mucus from the scattered gland cells in the respiratory epithelium of the filament, and are finally carried to the apex by the abfrontal ciliary tract.
osphradium
ciliated cell
gland eel!
TEXT-FIGS. 13-14
Fig. 13. Transverse section through the ctenidial axis, x 50. Fig. 14. Portion of the endostylar
epithelium. X 500.
The termination of each filament (Text-fig. 12) is bluntly rounded and
slightly expanded; there are no special cilia creating a forward current along
the gill as in Crepidula and Vermetus (Yonge, 1938), but a uniform coat of
short terminal cilia beating towards the tip, the columnar ciliated cells being
interspersed with a few mucus-secreting cells. Just behind the tip of the filament on the ventral (or frontal) side is a small depression where the frontal
and abfrontal currents converge, the abfrontal current with its particles having
passed around the apex. Within the depression the particles of the two
streams are intermingled by a rapid ciliary rotation, and—assisted by a small
amount of mucus—are rounded off into a tiny spherical bolus. The series of
depressions on successive filaments together constitute a shallow longitudinal
food-collecting groove, and the mucous boluses become continuous to form
a thin thread of food material clearly visible to the naked eye along the ventral
edge of the gill.
In the living animal the down-curved gill projects into a well-marked
excavation of the dorsal surface of the trunk, occupying the right-hand portion
of the pallial cavity floor, and referred to as the food groove (Text-fig. 8). It
continues forward in front of the pallial cavity along the right side of the
trunk as far as the base of the right tentacle, becoming considerably narrower
and bounded on either side by tall integumentary folds which may be temporarily approximated to form a closed tube. The bounding fold along the
Struthiolariidae {Gastropoda)
11
right side encloses beneath its outer edge the ciliated genital furrow in both
sexes. The marginal folds of the groove are extremely labile, being liberally
supplied with blood and capable of considerable muscular movement. The
ciliated epithelium is richly beset with unicellular mucous glands, v/hose
contents render the integument a characteristic greenish-grey in colour, and
stain black in haematoxylin.
From time to time the narrow thread of mucus along the edge of the gill is
rolled off by ciliary rotation into the posterior part of the food groove. Other
particles enter the groove from the surface of the trunk, passing between
small muscular crenulations of the left wall. The wide floor of the groove,
while less glandular than the margins, maintains a rapid ciliary current which
sweeps particles forward towards the region of the head. At the same time a
liberal secretion of mucus is received, while the ciliated coat of the side-walls
begins to rotate the contents passing forward through the temporary tube,
so as to form a long spiral mucous cord, which finally issues from the spoutlike opening of the groove near the base of the proboscis. The food string is
usually greyish-brown in colour, with a large content of recognizable detritus
from the substratum. In animals kept in clear water it becomes opaque white
consisting of almost pure mucus and resembling a strand of wool. The contents of the string are surrounded by a delicate pellicle of mucus which becomes condensed on contact with the external medium.
At regular intervals the proboscis is turned backwards to the opening of
the food groove and the paired jaws pluck at the tuft of issuing food material,
which is pulled away in strands and either rapidly ingested, or allowed to
accumulate in a small heap at the side of the animal. The radula appears to
be used principally to rake food material through the pharynx, after a bolus
has been picked up or detached by the jaws. It would seem likely that the
method of ciliary feeding provides the whole means of subsistence in Struthiolaria. The proboscis is evidently modified wholly for constructing the siphonal
tubes; though frequently seen to explore the ground like -a sensory organ, it
was never observed to pick up particles and does not appear adapted for
collecting food.
THE DIGESTIVE SYSTEM
The alimentary canal in Struthiolaria is highly adapted for the slow regular
intake of fine detrital particles. As in numerous other microphytophagous
mesogastropods a crystalline style is present, and the most distinctive features
of the digestive system are:
I. The loss of triturating function by the pharynx.
II. The reduction of the oesophagus to a mucus-secreting region conveying a food string to the stomach.
III. The reduction of muscular tissue in the gut in general and the
increased reliance on ciliary manipulation of food and faeces.
IV. The specialization of the stomach for the sorting of particles.
12
Morton—Ecology and Digestive System of
V. The absence of extracellular enzymes, apart from that of the style,
and the ingestiori of particles by the digestive diverticula.
VI. The adaptation of the intestine for producing firm faecal pellets to
avoid fouling of the pallial cavity.
VII. The frequent occurrence of wandering phagocytic cells performing
an accessory digestive function.
The course of the alimentary canal (Text-fig. 8) is relatively simple. The
mouth opens into a small pharyngeal bulb, leading into a long narrow oesophagus, which passes directly through the trunk cavity to open into the
stomach on the left side. The stomach is a large rounded chamber, occupying
TEXT-FIG. 15. S. papulosa. A single row of radular teeth.
with the crystalline style caecum the whole left aspect of the first visceral
whorl. It gives exit to paired digestive diverticula which ramify to form the
two massive, asymmetrical lobes of the digestive gland; the right or anterior
lobe is the smaller and embraces the deep aspect of the stomach, whilst the
left or posterior lobe is spirally coiled, comprising, with the gonad, the
greater part of the visceral hump. The style caecum and the proximal division of the intestine (Text-fig. 17) open forward together from the stomach,
the caecum on the right side overlying and partly concealing the intestine.
Just behind the pericardium the intestine turns sharply below the apex of
the caecum, and emerges on the right side of the visceral spire as the narrow
middle intestine which loops back around the renal organ and then passes
forward along the right pallial wall into the wider rectum. The anus opens
anteriorly upon a small spout-like papilla, immediately behind the tentacle
on the right pallial margin.
The Buccal and Oesophageal Regions
The pharynx presents no special features in Struthiolaria, being greatly
reduced in consequence of its loss of function. A pair of cuticular jaws is
retained in the form of small triangular plates lining the pharynx wall just
within the slit-like mouth aperture. This region is readily reversible, and the
sharp chitinized margins of the jaws serve to strengthen the edges of the
mouth for grasping mucous boluses from the food groove. The radula,
although equipped with sharp, curved marginal teeth as in other ciliary
feeding gastropods, was not observed to come into play in seizing food. It is
exceptionally small in relation to the animal, and its caecum is very short,
scarcely emerging through the floor of the pharynx. There is the typical
taenioglossan formula (Text-fig. 15) of seven teeth in each row: the laterals
Struthiolariidae (Gastropoda)
13
are rectangular in shape with a finely denticulate cusp at the mesial edge.
The quadrangular or five-sided central tooth carries a broad, finely serrate
triangular cusp. The salivary glands are vestigial, reduced to a pair of tiny
white lobules closely flattened against the roof of the pharynx at the base of
the oesophagus. They are histologically simple, the epithelial cells each containing a large mucous spherule with no apparent enzymatic contents.
The ciliated, glandular dorsal food channel of the pharynx continues back
along the anterior division of the oesophagus, where it is bounded by a pair
of rather prominent dorso-lateral folds. There are- other less permanent epithelial folds, and the whole region forms a thin-walled narrow tube, lined
with columnar cells bearing a tall ciliary coat (18/x) interspersed with very
numerous fusiform mucous cells of the same type as those in the margins of
the food groove. The glandular tracts of the oesophagus are thus a conspicuous grey-green in colour. The middle region of the oesophagus, commencing immediately behind the nerve ring, shows a condition somewhat
less advanced than in the ciliary feeders Crepidula and Turritella (Graham,
1939): its topographically dorsal portion forms a structural remnant of the
spacious oesophageal crop of less specialized prosobranchs, the food channel
passing, as a result of torsion, around the left side to the floor of the oesophagus where it proceeds backward as a wide greenish epithelial tract. The
more extensive dorsal portion is transparent and non-ciliated with the lining
thrown into small, papillose longitudinal folds. Its epithelium is small-celled
and cubical, devoid of glandular elements.
The most posterior part of the oesophagus (Text-fig. 16) possesses—unlike
the rest of the alimentary canal—a fairly thick coat of circular muscle (sometimes reaching 100/z). The lining epithelium is uniformly ciliated, thrown
into 12-20 regular longitudinal folds. The mucous glands—though less
abundant than anteriorly—are still frequent, and it is in this region that the
food string receives its final shape, being carried back by the cilia along the
summits of the folds to the stomach.
The Stomach and Crystalline Style Caecum
The stomach, style caecum, and proximal intestine form a single functional
unit of the alimentary canal (Text-fig. 17). The stomach is roughly flaskshaped, consisting of a wide posterior chamber receiving the oesophagus, and
opening forward into a smaller anterior chamber, which leads in front
by a common aperture to the style caecum and proximal intestine. The caecum remains in wide communication with the intestine for about threequarters of its length, the two cavities being incompletely separated by a pair
of typhlosoles—the dorsal one very large, and the ventral a low glandular
ridge.
The crystalline style projects in life into the anterior chamber, its head
bearing like a pestle against the gastric shield, a triangular outgrowth of the
ventral stomach wall—transparent and brittle in texture and superficially
14
Morton—Ecology and Digestive System of
resembling cartilage in appearance. The surface of the shield is slightly concave
and the free edge curves backward towards the posterior chamber. Close
to the gastric shield open the paired digestive diverticula. The anterior
aperture lies just behind the opening of the style caecum adjacent to the head
of the style; the posterior diverticulum opens by a spout-like lip, just below
the left side of the gastric shield.
The dorsal wall of the stomach is occupied by an extensive ciliary sorting
area, a series of close-set ridges commencing posteriorly and passing obliquely
ciliary coab
gland cell
phatjocyte
•'blood vessel
TEXT-FIC 16. Portion of the wall of the posterior region of the oesophagus. X 500.
forward around the left side of the stomach to the opening of the proximal
intestine. The sorting area is a structure highly typical of ciliary and detritus
feeding molluscs, being especially well developed in Struthiolaria. Its limits
are easily seen externally through the transparent wall of the stomach, being
marked on the right by a broad S-shaped ridge which continues backwards
around the fundus of the posterior chamber. Graham (1939) points out that
this ridge—with the sorting area within its crescent—probably represents a
vestige of the spiral stomach caecum found in archaeogastropoda.
The crystalline style caecum. The style caecum in Struthiolaria is a short
stout sac of 6 mm. diameter, recognizable externally by its deeply pigmented
wall. Its epithelial lining is very regular, beset with small, close-set transverse
rugae. The dorsal typhlosole which serves to delimit the caecum from the
intestine and to grasp the style in the living animal, forms a wide double fold,
L-shaped in section along most of its length, and produced along the right
side into a broad style flange (Text-fig. .19, 20) which depends into the caecum
Stnithiolariidae {Gastropoda)
15
and enwraps the style from below. A narrow strip of tall epithelium runs the
whole length of the typhlosole, just behind the free edge of the style flange.
This is the region of style secretion (Text-fig. 18), the epithelium staining
communication between
sti/le caecum and
intestine
«
communication between
style caecum sndincestine
styie-secrrting
epithelium
posterior intestine
donal hjphbsole-
oesophagus
ciliated sorting area
posterior intestine
TEXT-FIGS.
17-20
Fig. 17. Stomach and crystalline style caecum, opened along the right side, showing the
style in situ and the course of the ciliary currents, and path of the food string, x 6. Fig. 18.
Crystalline style caecum, with the style removed and the dorsal typhlosole reflected back.
X 6. Figs. 19 and 20. Diagrammatic transverse sections through the style caecum and
proximal region of the intestine, mid-way along (19) and near the apex (20).
very darkly and forming secretory droplets of similar appearance to the style
substance. Posteriorly towards the stomach (Text-figs. 17, 18), the style
flange with its secretory ridge becomes very wide and is reflected back across
the flat summit of the typhlosole, forming a wide sleeve which completely
invests the style from above. Anteriorly the apex of the caecum separates
16
Morton—Ecology and Digestive System of
completely from the intestine (Text-fig. 20) by the coalescence of the left
typhlosole margin with the ventral wall of the common caecum-intestinal
chamber. The now narrow style flange remains in contact with the style
within the caecum. The line of fusion lies to the left of the small ventral
typhlosole which is thus also enclosed within the caecum, together with a
narrow remnant closed off from the intestinal lining.
The crystalline style forms an extremely delicate taper.ed rod, 2 cm. in
length, hyaline golden brown in colour, and very flexible. It is rapidly dissolved after cessation of feeding, and was best examined immediately upon
removing the animal from water, being completely resorbed within an hour
or two of collecting.
Histology. The lining epithelium of the stomach, in contrast to that of the
oesophagus and of the intestine, is devoid of gland cells. There are two main
histological regions, the ciliated sorting area, and the cuticulated area surrounding the base of the gastric shield. The sorting ridges are due entirely
to differences in the height of the cells, varying from 80 //. along the folds to
30^. in the grooves. The nuclei are elongate-ovoid, binucleolate, forming a
subcentral row, and the ciliary fringe is especially well developed (12-15 fi),
supported by dense clusters of fibrillae. The epithelium is conspicuously
invaded by wandering phagocytes from the underlying zone of connective
tissue and a basal supporting reticulum traverses a series of intra-epithelial
canals. The cuticulate epithelial cells are extremely tall and narrow, reaching
200 //, in height, while the cells secreting the gastric shield proper become as
tall as 750 JU.. The nuclei are compressed and rod-like, forming a crowded
subcentral row, while the secreted cuticle (10 fi thick) is hyaline and structureless, attached to the epithelium by fine perpendicular strands resembling cilia.
The epithelium of the style caecum (Text-fig. 21) possesses extremely
robust cilia forming a dense coat 25 p in height. The ciliary basal granules
form a prominent refractile line, and the cell fibrillae form dense bundles
passing from the sides of the nuclei to the bases of the cells. The ovoid to
spherical nuclei are izfj- in length, binucleolate and with sparse chromatin.
The cytoplasm is uniformly granular and without secretory contents. At the
bases of the cells is developed a system of intracellular supporting fibres,
intra-epithelial canals appearing in section as small, non-staining vacuoles.
The Digestive Diverticula
The digestive gland in Struthiolaria shows typical alveolar structure, each
diverticulum ramifying into a system of smaller ductules, which ultimately
give rise to clusters of small, dark-coloured digestive lobules, each about
200^ across. The ductules are lined throughout with columnar ciliated epithelium, the cells reaching 55/z in height, with a ciliary coat 5-6 [j. wide and
fibrillar bundles well developed. The basal nuclei are ovoid, binucleolate, and
7 jii in length.
The glandular cells of the terminal lobules (Text-fig. 22) are of two distinct
types, digestive and excretory. The lumen is generally triangular, bounded on
Struthiolariidae {Gastropoda)
17
three sides by tall columnar digestive cells which by increase in height may
reduce the space to a triradiate cleft. At the bottom of each crypt a smaller
pyramidal group of darkly pigmented excretory cells is intercalated between
the digestive cells. The digestive cells possess small, darkly staining basal
nuclei. The free surfaces—though always intact—are commonly rather convex, sometimes bulging and somewhat pseudopodial. There is some evidence
ciliary coat
phagocyte
intra-epithelial
canal
muscle fibres
pigmented cell
TEXT-FIG, SI. Portion of the wall of the style caecum, showing ciliated cells. X 500.
that the border is normally ciliated in the resting condition, though cilia are
not apparent after fixation. A row of tiny refractile granules underlies the
free surface, with a short fan of fibrillae radiating through the superficial
cytoplasm. The distal cytoplasm of the digestive cell is very coarsely granular
and evidently contains ingested material, while the basal half of the cell is
packed with small greenish spherules, 2-3 p across, somewhat oily in appearance and containing irregular clumps of particulate matter. The digestive
epithelium is frequently invaded by phagocytes from the vascular interstitial
connective tissue.
The pigmented excretory cells in the crypts appear to be of several types.
There is usually a centrally placed, broad-based, flask-shaped cell, with a
constricted neck, containing a single large dark pigment spherule, sometimes
25-30/n. across, round and dark-brown or black with a greenish oily iridescence. The nucleus is small and pressed flat against the cell base. Flanking
the central cell on each side are several columnar excretory cells, of the
second type, with small round nuclei as in the digestive cells. The free surface is rounded and pseudopodial, and the distal third packed with rather
18
Morton—Ecology and Digestive System of
lightly staining granular contents; the basal portion is uniformly dark-brown
pigmented, occasionally invaded by phagocytes. That there are probably two
types of columnar cell is indicated by the presence in some cases of much
gland cell
ciliated cell
muscle
superficial portion of*
digestive cell
basal portion of
digestive cell with
clumps of participate
material
ciliated cell of
digestive diverticulum
excretory cell
excretory spherule
gland celt
ciliated cell
gland cell
ciliated cell—-S;:
24
TEXT-FIGS. 22-5
Fig. 22. Portion of transverse section of digestive lobule, with ciliated epithelium of diverticulum. X500. Fig. 23. Epithelium of proximal division of intestine. X 350. Fig. 24.
Epithelium of middle intestine, x 350. Fig. 25. Epithelium of rectum. X 350.
larger, ovoid or flattened nuclei, 10 ft across and with a single prominent
nucleolus. From the nature of the granular inclusions in the distal cytoplasm
it would seem that some at least of these pigmented cells approach in character
the lime cells typically found in the gastropod digestive gland.
Struthiolariidae {Gastropoda)
19
The Mechanism of Digestion
In Text-figs. 17 and 18 are illustrated the system of ciliary currents in the
stomach and style caecum which together comprise the most specialized
region of the gut. In this region the wall of the gut is firmly attached by
muscle strands to the external body-wall, and is incapable of peristalsis; the
ciliary fields are thus all-important in securing movement of contents. The
long robust cilia of the style caecum serve by their transverse beat to rotate
the style on the bearings formed by the epithelial folds. The direction of
rotation is clockwise, and in the transparent veliger larva the speed was
observed to be about 40 turns a minute. At the same- time the dense but
shorter cilia covering the style flange of the typhlosole maintain a strong beat
towards the stomach, by which the rotating style is gradually thrust downward so that its head bears against the gastric shield. Yonge (1932) has
emphasized the importance of the style as a mechanism for the continuous
liberation of amylase in those molluscs, lamellibranchs, and micro-herbivorous
prosobranchs, which have a slow continuous feeding process. Strong amylolytic action was detected by digestive experiments on the style of Struthiolaria,
while no action was observed on either dissaccharides or cellulose. It would
seem, however, that a possibly equally important function of the style is to
afford mechanical assistance to the movement of the food contents in the
stomach. The soft, rotating style head becomes securely attached to the end
of the oesophagal food string, which is slowly but continuously drawn into
the stomach, around the fundus of the posterior chamber and forward on
the right side to the surface of the gastric shield. The cord is thrown into a
close spiral by the style rotation, while the attached end is broken down and
the contents freed, partly by attrition by the style head, but also, no doubt,
by the lowered viscosity of the mucus in the stomach, brought about by the
reduction of hydrogen ion concentration (Yonge, 1935).
The rotation of the style also effects a constant stirring of the dispersed
stomach contents by which particles are repeatedly drawn across the ridges
of the ciliary sorting area. In Struthiolaria a large amount of non-nutritive
material must enter the stomach. The sorting area consists of flat-topped
primary ridges alternating with smaller triangular secondary ridges running
along the intervening grooves. The primary ridges bear tall ciliary fringes
keeping up a steady transverse beat across the stomach wall at right-angles to
the direction of the ridges. Coarser, heavier particles such as sand grains,
thrown against the sorting area by style rotation, sink into the grooves, and
are carried directly forward by the cilia of the secondary ridges to the proximal intestine. The lighter particles, on the other hand, are flicked across the
sorting area by the ciliary tufts of the primary ridges, and are conveyed by
special ciliary currents into the digestive diverticula.
The diverticula do not secrete; apart from the action of the style amylase,
digestion is intracellular. The digestive gland forms the main absorptive
region of the gut, and a series of simple spotting tests on extracts showed a
normal complement of intracellular enzymes. Of proteins, fibrin and also
20
Morton—Ecology and Digestive System of
powdered peptone were readily digested, best in slightly acid media; 5 per
cent, methyl acetate was easily hydrolysed showing the presence of an
esterase (probably a lipase), while a strong amylase was demonstrated by
complete hydrolysis of starch solution. There was no action on the cellulose
of cotton fibres and it is probable that, as in other detritus feeders, cellulose,
if assimilated at all, demands previous bacterial or autolytic breakdown.
Fine particles appear to be ingested by the epithelium of the digestive lobules in its pseudopodial phase. The basal greenish spherules of the
digestive cells invariably contain clumps of solid particles, which apparently
represent the non-assimilable residue after intracellular digestion, probably
surrounded by enzyme to form a fluid vacuole. At regular intervals these basal
cell contents are returned to the stomach by the fragmentation of the digestive
cells, and can be detected in sections in the form of tiny boluses of egesta,
approximately 50 fi across, passing forward along the sorting area to the
intestine. Each bolus contains closely compacted cell fragments containing
the greenish vacuoles, as well as nuclei, phagocytic cells, and brown excretory
spherules. Mansour (1946) claims that in the lamellibranchs enzymes are
liberated into the stomach by the fragmentation of holocrine digestive cells.
In Struthiolaria, however, it is quite clear that the fragmented particles are
always in the nature of egesta, and pass directly to the intestine. Small traces
of enzyme are doubtless liberated in this way into the stomach; in general,
however, Struthiolaria conforms entirely to Yonge's rule as to the intracellular nature of digestion in style-bearers.
Following Macmunn (1900) it may be concluded that the large dark spherules
discharged from the excretory cells consist of a chlorophyllous pigment derived from food substances and extracted from the blood by special cells in the
digestive lobules. Intracellular digestion of detrital particles must be accompanied by large absorption of plant pigments, and in style-bearing gastropods
in particular the excretory mechanism of the digestive gland is well developed.
The abundance of wandering phagocytic cells in the subepithelial layer of
most parts of the gut has already been mentioned. These cells readily invade
the epithelium and ingest solid particles, though it is questionable whether
they are primarily nutritive or are concerned with the removal of waste particles. It is certain that particles of no food value may be ingested, as was
demonstrated by the accumulation of neutral red particles within the phagocytic cells of the sorting area of the veliger larva. The most probable hypothesis, in light of the work of Yonge (1926), is that the phagocytes emerge
into the lumen where they ingest both free food particles, which are then
intracellularly digested, as well as particles of rejected material. The presence
of a very thick zone of phagocytes in the wall of the proximal intestine of
Struthiolaria would point also to rejectory function.
The Intestinal Region
The intestine, adapted solely for compaction of faeces, consists of three
regions, the wide proximal intestine communicating with the style caecum,
Struthiolariidae {Gastropoda)
21
a harrow middle intestine, and a terminal rectum. The lining is ciliated and
glandular throughout (Text-figs. 23, 24, 25), and in the proximal intestine the
epithelium is disposed in tall longitudinal tracts, separated by narrower
intervening grooves lined by much shorter cells. The ventral wall has two
broad tracts, separated by a deeply incised groove along which are carried
indigestible particles from the grooves of the gastric sorting area. The dorsal
wall consists also of two broad tracts with a narrower suture, while along the
left side runs a wide shallow channel of low-celled epithelium. The wall of
the proximal intestine is not, as in the stomach, secured to the body-wall,
and the edges of the broad tracts work freely upon the contents of the grooves,
by means of a thin, continuous zone of muscle in the hind-gut wall. The
faecal material is all the while liberally admixed with mucus, and particles
are carried by ciliary currents across the tracts into the grooyes, where they
are conveyed forward to the middle intestine.
The faeces are formed into pellets during passage through the middle
intestine, which has a characteristic trihedral structure, the lumen being
bounded by three broad ciliated tracts sutured by three grooves of low epithelial cells. The ciliated cells of the broad tracts are extremely tall and narrow (120/x in height as compared with 80ju. in the proximal intestine). They
possess ovoid-elongate central nuclei, and are regularly interspersed with a
series of greatly attenuated mucous cells, with a distal rank of cigar-shaped
secretion droplets, and a basal row of rounded uninucleolate nuclei (Text-fig.
24). In passing along the narrow grooves the faeces are firmly kneaded into
a coherent mucous string, from which individual pellets are from time to time
nipped off by slight peristaltic movements of the bounding tracts. The pellets
are given their final compact form by ciliary rotation against the rectum wall,
producing firm grey-green ovoid masses, approximately 0-25 mm. long.
The rectum is a long straight tube with its walls smooth or thrown when
empty into small impermanent folds. The columnar ciliated cells (Text-fig.
25) are much shorter (40-50/x) than in preceding regions, with ovoid basal
nuclei. The gland cells are simple and ovoid, with light-staining contents
which form the transparent coat finally surrounding the large masses of faecal
pellets. The rectal wall near the anus is somewhat muscular, and the faeces
are expelled by slight contractions in coherent strings which are immediately
carried away in the exhalant pallial current.
COMPARATIVE DISCUSSION
Ciliary feeding in prosobranchiate gastropods has now been reported as the
result of independent evolutionary change in five style-bearing families which
otherwise have little in common, namely, the sessile Calyptraeidae (Orton,
1912), Vermetidae (Yonge, 1932), Capulidae (Yonge, 1938), and in the freemoving Turitellidae (Graham, 1938). To these the also active Struthiolariidae must now be added. Similar pallial adaptations have been acquired in
each family, including strongly ciliated, linear gill filaments, and mucusproducing endostyle and food groove. The Calyptraeidae [Calyptraea and
22
Morton—Ecology and Digestive System of
Crepidula) are the most highly specialized group, being suspension feeders,
largely on diatoms, and having the gill filaments free and rod-like along their
whole length, with the blood space reduced, and the membranous respiratory
area entirely lost. Yonge correlates the extreme specialization of the gill filament with a reduction in respiratory needs of the sessile Crepidula; in the
actively moving Struthiolaria the filament has, in the proximal region at
least, retained its respiratory function.
The Struthiolariidae most closely resemble in their biology the family
Turritellidae (Graham, 1938; Yonge, 1946), as typified in New Zealand by
Maoricolpus rosea, examined during the present work. These two groups are
the only recorded ciliary feeding prosobranchs free-moving in a soft substratum. In neither case has the gill filament become free along its whole
length, while in both groups there are convergent adaptations for dealing
with the large amounts of non-nutritive bottom material that must enter the
pallial cavity during feeding. The unicellular mucous glands of the gill filament, and the large hypobranchial gland are retained, while the food groove
—a mere shallow depression in Crepidula—forms in Struthiolaria and Turritella a muscular, temporarily closed tube, capable of compacting large
amounts of imperfectly sorted surface detritus. In both forms the gastric
ciliary sorting area, and the faeces-compacting region of the proximal intestine, only slightly. represented in Crepidula, are prominently developed.
Turritella, with its long tapering shell, is pre-eminently adapted for trailing
through mud, and the pallial cavity is screened from sediment by a curtain
of pinnate pallial tentacles. The absence of such a mechanism in Struthiolaria
may probably be ascribed to the cleaner, sandy habitat, and to the efficient
mucus-lined siphonal tubes.
The Struthiolariidae are classified by Thiele (1931) in his Stirps Strombacea, along with the families Aporrhaidae, Strombidae, and Xenophoridae.
Unpublished observations of the present writer indicate that the Xenophoridae are somewhat removed from the remaining three families, which together
form a compact natural assemblage—with an especially close affinity between
the Aporrhaidae and Struthiolariidae. In general characters Aporrhais pespelicani, as described by Yonge (1937), is very similar to Struthiolaria. The
habitat is alike in both groups, and in mode of locomotion Aporrhais agrees
with Struthiolaria in showing both creeping and lunging movements with the
widely expanded sole. Yonge states that the reduced operculum in Aporrhais
is never used in locomotion, and that the righting movement of the upturned
animal is effected not with the operculum after the strombid fashion, but by
leverage obtained by placing the sole flat on the substratum. However,
examination of the operculum in preserved Aporrhais pes-pelicani reveals
that the distal edge is produced into a strong, spade-like plate, not figured by
Yonge, which has all the appearance of a locomotor organ like the claw in
Struthiolaria.
Aporrhais, like Struthiolaria, constructs paired, mucus-lined siphonal tubes
by the action of the proboscis. This adaptation, which is recorded nowhere
Struthiolariidae {Gastropoda)
23
else among gastropods, would appear to have arisen as a single evolutionary
development in a common ancestral form of the Aporrhaidae and Struthiolariidae. Aporrhais has not acquired a ciliary feeding mechanism; the pallial
organs, while forming an efficient cleansing and rejection system, are not
modified for food collecting, and the gill filaments remain triangular. The
inhalant current brings detrital particles to the vicinity of the rostrum and
according to Yonge feeding takes place as readily upon the surface as when
buried. 'The animal presumably feeds normally by collecting by means of
the extensible proboscis all particles of plant matter which occur in the mud
in the region below and around the expanded lip.' Yonge stresses the creation
of powerful water currents by the gill in Aporrhais and the elaboration of
ciliary currents for the rejection of sediment. He emphasizes that these
developments 'have an added interest in that they indicate the way in which
ciliary feeding in gastropods may have been evolved'. The exhalant currents
might further be modified to form the food channel, while modifications of
the tips of the gill filaments would convert the gill into the food-collecting
organ found in Crepidula. Such a process is exactly what is now found to
have occurred in the Struthiolariidae, which apparently represent an almost
direct continuation of the aporrhaid trend of evolution. It is of considerable
interest, since Struthiolaria has not hitherto been investigated in life, to find
Yonge's hypothetical conclusion actually realized in the closest living relatives
of the Aporrhaidae.
In the digestive system Struthiolaria shows in comparison with Aporrhais
a number of structural advances associated with ciliary feeding. The alimentary canal of Aporrhais (Yonge, 1937) examined by the present writer from
fixed material has an essentially similar plan to that of Struthiolaria] the
foregut, however, is a good deal more generalized, and the condition of the
digestive and other systems indicates that the Aporrhaidae may have given
rise fairly directly both to the Struthiolariidae and to the somewhat less
closely related Strombidae. The buccal bulb is much less reduced than in
Struthiolaria, and the radula—while already small—remains large enough for the
long marginal teeth to be employed with thejaws in seizing particles. The anterior
oesophagus is much wider than in Struthiolaria, and the mid-oesophagus
retains as in the Strombidae a long cylindrical crop traversed by the ciliated
glandular food channel, ventral in position following torsion. The salivary
glands remain as large lobulated masses within the trunk cavity, sending forward through the nerve ring a pair of long ducts which run along the oesophagal roof to the pharynx. The stomach and style sac complex of Aporrhais
is closely similar to that of Struthiolaria, the figure of Yonge (1937) requiring
correction by the transposition of the captions of the oesophagus and anterior
digestive diverticulum.
Struthiolaria possesses further specializations upon the aporrhaid plan,
especially in the nervous system, and the reproductive organs and life-history.
The Aporrhaidae are a somewhat ancient family with a world-wide Jurassic
range, and are represented by several genera in the New Zealand Cretaceous
24
Morton—Ecology and Digestive System of
(Struthioptera, Drepanochilus, Hemichenopus, Dicroloma, Perissoptera). The
first undoubted struthiolariids belong to the earliest South American Tertiary1
(Marwick, 1924).
The present writer has examined the shell and animal of Perissodonta
georgiana, of South Georgia, one of the two species of the most archaic living
genus. On both shell and dentition features this group appears to stand close
to the line of descent from an aporrhaid stock. In all essential features, however, the animal is a true struthiolariid, and the pallial organs are already fully
adapted for ciliary feeding.
ACKNOWLEDGEMENTS
The writer wishes to thank Prof. W. R. McGregor, Head of the Zoology
Department, Auckland University College, for assistance during the preparation of the thesis of which these results formed part, Mr. A. W. B. Powell,
Assistant Director, Auckland Museum, for much helpful discussion and
frequent loan of specimens, and the Director, Marine Biological Association
of the United Kingdom, Plymouth, for generously supplying preserved
material of Aporrhais. Finally, the writer has had the special advantage of
Professor C. M. Yonge's kindly criticism of the manuscript.
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GRAHAM, A., 1938. 'On a ciliary process of food-collecting in the gastropod Twritella communis Risso.' Proc. Zool. Soc. Lond. A, 108, 453.
I939- 'On the structure of the alimentary canal in the style-bearing prosobranchs.'
Ibid. B, 109, 75.
HULBERT, G. C. E. B., and YONGE, C. M., 1937. 'A possible function of the osphradium in
the Gastropoda." Nature, 139, 840.
HUTTON, F. W., 1882. 'Notes on the structure of Struthiolaria papulosa'. Trans. N.Z. Inst.,
15, 117.
MACMUNN, C. A., 1900. 'On the gastric gland of Mollusca and decapod Crustacea.' Phil.
Trans. Roy. Soc. B, 193.
MANSOUR, K., 1946. 'Food and digestive organs of lamellibranchs.' Nature, 158, 378.
MAECTN, T., 1784. The Universal Conchologist. London.
MARWICK, J., 1924. 'The Struthiolariidae.' Trans. N.Z. Inst., 55, 161.
OLIVER, W. R. B., 1923. 'Marine littoral plant and animal communities in New Zealand.'
Ibid., 54, 496.
ORTON, J. H., 1912. 'The mode of feeding of Crepidula with an account of the currentproducing mechanism in the mantle cavity, and some remarks on the mode of feeding in
gastropods and lamellibranchs.' J. mar. biol. Assoc. U.K., 9, 444.
POWELL, A. W. B., 1937. 'Animal communities of the sea bottom in the Auckland and Manukau Harbours.' Trans. Roy. Soc. N.Z., 66, 354.
QUOY and GAIMARD, 1833. Voyage autour du tnonde de I'Astrolabe, 1826-29. Zoologie. Illustrations, vol. i.
THIELE, J., 1931. Handbuch der systematischen Weichtierkunde, I. Jena, Fischer.
YONGE, C. M., 1923. 'Studies on the comparative physiology of digestion. I. The mechanism
of feeding, digestion and assimilation in the lamellibranch Mya.' Brit. Journ. exp. Biol.,
1,15.
1926. 'The digestive diverticula in the lamellibranchs.' Trans. Roy. Soc. Edin., 54,
7O31932. 'Notes on feeding and digestion in Pterocera and Vermetus, with a discussion on
the occurrence of the crystalline style in the Gastropoda.' Sci. Repts. Gt. Barrier Reef
Exped. 1928-1929, Brit. Mus. (Nat. Hist.), 1, 259.
Struthiolariidae {Gastropoda)
25
YONGE, C. M., 1935. 'On some aspects of feeding and digestion in ciliary feeding animals.' J.
mar. biol. Assoc. U.K., 20, 341.
1937- 'The biology ot Aporrhais pes-pelicani, Linn, and A. serresiana (Mich.).' Ibid.,
21,687.
1938. 'Evolution of ciliary feeding in the Prosobranchia with an account of feeding in
Capulus ungaricus.' Ibid., 22, 453.
1946. 'On the habits of Turritella communis Risso.' Ibid., 26, 377.
1947- 'The pallial organs in the aspidobranch Gastropoda and their evolution throughout the Mollusca.' Phil. Trans. Roy. Soc. B, 232, 443.