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VOL. 12 1973

MALACOLOGIA

International Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie
Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

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MALACOLOGIA, VOL. 12

CONTENTS

М. В. CARRIKER and Н. Н. CHAUNCEY

Effect of carbonic anhydrase inhibition оп shell penetration

by the murieimd gastropod! Охоза рт сте ns 2) ose
M. CASTAGNA and P. CHANLEY

Salinity tolerance of some marine bivalves from inshore

and estuarine environments in Virginia waters on the

westernÍMidatlanticicoastist. о one cote ER CO
J. N. CATHER

Regulation of apical cilia development by the polar lobe of

MyanassolGastropoda: Nassariidae) an a... u. „ae ee
P. T. CLAMPITT

Substratum as a factor in the distribution of pulmonate

Snalls=ın,Douslas’Take,; Michigan... er a see ео ee memes
Е. 5. DEMIAN and Е. YOUSIF

Embryonic development and organogenesis in the snail

Marisa cornuarietis (Mesogastropoda: Ampullariidae).

rGeneraloutlinesiofdevelopmentens Qt ое ее
Е. 5. DEMIAN and Е. YOUSIF

Embryonic development and organogenesis in the snail

Marisa cornuarietis (Mesogastropoda: Ampullariidae).

Ш. Development of the’alimentary System в 2 SO ne
Е. S. DEMIAN and Е. YOUSIF

Embryonic development and organogenesis in the snail

Marisa cornuarietis (Mesogastropoda: Ampullariidae).

Ш. Development of the circulatory and renal systems............
Е. 5. DEMIAN and Е. YOUSIF

Embryonic development and organogenesis in the snail

Marisa сотпиатей$ (Mesogastropoda: Ampullariidae).

IV. Development of the shell gland, mantle and

TESMTALO OT ans nr. Mi, о а O ЗО
Е. а. DRISCOLL and D. Е. BRANDON

Mollusc-sediment relationships in northwestern Buzzards

Bay Massachusetts, USHA.) LU A. ee ee ae Thin ae to cc ot
E. FISCHER-PIETTE and D. VUKADINOVIC

Sur les mollusques fluviatiles de Madagascar. .................

MALACOLOGIA, VOL. 12

CONTENTS (cont.)

M. J. IMLAY

Effects of potassium on survival and distribution of

FPOSDWALOT MUSSCl Gy. co... acc. e's en oies es ee oe оо ое 97
M. L. M. LE PENNEC

Morphogenése de la charniere chez 5 especes de Veneriidae........ 225

B. MORTON

Some aspects of the biology and functional morphology of
the organs of feeding and digestion of Limnoperna fortunei
(Dunker) (Bivalvia: Mytilacea). „no... « a aS ER 265

S. K. PIERCE

The rectum of “Modiolus” demissus (Dillwyn) (Bivalvia:

Mytilidae): А clue to solving a troubled taxonomy ............... 283
R. H. POHLO

Feeding and associated functional morphology in Tagelus

californianus and Florimetis obesa (Bivalvia: Tellinacea).......... 1

W. F. PONDER
The origin and evolution of the Neogastropoda ............... 2.1298

G. WIUM-ANDERSEN

Electrophoretic studies on esterases of some African
Bromphalaria spp. (Planorbidae) ser сн. un ec ae 115

im, oe Раб, =

BOL. 12 мо 1 MUS. COMP. ZOOL, 19723
LIBRARY
AUG 10 1913
HARVARD

UNIVERSITY,

rnational Journal of Malacology

в is у . .
Revista Internacional de Malacologia
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Journal International de Malacologie

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12 Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

Editor-in-Chief
J. В. BURCH

Associate Editor
R. NATARAJAN

Secretaries
E. PERISHO KAWAMURA
J. WHITE-RUDOLPH

Editorial Office

Museum of Zoology
University of Michigan
Ann Arbor, Michigan 48104
U.S.A.

EDITORIAL BOARD

| O) ACOCSY. Budapest, Hungary

. E. BINDER, Geneva, Switzerland

. В. BOETTGER, Braunschweig, Germany
. Н. CLARKE, Ottawa, Canada

. 5. DEMIAN, Cairo, Egypt

. J. DUNCAN, Liverpool, U.K.

A. FILATOVA, Moscow, U.S.S.R.
FISCHER-PIETTE, Paris, France
FRANC, Paris, France

FRETTER, Reading, U.K.

. GALTSOFF, Woods Hole, U.S.A.

V. GROSSU, Bucharest, Rumania
HABE, Tokyo, Japan

. D. HARRISON, Waterloo, Canada

. HATAI, Sendai, Japan

. A. HOLME, Plymouth, U.K.

. HUBENDICK, Göteborg, Sweden

‚ Р. KANAKOFF, Los Angeles, U.S.A.

. М. KEEN, Stanford, U.S.A. ;
M. A. KLAPPENBAC H, Montevideo, Uruguay
Y. KONDO, Honolulu, U.S.A.

T. KURODA, Kyoto, Japan

Н. LEMCHE, Cópenhagen, Denmark
AKLILU LEMMA, Addis Ababa, Ethiopia
J. LEVER, Amsterdam, The Netherlands

A. LUCAS, Brest, France

N. MACAROVICI, Iasi, Rumania

D. Е. MeMICHAEL, Sydney, Australia

i. MEIER- BROOK, Tubingen, Germany

11

ее

MALACOLOGIA |

А. ZILCH, Frankfurt, Germany _

С: J. BAYNE ANNE GISMANN

Managing Editor
S. K. WU

Subscription Office

Department of Mollusks
Academy of Natural Sciences
Philadelphia, Pennsylvania 19103
ISA:

J. Е. MORTON, Auckland, New Zealand

W. К. OCKELMANN, Helsinggr, Denmark

N. ODHNER, Stockholm, Sweden

J. OKLAND, Oslo, Norway

W. L. PARAENSE, Brasilia, Brazil

J. J. PARODIZ, Pittsburg, US Ar

С. M. PATTERSON, Ann Arbor, U.S.A.

W. F. PONDER, Sydney, Australia

А. W. В. POWELL, Auckland, New Zealand

R. D. PURCHON, London, U.K.

C. P. RAVEN, Utrecht, The Netherlands

O. RAVERA, Ispra, Italy

C.F.E, ROPER, M cion Die USA.

N. W. RUNHAM, Bangor, U.K.

5. С. SEGERSTRALE, Helsinki, Ein

R. V. SESHAIYA, Porto Novo, India ben:

F. STARMÜHLNER, Wien, Austria

J. STUARDO, Concepcion, Chile

Е. TOFFOLETTO, Milano, Italy A

W. $. S. VAN BENTHEM JUTTING, к
Domburg, The Netherlands —

J. A. VAN EEDEN, Potchefstroom, S

С. О. VAN REGTEREN ALTENA, |
Neth. ae

В. В WILSON, Perth, Australia =

C. M. YONGE, Edinburgh, U.K.

H. ZEISSLER, Leipzig, G. О. В.

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101 Mystic

International Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie
Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

UNITAS MALACOLOGICA EUROPAEA

RESOLUTION

The Unitas Malacologica Europaea, representing malacologists and conchologists
in Europe, is much concerned by the rapidly increasing destruction of the natural
environment.

It therefore supports all measures being taken to avoid and reduce pollution.

Unitas Malacologica Europaea urges all who are concerned throughout the
world to accept responsibility for ensuring the future existence of Mollusca and
their habitats.

We, the members of Unitas Malacologica Europaea, realise that this will neces-
sitate a curtailment of collecting activities, but we are sure that, as responsible
naturalists, all conchologists and malacologists will wish to support appropriate
conservation measures.

Unitas Malacologica Europaea therefore urges that for all purposes whatsoever
only about the minimum number of specimens should be collected.

Observations as well as photography of living specimens in their natural
habitats may be a much more rewarding activity than mere collecting. This
applies equally to the work of the amateur and the professional.

Such an approach to field studies would result in the acquisition of much of the
information which is so urgently needed to ensure the success of the efforts
being made to conserve these animals. The European national malacological

societies fully associate with this resolution and will publish it in their periodicals.

Dr. Oliver E. PAGET
Secretary

Erratum, Vol. 11, No. 2, page 378. The legends for Figs. 14 and 15 in the paper by F.R. Bernard
were mistakenly transposed.

MALACOLOGIA, 1973, 12(1): 1-11

FEEDING AND ASSOCIATED FUNCTIONAL MORPHOLOGY
IN TAGELUS CALIFORNIANUS
AND FLORIMETIS OBESA (BIVALVIA: TELLINACEA)

Ross H. Pohlo

Department of Biology
California State University at Northridge
Northridge, California 91324, U.S.A.

ABSTRACT

A study was made comparing 2 species, Tagelus californianus (Conrad, 1837) and
Florimetis obesa (Deshayes, 1855), with other members of the superfamily Tellinacea.
The nature of their feeding was investigated and an attempt was made to relate aspects
of their morphology to feeding behavior.

Field and laboratory studies, particularly of the behavior of the inhalant siphon, and
an analysis of mantle cavity and stomach contents were performed to ascertain the mode
of feeding of these species. Although many Tellinacea are deposit feeders, these 2 species
feed primarily on suspended particles. Deposits, however, can and do fall into the
inhalant siphons. This is more prevalent in Florimetis obesa than in Tagelus califor-
nianus.

Tagelus californianus resembles suspension feeding bivalves by having large ctenidia
which possess well developed marginal grooves, the outer demibranch is not upturned,
the dorsal hood is large, incipient straining tentacles exist on the inhalant siphon, the
animal is upright in the burrow and a mantle fold is lacking. The only major features
common to this species and deposit feeders are separated siphons.

Florimetis obesa resembles deposit feeders by having upturned outer demibranchs,
the presence of a mantle fold, separate siphons which lack straining tentacles and the
organism lies on its side. It resembles suspension feeders by having relatively large

ctenidia.

INTRODUCTION

As has been shown (Pohlo, 1969) there
has been some confusion concerning the
type of feeding that occurs in the super-
family Tellinacea. Yonge (1949) regarded
the Tellinacea as fundamentally deposit
feeders; later other authors such as Morton
(1960) and Jorgensen (1966) repeated this
assertion. Meanwhile, several authors
(Holme, 1961; Brafield & Newell, 1961;
Purchon, 1963; Wade, 1965; Pohlo, 1966,
1967, 1969; Maurer, 1967; and Reid &
Reid, 1969) have shown that suspension
feeding also occurs in this superfamily. It
is of interest, therefore, to examine other
species of tellinaceans to ascertain the type
of feeding they employ and to note, where
possible, which features of anatomy and
behavior may be associated with a par-
ticular type of feeding. To this end the

morphology and feeding behavior of
Tagelus californianus (Conrad, 1837) and
Florimetis obesa (Deshayes, 1855) were
studied and compared with а typical
deposit feeding tellinacean such as
Macoma nasuta and a suspension feeder
such as Donax gouldi.

MATERIALS AND METHODS
OF STUDY

Florimetis obesa and Tagelus califor-
nianus were collected at Newport Bay and
Mugu Lagoon in Southern California. T.
californianus was found in various fine to
medium grained substrata and occurs in
great abundance in the banks of small tidal
channels. As described by Weymouth
(1920) and Yonge (1952) the animal
occurs upright in a permanent burrow that
can reach a depth of 50 cm. Its range is
from Humbolt Bay, California to Panama

bo

В. Н. POHLO

lem

FIG. 1. Organs of the mantle cavity of Tagelus californianus viewed from the right side. Right valve and mantle
lobe removed. Arrows indicate the direction of particle movement. Dotted arrows indicate movement on the
underside of the surface. AA—anterior adductor; CM—cruciform muscle; ES—exhalant siphon; F—foot;
ID—inner demibranch; IS—inhalant siphon; L—ligament; L P—labial palp; ML—mantle lobe; OD—outer
demibranch; PA—posterior adductor; PR—posterior retractor.

(McLean, 1969).

Florimetis obesa was found intertidally
in clean sand as well as in sand that
contains some rocks or shell fragments.
The adult organisms live about 15-25 cm
below the surface where they lie on their
left side. They have a geographic range
from Point Conception, California to
Magdalena Bay, Baja California, Mexico
(McLean, 1969).

Feeding behavior as reflected by the
position and movements of the inhalant
siphon was observed in the field, by using
an underwater viewer, and on specimens
maintained in laboratory aquaria. Move-
ment of particles in the mantle cavity was
observed by removing the right valve,
along with its mantle lobe, and placing
fine carborundum or carmine particles on
various parts of the anatomy.

To study the stomach contents of these
organisms, the animals were dug in the
field, the mantle cavity was opened, and
the body was immediately preserved. The
alimentary canal was later dissected out
and the anatomy of the stomach and the
nature of its contents were then observed.
The movement of particles in the stomach
of live specimens was noted by opening
the stomach from the dorsal aspect and
placing carmine or carborundum particles
in various areas.

FUNCTIONAL MORPHOLOGY

External morphology

Tagelus californianus (Fig. 1). This
species is highly elongated being about 4
times as long as it is high. Large specimens
are about 11 cm long and 2.7 cm high. The
shell is covered by a brownish yellow
periostracum that is often extensively worn
in larger specimens. The ligament is exter-
nal, thin and elongated, reaching a length
of about 1.9 cm on the large specimens.

Florimetis obesa (Fig. 2). In this species
the shell is somewhat circular in outline,
large specimens being about 7 cm long
and 6 cm high. The valves are
asymmetrical; the left valve has 2 grooves
running from the umbo to the posterior
edge, a condition that is absent in the right
valve. The right valve is indented slightly
along the ventral margin while the left
valve is correspondingly convex in this
region. Both valves are notched in the area
of the siphons and both have rather heavy
growth rings. The ligament is recessed
internally in a deep pit, but can be seen
from an external dorsal view. It is ap-
proximately 1.1 cm long on the large
specimens.

Mantle cavity
Tagelus californianus (Fig. 1). The

FEEDING IN TAGELUS AND FLORIMETIS 3

OD
fee

№
N

FIG. 2. Organs of the mantle cavity of Florimetis obesa viewed from the right side. Right valve and mantle lobe
removed. Arrows indicate the direction of particle movement. MF—mantle fold. For other abbreviations see

Fig. 1.

3

A B С

FIG. 3. Transverse section of the gills of A. Tagelus californianus. В. Florimetis obesa, and С. Macoma nasuta.
Arrows indicate direction of major currents, solid circles indicate currents toward the mouth. Stippled area is the

body and foot.

demibranchs are large and _ elongated
while the labial palps are small. The
relationship of the ctenidia and labial
palps is of category Ш, i.e., the anterior
filaments of the inner demibranch are not
inserted into the distal oral groove (see
Stasek, 1963). Well developed marginal
grooves are present on both demibranchs
(Fig. 3A). As in most other tellinaceans a

FIG. 4. Inhalant siphons of A. Tagelus californianus and B. Florimetis obesa.

cruciform muscle is present but a mantle
fold, present in Florimetis obesa and many
others, is lacking.

The ciliary feeding and rejection
currents are shown in Fig. 1. Particles
move in a ventral direction on the outer
demibranch. When they reach the ventral
edge of this structure, they move in 1 of 3
different directions. Some particles enter

4 R. H. POHLO

the marginal groove and move toward the
mouth. Others move ventrally onto the
inner demibranch. The material may also
move under the outer demibranch, then
dorsally toward a food tract on the axis and
then move toward the mouth (Fig. 3A).

Once particles reach the labial palps,
they move either in an anterior direction,
perpendicular to the long axis of the palp
plications, toward the mouth, or in a
posterior direction parallel to the
plications. Small particles combine these 2
movements, i.e., move a short distance
parallel to the plication, then change
directions and move perpendicularly to
the plication. Rejected material moves to
the anterior margins of the labial palps and
then moves ventrally towards the foot.
Eventually these particles accumulate as
pseudofeces below the base of the inhalant
siphon.

Florimetis obesa (Fig. 2). The
demibranchs are quite large while the
labial palps vary in size from specimen to
specimen. The labial palps are shown
approximately at their maximum size in
Fig. 2. The gill labial palp association is of
type Ш, as described above for Tagelus
californianus. The outer demibranch is
upturned as shown in Fig. 3B. From this
figure it can be seen that although the
outer-demibranch is upturned, it is not
flattened against the body as in Macoma
nasuta (Fig. 3C). The plications are ex-
tremely fine on both demibranchs. As in
the case of T. californianus a cruciform
muscle is present.

Ciliary currents are shown in Fig. 2.
Material moves from the outer
demibranch to the ctenidial axis. Here the
particles move either in an anterior direc-
tion toward the mouth or they continue
ventrally on the inner demibranch to a
very small marginal groove and then
toward the mouth. Particles are then
further sorted on the labial palps.
Accepted particles can move either
perpendicular (i.e., in a dorsal direction) or
parallel (i.e., in a posterior direction) to the
long axis of the palp plications. Rejected
materials move to the anterior edge of the
labial palps and then ventrally on to the

foot. From here, these particles move in a
posterior-ventral direction and eventually
accumulate beneath the mantle fold in
what Yonge (1949) terms the waste canal.

Siphons

Tagelus californianus (Fig. 4A). The
siphons are separate as they are in
Florimetis obesa. The exhalant siphon
contains 6 small blunt lobes, as in many of
the Tellinacea. The entrance to the in-
halant siphon also has 6 lobes but on these
lobes are rudimentary straining tentacles.
A similar condition was described but not
illustrated for Solecurtus scopula by Yonge
(1949).

Florimetis obesa (Fig. 4B). The inhalant
siphon has 6 lobes that are drawn out into
finger-like processes. There are no ten-
tacles present on these lobes. The exhalant
siphon is devoid of lobes.

Stomach

In both Tagelus californianus and
Florimetis obesa the stomach is
characterized by the major typhlosole (T)
and its corresponding intestinal groove
(IG) entering both the right and left caeca
(RC, LC). This feature classifies both of
these species as possessing stomach type V
(gastropemptan, see Purchon, 1960).

Tagelus californianus (Fig. 5). The dor-
sal hood (H) is quite large and elongated,
being a prominent feature of the left side
of the stomach. There is also an extension
of the stomach on the right-posterior side,
which appears somewhat similar to what
Purchon (1963) describes as a depression
(D) on the posterior wall of Egeria radiata.
It is much less drawn out to the side than
the dorsal hood but it has a much greater
ventral extent. The function of this embay-
ment appears to be for temporary storage
of sand grains, for they are often located in
this area. Grooves and ridges (G) are
located near the entrance to and deep
within this structure. There is an appendix
(X) resembling a cluster of grapes located
posteriorly, which also contains sand
grains,

The major typhlosole and intestinal
groove pass anterio-dorsally from the

FEEDING IN TAGELUS AND FLORIMETIS 5

ST RG O
; 4 | He

FIG. 5. Stomach of Tagelus californianus. Gastric shield removed. Arrows indicate direction of particle
movement. Dotted arrows indicate movement on the underside of the structure. D—depression; G—irregular
grooves and lobes; H—dorsal hood; IG—intestinal groove; LC—left caecum; LP—left pouch; MG—mid gut;
O—oesophagus; RC—right caecum; RG—rejection groove; SA—sorting area; SS—style sac; ST—shield tract;
T—major typhlosole; T—minor typhlosole; X—appendix.

RG О

Imm

FIG. 6. Stomach of Florimetis obesa. Gastric shield removed. Arrows indicate direction of particle movement.
Dotted arrows indicate the movement on the underside of a surface. PP—posterior pouch; SG—sorting groove;
XO—opening to appendix. For other abbreviations see Fig. 5.

6 В. Н. POHLO

midgut (MG) into the stomach and enter
the right caecum. They then enter the left
caecum dorsally from the right side and go
very deeply into this structure. In both
caeca the typhlosole is upcurled and sends
flares into the caecal ducts to form a type
C sorting mechanism (see Reid, 1965). A
minor typhlosole (t) originates at the
beginning of the midgut and terminates
on the posterio-ventral floor of the
stomach. The style sac (SS) and midgut are
conjoined.

The dorsal hood receives a curved por-
tion of the gastric shield, as does the left
pouch (LP). There is a sorting area, the
shield tract (ST), in this structure and
particles move out of the dorsal hood via a
rejection groove (RG). Particles move from
the rejection groove to the intestinal
groove and then to the midgut. This
condition was also found by Reid & Reid
(1969) for 8 species of Macoma. The left
pouch is also large and it has a sorting area
on its ventral side. It contains about 6
openings to the digestive diverticulum.

Florimetis obesa (Fig. 6). The stomach
of this species is similar to that of Tagelus
californianus. The main difference is that
F. obesa has a prominent triangular struc-
ture on the posterior margin near the
appendix (X). A portion of the gastric
shield enters this structure and, like the
appendix, contains sand grains. This struc-
ture is here referred to as the posterior
pouch (PP). This structure seems to be
more involved in anchoring the gastric
shield than as a temporary storage area for
sand grains.

Other differences from the stomach of
Tagelus californianus are: the appendix
has finger-like extensions; the dorsal hood
(H) is smaller and contains no sorting area,
and the right depression is absent, while a
posterior sorting groove is present.

FEEDING OBSERVATIONS
The behavior of the siphons was quite
different in the 2 species. The inhalant
siphons of many specimens of Tagelus
californianus were observed to be т
motion much of the time. The species were
observed in a stream-like portion of Mugu

Lagoon where the water has a unidirec-
tional flow either coming in or going out
with the tide. Specimens of T. califor-
nianus would thrust the inhalant siphon
against the direction of water flow and curl
back the tentacles exposing а trumpet-
shaped opening to these currents. In this
position the siphon would be about 1-3
mm above the level of the substratum.
After 30 sec. to 1 min. the siphon would
move below the level of the substratum.

‘Subsequently it re-emerges and this

behavior is repeated. When withdrawn
into the burrow, the siphons are partially
closed. At this point the incipient tentacles
(Fig. 4A) may help to keep deposits from
entering. These tentacles, of course, can
perform no straining function while the
siphon is open wide, and clumps of algae
about 1-2 mm in diameter that were
carried along by the current were seen to
enter the siphons. At no time did the
animal press the inhalant siphon to the
substratum and ingest deposits, and only
material suspended in the water column
was seen to enter.

In most specimens of Florimetis obesa
the inhalant siphon was oriented just
below the level of the substratum. Others
held this siphon slightly above the level of
the substratum and in a few it was below
the substratum in a small pit. The inhalant
siphon was not active, remained in one
spot and was usually partially closed. The
species was never observed actively in-
gesting deposits as is commonly seen in
Масота пазиа (MacGinitie, 1935),
Масота secta (Reid & Reid, 1969), and in
species of Tellina, Macoma, Scrobicularia
and Abra (Yonge, 1949).

The mantle cavity and stomach of
Tagelus californianus contained only a few
sand grains. The stomach contained many
diatoms and a lot of green debris, probably
derived from various algae other than
diatoms. The feces were compact and
contained a few sand grains.

Fine sand grains were usually present in
the mantle cavity of Florimetis obesa
especially in the area of pseudofeces ac-
cumulation just below the mantle fold.
The gills were usually free of sand but

FEEDING IN TAGELUS AND FLORIMETIS ih

there was some present at the margins of
the labial palps. The stomach often con-
tained sand. From visual estimates the
amount of sand was less than that in
deposit feeders such as Macoma secta or
Macoma nasuta, but more than in
organisms such as Tagelus californianus or
Donax gouldi. The stomach also contained
diatoms, flagellates and а considerable
amount of green debris. The feces were
well compacted and contained a few sand
grains.

DISCUSSION

The study of the behavior of the in-
halant siphon and of the contents of the
mantle cavity and alimentary tract show
that material suspended in the water
column rather than deposits is the main
source of food in Florimetis obesa and
Tagelus californianus. The orientation of
the siphons in T. californianus does not
permit a large quantity of deposits to drop
passively into the inhalent opening.
Although the siphons are often wide open
they are slightly above the substratum
allowing only suspended material to enter.
The paucity of sand in the mantle cavity
and stomach also supports the view that
feeding is on suspended material.

In Florimetis obesa the siphons are flush
with or just below the substratum and this
allows deposits to fall into the inhalant
opening, the tentacles being incapable of
rejecting this material. An analysis of the
mantle cavity and stomach contents is
consistent with this view and shows that
deposits can and do fall into the inhalant
aperture and find their way into the
stomach. But the quantity of diatoms and
algae in the stomach indicates that most of
the food comes from material suspended in
the water. Both of these species, therefore,
would be classified as non-selective
suspension feeders with Tagelus califor-
nianus ingesting less and F. obesa in-
gesting more deposits.

Having established the feeding type of
these organisms it is of interest to see
which features of morphology and
behavior are associated with deposit or
suspension feeding.

Yonge (1949) has indicated that the
following features are associated with
deposit feeding (some of these features are
illustrated in Fig. 7A, which shows
Macoma nasuta, a deposit feeding
tellinacean): i) the presence of separate
inhalant and exhalant siphons and the
absence of true straining tentacles on the
inhalant siphon; ii) a mantle fold is present
and this allows a powerful flow of water to
continue but prevents the pseudofeces
from fouling the ctenidia; iii) there
appears to be a tendency to keep the gill as
small as possible in view of the problems
presented by a large influx of material; iv)
the outer demibranch is upturned to pre-
vent clogging when immense quantities of
bottom material are taken in; v) a marginal
groove is absent and this is associated with
the need to reduce the volume of material
carried forward.

To this list I would add that where the
gills are small in such deposit feeding
forms as Macoma secta, M. nasuta, and M.
balthica the labial palps are large. Also the
deposit feeding Tellinacea lie on their side
in the substratum.

According to Yonge (1949) suspension
feeders have some of the following
characteristics (some of the general
features are illustrated in Fig. 7B, which
depicts Donax gouldi, a suspension
feeding tellinacean): straining tentacles
present on the inhalant siphon; the lack of
a mantle fold, indicating a gentle inflow of
water, and a large dorsal hood. Also, from
the above mentioned features that are
correlated with deposit feeding I reason
that the presence of a marginal groove(s),
large ctenidia with an outer demibranch
that is not reflected, small labial palps and
an upright position in the burrow are also
features associated with suspension
feeding. These features are noted in Donax
gouldi (Pohlo, 1967) and other non-
tellinacean suspension feeders such as
Protothaca, Treses, Chione, ес.

This study shows that Tagelus califor-
nianus has none of the features that would
be directly associated with deposit
feeding, with the exception of separate
siphons, a condition that is universal in the

8 R..H..POHLO

FIG. 7. Generalized diagram showing some features of a deposit feeder (A) and a suspension feeder (B). A.
Macoma nasuta. Note the up-turned outer demibranch (OD), mantle fold (MF) and the size relations of the
demibranchs (ID and OD) compared with the labial palps (LP). B. Donax gouldi. Note that the outer
demibranch (OD) is not upturned, the lack of a mantle fold and the size relations of the demibranchs (ID and
OD) compared with the labial palps (LP). For other abbreviations see Fig. 1.

Tellinacea. The features it shares with
suspension feeders are: large gills, outer
demibranch not upturned; relatively small
labial palps; the presence of marginal
grooves; straining tentacles (although in-
cipient); the absence of a mantle fold, and
a large dorsal hood. The organism is in an
upright position in the burrow.

Florimetis obesa resembles a deposit
feeder by having the outer demibranch
upturned. However, it is not flattened
against the body as in Macoma secta or M.
nasuta (compare Fig. 3B and 3C). A
mantle fold is present while straining
tentacles on the inhalant siphon are ab-
sent. Also, these species lie on their side.

FEEDING IN TAGELUS AND FLORIMETIS 9

This species resembles a suspension
feeder by having relatively large ctenidia,
and a small marginal groove is present on
the inner demibranch. In many specimens
the labial palps are large but in others they
are small. Therefore, this characteristic
cannot be associated solely with deposit or
suspension feeding.

ACKNOWLEDGEMENTS

I wish to thank Dr. Marvin Cantor and
Dr. Joseph Moore for reading the
manuscript.

LITERATURE CITED

BRAFIELD, A. W. & NEWELL, G. E., 1961,
The behavior of Macoma БаШиса (L.) J.
mar. biol. Assoc. U. K., 41: 81-87.

HOLME, №. A., 1961, Notes on the mode of
life of the Tellinidae (Lamellibranchia).
J. mar. biol. Assoc. U.K., 41: 699-703.

JORGENSON, C. B., 1966, Biology of Suspen-
sion Feeding. Pergamon Press, New York.
357 p.

MACGINITIE, G. E., 1935, Ecological aspects
of a California marine estuary. Amer. М.
Natur., 16: 629-765.

MAURER, D., 1967, Mode of feeding and diet,
and synthesis of studies on marine pelecy-
pods from Tomales Bay, California. Veliger,
10:72-76.

McLEAN, J. H., 1969, Marine shells of south-
ern California. Los Angeles County Museum
of Natural History. Science Series 24,
Zoology No. 11 (104 р, 54 text fig).

MORTON, J. E., 1960, Mollusca: An Intro-

POHLO, R. H., 1966, A note on the feeding
behavior in Tagelus californianus (Bivalvia:
Tellinacea). Veliger, 8: 225.

POHLO, R. H., 1967, Aspects of the biology of
Donax gouldii and a note on the evolution
in Tellinacea (Bivalvia). Veliger, 9: 330-337.

POHLO, R. H., 1969, Confusion concerning
deposit feeding in the Tellinacea. Proc.
malacol. Soc. London, 38: 361-364.

PURCHON, R. D., 1960, The stomach in the
Eulamellibranchia: stomach types IV and У.
Proc. 001. Soc. London, 35: 431-389.

PURCHON, R. D., 1963, A note on the biology
of Egeria radiata Lam. (Bivalvia, Don-
acidae). Proc. Malacol. Soc. London, 35:251-
DL:

REID, R. G. B., 1965, The structure and funct-
ion of the stomach in bivalve molluscs. J.
Zool., 147: 156-184.

REID, R. G. B. & REID, A., 1969, Feeding
processes of members of the genus Macoma
(Mollusca: Bivalvia) Can. J. Zool., 47: 649-
657.

STASEK, С. R., 1963, Synopsis and discussion
of the association of ctenidia and labial palps
in the bivalved Mollusca. Veliger, 6(2):
91-97.

WADE, B. A., 1965, Notes on the Ecology of
Donax denticulatus (Linné). Proc. Gulf
Caribb. Fish. Inst., 17th Annual Session,
p 36-41.

WEYMOUTH, F. W., 1920, The edible clams,
mussels and scallops of California. Fish.
Bull., Sacramento, no. 4.

YONGE, C. M., 1949, On the Structure and
Adaptations of the Tellinacea, Deposit-
feeding Eulamellibranchia. Phil Trans. Roy.
Soc., B., 234: 29-76.

YONGE, C. M., 1952, Studies on Pacific
coast mollusks. IV. Observations on Siliqua
patula Dixon and on the evolution within the

duction to their form and functions. Harper. Solenidae. Univ. Calif. Publs. Zool., 55:
232 p. 421-438.
ZUSAMMENFASSUNG

NAHRUNGSAUFNAHME UND FUNKTIONALE MORPHOLOGIE
DES ERNAHRUNGSTRAKTES BEI TAGELUS CALIFORNIANUS
UND FLORIMETIS OBESA (BIVALVIA: TELLINACEA).

R. H. Pohlo

Eine Untersuchung wurde vorgenommen, Tagelus californianus (Conrad 1837) und
Forimentis obesa (Deshayes 1855) mit anderen Arten der Oberfamilie Tellinacea
zu vergleichen. Ihre Nahrungsaufnahme wurde beobachtet und versucht, Einzelziige
ihrer Morphologie mit ihren Ernahrungsgewohnheiten in Verbindung zu bringen.

10

В. Н. POHLO

Gelánde- und Laboratoriumsbeobachtungen, besonders der Funktion des
Branchialsiphos, und Untersuchungen der Mantellhöhle und des Mageninhaltes wurden
vorgenommen, um die Art Nahrungsaufnahme bei diesen Arten festzustellen. Obwohl
viele Tellinaceen Schlammfresser sind, nehmen diese zwei Arten hauptsächlich suspen-
dierte Teilchen auf. Allerdings tritt auch Schlamm in den Branchialsipho ein. Dies
geschieht bei Florimetis obesa in starkerem Masse als bei Tagelus californianus.

Tagelus californianus ähnelt anderen suspendierte Partikel fressenden Muscheln
durch seine grossen Kiemen, die gut entwicktelte Marginalrinnen besitzen. Die äussere
Kieme ist nicht aufwärts gedreht. Die Rückenkappe ist gross, an dem Branchialsipho
stehen Tentakel, die das einströmende Wasser seihen, das Tier steht autrecht in seiner
gegrabenen Höhle und eine Mantelfalte fehlt. Das einzige wichtige Merkmal, das
Schlammfresser mit dieser Art gemeinsam haben, sind getrennte Siphonen.

Florimetis obesa ahnelt den Schlammfressern dadurch, dass sie aufwärts gewendete
äussere Kiemen hat, eine Mantelfalte, getrennte Siphonen ohne seihende Tentakel, und
dass der Organismus auf der Seite liegt. Den Arten, die suspendierte Partikel
aufnechmen, ähnelt sie nur dadurch, dass sie verhaltnismass ig grosse Kiemen hat.

Нд.

RESUME

ALIMENTATION ET MORPHOLOGIE FONCTIONNELLE
ASSOCIEE CHEZ TAGELUS CALIFORNIANUS
ET FLORIMETIS OBESA (BIVALVIA: TELLINACEA).

R. H. Pohlo

Une étude comparative a été faite entre 2 espèces, Tagelus californianus (Conrad
1837) et Florimetis obesa (Deshayes, 1855) avec d'autres représentants de la supertamille
des Tellinacea. La nature de leur alimentation a été recherchée et on a tenté d'établir
une relation entre leur morphologie et leur mode de nutrition.

Des études dans la nature et au laboratoire, en particulier sur le comportement du
siphon inhalant et l'analyse de la cavité palléale et des contenus stomacaux ont été
effectués pour s'assurer du mode alimentaire de ces espèces. Bien que beaucoup de
Tellinacea soient des déposivores, ces 2 езрёсез se nourrissent en premier lieu de
particules en suspension. Les dépéts, cependant, peuvent tomber dans le siphon
inhalant, et effectivement le font. Ceci est plus manifeste chez Florimetis obesa que chez
Tagelus californianus.

Tagelus californianus ressemble aux bivalves suspensivores par ses grandes cténidies
qui possedent des sillons marginaux bien développés, la demibranchie externe поп
relevée, le capuchon dorsal développé, l'existence d'une ébauche de tentacules filtrants
sur le siphon inhalant, le fait que l'animal est placé verticalement dans son trou et
l'absence de bourrelet palléal. Le seul caractère important commun entre cette espèce et
les deposivores est la séparation des siphons.

Florimetis obesa ressemble aux déposivores par les demibranchies externes relevées, la
présence d'un bourrelet palléal, les siphons séparés mais sans tentacules filtreurs et le fait
que l'animal est couché sur le côté. Il ressemble aux suspensivores par ses cténidies
relativement grandes.

А
ВЕЗОМЕМ
MORFOLOGIA FUNCIONAL ASOCIADA А LA ALIMENTACION
EN TAGELUS CALIFORNIANUS Y FLORIMETIS OBESA
(BIVALVIA: TELLINACEA)
R. H. Pohlo

Este estudio compara dos especies, Tagelus californianus (Conrad), 1837 y Florimetis

FEEDING IN TAGELUS AND FLORIMETIS

obesa (Deshayes), 1855, con otros miembros de la superfamilia Tellinacea, e investiga
aspectos de sus morfologías relacionados con el comportamiento alimenticio, en estudios
de campo y laboratorio, especialmente el comportamiento del sifón inhalante, análisis de
la cavidad paleal y contenido estomacal. Aunque muchos Tellinacea se alimentan de
sedimentos, estas especies lo hacen de materiales es suspensión; sin embargo, substan-
cias de deposito pueden caer, y también se encuentran, en los sifones inhalantes. Esto
cuenta más en Florimetis obesa que en Tagelus californianus.

Tagelus californianus se asemaja a otros bivalvos que se alimentan de materias en
suspensión, por tener largos ctenidios con surcos marginales bien desarrollados,
demibranquia externa no doblada hacia arriba, largo capuchón dorsal, tentaculos
filtradores incipientes en el sifón inhalante, sin replieque paleal, y el animal se mantiene
vertical en la cavidad del substrato donde se aloja. El único, y principal caracter, común a
estos dos especies y los sedimentivoros, es la de poseer sifones separados.

Florimetis obesa se asemeja a los sedimentivoros por tener las branquias dobladas
hacia arriba, repliegue en el manto, sifones separados con tentaculos filtradores, y el
animal descansa de costado en el habitáculo. Pero, como los que se alimentan de materias
suspendidas, tienen los ctenidos relativamente grandes.

ТЛВ.

АБСТРАКТ

ПИТАНИЕ И СВЯЗАННАЯ С НИМ МОРФОЛОГИЯ TAGELUS CALIFORNIANUS
И FLORIMETIS ОВЕЗА (BIVALVIA: TELLINACEA)

Е. Хх. РОЛО

Сравнивали 2 вида: Tagelus californianus (Conrad, 1837) и Florimetis obesa
(Deshayes, 1855) с другими членами надсемейства Tellinacea. Исследована их
природа питания и сделана попытка связать аспекты их морфологии с
поведением питания.

Проведены полевые и лабораторные исследования для выяснения способа
питания этих видов и действия дыхательного сифона, сделан анализ
мантийной полости и содержимого желудков. Хотя многие ТеШтасеа питаются.
осадком, эти 2 вида первично питаются взвешенными частицами. Осадки,
однако, могут попадать и попадают в дыхательные сифоны. Это в большей
степени свойственно Florimetis obesa, чем Tagelus californianus.

Tagelus californianus напоминает двустворок-сестонофагов наличием крупного
ктенидия, снабженного хорошо развитыми маргинальными бороздами, наружным
жаберным листком, не повернутым вверх, зачаточными щупальцами на
дыхательном сифоне, вертикальным положением животного в ходе и
отсутствием мантийной скдадки. Единственный существенный признак,
общий для этого вида и для детритоедов, - раздельные сифоны.

Florimetis obesa схож с детритоедами тем, что наружный жаберный листок
его повернут вверх, имеется мантийная складка, на раздельных сифонах
отсутствуют щупальца, а само животное лежит на боку. С сестонофагами
его сближают относительно широкие ктенидии.

Z.A.F.

11

MALACOLOGIA, 1973, 12(1): 13-46

MOLLUSC-SEDIMENT RELATIONSHIPS IN
NORTHWESTERN BUZZARDS BAY, MASSACHUSETTS, U.S.A.

Egbert G. Driscoll and Dale E. Brandon!

Department of Geology, Wayne State University, Detroit, Michigan 45202
and Departmeni of Meteorology and Oceanography
University of Michigan, Ann Arbor, Michigan 48104

ABSTRACT

Four facies are defined in the Recent sediments of the north-western part of Buzzards
Bay, Massachusetts. These are characterized by differences in mean grain diameter, sor-
ting, silt-clay content and fauna. A mean grain diameter of less than 2.5ф(0.18 mm )is
characteristic of three of these facies which are found in protected areas. The fourth,
developing on current-swept bottoms, typically is composed of coarser sediments.
Calcium carbonate content of the sediment is a reflection of dead shell abundance
throughout the area.

Faunas of the 3 fine-grained facies are characterized respectively by (1) Nucula
proxima, (2) Yoldia limatula and Nassarius trivittatus and (3) Macoma tenta, Nucula
proxima, Eupleura caudata and Nassarius trivittatus. No more than 8 species compose
1% or more of the molluscan fauna in any of the 3 fine-grained facies. In the coarser
sediments of the 4th facies 11 species comprise in excess of 1% of the molluscs. Dom-
inant species in this facies are Nassarius trivittatus, Anachis avara similis, Chaeto-
pleura apiculata, Anadara transversa and Crepidula fornicata.

The distribution of more than 35 molluscan species is discussed. The majority have
hard parts which are potentially preservable. Mean grain diameter, abundance of silt
and clay, and presence of dead shells are important factors in molluse distribution.
Macoma tenta, Yoldia limatula, Nucula proxima and Solemya velum increase in abun-
dance with decreasing mean grain diameter and increasing silt-clay content of the sedi-
ment. Chaetopleura apiculata, Anadara transversa, Crassinella mactracea and many
other species increase in abundance with increasing mean grain diameter and decreasing
silt-clay content of the sediment. Greater abundance and diversity of epifaunal species
is found on bottoms having higher concentrations of dead shells.

Potential faunal-lithic associations, indicate that suspension feeding bivalves and
carnivorous gastropods are available for preservation in the coarse-grained facies. Poten-
tial fossils of the proto-graywacke, which makes up the 3 fine-grained facies, are mostly
deposit feeding bivalves.

INTRODUCTION

Relationships between benthos distribu-
tion and various characteristics of the
bottom sediment have been of interest to
ecologists for many years. Recent work in
this area includes that of Bader, 1954;
Craig & Jones, 1966; Gamulin-Brida,
1967; Parker, 1956, 1963; Peres & Picard,
1964; Purdy, 1964; Rhoads & Young,
1970; Sanders, 1958, 1960; Thorson, 1966;
and others.

The present paper examines certain of
these relationships in a shallow bay off the

Massachusetts coast. The principal in-
vertebrate group with hard parts suitable
for preservation in the fossil record in this
area is molluscs, despite the much greater
numerical abundance of such in-
vertebrates as polychaetes, unsegmented
worms, and crustaceans. The latter taxa
are of considerable ecologic and paleo-
ecologic importance, particularly as
regards reworking of the sedimentary sub-
stratum, but are unlikely to be preserved
in the fossil record except as trace fossils.
Our efforts are directed toward presenting
a picture of the distribution and sediment-

'Present address: Esso Production Research Co., P.O. Box 2189, Houston, Texas 77001

14 DRISCOLL AND BRANDON

fauna relations of living forms which
might be preserved. Consequently, only
molluscs are considered. Furthermore,
only large and abundant species are
treated in any detail. These are the forms
which make up the bulk of the
macroinvertebrate assemblage.

The present study of a limited shallow
water area off the Massachusetts coast was
initiated in 1965. The area is located in the
north-western part of Buzzards Bay (Fig.
1). Certain characteristics of this area
make it particularly interesting. A diver-
sified fauna is present, coves and
headlands provide numerous protected
and open environments for benthic in-
vertebrates, and there is a variety of clastic
sediment types.

The distribution and abundance of
molluscan species are considered in rela-
tion to the maximum and minimum mean
grain diameters of the sediments in or on
which they are found, as well as in relation
to the maximum and minimum silt-clay
contents of the substratum. Scatter
diagrams of species abundance versus
mean grain diameter and silt-clay content
are presented. Potential faunal-lithic
associations are discussed.

METHODS

Fifty-four stations were sampled within
the study area. Station locations were
determined from a plot of random
numbers on a grid overlay of the area (sta.
51-54 are exceptions and are not randomly
located). Two sediment samples of ap-
proximately 100 g each were collected by
divers at each station. Samples were taken
approximately 4 m apart, the position of
the anchor serving as an arbitrary mid-
point between them. Sedimentary
parameters presented here (Table 1) are
mean values of the 2 samples.

Faunal samples were collected by a
modified scallop dredge equiped with
additional weight on the front part of the
towing bar, 8 cm teeth on the cutting
edge, and 2 mm mesh netting backed by
coarser net and a chain link bottom.
Observation of the dredge on various

substratum types by SCUBA divers in-
dicated that a continuous and even bite
was obtained by appropriate variations in
the length of the tow line. Samples were
sieved on 2 mm mesh screens. Molluscan
abundances reported here are the sum of 2
dredge hauls taken at each station. Each
dredge haul was for 1.5 min at a slow and
constant speed. Diver observation at a
number of stations indicated that the 70
cm wide dredge covered a distance of
approximately 50 m in this time interval.

This sampling procedure is, at best,
semi-quantitative. It was utilized because
no type of grab sampler, nor any more
sophisticated dredge of the epibenthic sled
type (Hessler & Sanders, 1967) backed
with fine mesh netting or canvas can
provide data on the abundance of the large
and widely scattered faunal elements for-
ming a significant portion of the fauna
examined here. Because of the sampling
errors inherent in our dredging technique,
no data are presented here on animal
abundance per unit area. All samples are
assumed to be of approximately equal size
and only relative abundance of the various
species in and on different substrata is
discussed. Figs. 10-32, in which numbers
of specimens are indicated, were con-
structed from the total number of
specimens taken in both dredge hauls at
each station. They are intended to
demonstrate relative abundance only and
not absolute abundance per unit area.

Mechanical size analysis of the
sediments was carried out by standard
techniques. U.S. Standard Sieves arranged
according to the Wentworth grade scale
were utilized in separation of the coarser
fractions. Size analysis of the silt and clay
fraction was accomplished with an ASTM
hydrometer 152H. Calcium carbonate
content was determined from aliquots of
the sediment samples by dry weight
difference before and after digestion in
dilute НС].

The phi ($) scale is utilized here in the
treatment of sedimentary data and the
comparison of such data with benthos
distribution patterns. This scale was
developed by Krumbein (1934) as a

MOLLUSC-SEDIMENT RELATIONSHIPS 15

\ y

||
| |
NN)
| /. |
Pass ja Nautical mile ads
4 3 44 43 42

e
454 A

404

Nautical mile
44 43

——

205 00 05 10 “Le 150 25 30 35
MEAN GRAIN DIAMETER - РН!

FIG. 1. Index map of the study area. General locations is in the northwestern part of Buzzards Bay,
Massachusetts, U.S.A. Station numbers are indicated.

FIG. 2. Mean grain size distribution map. Grain size is given in phi units.

FIG. 3. Per cent silt-clay distribution. The offshore concentration of silt-clay corresponds with a portion of the
Pleistocene drainage pattern.

FIG. 4. Relationship between % silt-clay content of the sediment and mean grain diameter in phi units.

OLL AND BRANDON

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EDIMENT RELATIONSHIPS

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MOLLUSC-SEDIMENT RELATIONSHIPS 19

statistical device to enable sedimentary
data to be examined with conventional
statistics. The phi scale has integers for
Wentworth scale class limits and increases
with decreasing grain size (1 mm = 09; 0.5
mm = 19; 0.25 mm = 2¢; 0.12 mm = 39;
etc. ). The sorting or spread of the sediment
is described in terms of the Trask sorting
coefficient. This measure has been used
extensively in classical studies of sediments
and may be easily converted to other types
of sorting measures by graphical methods
(Krumbein & Pettijohn, 1938).

GENERAL GEOLOGY

The geologic framework of Buzzards
Bay has been examined by Hough (1940),
Mather, Goldthwait & Thiesmeyer (1942),
Moore (1963) and others. Sediments of the
bay are derived from glacial moraine. The
great majority of rock types, both in
Buzzards Bay sediments and in local
moraine, consist of granite, gneissic
granite and gneiss. The Dedham
granodiorite undoubtedly acted as an im-
portant glacial source area for much of this
material. The petrology and chemistry of
Buzzards Bay sediments have been dis-
cussed by Moore (1963) who also deter-
mined that a dentritic Pleistocene stream
pattern is still present on the floor of the
bay and is of considerable importance in
controlling sediment distribution.

SEDIMENT DISTRIBUTION

Moore (1963) has demonstrated the
importance of tidal currents and bottom
topography as factors affecting sediment
distribution in Buzzards Bay. He observed
a general correspondence between strong
tidal currents and coarse detritus. He also
suggests that deeper troughs, commonly
reflecting the Pleistocene drainage
pattern, act as traps for fine sediment. We
confirmed a general correspondence
between coarser clastics and stronger tidal
currents as recorded by Moore. Deviations
from this pattern would seem to be due
partially to the fact that Moore recorded
only surface currents. Using SCUBA, we
noted that in some areas the bottom
current direction deviated considerably

from that of the surface currents, although
they were generally in close agreement.
We also observed that deeper waters, par-
ticularly those in the southeastern portion
of the area, act as sediment traps for the
finer-grained sediment. We suggest,
however, that tidal currents and bottom
topography are not sufficient to complete-
ly explain sediment distribution in the bay
and that wind action, particularly in
nearshore areas, is a significant factor.

The prevailing wind direction is from
the southwest. Waves generated by this
wind introduce high energy conditions in
shallow water areas which are unprotected
by headlands. These higher energy con-
ditions are clearly reflected in a correspon-
ding coarseness of the sediment in such
areas. Mean grain size and the percentage
of silt-clay distributions are shown in Figs.
2 and 3 respectively. It is apparent, from
an examination of these figures, that a
greater amount «of fine sediment ac-
cumulates on the southwesterly than on
the northeasterly margins of the harbors
and coves that comprise the northwestern
border of the bay. The headlands project
southeastward into the bay and are
characterized by rocky points and an
abundance of eroded boulders, derived
from wave reworked glacial moraine,
which act as natural riprap along their
southwestern shores. The very coarse
detritus occurring near the southwest
shore of Sippican Neck, Sta. 41 (Fig. 2),
is a result of wave action upon a number of
such boulders which occur in this area.
The relationship between mean grain
diameter and silt-clay content at all
stations is shown in Fig. 4.

Distribution of sorting is illustrated in
Fig. 5. Although the sorting pattern
described within the same area by Moore
(1963) was based upon only 11 stations,
the distribution described here, based
upon 54 stations, is not markedly different.
Refinements of the sorting distribution
pattern have been possible, but our work
does not affect the general distribution
described by Moore in any significant
manner.

The areal distribution of calcium car-

20 DRISCOLL AND BRANDON

Nautical mile Nautical

404

COEFFICIENT
wo
wo

Le
o
—

SORTING
m
u
=
LI

2.07 a

oe ae
= ai $? un. о

Nautical

т т r + = > —__—_—
=0S 00/07 40,5 0. 1.5 20-25 30155
MEAN GRAIN DIAMETER — PHI

FIG. 5. Sediment sorting. Isopleths are drawn in terms of standard deviations. Stippled area has sorting values
in excess of one standard deviation.

FIG. 6. Distribution of calcium carbonate (% by weight of total sediment) in area of study. Isopleths are drawn
with increments of 2%.

FIG. 7. Facies distribution within the area of study. Vertical and horizontal cross-hatch pattern indicates the
shallow protected facies (1), stippled pattern indicates the nearshore facies (II), diagonal lines indicate the open
bay facies (III), and narrow horizontal lines indicate the offshore facies (IV).

FIG. 8. Relationship between Trask sorting coefficient and mean grain diameter in the 4 facies recognized
within the area. Symbols are: black circles, open bay facies; black squares, nearshore facies; black triangles,
offshore facies; open circles, shallow protected facies.

MOLLUSC-SEDIMENT RELATIONSHIPS 21

bonate is illustrated in Fig. 6. This dis-
tribution pattern corresponds with areas
rich in shell material (Driscoll, 1967).

FACIES DISTRIBUTION

Within the restricted geographic area
which has been examined it is possible to
recognize 4 distinct facies. Although mix-
ing between these facies is occasionally
present, each is generally characterized by
certain sedimentary parameters and by a
characteristic faunal assemblage. The

facies are (I) shallow protected; (II)
nearshore; (ПТ) open bay; and (IV)
offshore (Fig. 7). It should be emphasized
that facies boundaries are gradational and
are not based on a single characteristic. In
order to recognize any given facies it is
necessary to examine both the faunal
association and the sedimentary
parameters.

The shallow protected (I), nearshore
(11), and offshore (IV) facies are
characterized by sediments with a mean

TABLE 2. Five species are particularly useful in distinguishing between the 3 facies in which mean
grain size is less than 0.18 mm. The normalized % of each of these species which occurs in
each of the 3 fine-grained facies is given here. It should be noted that some of these forms
also occur, though less commonly, in the open bay facies. In this table the total number of
individuals found at the 17 stations representing fine grained facies was taken as 100%.

Facies

Species Offshore Shallow Protected Nearshore Total

(5 Stations) (4 Stations) (8 Stations)
Масота tenta leg 4.0 94.3 100.0
Yoldia limatula 50.4 0.0 44.6 100.0
Nucula proxima 0.0 99.4 0.6 100.0
Nassarius trivittatus 78.7 0.7 20.6 100.0
Eupleura caudata 3.3 0.0 96.7 100.0

TABLE 3. Total number of identified species
and number of species composing
1% or more of fauna in 4 different

facies.
Facies No. of No. of Species
Species Composing 1% or
more of fauna
Offshore 16 3
Shallow
Protected 19 8
Nearshore 23 m
Open Bay 34 1]

size of 2.54(0.18 mm) or smaller, and are
referrred to here as the “fine-grained”
facies. They constitute subdivisions of the
Nucula proxima-Nephtys incisa communi-
ty defined by Sanders (1958), 1960). These
3 facies are clearly distinct in faunal
community and in sedimentary
characteristics from the open bay facies
(III) which is characterized by sediments
with a mean grain diameter larger than
2.59, and is analogous to Sanders (1958,
1960) Ampelisca (amphipod) assemblage.

The relationships between the Trask
sorting coefficient and the mean grain
diameters in phi units for all stations
sampled is shown in Fig. 8. The Trask
sorting coefficient used here is calculated
by determining the square root of the ratio

22 DRISCOLL AND BRANDON

of the quartiles (25th and 75th percen-
tiles). The larger quartile is taken as the
numerator. Sediments from the 3 different
“fine-grained facies (I, II, IV) fall into
separate areas on this diagram. In all of
these, sorting becomes poorer as grain size
decreases.

Offshore Facies

This facies (Stas. 19, 25, 42, 45, 49) is
generally characterized by water deeper
than 9 m (mean low tide). The sediments
are fine sands with a high silt-clay content.

Mean grain diameters found at all
stations in the offshore facies are smaller
than 3.064 (0.125 mm). Sorting of the
sediment is better than in the nearshore
facies, but is somewhat variable (Trask
sorting coefficient 1.40-1.80). The physical
conditions producing the offshore facies
involve a number of factors. Most impor-
tant of these is the presence of a
Pleistocene drainage pattern on the floor
of Buzzards Bay. This pattern has been
documented by Moore (1963) who has also
shown that both sediment type and
bathymetry are reflections of this sub-
merged dendritic stream pattern. Each
major inlet to the bay has a trough-like
depression extending from the bay to near
the mouth of the inlet. Even minor inlets
such as those of Wings and Aucoot Coves
are reflected by depressions which extend
bayward from their mouths (Fig. 9).

Moore (1963) has demonstrated that a
general correspondence exists between
areas of silt-clay deposition and the
Pleistocene stream pattern in the deeper
portions of Buzzards Bay. The offshore
facies corresponds to one of the troughs
(stream valleys) indicated by Moore.
However, comparison of silt-clay distribu-
tion (Fig. 3) and of mean grain size
distribution (Fig. 2) with the bathymetry
(Fig. 9) in other parts of the study area
indicates little correspondence between
Pleistocene geomorphology and sediment
distribution.

In the offshore facies, depth of water is
such that the effect of waves on sediment
distribution is negligible. Although no
bottom current studies have been con-

ducted in the bay, Moore (1963) has shown
that surface currents have lower velocities
in the central portion than in the marginal
areas. If a general correspondence
between surface and bottom current
velocities exists in Buzzards Bay, velocities
in the area of the offshore facies are low.

The silt and clay-rich sediments of the
offshore facies are attributable to 3 factors:
(1) the presence of Pleistocene stream
valleys which act as sediment traps; (2) the
reduced velocity of tidal currents in the
central part of the bay; and (3) minimal
effects of wave action on the sediments
due to water depths.

Fauna—Sixteen species were collected
from sediments representing the offshore
facies. These are listed below. The percen-
tage of the offshore molluscan macrofauna
attributable to each species is indicated.

Nassarius trivittatus 85.3
Yoldia limatula 5.5
Laevicardium mortoni 3.4

—
©

DOS eee SS

Pitar morrhuana
Anachis avara similis?
Macoma tenta
Anadara transversa
Ensis directus
Lyonsia hyalina
Mitrella lunata
Pandora gouldiana
Anachis avara?
Crepidula fornicata
Solemya velum
Eupleura caudata
Retusa obtusa

АЛЛА AAN TS IN AN IX FDS, AN

Two of these species (Nassarius trivit-
tus and Yoldia limatula) make up 90% of
the fauna collected. Both are deposit
feeders. N. trivittatus is common through-
out the area of study but is a more im-
portant faunal constituent in the offshore
facies than in any other.

Examination of Tables 2 and 3 indi-
cates that the offshore fauna may be dis-
tinguished from that found in the fine
sediments of the shallow protected facies
by the much larger numbers of Nassarius
trivittatus, the abundance of Yoldia lima-
tula, and the absence or near absence of

MOLLUSC-SEDIMENT RELATIONSHIPS 23

SHE!

. IN .
Nautical mile и le Nautical mile a le
70° 45' 44 43 42 4 44 43 42

1 1 #(567) (298)8

67)4 RE)

D

eo!
x
с
I
= 20
N o
Е <
©
o o
y ES = Е
= 54 т
| N a
154
n
if |
<
= 9
z <
< =
10 =
u <
о 104
u
œ . o
ш
ao x a
= ш
> = o
z = a
54 в. о 5 |
z 5 aes
8 s
a a
Г .
a A
. a = . a a a a
. s à a
| Denn
EA u

iF Y Y т

10 20 30 40 50 =05) 100 Fos? OMIS (2101 2,577 30 35
PER CENT SILT-CLAY MEAN GRAIN DIAMETER — PHI

FIG. 9. Bathymetry. Isobaths are indicated at 1 fathom intervals below mean low sea level. After Coast and
Geodetic Survey Chart 251 in part.

FIG. 10. Areal distribution of Macoma tenta. Isopleths are drawn at intervals of 100 specimens. Note that this
selective deposit feeder is concentrated in the silt and clay rich sediments of the nearshore facies, occurs in
sediments of the offshore and shallow protected facies, and is nearly absent from the open bay facies.

FIG. 11. Relationship of Macoma tenta to silt-clay content of the sediment. This selective deposit feeder becomes
more abundant with increasing abundance of silt-clay. Zero occurrences shown below
dashed line. Twenty-five of the 51 stations at which faunal samples were taken have less than 5% silt-clay and
yielded no specimens of M. tenta.

FIG. 12. Relationship of Macoma tenta to mean grain diameter. The species is uncommon in sediments with
a mean grain diameter greater than 0.18 mm (2.5 4). Zero occurrences shown below dashed line.

24 DRISCOLL AND BRANDON

Nucula proxima. It may be distinguished
from the fauna of the nearshore facies by
the somewhat larger numbers of Nas-
sarius trivittatus, the absence or near
absence of Eupleura caudata and the less
abundant occurrence of Macoma tenta.
This molluscan fauna is more restricted in
number of species than that of either of the
other 2 “fine-grained” facies (LIL).

Shallow Protected Facies

This facies (Stas. 29, 30, 31, 51) is lim-
ited to those areas with a water depth of
less than 3 m (mean low tide). The sedi-
mentary parameters and faunal associa-
tions characteristic of the facies are devel-
oped in coves and inlets (Fig. 7). The rela-
tionship between sorting coefficient and
mean grain diameter within this environ-
ment is shown in Fig. 8. Sediments are fine
grained, not exceeding a mean diameter of
2.59 (0.18 mm). Sediment sorting becomes
increasingly poorer with decreasing mean
grain diameter but the sorting range is
nearly identical to that present in sedi-
ments from the offshore facies. Mean
diameters of these sediments overlap those
found in the offshore facies. However,
sediments from the shallow protected
facies are consistently somewhat coarser
than those with a comparable degree of
sorting collected from the offshore facies.

Areas in which the shallow protected
facies are developed are sheltered from the
prevailing southwest wind by headlands.
Another factor contributing to low energy
conditions is the presence of eel grass
throughout major portions of this facies.
The eel grass has a net effect of damping
wave action on the sediment-water inter-
face, thereby insuring a relatively low
energy environment. Furthermore, this
protection prohibits any substantial addi-
tion of coarser sediments from offshore
areas during storms. Finer sediments may
be moved into this facies from offshore
areas via the mechanisms detailed Бу
Postma (1967). However, very fine sedi-
ment is removed by tidal currents and not
replenished from offshore areas. Pre-
sumably this is because concentration of
the very fine fraction in the shallow pro-

tected facies is not accomplished through
settling lag and scouring lag (Postma,
1967).

Two different sets of physical condi-
tions have given rise to similar, though not
identical, sediments in the shallow pro-
tected ( 3 m in depth) and offshore (9 m in
depth) facies. In the shallow protected
facies, protection from wave action, and
the presence of eel grass are effective in
producing low energy conditions which
are reflected in a sediment consisting of
fine grained, silt and clay-rich sand.
Similar sediments of the off-shore facies
are accumulated because of the lower
energy conditions associated with greater
depth, lower current velocities, and the
protection afforded by troughs and stream
valleys of the Pleistocene drainage system.

Fauna—Nineteen species were col-
lected from sediments representing the
shallow protected facies. These, and the
percentage of the shallow protected
molluscan macrofauna made up by each
species, are listed below:

Crepidula fornicata 47.4
Nucula proxima 30.3
Crepidula plana 7.3
Bittium alternatum 4.4
Laevicardium mortoni 3.3
Crepidula convexa 17
Argopecten irradians 1.0
Macoma tenta 10
Nassarius vibex N)
Anomia simplex 0
Nassarius trivittatus <0
Solemya velum < 1.0
Mitrella lunata 0
Anachis avara similis? < 10
Lunarca ovalis < 1.0
Busycon canaliculatum < 10
Natica clausa <1:0
Pandora gouldiana <0)
Retusa obtusa < 10

Eight of these species comprise more
than 96% of the collected fauna. The
abundant occurrence of Crepidula (a
suspension feeding gastropod) ш this
facies is probably the result of the presence
of scattered cobbles and boulders through-
out the area (particularly at Sta. 31) and

MOLLUSC-SEDIMENT RELATIONSHIPS 25

possibly to a profuse growth of eel grass in
portions of the environment. These hard
surfaces provide points for fixation of
Crepidula and other attached epifaunal
forms. It has been suggested (Van Straaten
& Kuenen, 1958; Rhoads & Young, 1970)
that shallow subtidal mud bottoms tend to
be stabilized by the binding properties of
marsh grass and benthic diatoms. Rhoads
€ Young (1970) present a convincing
argument that stability of the substratum
is a controlling factor in the distribution of
suspension feeders in Buzzards Bay. It
seems probable that the shallow protected
facies is less subject to resuspension of
sediment than either of the other 2 “fine
grained” facies. This appears to be the
case despite the fact that Nucula proxima,
an active burrowing deposit feeder, is
abundant in the shallow protected facies.

Examination of Tables 2 and 3 indi-
cates that the fauna of the shallow pro-
tected facies may be distinguished from
that of both the offshore and the near-
shore facies by the absence or near absence
of Yoldia limatula and by the small
numbers of Nassarius trivittatus. Perhaps
the single most important faunal criterion
for distinguishing this facies from others is
the abundance of Nucula proxima. This
species makes up approximately 30% of
the molluscan fauna of the shallow pro-
tected facies but is absent, or nearly ab-
sent, from other parts of the study area.
Table 2 indicates that over 99% of all
Nucula proxima collected were found in
the shallow protected facies. It is in-
teresting to note that Parker (1956), in his
study of the Mississippi delta region, com-
ments that Nucula proxima is a form
which is characteristic of the deeper con-
tinental shelf of the Gulf of Mexico be-
tween 24 and 91 meters. Hampson (1971)
has distinguished 2 distinct species of
Nucula in Buzzards Bay, N. proxima
and N. annulata. These appear to be geo-
graphically separated in their distribution
patterns.

It should also be noted that Laevi-
cardium mortoni is more common in the
shallow protected than in other “fine
grained facies and that Macoma tenta

and particularly Eupleura caudata are less
common than in the nearshore facies. The
presence of Bittium alternatum in this
fauna is a reflection of the abundance of
eel grass in the environment.

Nearshore Facies

This facies (Fig. 7) is characteristic of
harbor mouths which open to the south
and are therefore only partially protected
from wave action generated by the pre-
vailing southwest wind. Stations
demonstrating characteristics of the near-
shore facies (1, 4, 10, 20, 32, 44, 47, 50) are
found in waters of intermediate depths of
between 3 and 7.5 m. (Sta. 20, an excep-
tion, is discussed below). The relationship
between mean grain diameters and sedi-
ment sorting in the nearshore facies is
shown in Fig. 8. Although these 8 stations
have a mean grain size comparable to that
of the deep offshore and shallow pro-
tected facies (mean grain diameters not
larger than 2.54) the sorting is generally
poorer than in either of these other “fine
grained’ facies. (Trask sorting coefficient
from 1.81-2.88. )

Sedimentary parameters of the near-
shore facies may be explained by a num-
ber of factors. The streams emptying into
the harbors in which this facies is de-
veloped come from areas of relatively low
relief, supplying little or no coarse detritus.
Consequently, the area exhibits “fine
grained’ sediments. The poorly sorted
character of the sediments is due to the ex-
posure of this area to variable energy con-
ditions. These range from the relative calm
of low velocity tidal currents to the
violence of storm waves with a wave
length of 7 m or more. Moore (1963)
indicates that current velocity is reduced
near harbor mouths. Consequently, the
sorting and washing of sediments which is
characteristic of the open bay facies is not
found here.

In Fig. 7, a band of the nearshore facies
is shown on the east side of the study area
intermediate between the offshore and
open bay facies. This area, which is sug-
gested on the basis of a single station (Sta.
20), is the result of gradation between the

26 DRISCOLL AND BRANDON

offshore fine grained facies and the coarser
sediments characteristic of the open bay
facies. The fauna of Sta. 20 is also inter-
mediate in nature.

Fauna—Twenty-three species were col-
lected from sediments of the nearshore
facies—more than from either of the other
2 “fine grained” units. These, and the per-
centages of the molluscan fauna of the
nearshore facies made up by each species,
are listed below:

Macoma tenta 49.8
Nassarius trivittatus 31.0
Yoldia limatula 6.6
Eupleura caudata 3.4
Laevicardium mortoni 2.8
Bittium alternatum 17
Crepidula plana < 1.0
Anachis avara similis? < 1.0
Solemya velum < 1.0

Crepidula fornicata
Nucula proxima
Polinices duplicatus
Chaetopleura apiculata
Lyonsia hyalina

Mitrella lunata < 1.0
Pitar morrhuana <1:0
Urosalpinx cinerea LO
Lunarca ovalis a1)
Pandora gouldiana < 1.0
Mulinia lateralis < 1.0
Anachis avara? =1:0
Argopecten irradians <1.0
Busycon canaliculatum =10

Four species make up over 90% of the
fauna. The most important form is Ma-
coma tenta. Over 90% (normalized) of all
specimens of M. tenta collected were
found in the nearshore facies.

The fauna may be distinguished from
that of both the shallow protected and off-
shore facies by the much greater relative
abundance of Macoma tenta and Eu-
pleura caudata. It further differs from the
shallow protected fauna in the near
absence of Nucula proxima and from the
offshore fauna in the relatively less abun-
dant occurrence of Nassarius trivittatus.

Open Bay Facies
Sands with a mean grain diameter larger

than 2.56 comprise the bulk of the
sediments in the study area. These sands,
found at depths of from 3-9 m, constitute
the open bay facies (Fig. 7).

With the exception of a few stations
having very coarse grained sediments,
sorting is better than in the “fine grained”
facies (Fig. 8) and further improves as
mean grain size decreases. This trend con-
trasts with the 3 “fine grained” facies in
which sorting becomes poorer as mean
grain diameter decreases. These tenden-
cies are in agreement with similar observa-
tions concerning sedimentation in Buz-
zards Bay by Sanders (1958).

Inman (1949) suggested that sedi-
mentary particles having a diameter of
approximately 2.5 ф are more easily trans-
ported than coarser or finer sediments.
Krumbein & Aberdeen (1937); Hough
(1942): Shukri € Higazy (1944) and
Sanders (1958) have all described environ-
mental situations in which better sorting
occurs as transported sediments approach
this diameter. Recent experimental work
by White (1970) indicates that under
certain conditions, sedimentary particles
finer than 2.59 become increasingly dif-
ficult to transport as grain size decreases.
However, it is doubtful that these condi-
tions represent a common situation in
nature.

Postma (1967) and Rhoads & Young
(1970) have demonstrated that the energy
required for resuspension and transport of
silts and clays is correlated with the water
content of the sediment. Sediments with a
higher water content are more easily trans-
ported than those which are more com-
pacted. Rhoads & Young (1970) have
further shown that reworking of the sub-
stratum by deposit feeding organisms is
effective in increasing the water content of
fine grained sediments. Consequently, the
particle size which is most easily trans-
ported in any given environment is de-
pendent upon a number of variables. In
the open bay facies characterized by a near
absence of fine grained sediments and a
paucity of deposit feeders, it appears that
the better sorting of fine sands may be ex-
plained on the basis of ease of transport.

MOLLUSC-SEDIMENT RELATIONSHIPS 27

The poorest sorting and largest mean
grain diameters in the open bay facies are
found at Stations 35 and 41. Station 35 is
located near the southern entrance to the
Cape Cod Canal in an area indicated by
Moore (1963) as having high tidal current
velocities. It seems probable that the
coarse grained, poorly sorted character of
sediment at this station is the result of
these high velocity currents. Station 41 is
located near the southwestern shore of Sip-
pican Neck in an area of strong wave
action and numerous glacially derived
boulders. Sediment in this area is, at least
in part, debris accumulated locally from
these glacial boulders. These 2 stations are
extreme examples of the importance of
wave action and tidal current velocity on
sedimentary parameters within the study
area. At both stations high energy condi-
tions prevail. Easily transported detritus
approaching 2.56 in diameter is rapidly
winnowed out and removed. The coarse
and poorly sorted residue at both stations
is similar, although it is the result of
different physical agents.

In general, the sedimentary char-
acteristics of the open bay facies are
largely attributable to the action of tidal
currents. Moore (1963) has indicated that
this area is subjected to relatively high cur-
rent volocities. Regular fluctuation of
these currents results in a washing out of
finer sedimentary particles and concentra-
tion of coarse grained, well sorted sand.

Fauna—Thirty-four species were
collected and identified from the open bay
facies. These and the percentage of the
open bay molluscan macrofauna made up
by each species are listed below:

Nassarius trivittatus 39.0
Anachis avara similis? 12.6
Chaetopleura apiculata 10.5
Anadara transversa 9.9
Crepidula fornicata 5.1
Eupleura caudata 4.9
Crepidula plana 4.2
Crassinella mactracea 3.6
Laevicardium mortoni 3.4
Anachis avara? 2.5
Yoldia limatula 1.2

Argopecten irradians

Mitrella lunata <0
Pandora gouldiana <0
Urosalpinx cinerea < 10
Nucula proxima SLO
Anomia simplex < 1.0
Cerastoderma pinnulatum < 10
Lyonsia hyalina < 10
Pitar morrhuana 0
Busycon canaliculatum < 10
Cerithiopsis subulata <1:0
Ensis directus < 1.0
Macoma tenta - 10
Crepidula convexa < 150)
Lunarca ovalis SO)
Seila adamsi < 1.0
Bittium alternatum то
Lunatia triseriata < 0
Mercenaria mercenaria то
Modiolus modiolus < 1.0
Natica clausa < 1.0
Spisula solidissima < то
Tagelus divisus <1.0

The first 10 of these species make up
91% of the fauna in the open bay facies.

These 10 species are suspension feeders,
carnivores, herbivores, or non-selective
deposit feeders. In contrast to the 3 “fine
grained” facies, no selective deposit
feeders are important elements of this
fauna. The fauna turther differs from those
of the 3 “fine grained’ facies in pos-
sessing a much higher degree of faunal
diversity. This observation is in agreement
with Sanders (1968) suggestion that the
fauna of stable sand bottoms is probably
inherently more diverse than that of mud
bottoms. For a more comprehensive treat-
ment of faunal diversity of Buzzards Bay
see Saunders (1968, 1969). The paleo-
ecologic implications of faunal diversity
are discussed by Bretsky € Lorenz (1970).

DISTRIBUTION OF SPECIES
AND SUBSTRATE RELATIONS

A faunal list and relevant ecological data
are given in Table 4. There are 13 species
which individually contribute more than
1% of the total collected molluscan fauna
(numbers of specimens) from all of the
facies in the study area. These forms are
listed below with their respective per-
centages. Those species whose feeding

28 DRISCOLL AND BRANDON

habits are not fully known are indicated by
an asterisk. Bittium alternatum was not
included in the percentage calculations,
but does occur in enormous numbers in
areas of eel grass.

Selective Deposit Feeders %
Macoma tenta 9.4
Nucula proxima 6.1
Yoldia limatula 2.7

Suspension Feeders

Crepidula fornicata 11.5
Anadara transversa 3.0
° Laevicardium mortoni 2.8
Crepidula plana 3.6
°Crassinella mactracea 2.9
Carnivores and Nonselective Deposit
Feeders
Nassarius trivittatus 39.5
Anachis avara similis? 6.3
Eupleura caudata 3.0
Anachis avara? ie
° Bittium alternatum -
Herbivores and Grazers
Chaetopleura apiculata 5.1

The areal distribution of most of these
species is illustrated in Figs. 10-32 and is
briefly discussed below. Isopleths in the
figures refer to the relative density of the
animals. Species are grouped according to
the similarity of their distribution patterns.
The mean grain diameter in which each
species is found, the mean silt-clay con-
tent associated with each species, the
ranges of mean grain diameters, and the
ranges of the silt-clay content associated
with each species are presented in Figs. 33
and 34.

Relationships existing between trophic
groups, current velocities, and various
sedimentary parameters have been dis-
cussed by many writers (Bader, 1954;
Sanders, 1958; Purdy, 1964; Craig &
Jones, 1966; Jorgesen, 1966; Driscoll,
1969; Rhoads & Young, 1970; Newell,
1971). In Buzzards Bay, infaunal suspen-
sion feeders become more abundant in
sediments with a mean grain diameter
approaching 2.56. Sessile epifaunal
suspension feeders are commonly most
abundant in sediments with a mean grain
diameter coarser than 2.5¢@ and selective

deposit feeders in sediments with a mean
grain diameter finer than 2.54.

Масота tenta. This selective deposit
feeder is found in “fine grained” sedi-
ments with a relatively high silt-clay con-
tent (Fig. 10). Occurrences in the open bay
facies, in sediments with a mean grain
diameter coarser than 2.59, are unusual.
The form reaches maximum abundance in
the nearshore facies. Parker (1956) reports
M. tenta as being most common in his
Upper Sound Division of the Mississippi
delta region. Both areas are characterized
by sands rich in silt and clay, shallow
depths, and salinities somewhat below that
of normal sea water.

The relationships between increasing
silt-clay content of the sediment and in-
creasing abundance of М. tenta are il-
lustrated in Fig. 11. Inasmuch as the
correlation between silt-clay content and
mean grain size is high (Fig. 4), it is not
unexpected that this species is also found
to increase in abundance with decreasing
mean grain diameter (Fig. 12).

Yoldia limatula. The areal distribution
pattern of this selective deposit feeder
(Fig. 13) shows a high correlation with the
distribution of silt-clay throughout the
area (Fig. 3). Maximum occurrences are in
areas protected from wave action by
headlands (Sta. 50) or in deeper areas
removed from the zone of severe wave
action (Sta. 19). Presumably this distribu-
tion pattern is a reflection of the abun-
dance of clay and organic detritus rather
than a direct negative response of Y.
limatula to moderate wave agitation.

Although Hunter € Brown (1964) in-
dicate that Y. limatula may occur inter-
tidally as well as below the low water mark
the species was not found in the shallow
protected facies. Depths of only a few feet
do not appear to favor abundant develop-
ment of the species in the study area. A
marked increase in abundance of Y.
limatula is found with increasing silt-clay
content and with decreasing mean grain
diameter (Figs. 14-15).

Nucula proxima. Comparison of the
areal distribution pattern of the species
(Fig. 16) with Fig. 7 and Table 2 indicates

29

MOLLUSC-SEDIMENT RELATIONSHIPS

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MOLLUSC-SEDIMENT RELATIONSHIPS 31

|
254

20

ANIMALS — Yo/dia limotu/a

NUMBER OF

Y Y Y
10 20 30 40 50

a | Sel
Nautical mile Y le
. PER CENT SILT —=CLAY:

\
N
44 43 42

md
Un

Nn
a

NUMBER OF ANIMALS — Yo/día limatu/a

[|

NE
Nautical mile У le
44 43 42

-0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5
MEAN GRAIN DIAMETER — PHI

FIG. 13. Areal distribution of Yoldia limatula. Isopleths are drawn at intervals of 10 specimens. Note that this
selective deposit feeder is abundant in the nearshore and offshore facies, but is uncommon in both the shallow
protected and open bay facies.

FIG. 14. Relationship of Yoldia limatula to silt-clay content of the sediment. This selective deposit feeder
increases in abundance with increasing silt and clay. Zero occurrences are shown below the dashed line. Twenty-
two of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens
of Y. limatula.

FIG. 15. Relationship of Yoldia limatula to mean grain diameter. This species is uncommon in sediments with
a mean grain diameter greater than 0.5 mm (1.04). Zero occurrences shown below dashed line.

FIG. 16. Areal distribution of Nuclua proxima. Isopleths are drawn at intervals of 100 specimens. This selective
deposit feeder is abundant only in Planting Island Cove and Blankenship Cove. These areas are in the
shallow protected facies.

32 DRISCOLL AND BRANDON

that this selective deposit feeder is most
characteristic of the shallow protected
facies. The species was not taken in the
offshore facies and was uncommon in the
nearshore facies. The distribution of N.
proxima relative to silt-clay content and
mean grain diameter of the sediment is
shown in Figs. 17 and 18. Sanders (1956,
1958) has discussed the species” dis-
tribution characteristics in some detail.
Rhoads & Young (1970) demonstrate that
N. proxima is an important agent in the
reworking of fine sediments. .

Anadara transversa. This suspension
feeding bivalve is most abundant in the
open bay facies (Fig. 19). The relationship
between species abundance and mean
grain diameter of the sediment is illus-
trated in Fig. 21. It appears that A. trans-
versa is most successful in sediments with a
mean grain diameter between 0.56 and
1.54. However, many of the stations with-
in this sediment size range possess an
abundance of dead shell material.
Juveniles, which require a hard surface for
fixation, are usually found byssally at-
tached to the interior of the umbonal
region of dead bivalve shells. Con-
sequently, the areal distribution of the
species is related to dead shell distribution
as well as mean grain diameter of the
sediment.

Fig. 20 illustrates the relationship
between the abundance of A. transversa
and the percent silt-clay in the sediment.
This species is uncommon in sediments
with more than 5% silt-clay. A. transversa
appears to require a medium to coarse
sand bottom (Fig. 21), a low silt-clay con-
tent in the sediment, and the presence of
dead shell material for successful juvenile
settlement.

Chaetopleura apiculata. The only local
polyplacophoran occurs primarily in
sediments having a low silt-clay content
and large amounts of associated dead shell
material. It is attached to hard surfaces,
commonly the dead shells of bivalves, and
is characteristic of the open bay facies in
areas of dead shell accumulation (Fig. 22).
The low silt-clay content and mean grain
diameters ranging between 0.5¢ and 1.59

(Fig. 23), which are associated with the
abundant occurrence of C. apiculata, in-
dicate that finer sediments, particularly
clays, may be detrimental to the animal.
Parker (1956) reports that C. apiculata
occurs only in inlets and passes in the
Mississippi delta area. These areas are also
characterized by concentrations of dead
shell material.

Crassinella mactracea. This small
bivalve is reported by Hunter € Brown
(1964) from sand and shell bottoms in shal-
low water. The species was collected only
in the open bay facies and was partic-
ularly abundant in areas rich in dead shell
material (Fig. 24). All specimens were col-
lected from sediments having mean grain
diameters ranging between 0.59 and 1.59
(Fig. 25).

Laevicardium mortoni. Areal distribu-
tion of L. mortoni is illustrated in Fig. 26.
An interesting aspect of the distribution
pattern is that L. mortoni is most abundant
in the shallow protected facies (Planting
Island Cove and, to a lesser extent, Wings
Cove). However, it also is present in the
open bay facies and has been observed in
the offshore facies (Sta. 45). No specimens
of L. mortoni were collected from any of
the 8 stations representing the nearshore
environment. In Fig. 26 the areal distribu-
tion of the species, extending into the
nearshore facies, may be noted, but this
extension is inferred rather than observed.

Relationships between the distribution
of Laevicardium mortoni, the silt-clay
content, and the mean grain diameter of
the sediment are illustrated in Figs. 27 and
28 respectively. A clear trend cannot be
seen in either of these distribution
patterns. The species commonly occurs in
sediments with a silt-clay content ranging
from near 0% to 50%. It shows little
sensitivity to changes in mean grain
diameter. This exceptional adaptability to
varying environmental conditions is dif-
ficult to explain. Detailed examination of
the feeding habits of L. mortoni may
reveal a mechanism which allows the
species to thrive in environments suitable
to both deposit and suspension feeding
organisms. Examples of single species

MOLLUSC-SEDIMENT RELATIONSHIPS 33

17 #76) #251) 18 & (1764251)
304 304
o
Е ©
à E
2 x
o
254 a
2 &25-
S 2
> 3
я S
| 20 2
te 204
E . |
<
= Ф à
= ar
2 154 <
=
u | = |5]
о <
x u
= 104 о
=
5 & 104
z . o
=
5, ® =)
ses г a
.
. 5 >
a Е aaa
о | : == в в *
à A ; = :
10 20 30 40 50 a a
РЕВ “CENT ЭТ — СГАУ o — = a а yes à Ам АЕ A
0 T TS TT
—0.5 0.0 0.5 1.0 1:5 2.0 225 3.0 219

MEAN GRAIN DIAMETER — PHI

133)
20°

ч
о
TE

nm
u
1

nm
о
= E

ANIMALS — Anadara transversa
a
ak

NUMBER OF

La

1 .
о N: / / sel s в |
Nautical mile N o mea У: = = acy i x. — x
70° 45' 44 43 42 ar т hr —— LE a т
N 1 10 20 30 40 50

PER CENT SILT = CLAY

FIG. 17. Relationship of Nucula proxima to silt-clay content of the sediment. Zero occurrences are shown below
dashed line. Twenty-one of the 51 stations at which faunal samples were taken have less than 5% silt-clay and
yielded no specimens of N. proxima.

FIG. 18. Relationship of Nucula proxima to mean grain diameter. The species is uncommon in sediments with
a mean grain diameter greater than 0.5 mm (1.0¢). Zero occurrences are shown below dashed line.

FIG. 19. Areal distribution of Anadara transversa. Isopleths are drawn at intervals of 100 specimens. This
suspension feeder is most abundant in the open bay facies, particularly in areas rich in dead shell material.
FIG. 20. Relationship of Anadara transversa to silt-clay content of the sediment. This suspension feeder is not
abundant in sediments with more than 5% silt and clay. Zero occurrences are shown below dashed line. Fourteen
of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens of A.
transversa.

34 DRISCOLL AND BRANDON

2] м = - |

fransversa
>»

Anadora

m n
o o
i 1

ANIMALS —
u
1

o
1
>

NUMBER OF

u
4

aa 11
= à te 4 4 Е

Sal
QT a— — — — rum mp gee Nautical mile le

r - + 7 r 70* 45 44 43 42
-0.5 0.0 0.5 1.0 15 120255055 | Е —

MEAN GRAIN DIAMETER — PHI

Choetopleuro apiculata
i
>»

ANIMALS

ul
»

NUMBER OF

Ц «

N ` D \
0+ a Tey: ut ik Ey pi Ba x \ |
Е 00 05 о 5 20 25 30 38 о ye и
MEAN GRAIN DIAMETER — РН! Nautical mile N o

44 43 42

FIG. 21. Relationship of Anadara transversa to mean grain diameter. The species is most common in sediment
with a mean grain diameter between 0.54 and 1.5%. Zero occurrences are shown below dashed line.

FIG. 22. Areal distribution of Chaetopleura apiculata. Isopleths are drawn at intervals of 50 specimens. This
macrophagous herbivore is most abundant in the open bay facies, particularly in areas rich in dead sheil
material

FIG. 23. Relationship of Chaetopleura apiculata to mean grain diameter. The species is most common in
sediment with a mean grain diameter between 0.5 ¢and 1.54. Zero occurrences are shown below dashed line.

FIG. 24. Areal distribution of Crassinella mactracea. Isopleths are drawn at intervals of 25 specimens. This form
is most abundant in the open bay facies on current-swept sand and shell bottoms.

MOLLUSC-SEDIMENT RELATIONSHIPS

NUMBER OF ANIMALS — Crassinella mactracea
a

446 39)

4 à à

A Zum

Be вы Mee м dl

т

т т т =
0.0 0:5 10 15 2.0 2.5 3.0 3.5

MEAN GRAIN DIAMETER — PHI

307

254

Loevicardium mortoni

2078

ANIMALS

NUMBER OF

10 20 30 40 50
РЕВ (GE Nit SILT=CLAY

35

41° 42

‚ 2 D Ju
N Lye = 40
Xx \ ea / /
x Ro -
N 4 //
ake (EN 10 El
SS Sara \ A ;
< 39
aS Nea
| It
Sabu
K \
ON ey
0 |
EN 38
Nautical mile u le
70° 45' 44 43 42 ar
= |
$ 304 a
Xj
o
E
Е
>
S 254
LL
o
2 a
à |
%
© |
=
20-
т
atl a
= a
= 155
A a
[re
о
a 10- a
Lu
o
=
>)
= a 422
54 a a
t
a a a a a
~~ a aa
a a Ada aa a
1 =n хр ам gai fi à À
-05 00 05 Kor us ВИ os

MEAN GRAIN DIAMETER — РН!

FIG. 25. Relationship of Crassinella mactracea to mean grain diameter. The species is most abundant in
sediments with mean grain diameters between 0.54 and 1.54. Zero occurrences are shown below dashed line.

FIG. 26. Areal distribution of Laevicardium mortoni. Isopleths are drawn at intervals of 10 specimens. This form
is present in all facies within the area, but shows some apparent preference for areas with a substantial silt-clay

content.

FIG. 27. Relationship of Laevicardium mortoni to silt-clay content of the sediment. The occurrence of this
species is exceptional in that there appears to be little correlation with sedimentary parameters. Zero occurrences
are shown below dashed line.
FIG. 28. Relationship of Laevicardium mortoni to mean grain diameter. The species shows little correlation
with this sedimentary parameter. Zero occurrences are shown below dashed line.

36 DRISCOLL AND BRANDON

utilizing more than 1 feeding mechanism
are not unknown (Stasek, 1965). Alterna-
tively, as has been suggested for Mulinia
lateralis by Levinton & Bambach (1970),
the low bulk density of L. mortoni might
enable it to survive in soft substrates which
otherwise would be lethal.

Anachis translirata and Anachis avara.
During the field work and preliminary
laboratory phases of this study the writers
were aware that 2 easily confused species
ot Anachis were present in the study area.
These were tentatively designated as “A.
avara similis?” and “A. avara?. Since that
time Scheltema (1968, 1969) has com-
pleted detailed redescriptions and life
history studies of both species. Our “А.
avara similis?” is equivalent to A.
translirata. Our “A. avara? is, in fact, A.
avara. We are retaining the tentative
designations here to indicate that iden-
tification of these forms was imprecise.

In this discussion reference is made only
to “Anachis avara similis?’ (=Anachis
translirata), but cursory examination of the
distribution patterns of “ Anachis avara?”
(=Anachis avara) indicates that both
species are similar in their areal distribu-
tion and in relation to silt-clay content and
mean grain diameter of the sediment. This
is in agreement with Scheltema's (1968)
observation that the species commonly
occur together.

The areal distribution of * Anachis avara
similis?” is illustrated in Fig. 29. This
carnivore is most plentiful in the open bay
environment, but is also present else-
where. Although illustrations of the rela-
tionships between species distribution, silt-
clay content and mean grain diameter are
not presented here, such relationships do
exist. The stations at which “A. avara
similis?’ was most abundant are in areas of
low silt-clay content and in sediments
having mean grain diameters ranging be-
tween 0.5ф and 1.54.

Parker (1956) indicates that Anachis
avara similis? is characteristic of his Lower
Breton Sound and Pro-Delta Slope areas in
the Mississippi delta region. This environ-
ment, possessing a silty clay to clayey silt
bottom, is quite different from the en-

vironment in which “A. avara similis?”
finds its maximum development in the
area of the present study.

Eupleura caudata. This boring carni-
vorous gastropod is present throughout
much of the area, but no specimens were
collected in the shallow protected facies
and only a single occurrence was found in
the offshore facies (Sta. 49). Areal distribu-
tion of the form is illustrated in Fig. 30. As
is typical of carnivores, no close correla-
tion exists between the occurrence of the
species and silt-clay content or mean grain
diameter of the sediment. The largest
numbers of E. caudata were found in the
open bay facies (Stas. 12, 15) in relatively
coarse sediment, presumably because of
predator-prey relationships between this
species and the abundant epifaunal com-
munity in the open bay facies.

Nassarius trivittatus. This prosobrach is
the most common large mollusc in the area
of study (Table 4). Its occurrence, usually
in considerable numbers, was observed at
all but one of the stations which were
sampled. No clear relationship between
the distribution of N. trivittatus and silt-
clay content exists within the area (Fig.
31), although the 3 stations yielding N.
trivittatus in greatest abundance have
mean grain diameters in the fine and very
fine sand range.

Scheltema € Scheltema (1964) have ob-
served that Nassarius trivittatus typically
occurs in offshore waters of several meters
or more, in contrast to its nearshore
counterparts, N. obsoletus and N. vibex.
Although commonly present in nearshore
regions in the study area, № trivittatus
becomes increasingly abundant with in-
creasing depth (Fig. 32).

ANIMAL RANGES

Figs. 33 and 34 illustrate the ranges of
important species relative to mean grain
diameters and silt-clay content of the sedi-
ment. Also presented here is the mean
occurrence of each species within its
range. It is obvious that the reliability of
the indicated ranges depends upon the
number of stations examined and the num-
ber of animals collected. Thus, the mean

MOLLUSC-SEDIMENT RELATIONSHIPS 37

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FIG. 29. Areal distribution of ““Anachis avara similis” (= A. translirata). Isopleths are drawn at intervals of 25
specimens. This carnivore, though present in all facies in the area, shows some preference for the open bay facies.
FIG. 30. Areal distribution of Eupleura caudata. Isopleths are drawn at intervals of 25 specimens. This
carnivore is most abundant in the open bay facies, plentiful in the nearshore facies and absent, or nearly absent,
from the shallow protected and offshore facies.

FIG. 31. Areal distribution of Nassarius trivittatus. Isopleths are drawn at intervals of 100 specimens. This non-
selective deposit feeder is the most abundant form in the area.

FIG. 32. Occurrence of Nassarius trivittatus plotted against depth in feet below mean low tide level. Note that
N. trivittatus was not found to be abundant in very shallow waters and that abundance of the species
increases as depth increases.

38 DRISCOLL AND BRANDON

silt-clay value associated with Nassarius
trivittatus (3095 individuals collected from
50 stations) is considerably more meaning-
ful than that of Natica clausa (2 individ-
uals collected from 2 stations). Reference
to Table 4 enables one to evaluate the data
in these 2 figures.

The sequence of species indicated in
Fig. 33 is very nearly identical to the
sequence found in Fig. 34. This cor-
respondence is due to the close correlation
between increasing mean grain diameters
and decreasing silt-clay content (Fig. 4). In
Fig. 34 a distinct break is evident in the
otherwise more or less continuous distribu-
tion of mean occurrences of species
relative to silt and clay at the 5% silt-clay
level. It is interesting to note that the 5%
silt-clay level was also found to be signif-
icant in the delineation of feeding and
habitat types in Cape Cod Bay, Massa-
chusetts (Young, et. al., 1971).

The distribution of trophic groups in
Figs. 33-34 is consistent with the previous
discussion. Those species having their
mean occurrences in coarse grained sedi-
ments with low silt-clay contents are all
suspension feeders, herbivores, or car-
nivores. All selective deposit feeders have
their mean occurrences in fine grained
sediments with high silt-clay contents.
Rhoads & Young (1970) have presented
convincing evidence that the exclusion of
suspension feeders from many fine grained
bottoms in Buzzards Bay is due to fre-
quent resuspension of biogenetically
reworked sediments. Species with more
generalized feeding habits (e.g. Nassarius
trivittatus) have their mean occurrences in
sediments with intermediate mean grain
diameters and silt-clay contents. This does
not indicate that such sediments are more
suitable for success of the species, but that
the species is adapted for survival on a
variety of substratum types.

POTENTIAL FAUNAL-

LITHIC ASSOCIATIONS
Moore (1963) has examined the
sediments of Buzzard Bay with respect to
their potential rock types. Three of the 4
major rock types which he recognized are

represented in the area of study. Certain
observations concerning the fossils which
may be preserved within these types are
possible. The fauna examined here is com-
posed entirely of animals possessing hard
parts suitable for fossilization. These
species must be considered the source for
nearly all potential fossil material.

The 3 compositional types within the
area are proto-graywacke, feldspathic
sand, and quartzose sand. As indicated by
Moore (1963), silts have a distribution pat-
tern similar to that of the proto-graywacke.
Moore's proto-graywacke facies includes
all of the offshore and shallow protected
facies as well as most of the nearshore
facies of the present study. It is essentially
analogous to Sanders’ (1958, 1960) Nucula
proxima - Nephtys incisa community in
areal extent. His feldspathic and quart-
zose sands are found within the open bay
facies of the present study and are analog-
our to Sanders (1958, 1960) Ampelisca
(amphipod) assemblage.

It has been pointed out that clear faunal
differences exist between the 3 “fine
grained’ facies and the open bay facies.
These differences, attributable to a variety
of factors, should be reflected by con-
trasting fossil faunas in the graywacke and
the feldspathic and quartzose sandstones.

Species of importance in the area of
feldspathic and quartzose sands which are
suitable for preservation are largely sus-
pension feeding bivalves and carnivorous
gastropods. These, or comparable forms,
might therefore be expected to constitute
the bulk of preserved species in rocks that
were formed in similar environments with
similar sedimentary parameters in the
geologic past.

Sandstones demonstrating faunal
assemblages that are analogous in some
respects to this recent molluscan com-
munity are not uncommon even during
the Paleozoic. Two fossil assemblages
serve as examples. McAlester (1962) has
described the bivalve fauna of the Devo-
nian Chemung Stage of New York. In this
sandstone the majority of the bivalves
appear to represent suspension feeding
species. Certainly Leptodesma, the most

39

MOLLUSC-SEDIMENT RELATIONSHIPS

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51
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where N

FIG. 33. Species relationship to mean grain diameter of sediment. The thin line
species within this range. Mean occurrence is calculated as follows:

Station i.

DRISCOLL AND BRANDON

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MOLLUSC-SEDIMENT RELATIONSHIPS 4]

common genus, seems to have been a
suspension feeding, and probably an
epifaunal, form. This is suggested by a
shape unsuitable for rapid burrowing, the
possible presence of a byssal notch, and
the general pterioid character of the
genus.

A second example is represented by the
Mississippian Marshall Sandstone of
Michigan. The bivalves described from
this formation (Driscoll, 1965, 1969;
Hutchison & Stumm, 1965) are largely
suspension feeders. Both infaunal and
epifaunal species are abundant. Suspen-
sion feeding brachiopods also comprise a
significant portion of the fauna.
Gastropods are not common, but the car-
nivorous element of the fauna can be
recognized in the wide variety of
cephalopods described from this formation
by Miller & Garner (1953a, 1953b, 1955).
Bretsky (1968, 1969a, 1969b, 1970a,
1970b) has presented a well documented
case for the areal separation of trophic
groups in Paleozoic strata.

The writers believe that the suspension
feeding and carnivorous fauna reported
here from the open bay facies of Buzzards
Bay may be generally typical of many
feldspathic and quartzose sands. It appears
that, with the obvious exception of those
rocks subjected to unfavorable diagenetic
processes, evidence of comparable faunal
associations may be expected in similar
lithologies in the geologic past.

The proto-graywacke recognized т
Buzzards Bay by Moore (1963) is
associated with those species common in
the 3 fine grained facies (shallow pro-
tected, nearshore, and offshore). These are
largely infaunal selective deposit feeders
such as Macoma, Yoldia, and Nucula.
Carnivorous gastropods are of somewhat
lesser abundance.

Inasmuch as deposit feeding bivalves
are important preservable elements in the
proto-graywacke it would seem that they
should constitute an important fossil fauna
in older graywackes. However, many gray-
wackes are unfossiliferous.

We suggest that the thin shells of typical
deposit feeding bivalves are easily

destroyed by post-mortem processes and
are poorly suited for preservation. These
shells are delicate and differ markedly
from the thicker, usually more compact,
heavily ridged forms characteristic of the
suspension feeders examined here. Al-
though many graywackes may have sup-
ported large populations of deposit feed-
ing species during deposition, the shells of
these species are not generally preserved
as fossils. Moore (1963) points out that
leached shell material is present in most of
his proto-graywacke samples. Thus, shell
destruction is occuring even in this early
stage of diagenesis. Driscoll (1970), on the
basis of a 3 year field study, suggests that
differential burial of shells of varying
architectural types in the nearshore facies
may result in the selective destruction of
thinner and lighter valves by shell-boring
organisms active above the sediment-
water interface.

SUMMARY

1. Four facies are defined within north-
western Buzzards Bay. These are the
shallow protected, offshore, nearshore,
and open bay facies. The shallow рго-
tected facies is characterized by depths of
less than 3 m, mean grain diameters
smaller than 2.5 (0.18 mm), sorting that
becomes better with increasing mean grain
diameter, high silt-clay percentages, and
an abundance of selective deposit feeders
of which Nucula proxima is the most
common. The offshore facies is character-
ized by water depths greater than 9 m,
mean sediment diameters smaller than 34
(0.125 mm), Trask sorting coefficients
from 1.40-1.81, high silt-clay percentages,
and an abundance of deposit feeders, of
which Yoldia limatula and Nassarius trivit-
tatus are most common. The nearshore
facies, found in an area of partially pro-
tected harbor mouths, is characterized by a
water depth of between 3 and 7.5 m, a
mean grain diameter not larger than 2.5@
(0.18 mm), sorting coefficients between
1.81 and 2.88, relatively high silt and clay
content, and an abundance of deposit
feeders and carnivores, of which the most
common are Macoma tenta, Yoldia

42 DRISCOLL AND BRANDON

limatula, Eupleura caudata, and Nassar-
ius trivittatus. The open bay facies is
strikingly different from all others in the
area. It is characterized by sediments with
a mean grain diameter larger than 2.56, a
high degree of sorting, a low silt-clay con-
tent, and a more diverse fauna which
consists largely of suspension feeders and
carnivores.

2. The areal distribution and relation-
ship to mean grain diameter, silt-clay con-
tent, abundance of dead shell material,
and feeding type of 39 molluscan species
are discussed. The factors most clearly cor-
related with the distribution of these
species are feeding type, clay content of
the sediment, abundance of dead shell
material and substratum stability. In-
faunal suspension feeders are most sen-
sitive to sediment mean grain diameter (a
reflection of current velocity). Attached
epifaunal suspension feeders are most sen-
sitive to the presence of dead shell material
to which they become fixed and to the
stability of the surrounding substratum.
Selective deposit feeders are most sensi-
tive to the abundance of clay sized par-
ticles—a reflection of the availability of
organic detritus in the sediment.

3. Potential faunal-lithic associations
are discussed. The shallow protected, off-
shore, and nearshore facies are proto-
graywackes. The potential fossil fauna is
composed largely of selective deposit
feeders. It is suggested that the common
absence of representatives of this trophic
group in the fossil record is due to the
effects of post-mortem processes upon
these mostly thin-shelled species. Thick-
shelled suspension feeders make up a
significant portion of the potential fossil
assemblage of the open bay facies. These
species are generally comparable to those
found in similar lithified sediments in the
geologic past.

ACKNOWLEDGEMENTS
We wish to express our appreciation to
the Old Rochester Regional School Board,
Rochester, Massachusetts, and to Donald
N. Gavin, David S. Hagan, Joseph С.
Kunces, and Benjamin R. Tilden for pro-

viding laboratory space and equipment
throughout the summer of 1965. Alicia M.
Crabbe, Maureen C. Duff, Dennys A.
Grady, Phyllis C. Hartley, and Johanna
Teachman acted as laboratory assistants.
Ruth A. Swanson assisted in the labora-
tory phases of the work and in final
preparation and reading of the manu-
script. We are grateful to C. J. Bayne,
Oregon State University, and D. C.
Rhoads, Yale University, for reading the
manuscript and providing many helpful
suggestions. This work was partially sup-
ported by a Wayne State University Facul-
ty Fellowship and was completed at the
Marine Biological Laboratory, Woods
Hole, Massachusetts.

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44 DRISCOLL AND BRANDON

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ZUSAMMENFASSUNG

DIE BEZIEHUNGEN ZWISCHEN MOLLUSKEN
UND IHREM SUBSTRAT IN DER NORDWESTLICHEN
BUZZARDS BAY, MASSACHUSETTS, U.S.A.

E. G. Driscoll und D. E. Brandon

Viererlei Beschaffenheit findet man bei dem Grund des nordwestlichen Teils der
Buzzards Bay, Massachusetts. Diese sind gekennzeichnet durch Unterschiede in der
durchschnittlichen Korngrósse, Zusammensetzung, Gehalt an Tonschlamm und Fauna.
Eine mittlere Korngrösse unter 2,54(0,18mm) ist charakteristisch für 3 dieser Böden, die
an geschutzten Stellen vorkommen. Der vierte, den man an Stellen findet, die der
Strömung ausgesetzt sind, ist normalerweise aus groberem Material zusammengesetzt.
Der Gehalt an kohlensaurem Kalk ist eine Folge des Reichtums an leeren Schalen im

ganzen Gebiet.

Die Faunen der 3 feinkörnigen Substrate sind charakterisiert durch (1) Nucula
proxima, (2) Yoldia limatula und Nassarius trivittatus, und (3) Macoma tenta, Nucula
proxima, Eupleura caudata und Nassarius trivittatus. In den feinkörnigen Böden sind
weniger Molluskenarten vorhanden als in den groberen Ablagerungen des vierten.

Mehr als 35 Molluskenarten werden besprochen, von denen die Mehrzahl dauerhafte
Hartteile hat. Die Beziehung von Korngrösse, Schlamm- und Tongehalt und Vorhanden-
sein toter Schalen zu der Verteilung wichtiger Faunenelemente wird untersucht.
Macoma tenta, Yoldia limatula, Nucula proxima und Solemya velum werden häufiger
bei Abnahme der Korngrösse und Zunahme des Schlamm- und Tongehaltes des Bodens.
Chaetopleura apiculata, Anadara transversa, Crassinella mactracea und viele andere
Arten werden bei Zunahme der Korngrösse und Abnahme des Schlamm- und
Tongehaltes häufiger. Die Menge der toten Schalen auf dem Boden hängt eng mit der
Entwicklung der daran gehefteten Epifauna zusammen.

MOLLUSC-SEDIMENT RELATIONSHIPS

Die vorkommenden Faunengesellschaften zeigen, dass Muscheln, die suspendierte
Kleinpartikel fressen, und räuberische Gastropoden sich in dem grobbkörnigen
Untergrund aufhalten, und dort fossil werden. Mogliche Fossilien der Proto-Grauwacke,
die die 3 feinkörnigen Boden bildet, sind Muscheln, die vorwiegend Schlamm fressen.

HZ.
RESUME

RELATIONS ENTRE MOLLUSQUES ET SEDIMENTS DANS LE NORD-OUEST
DE BUZZARDS BAY, MASSACHUSETTS, U.S.A.

E. G. Driscoll et D. E. Brandon

Quatre facies ont été definis dans les sédiments actuels de la portion Nord-Ouest de
Buzzards Bay, Massachusetts. Ceux-ci sont caracterisés par des différences dans le
diamétre moyen des grains, le triage, le contenu argilovaseux et la faune. Un diametre
moyen de moins de 2,5¢ (0,18 mm) est caracteristique de 3 de ces facies, qui se
rencontrent dans des zones protégées. Le 4eme, qui se développe sur des fonds balayés
par les courants, est typiquement constitué de sédiments plus grossiers. La quantité de
carbonate de calcium dans les sédiments est en relation avec l'abondance de coquilles
vides dans l'ensemble de l'aire considérée.

Les faunes des 3 facies à granulométrie fine sont caractérisées comme suit: (1) Nucula
proxima, (2) Yoldia limatual et Nassarius trivittatus, (3) Macoma tenta, Nucula proxima,
Eupleura caudata et Nassarius trivittatus. Пу a moins d'espèces de mollusques dans ces
facies & granulometrie fine que dans les sédiments grossiers du 4eme facies.

Plus de 35 especes de mollusques ont été analysées, la plupart ayant des parties dures
conservables. On a examiné la relation entre le diamètre moyen des grains, l'abondance
de vase et d’argile, la présence de coquilles vides et les elements importants de la faune.
Macoma tenta, Yoldia limatula, Nucula proxima et Solemya velum augmentent en
abondance quand décroit le diamètre moyen des grains et que s accrcit la quantité de
vase et d'argile dans le sédiment. Chaetopleura apiculata, Anadara transversa,
Crassinella mactracea et bien d'autres especes, augmentent en abondance quand le
diamètre moyen des grains augmente et que décroit la quantité de vase et d'argile du
sédiment. La quantité de coquilles vides sur le fond est étroitement en relation avec le
développement de l'épifaune fixée.

Les associations zoo-lithiques latentes montrent que les Bivalves suspensivores et les
Gastropodes carnivores sont disponibles pour une conservation dans les facies grossiers.
Les fossiles latents des proto-grauwackes, qui sont issus des 3 facies & grain fin, sont en
grande partie constitués de Pélécypodes déposivores. Me

RESUMEN

RELACIONES ENTRE MOLUSCOS Y SEDIMENTOS EN
EL NOROESTE DE BUZZARDS BAY, MASSACHUSETTS, U.S.A.

E. G. Driscoll y D. E. Brandon

En los sedimentos del Reciente del noroeste de Buzzards Bay, Massachusetts, se
definen cuatro facies, caracterizadas por diferencias en el término medio del diämetro de
los gránulos, el contenido de arcilla о limo, у la fauna. Un promedio de granos con
diámetro menor de 2.54 (0.18 mm) es caracteristico de tres de estas facies, la cuales
aparecen en áreas protegidas. La 4ta, que se desarrolla en fondos barridos por la
corriente, está tipicamente compuesta por sedimentos más gruesos. El contenido de
carbonato de calcio en el sedimento refleja la abundancia de conchas muertas en toda el
área.

Las faunas de las 3 facies de grano fino se caracterizan por: (1) Nucula proxima, (2)
Yoldia limatula y Nassarius trivittatus y (3) Macoma tenta, Nucula proxima, Eupleura

45

46

DRISCOLL AND BRANDON

caudata y Nassarius trivittatus. Е número de especies de moluscos es memor en estas
facies de grano fino que en la del 4to sedimento.

Se discuten más de 35 especies, la mayoría con partes duras conservables. La relación
del promedio de diámetro granular, abundancia de limo o arcilla, y la presencia de
conchas muertas, a la distribución de elementos faunisticos importantes, fueron
examinados. Macoma tenta, Yoldia limatula, Nucula proxima y Solemya velum, crecen
en abundancia en proporción inversa al aumento del promedio de diámetro granular, y el
aumento del contenido limo-arcilla del sedimento. Chaetopleura apiculata, Anadara
transversa, Crassinella mactracea y muchas otras especies son mas abundantes cuando el
promedio del diámetro de los granos es mayor y el sedimento contiene menos limo-
arcilla. La cantidad de conchas muertas en el fondo esta estrechamente relacionada al
desarrollo de epifauna adherida.

Asociaciones fauno-liticas potenciales indican que los bivalvos que se alimentan de
materias en suspención y gastropodos carnivoros son preservados en las facies de grano
grueso. Fósiles potenciales de la proto-arenisca gris, la cual compone las tres facies de
grano fino, son en su mayor parte pelecipodos que se alimentan de materias en

deposición.
JJ.P.

ABCTPAKT

ОТНОШЕНИЕ МОЛЛКСКОВ К ДОННЫМ ОСАЛКАМ (В СЕВЕРО-ВОСТОЧНОЙ
ЧАСТИ ЗАЛИВА БУЦЦАРД, МАССАЧУЗЕТС, C.I.A.)

Е.ДЖ. ДРИСКОЛЛ И Д.Е. БРЕНДОН

В современных осадках северо- восточной части залива Буццард, Масс.,
было найдено 4 фации. Они характеризовались различиями среднего
диаметра гранул осадков, их размерным составом, содержанием силта.и
фауны. Средний размер гранул менее 2.508 (0.18 мм), был характерен для
3-х из этих фаций, встречающихся в защищенных районах залива. Четвёртая
встречена на дне, омываемом быстрым течением, и, как правило состояла из
более грубых осадков. Содержание карбоната кальция указывало на обилие
повсюду отмерших раковин моллюсков.

Фауна трех тонко-зернистых фаций характеризуется наличием
1) Nucula proxima; 2) Yoldia limatula и Nassarius trivittatus, и 3) Масота tenta,
Nucula proxima, Eupleura caudata и Nassarius trivittatus. B этих тонко-зернистых
фациях количество видов моллюсков меньше, чем на более ‘грубых осадках
4-ой фации. В работе рассматривается более 35 видов моллюсков, большая
часть которых имеет твердые защитные части. Изучалось соотношение
среднего гранулометрического состава осадков, обилие силта и глин и
наличия отмерших раковин - к распространению главных элементов фауны.
Обилие Масота tenta, Yoldia limatula, Nucula proxima и Solemya velum
увеличивается по мере уменьшения среднего диаметра гранул осадка и
увеличения содержания силта и глин.

Обилие Chaetopleura apiculata, Anadara transversa, Crassinella mactracea и пругих
видов увеличивается по мере увеличения среднего диаметра гранул осадка и
уменьшения содержания в нем силта и глин. Количество отмерших в нем
раковин на дне тесно связано с развитием прикрепленной фауны.

Потенциальные Ффаунистическо-литологические ассоциации указывают, что
фильтраторы Bivalvia и хищные Gastropoda сохраняются на более жестких
грунтах. Потенциально-фоссильные моллюски, населяющие 3 тонко-зернистых
фации, являются, в основном, двустворчатыми моллюсками, собирающими детрит

с поверхности осадков.

MALACOLOGIA, 1973, 12(1): 47-96

SALINITY TOLERANCE OF SOME MARINE BIVALVES
FROM INSHORE AND ESTUARINE ENVIRONMENTS
IN VIRGINIA WATERS ON THE WESTERN MID-ATLANTIC COAST!

М. Castagna and P. Chanley?

ABSTRACT

Many species of estuarine bivalves have a distribution pattern closely cor-
related with salinity, indicating the importance of salinity in determining these
patterns. The approximate salinity tolerance range for 36 species of bivalves. is
described. Tolerance limits for 29 species were determined in laboratory experiments.
Most of these species display a remarkable degree of euryhalinity. All survived
a minimum salinity of at least 17.5% ап4 25 species survived at 12.5%. Twenty species
survived at various lower salinities.

Salinity tolerance for a given species is not constant but varies with season,
salinity experience, and temperature. Burrowing, feeding and reproduction usually
occur at nearly all salinities at which survival is possible. Byssal formation requires a
higher salinity than is necessary for other activities.

In Virginia about two-thirds of the species of salt-water bivalves discussed can be
found over the entire salinity range they are capable of tolerating in the laboratory.
Eleven species do not occur over their entire potential salinity range. Eight of the 11
species, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina multilineata,
Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis, are near the
geographic limit of their range; their distribution locally may be limited primarily by
the tactors that determine their geographic range. The distribution of 5 species,
Argopecten irradians, Congeria leucophaeta, Macoma mitchelli, Donax variabilis
and Spisula solidissima, may be influenced by predation, competition, or special
environmental requirements. Four of the 11 species, Congeria leucophaeta, Macoma
mitchelli, Donax variabilis, Rangia cuneata, occur in specialized habitats with low
species diversity.

INTRODUCTION

Бу graphically

distributional patterns
Temperature is usually considered the illustrating a variation in the relative
most important ecological factor in- numbers of species found at various

fluencing the distribution of animals
(Gunter, 1957). Within an estuarine sys-
tem, salinity is generally the more ob-
vious environmental factor (Pearse &
Gunter, 1957). Many species have a dis-
tribution pattern closely correlated with
salinity, and often are categorized accord-
ing to the salinities in which they are
found (Wass, 1965; Menzel, 1964; Wells,
1961) or identified with certain as-
semblages that characteristically occur
in a given salinity range (Ladd, 1951;
Parker, 1959). Pennak (1953) summarizes
the importance of salinity in determining

salinities. Carriker (1967) reviewed the
classification and distribution of organ-
isms in an estuary.

The distribution of most adult bivalve
mollusks may be especially influenced by
salinity since the relative immobility of
these animals usually precludes migration
from adverse salinity conditions. The
literature abounds with accounts of mass
mortalities associated with abnormal
salinity conditions (Baughman, 1947).
However, because of the variable nature
of the environment, it is frequently
difficult to ascertain from field ob-

‘Contribution No. 476 from Virginia Institute of Marine Science.
“Present address: Shelter Island Oyster Company, Greenport, L.I., New York 11944, U.S.A.

48 CASTAGNA AND CHANLEY

servations the precise effect of salinity
on natural distribution. The ability of most
bivalves to adapt to transient conditions of
unfavorable salinities by physical exclusion
(closing of shell, retreat into burrows,
closing of burrows, etc.) rather than by
physiological adaptation further confuses
attempts to determine their salinity
tolerance limits from distributions (Kinne,
1967). Finally, from observations on
natural distribution, it is difficult to
differentiate between the influence of
salinity and several other physical and
biological factors (Kinne, 1967). For exam-
ple, the edible mussel (Mytilus edulis L.) is
limited to high salinity oceanic waters in
Virginia not by salinity but because the
low-salinity bay and inshore waters reach
lethal temperatures in the summer
(Hutchins, 1947; Wells & Gray, 1960;
Read, 1967). The distribution of other
species (Mya arenaria L. and Crassostrea
virginica Gmelin), although overtly
associated with low salinities in certain
areas, may in reality reflect the influence
of predation or biological competition
(Nichy & Menzel, 1962; Menzel, Hulings
& Hathaway, 1958).

Although the bivalve mollusks соп-
situte a sizable biomass of the benthic
and planktonic (as larvae) communities
and are important economically and
ecologically, very few data are avail-
able on the salinity tolerances of most
species. Furthermore, available infor-
mation is based primarily on field obser-
vations.

We have undertaken a study to demon-
strate more precisely the salinity toler-
ance of many species of bivalves occurring
in the study area and with this informa-
tion determine the influence of salinity
on natural distribution. This includes a
review of literature, experimental work
and a discussion to correlate and evaluate
results.

The scope of these studies has been
limited to the effects of salinity on
bivalves from the inshore marine and
estuarine environments of Virginia as
listed by Wass (1965). Since it is our
purpose to survey the salinity tolerances

of many species rather than to treat a
few exhaustively, emphasis has been
placed on the effects on activity and
survival of adults. The influence of
salinity on growth and reproduction and
its possible effect on the distribution
of a species has received only cursory
treatment in our experimental work.

PROCEDURE, METHODS, AND
MATERIALS

Collections were made from 24 inshore
and estuarine sites (Fig. 1). Spisula solidis-
sima collections were supplemented by
specimens from a commercial dredge boat
working off Point Pleasant, New Jersey, in
depths of 50-100 feet. Most collections
were made in estuarine areas, such as the
James and York Rivers, or in small tidal
creeks, such as Occohannock ог
Pungoteague Creek. These creeks and
rivers drain into the Chesapeake Bay, and
are usually sand or sand-mud areas with
little or no vegetation. Plants, when pre-
sent, were predominantly Zostera or
Zostera and Rupia together. Salinities were
usually below 22%o.

The high salinity species were collected
from ocean beaches on the barrier islands
east of the Delmarva Peninsula (land
mass forming the eastern boundary of
Chesapeake Bay) or Нот the small
bays, creeks, or lagoons between these
barrier islands and the peninsula. These
were high salinity areas (27-32%) with
very turbid waters, peat or sand sub-
strata on the beaches and usually soft
mud or sand-mud in the bays and lagoons.
Specific information on collection sites
is shown in Table 2.

Salinity tolerances were determined
experimentally for 29 species. A few
species were not included because they
could not be collected in suitable numbers
for experimentation. No experimental
work was attempted when salinity
tolerances could be determined adequately
from published accounts. Except where
otherwise noted, geographical ranges are
from Abbott (1954). Attempts were made
to follow the experimental procedures
outlined below, but because of the

PACIFIC OCEAN

SALINITY TOLERANCE OF MARINE BIVALVES

af
Le,
\
\

MEXICO

SOUTH
AMERICA

FIG. 1. Sites collected for species used in salinity tolerance experiments.

49

50 CASTAGNA AND CHANLEY

uniqueness of each species, modifica-
tions were often necessary.

Experimental salinities ranged from
0-30% at intervals of 2.541%. At
the beginning of each experiment, a
group of 10 animals was placed
directly in each salinity. The control was
the group placed in the experimental
salinity that most closely approximated
the salinity from which the animals were
collected. The control was maintained at
the same salinity throughout the ex-
periment.

After animals had adapted to ex-
perimental salinities, as determined by
survival, filtering?, burrowing or other
activity, groups were transferred by steps
to different salinities at а rate of
2.5+1% per 48 hours or on occasion per
24 hours in an attempt to further extend
the salinity range. When the maximum
salinity range was determined in this man-
ner, surviving groups were transferred
directly to either the opposite extreme
salinity at which any had survived or to the
control salinity to determine if they could
adapt to greater salinity changes in the
reverse direction.

Observations were made daily and con-
sisted of counting survivors, removing and
measuring length of dead animals, coun-
ting those that had burrowed or attached
by byssus, and observing the ability of
animals to filter algae. Observations were
also made of nest-building by Amygdalum
papyria (Conrad) and reproduction by
Gemma gemma (Totten). Animals were
not considered dead unless they gaped and
failed to respond to repeated tactile
stimuli or were obviously putrescent.
Ability to burrow was assumed if the
animal was wholly or partly buried in a
natural position. Burrowing animals were
dug up weekly to determine continued
ability to burrow. Ability to filter was
noted by the clearing of algae from the
water and by fecal deposition.

Experimental animals were collected
from many areas throughout the entire

year. Collection details are summarized in
Table 1. Since smaller individuals were
more active and adapted better to labora-
tory life, the smallest specimens available
were used. Sufficient animals were ob-
tained so that 10 could be maintained
in each experimental container. Whenever
possible, experiments were repeated until
at least 40 animals were exposed to each
experimental salinity. Although repeat
experiments with the same species often
included different populations, or were
conducted at different seasons of the year,
experimental results involving one species
have been combined. It was sometimes
necessary to hold animals until there was a
sufficient number for an experiment. They
were held in water of the same salinity
as the area in which they were collected.
All weak, damaged or dying animals were
discarded before starting an experiment.

Experimental details are summarized in
Table 2. In each experiment, animals were
maintained in containers with 400 cc,
3 liters or 6 liters of standing water
(depending on the size of the animals).
Aeration was provided for those species
that displayed poor survival in holding
containers or preliminary experiments
without it.

Experimental salinities were adjusted by
diluting salt water from the laboratory
sea water system with pond water from
the irrigation pond at the Virginia Truck
Experiment Station, Eastern Shore
Branch, Painter. This source of fresh
water was chosen because the volume of
water needed precluded the use of distilled
water and preliminary experiments
indicated that tap water was unsatis-
factory. The total salt content of the pond
water was 80 ppm.

Water temperature was taken daily and
the range for each experiment is given
in Table 2. No means of controlling
temperature were used. Since temperature
varied considerably, average range
was 7.4°C, no attempt has been made to
more precisely present mortality and

‘Throughout this paper, animals are reported as filtering if they cleared the water of suspended phytoplankton,
even though at high algal densities most of the algal cells may have been rejected in pseudofaeces.

51

SALINITY TOLERANCE OF MARINE BIVALVES

1991 ©)

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58

adaptation rates influenced by tempera-
ture.

Water was changed 3 times weekly,
and at each change a heterogeneous mix-
ture of phytoplankton was added (except
in fresh water) so that observations on the
filtering ability of the moilusks
could be made. The algal mixture was
predominantly Chlorella from a culture
obtained by fertilizing sea water with
commercial inorganic 5-10-5 fertilizer
(Loosanoff & Engle, 1942). After mixing,
salinity was checked by hydrometer and,
if necessary, corrected to within 1% of
the desired salinity.

Beach sand, collected from Cedar Island
or the Machipongo River, was used as the
substratum in all experiments except for
those involving species incapable of
burrowing. The depth of sand varied with
the size of the experimental animals.

Polyethylene, fiberglass or glass con-
tainers were used in the experiments and
for collecting and storing animals, sand
and water.

SALINITY TOLERANCE BY SPECIES

Order Protobranchia
Family Solemyidae
Solemya velum Say (Tables 1,2,3)
The awning clam is found commonly in

CASTAGNA AND CHANLEY

shallow muddy areas from Nova Scotia
to Florida. It is relatively scarce in
the collection area and is usually asso-
ciated with Zostera marina at salinities
above 15% (Wass, 1965).

Most Solemya survived direct transfer
from either 30.8 or 34.4 %o to experimental
salinities as low as 20% (Table 3). One
clam out of a group of 30 survived
transfer from 30.8% to 17.5%: none to
lower salinities. However, clams survived
at lower salinities after acclimation
to intermediate salinities. A few survived
at 12.5% after acclimation, but most
of the Solemya were unable to survive
below 15 %o .

Essentially the same salinity limits were
established for burrowing and filtering as
for survival. Again, the minimum salinities
could be reduced to 12.5% by gradually
acclimating clams to intermediate
salinities. Frequently, filtering and
burrowing were observed at salinities that
eventually proved lethal.

Family Nuculidae
Nucula proxima Say

The nut clam is a common subtidal
mud dweller found from Nova Scotia to
Florida and Texas. Menzel (1964) lists
this species as occurring at salinities

TABLE 3. Response of Solemya velum Say to different salinities. Salinity at collection sites was 34.4

and 30.8%.

% Surviving

Highest % burrowing

Feeding (0= попе, R=
reduced, N=normal)

After After After
Salinity direct After direct After direct After
%o transfer acclimation transfer acclimation transfer acclimation
0 0 0 O O
29 0 0 O O
5.0 0 0 O O
ES 0 0 O O
10.0 0 0 0 O O
19:5 0 7.4 0 64.1 O R
15.0 0 84.6 0 100 O N
17.5 3.3 92 26.7 100 R N
20.0 86.3 92.3 100 100 М М
22.5 90.0 100 100 100 М М
25.0 89.7 100 100 100 М М
DD 90.0 100 N
30.0 96.7 100 N

SALINITY TOLERANCE OF MARINE BIVALVES 59

above 25% in Florida. It occurs in
sand to silty sand, at salinities above
20% (Wass, 1965).
Family Nuculanidae
Yoldia limatula (Say)

The file yoldia is found along the
East Coast from Maine to New Jersey
but rarely in lower Chesapeake Bay
(Wass, 1965). Natural distribution
is probably limited to areas where salinity
is above 20% (Wass, personal communica-
tion).

Order Prionodontida

A major problem encountered with the
Arcacea was their sluggish response to
experimental conditions. In lower salinities
they sometimes seemed narcotized and
were often found gaping widely. They did
not react to stimuli but, after being
removed from the water, eventually
closed. Some animals may have been
removed as dead from earlier experiments
before this trait was discovered. Even-
tually, only putrescent individuals were
considered dead.

Family Arcidae

Anadara transversa (Say) (Tables 1, 2,
4)

The little blood clam occurs commonly
in subtidal mud from Cape Cod to Florida
and Texas. It is common in Chesapeake
Bay and its tributaries in intermediate
salinities (15-25% ) but is scarce at higher
salinities (Andrews, 1953). It has been
reported as occurring in areas where
salinity varies from 3-42% (Parker,
1955) and 16-40% (Ladd, 1951). In
Florida it is found at salinities above
25% (Menzel, 1964).

Anadara transversa were collected on 2
occasions from salinities of 17.5 and
25%, respectively. All died after direct
transfer to salinities of 7.5%) and lower
(Table 4). Only 2 clams out of 20
from 17.5% and none out of 20 from
25% survived direct transfer to 10%.
Ninety percent of all clams survived
direct transfer to salinities from 12.5-
30.0%. After acclimation, all clams sur-

vived at 10%, and 85% originally taken
from 17.5% survived at 7.5%, although
all those from 25% died at 7.5% (Table
4).

After acclimation, clams were trans-
ferred directly to the opposite extreme of
the salinity range. Transfers from 12.5 to
30% and 30 to 12.5% were effected
without mortality. Only 2 out of 18 sur-
vived transfer from 30 to 10%.

When clams were transferred directly to
experimental salinities, suspended algae
were cleared within the salinity range of
10-30%, but several days elapsed before
normal filtration occurred below 17.5%o
(Table 4). Filtering at 10 and 12.5 % was
always reduced unless clams were first
acclimated at 15%. After acclimation,
some clams cleared the suspended algae
from the water irregularly at 7.5%o.

At no time did a majority of blood
clams burrow into the substrate. Active
clams usually climbed the sides of
experimental containers by byssal attach-
ment. Consequently, few burrowed after
they became acclimated to experimental
conditions (Table 4). At salinities close
to the minimum for survival, burrowing
was more obvious, presumably because
clams were not active enough to reach
the sides of the containers. Byssal
attachment occurred at 7.5-30 %o but clams
were slow to attach below 12.5% and
then only after acclimation at intermediate
salinities (Table 4).

Anadara ovalis (Bruguiere) (Tables
12.5)

The round blood clam is common and
widely distributed from Cape Cod to the
West Indies and the Gulf states. It is
common subtidally in mud in both
Chesapeake Bay and Eastern Shore
lagoons. Andrews (1953) reported it as
occurring in salinities above 15 %. Menzel
(1964) found it at salinities above 25%
in Florida.

All clams transferred directly from a

‘salinity of about 30% to 12.5% and

lower died (Table 5). Only 45% survived
direct transfer to 15% while 90-100%
survived at all higher salinities. In 1 case

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62 CASTAGNA AND CHANLEY

a higher mortality occurred at 27.5 % in
1 container. Clams in replicate containers
survived well.

Most blood clams survived at 15%
if salinity was reduced gradually. Nearly
85% of the blood clams acclimated at
17.5 and 20% survived when moved
gradually to 12.5%. Clams surviving
direct transfer to 15% were moved to
12.5%: all died. Although acclimated
clams survived exposure to 10 and 12.5%
for extended periods, it is doubtful they
could survive indefinitely at these
salinities.

Two groups of Anadara ovalis, ac-
climated to intermediate salinities and
then kept at 10% and 12.5 % for 5 days,
were transferred directly to 30%o. Only
six out of 17 survived the transfer from
10 to 30% and none of these had
burrowed when the experiment was con-
cluded 13 days after the transfer. Of
the 19 clams moved from 12.5 to 30%o,
18 survived but 11 days elapsed before
the number burrowing was normal.

After direct transfer to experimental
salinities clams were slow to start filtering
but did clear the water of algae in salinities
down to 20%o during the second day.
Eventually, clams at 17.5%o filtered and
cleared the water consistently. Although
some filtering occurred at 10%, it was
never normal when clams were transferred
directly to salinities lower than 17.5%.
Filtering occurred at 7.5%, after acclim-
ation, but it was not consistent or
normal below 15%.

Anadara ovalis were slow to burrow at all
salinities and 5 days elapsed before 80%
had burrowed, even at 30%. Seven
days were required for a comparable
percentage at 22.5-27.5% and even
longer for those at 20%. At 17.5 % and
15 % a much lower percentage of clams
burrowed. After acclimation, more clams
burrowed at 17.5 and 15 % but burrowing
activity was still reduced at these salinities.
Acclimated clams also burrowed at 12.5%,
but activity was irregular.

Comparatively few blood clams
attached by byssus during the experi-
ments. These clams were much less motile

than Anadara transversa and, unless they
were near the sides of the container, had
no substratum for attachment. Byssal
attachment occurred at 17.5 %o and higher
but was far less common below 22.5%o
than at higher salinities. The minimum
salinity for byssal attachment could be
reduced to 12.5% by acclimating blood
clams to intermediate salinities. However,
only 1 clam attached by a byssus at 12.5 %o.
A few attached at 15 and 17.5% but
even after acclimation very few clams
attached by byssus below 22.5%o.

Noetia ponderosa (Say) (Tables 1,2,6)

The large blood clam is common in
shallow waters along the Atlantic Coast
from Virginia to Key West. It is a
common bivalve found on the seaside
of the Eastern Shore in channels between
Spartina marshes. It is also present in
deep river channels and in high-salinity
(above 20%) portions of Chesapeake Bay.
Parker (1955) lists this species with a group
found in an area where salinities ranged
from 3-42%. Menzel (1964) records
it in Florida in salinities above 25 %o.

Some blood clams survived for a lengthy
period after direct transfer to all salinities
down to 12.5% (Table 6). However,
mortality continued at 12.5% and 15%,
and eventually all died except 1 clam
at 15%. Mortality was heavy at 17.5%,
but over 75% of the clams kept at 20-30%o
survived. After acclimation to inter-
mediate salinities, blood clams survived
for long periods at 12.5 and 15% though
fewer survived than at 17.5 % and higher.

Clams acclimated to 15, 17.5 and 20%0
in the Ist experiment were transferred
directly to 30%. АП survived, and except
for clams transferred from 15 to 30%,
all were burrowing and feeding normally
within 4 days. Only 3 out of 11 clams
transferred from 15 to 30% burrowed.

Blood clams filtered normally im-
mediately after transfer to salinities of 25-
30%. Clams also filtered immediately
after transfer to 20 and 22.5 %o but did not
consistently clear the water by filtering out
the algae for almost 3 weeks. After the 3rd
week, clams also filtered at 17.5 and 15%

SALINITY TOLERANCE OF MARINE BIVALVES 63

but never consistently cleared the water.
Filtering was rarely observed at 12.5%o
and was never normal. No filtering was
observed below 12.5%. These limits were
not extended by acclimation to in-
termediate salinities.

Noetia ponderosa were especially
sluggish about burrowing in the sand
and required 3-4 days to dig in at
12.5-30.0%o salinity. At 27.5 and 30%,
over 50% burrowed by the 10th day.
Fewer clams burrowed after direct transfer
to 22.5 and 20% but 50% dug in at
22.5% between the 10th and the
20th day. No clams burrowed at 20%o
until the llth day, and only 17.8%
burrowed at this salinity even after 70
days. The minimum salinity at which
any clams burrowed was 17.5%o.

More clams burrowed at 20 and 17.5%o
after being acclimated to intermediate
salinities (Table 6). Even after acclimation,
however, animals did not burrow at lower
salinities.

Byssal attachment was usually observed
in clams burrowed into the bottom. One
clam was found attached to the poly-
ethylene container by byssus at 17.5%
and another at 20% after acclimation.

Byssal attachment was more common at
22.5% but still considerably less than
at 25% and higher. Fewer clams attached
by byssus during the 2nd experiment than
during the Ist, probably because addi-
tional sand left less substratum available
for attachment. Byssal attachment was
less common near the end of experiments.

Order Pteroconchida
Family Mytilidae
Mytilus edulis Linne

Along the eastern coast of North
America, the edible mussel is found from
the Arctic Ocean to South Carolina.
In the collection area, permanent pop-
ulations of M. edulis are apparently
limited by temperature (Hutchins, 1947;
Wells & Gray, 1960; Read, 1967) to the
cooler, highly saline areas around the
mouth of Chesapeake Bay, and to inlets
between the barrier islands along the
Eastern Shore. Catastrophic summer mor-
talities destroy new colonies periodically
established in warmer areas.

Andrews (1956) records M. edulis at
salinities above 15-18% in Virginia.
Dodgson (1928) reports survival from

TABLE 6. Response of Noetia ponderosa (Say) to different salinities. Salinity at collection sites was

30.6 and 32%.

% Surviving Average highest Feeding(0=none, R=
% burrowing reduced, N=normal)
Salinity After After After After After After
oo direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0
29 0 0 O
5.0 0 0 O
1) 0 0 O
10.0 0 0 0 0 O O
IIS 0 19.8 0 0 O O
15.0 275 67.8 0 0 O R
Wee 22:5 91.2 3.1 18.2 O R
20.0 80.0 97.0 17.8 26.2 O N
22.5 1285 100 BET 41.0 R N
2510 85.0 97.4 65.5 52.6 N N
DD 95.0 82.1 N
N

30.0 92.5 84.2

64 CASTAGNA AND CHANLEY

8.75-31%o, but notes defective byssus
formation below 16% and irregular
pumping below 12%. Schlieper (1953)
found a reduction of oxygen consumption,
ciliary activity and heart rate below 15%.
Prosser & Brown (1961), referring to other
works of Schlieper, report M. edulis as
occurring at 4-6%. Motwani (1955)
gives the optimum salinity as 20-40%
but says this is influenced by other
environmental factors.

Bayne (1965) found that larval M. edulis
failed to grow below 14% and that ор-
timum salinity for growth was 18-26%.
Apparently, М. edulis can survive at
salinities less than 10%o, but about 15%o is
necessary for optimum physiological func-
tioning and reproduction.

Modiolus demissus Dillwyn

The ribbed mussel is widely distributed
along the east coast from the Gulf of
St. Lawrence to Florida (Menzel, 1964).
It is found primarily in the intertidal
zone where it occurs at a higher level
than other bivalves. It is plentiful in
seaside salt marshes with near oceanic
salinities and is also found in estuaries
where salinities are considerably below
20%. Andrews (1953) reports it at all
salinities above 8-10 %o.

Wells (1961) experimentally determined
a ‘salinity death point for M. demissus
between 4 and 6%. Vernberg, Schlieper
& Schneider (1963) reported a minimum
salinity of 2% for ciliary activity of gill
filaments and noted a sharp decrease
in activity below 4%. In spite of the
ability of this species to survive at low
salinities, Nagabhushanam (1961) found a
marked reduction in rate of pumping
as salinities decreased from 32 to 10%.
However, his results may show the effects
of change in salinity rather than the
effects of salinity per se.

Brachidontes recurvus Rafinesque

The hooked mussel has been reported
as occurring from Cape Cod to the West
Indies but is probably not commonly
found living north of New Jersey. This
mussel is common in subtidal areas of

Chesapeake Bay and its tributaries where
salinities seldom exceed 20-25%. Pearse
& Wharton (1938) found it at 5%, while
Parker (1959) records it as belonging in
an ‘assemblage’ that occurs from 3-40 % .

In the laboratory Chanley (1958)
found that B. recurvus were not only
alive but had “recognizable” gametes
after 50 days exposure to salinities
from 2.5-27%. Those kept in fresh water
all died within 30 days. Allen (1960),
however, reported 95% mortality of all
mussels kept at salinities below 4.5%
and heavy mortality below 6% in only
19 days. Nagabhushanam (1965) noted
a decrease in heart rate from 35-31 beats
per min. with a drop in salinity from
18-7.2%. A further decrease to 16 beats
per min. occurred between 7.2 and 3.6%.
At 1.8% the heart beat was only 3 beats
per min. Again, these figures may indicate
the effect of salinity change rather than
salinity per se.

The minimum salinity for survival of
this species is probably between 2.5 and
6.0%o.

Amygdalum papyria Conrad (Tables
1,2,7)

The paper mussel is found from
Maryland south to the Gulf of Mexico.
It is found in areas of moderate salinity
such as the lower York and Rappahannock
rivers in Virginia. Although abundant
in limited areas, it is not generally
distributed and is probably the least
known of the mussels. It is apparently
euryhaline and has been reported аз
occurring in areas where salinity may be
as low as 10% (Wass, personal com-
munication) or as high as 45°%o (Parker,
1960).

All mussels transferred directly from
about 20%o to O and 2.5% died (Table 7).
In the 1st experiment all mussels trans-
ferred to 5%o also died. However, 55%
survived this transfer in the 2nd experi-
ment. Best survival was observed at
salinities from 12.5-20%o. The mortality
at higher salinities (22.5-30%0) was not as
abrupt as that at 0, 2.5 and 5% and
occurred only after mussels had apparently

SALINITY TOLERANCE OF MARINE BIVALVES 65

adapted to salinities by filtering normally,
burrowing, attaching by byssus and by
nest-building.

The salinity tolerance limits of Amygda-
lum papyria could be extended only
slightly by moving them gradually to
lower salinities. In the lst experiment 10
mussels surviving at 5% for 31 days
died within 4 days after transfer to 2.5%o.
In the 2nd experiment, however, 17 out
of 23 mussels survived and were main-
tained at 2.5 % for 5-15 days before being
moved to fresh water or before termina-
tion of the experiment. Mussels did not
survive when moved from 2.5% to fresh
water.

After direct transfer to experimental
salinities, some mussels burrowed in all
salinities from 2.5-30%o though the per
cent burrowing was reduced below 12.5%o.
After acclimation in intermediate salin-
ities, burrowing was apparently normal
whenever mussels survived. However, a
smaller percentage of mussels burrowed
late in the experiment regardless of
salinity. Some burrowing occurred at salin-
ities which eventually proved lethal. Three
mussels burrowed even in fresh water but
did not repeat the performance when dug

up 2 days later.

Filtering was apparently normal at
10% and higher, though in the 2nd
experiment it was initially reduced at
10%o. Normal filtering was occasionally
observed at 2.5 and 5% after prolonged
exposure to these salinities.

Byssal attachment and nest-building
were possible at any salinity in which
animals survived. A. papyria differs
from the more familiar Mytilus edulis
in this respect, since the latter is capable
of surviving in salinities at which byssus
formation is defective (Dodgson, 1928).

Family Ostreidae

Crassostrea virginica Gmelin

The American oyster is common inter-
tidally and subtidally from the Gulf
of St. Lawrence south to the Gulf of
Mexico. It is widely distributed in Virginia
where salinities are higher than 6-10%o
(Andrews, 1953).

The oyster has been the subject of
much research and no attempt is made
here to present a complete review of all
pertinent literature. Only a few references
are cited to establish the salinity tolerance
of this species. Baughman (1947) and,

TABLE 7. Response of Amygdalum papyria (Conrad) to different salinities. Salinity at collection

sites was about 21%o.

% Surviving Average highest Feeding (0= попе, R=

% burrowing reduced, N=normal)
Salinity After After After After After After

%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer

0 0 0 O 10)
29 0 JON 5.0 50.0 O R
5.0 27.5 60.5 27.9 53.0 R R
aS 55.0 86.0 65.0 45.6 В В
10.0 70.0 94.6 TOD) 52.8 N N
125 82.5 9741 97.5 76.0 N N
15.0 95.0 90.0 100 100 N N
7.5 75.0 100 М М
20.0 75.0 100 N N
22.9 40.0 100 N N
25.0 45.0 97.5 N N
27.9 45.0 95.0 N N
30.0 37.0 90.0 N N

66 CASTAGNA AND CHANLEY

more recently, Galtsoff (1964) give refer-
ences describing the salinity tolerance of
oysters.

Salinity limits for survival. Oysters can
survive over a wide range of salinities.
Ingle & Dawson (1951) report commercial
production in areas with an annual salinity
variation from 0-42.5%. Butler (1952)
found self-sustaining populations in areas
where salinity ranged from 0.2-3.6%o for 5
consecutive months annually. However,
field observations by many investigators
set the minimum salinity for indefinite sur-
vival at 4-5 % (Ryder, 1885; Arnold, 1868;
Belding, 1912; Loosanoff, 1932; and many
others). Parker (1960) observed that oyster
reef formation occurs only between
salinities of 10 and 30%o even though
oysters are found outside these limits. The
optimum salinity range for survival has
been described as 14.1-22.2%o (Moore,
1900). Galtsoff (1964) states, according to
the Venice system of classification of saline
waters adopted by the International
Association of Limnology and the Inter-
national Union of Biological Sciences in
1958, that the range of salinity favorable
for C. virginica falls within 2 zones, the
polyhaline (30-18%) and the mesohaline
18-5 oo ).

Laboratory experiments show close
agreement with these field observations.
Vernberg et al. (1963) found a marked
decrease of ciliary activity in excised gill
tissue below 4%. This agrees well with
Fingerman s (1959) earlier report that
ciliary activity occurred between 5 and
35%. According to Loosanoff (1952),
some oysters survived when kept con-
stantly at 5% although there was а high
mortality. Survival was normal at 7.5%o
and higher. Chanley (1958) reports similar
salinity limits for recently metamorphosed
C. virginica.

Salinity limits for growth and feeding.
In Canadian waters, oysters apparently do
not “fatten” or increase proportionally in
dry weight when salinity drops below 20 %0
(Medcof & Needler, 1941; Medcof, 1944).

According to Nelson (1923), the
minimum salinity at which growth and
feeding occur is based on the salinity

at which the oyster is acclimated.
Loosanoff (1952), however, maintains that
oysters adapt rapidly to salinity change
and resume pumping activities
within a few hours. He noted that a
salinity of 10% is the minimum for
normal growth of adult oysters. He
observed feeding at 5% but says no
growth occurred below 7.5%. Chanley
(1958) reported slight growth of recently
metamorphosed oysters at 5%, with
optimum growth between 12.5 and 25%.

Salinity limits for reproduction. The
minimum salinity for gametogenesis has
been reported as 6% by Butler (1949),
who noted delay of gametogenesis until
salinity rose above this level. Loosanoff
(1952) reported 7.5 % as the minimum for
gametogenesis.

Davis (1958) observed egg cleavage
from 7.5-35%o with good development
from 10-22.5%. Much higher limits were
given by Amemiya (1926) who records egg
development from 18-40.1%, with an
optimum range of 19.3-35.1%o. Larval
development has been reported as
occurring between 14 and 39%
(Amemiya, 1926), with optimum devel-
opment between 25 and 29%. Clark
(1935) is in general agreement with these
ranges. Nelson (1909), however, found
larvae in plankton samples when salinity
was as low as 11.5%. Furthermore, Davis
(1958) reported larval growth at as low as
5%, with the optimum between 17.5 and
22.5%. Under certain lighting conditions,
Haskin (1964) found that activity of oyster
larvae increased with increasing salinity
and that all larvae failed to swim when
salinity was less than 4.8%o.

Davis (1958) gives a minimum salinity
of 10% for metamorphosis of oyster
larvae, but Prytherch (1934) watched
larvae metamorphose at 5.6%. The
highest salinity at which he observed
metamorphosis was 32.2 %0.

Discussion. There are several explana-

tions for the apparent contradictions
between these reports. Davis (1958)
demonstrated that the salinity range

for optimum egg development is depen-
dent on the salinity at which game-

SALINITY TOLERANCE OF MARINE BIVALVES 67

togenesis occurred. Furthermore, it is
likely that the degree and rapidity of
change from environmental to experi-
mental salinity influenced survival and
development more than the actual salin-
ities in some experiments. Davis &
Calabrese (1964) have shown that the
influence of temperature on the salinity
tolerance of oyster eggs and larvae is
minimal, though temperature tolerances
are reduced at low salinities. Oyster
eggs and larvae are known to be extremely
sensitive to dissolved substances (Davis &
Chanley, 1956), and possibly an excess or
lack of some particular constituent in
experimental salinities may have deter-
mined limits rather than the actual salin-
ity used. The concept of physiologically
different races (Stauber, 1950) may also
explain some differences. Although races
of oysters have never been defined in
terms of salinity, the wide distribution of
this species could conceivably permit
development of races with different
salinity tolerances.

Family Pectinidae
Argopecten irradians Lamarck

The bay scallop is found from Nova
Scotia to northern Florida and along
the Gulf Coast to Texas. In Virginia this
species was abundant in Eastern Shore
seaside bays until the disappearance of
eel grass in the early 1930's (Wass, 1965).
Currently, bay scallops are found only
rarely in the Eastern Shore lagoons where
salinity is usually about 30%. According
to Belding (1910), scallops are found in
New England in areas where salinity
ranges from 14.1-36.3%. In North
Carolina, Gutsell (1930) reported a “distri-
butional minimum salinity of 20%
but noted that scallops survived exposure
to 16.2% after unusually heavy rains.
In Florida this species is found in
salinities above 25% (Menzel, 1964).

In the laboratory, Vernberg et al.
(1963) noted a reduction in gill ciliary
activity below 18% and a complete
cessation of activity below 12%. They
further observed that cold-acclimated
scallops were more resistant to adverse

salinity than were warm-acclimated
scallops.

The minimum salinity at which bay
scallops survive would appear to be about

14 %o.

Anomia
1.2.8)

simplex Orbigny (Tables

The jingle is a common fouling
organism found attached to shells, buoys,
wharfs and other solid substrata from Cape
Cod to Florida and in the Gulf of Mexico.
It is found subtidally and is frequently
associated with oysters. In Texas it has
been reported from areas where salinity
ranged from 11-40% (Ladd, 1951). It
is found at salinities above 15% in
Virginia (Andrews, 1953). Scheltema &
Truitt (1954) found recently metamor-
phosed individuals on test panels in
Chesapeake Bay at salinities from 15.2-
26.3 %o.

Most Anomia simplex survived direct
transfer from 31%o to salinities as low as
17.5 % but direct transfers to salinities
of 15% and lower resulted in complete
mortality (Table 8). When salinities were
reduced gradually, jingles survived to 12.5
and 10%, though it is doubtful that
indefinite survival would have been
possible at 10%. All jingles died in 5
days when kept at a salinity of 7.5%o
even after acclimation. Half of the
acclimated jingles survived a transfer
directly from 12.5 to 30%o in 1 experiment,
but in a 2nd experiment none survived
this treatment. Animals transferred to
30% from salinities of 15% and above
suffered по mortality and rapidly
readapted to 30%o.

Anomia simplex filtered and reacted
normally immediately after direct transfer
to 22.5% and higher. Two ог 3 days
elapsed before both filtering and the
closing reaction were normal at 17.5-
22.5%. After acclimation, the minimum
salinity at which these activities were nor-
mal was 12.5%, though some filtering was
observed as low as 7.5%.

Order Heterodontida

Family Carditidae

68 CASTAGNA AND CHANLEY

Venericardia tridentata Say
Venericardia tridentata has been
reported as common in more shallow water
from North Carolina to southern Florida.
In Florida this species occurs in salinities
above 25% (Menzel, 1964). It is found
only rarely in Virginia.

Family Corbiculidae
Polymesoda caroliniana Bosc

Polymesoda caroliniana is common in
low-salinity muddy areas from Virginia
south. Van der Schalie (1933) found this
species where salinity ranged from fresh
water (at low tide) to about 19%.
He also observed that most clams
survived for 2 weeks even when kept at
oceanic salinities in the laboratory.
Parker (1959) found P. caroliniana where
salinity is always less than 10% but never
in absolutely fresh water. In Virginia this
species has been found only in the
James River at salinities from almost fresh
water to 15% (Andrews € Cook, 1951).

Family Dreissenidae

Congeria leucophaeta (Conrad)
(Tables 1,2,9)

This species is common in brackish

and fresh water from New York to Florida.
In Virginia it is found at salinities below
10%o.
Congeria leucophaeta were collected at
a salinity of about 7%. However, they
were maintained in the laboratory at about
17.5%o for several weeks prior to these
experiments. Most survived direct transfer
to all experimental salinities from 0-30%o
(Table 9). Byssal attachment and filtering
were normal at these salinities. However,
nearly 2 weeks elapsed before animals
adapted to 0, 27.5 and 30%o. After
this 2-week period, 65.3% of those kept in
fresh water survived direct transfer to 30%o
and adapted to that salinity. Only 11%
(2 out of 18 clams) survived the reciprocal
direct transfer from 30%o to fresh water,
but these 2 clams did eventually show
evidence of filtering and attach by byssus
in fresh water. No mortality was associated
with similar reciprocal transfers between
2.5%o and 27.5%. Within 1 week of this
transfer, clams were attached and filtering
normally,
Family Lucinidae
Lucina multilineata Tuomey &
Holmes (Tables 1,2,10)

Lucina multilineata occurs commonly

TABLE 8. Response of Anomia simplex (Orbigny) to different salinities. Salinity at collection site

was about 31%o.

% Surviving

Feeding (0= попе, R=
reduced, N=normal)

Salinity After After After After
%o direct acclimation direct acclimation
transfer transfer
0 0 0
2,5 0 0
5.0 0 0
1.9 0 0 0 В
10.0 0 68.9 0 В
1925 0 86.6 0 М
15.0 0 97.3 0 М
17.5 76.7 98.1 М М
20.0 100 96.2 М М
22.5 83.3 94.7 М М
25.0 100 96.4 М М
21.5 94.3 N
30.0 96.3 N

SALINITY TOLERANCE OF MARINE BIVALVES 69

TABLE 9. Response of Congeria leucophaeta (Conrad) to different salinities. Salinity at collection
site about 7 %o.

% Surviving Highest % Feeding (0=noné, R=
attaching reduce, N=normal)
by byssus

Salinity After After After
%o direct transfer direct transfer direct transfer
0 85.0 94.1 М
Po) 95.0 100 N
5.0 100 100 N
1) 100 100 N
10.0 100 100 N
1949 100 95.0 N
15.0 95.0 84.2 N
1785 90.0 94.4 N
20.0 95.0 100 N
22.5 90.0 94.4 М
25.0 100 95.0 М
DO 80.0 94.1 N
30.0 95.0 100 N

TABLE 10. Response of Lucina multilineata to different salinities. Salinity at collection site about

22 Vo.
% Surviving Average highest Feeding (0=none, R=
% burrowing reduced, N=normal)
Salinity After After After After After After
% direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0 O
25 0 0 O
5.0 0 0 0 0 (0 O
1:9 20.0 100 10.0 95.0 R N
10.0 100 94.7 90.0 88.9 N N
12:5 100 100 80.0 100 N N
15.0 100 100 N
17.5
20.0
22.5 90.0 100
25.0
27.5 90.0 100 N
30.0 70.0 100 100 100 R N

from the shore to depths of over 700 ft mon in Virginia and is found in Chesa-
from North Carolina to both coasts of peake Bay at about 20% (Wass, 1965).

Florida. In Florida it is found in salinities Some Lucina multilineata survived
above 25% (Menzel, 1964). It is less com- direct transfer from 22% to experimental

70 CASTAGNA AND CHANLEY

salinities from 7.5-30% (Table 10).
Mortality was heavy after direct transfer
to 7.5% but negligible at higher
salinities. After acclimation to inter-
mediate salinities, survival was normal at
7.5%. Clams did not survive at 5%
even though gradually acclimated to that
salinity.

Burrowing and filtering were generally
normal at all salinities in which clams
survived.

Family Cardiidae

(Conrad)

Laevicardium mortoni
(Tables 1,2,11,12)

Morton s cockle is a small, active clam
common in shallow, protected sandy areas
from Cape Cod to Florida and the Gulf
of Mexico. Ladd (1951) found this species
in an area where salinity varies from 16-
42%o and Parker (1960) found it in an
“assemblage” occurring in а salinity
range of 30-45%. In Virginia, L. mortoni
is fairly common from 15-25% and is
periodically abundant in scattered areas of
Chesapeake Bay and its tributaries.

Laevicardium топот either quickly
adapted to experimental salinities or
died. Although some survived direct
transfer from about 20% to salinities from
7.5-30°%0, there was appreciable mortality
at 7.5 and 10% (Table 11).

The salinity limits could not be
extended by acclimating clams in inter-
mediate salinities, although the percent
survival at 7.5, 10 and 30% was improved.
There were minor differences between
experiments. In the Ist experiment all
of the 33 clams moved to 7.5 % were dead
within 2 days. In the 2nd experiment
clams survived and reacted normally at
7.5%. Almost no mortality occurred at
10% and higher in either experiment and
по clams survived at 5%o.

At the conclusion of these experiments,
clams surviving at low salinities were
transferred directly to high salinities and
survivors at high salinities were transferred
directly to low salinities. Those transferred
from 10 and 12.5% to 30% all died within
24 hours (Table 12). Only one clam out of

19 survived transfer from 10 to 27.5 %o.
Surprisingly, all clams survived reciprocal
transfers from 30% to 10 or 12.5%o. No
mortality was associated with changes
from salinities above 15 % to 30%. Fewer
clams burrowed after direct transfer to 7.5
and 10% than to higher salinities, and
none burrowed at lower salinities. After
acclimation to intermediate _ salinities,
burrowing was normal at 10%o and im-
proved at 7.5%. Some burrowing occurred
at 5% after acclimation though clams
eventually died at this salinity.

Filtering rapidly became normal at
10% and higher. Acclimated clams
eventually filtered normally after exposure
to 7.5% and some filtering occurred
at 5.0%o.

Family Veneridae
Mercenaria mercenaria (L.)

The commercially important hard clam
or quahog is abundant at moderately
high salinities along the east coast from the
Gulf of St. Lawrence to Florida. In
Virginia this species is found in a
variety of substrata intertidally and sub-
tidally at salinities above 10% (Wass,
1965). Belding (1931) gives the salinity
range of the quahog as 12.8-35%o,
but says their survival is possible in
salinities up to 46%. He does not
believe that salinity influences growth
within the normal range. Pratt &
Campbell (1956) found hard clams
occurring naturally from 21.4-31.9 % and
also expressed the opinion that growth
was unaffected by salinity within this
range. Turner (1953), however, reported
no growth of adult clams at 19-21%o
and optimum growth between 24 and
28%. Chanley (1958) reported similar
levels for optimum growth of juveniles
and growth decreasing with salinity
to little or none below 17.5%. Minimum
salinity for survival is given as 12.5%o.

Larvae appear to require a slightly
higher salinity than juveniles or adults.
Metamorphosis did not occur below 20%o
(Turner € George, 1955). Davis (1958)
found larval growth improved with

SALINITY TOLERANCE OF MARINE BIVALVES rik

TABLE 11. Response of Laevicardium mortoni (Conrad) to different salinities. Salinity at collec-

tion sites about 21%o.

% Surviving Average highest Feeding (0=none, R=
% burrowing reduced, N=normal)
Salinity After After After After After After
%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0
2.5 0 0 O
5.0 0 0 38.4 R
7.5 20.0 50.0 20.2 62.5 R R
10.0 85.0 98.7 83.5 99.1 N N
12.5 97.5 100 100 100 М М
15.0 97.5 100 100 100 М М
17.5 97.5 100 100 100 М М
20.0 92.5 100 100 100 М М
2230 95.0 100 100 100 N N
25.0 100 97.4 100 100 N N
27.5 97.5 100 100 100 N N
30.0 90.0 97.4 100 100 N N

TABLE 12. Survival of Laevicardium mortoni after direct transfer between the extreme experimen-
tal salinities to which they had become acclimated.

Transferred to
(Salinity in % )

Transferred from
(Salinity in %o )

Le 30.0
10.0 30.0
10.0 27.5
12.5 30.0
15.0 30.0
17.5 30.0
27.5 17.5
30.0 15.0
30.0 12.5
30.0 10.0

increasing salinity from 15-27.5% and
reports no metamorphosis below 17.5%o.
He also reports that eggs developed
normally from 20-35% with an optimum
salinity about 27.5 %o.

Dosinia discus Reeve

This species is found along the east
coast from Virginia to Florida but occurs
only rarely in Virginia. Menzel (1964)

Number transferred Number surviving

20 0
19 0
19 1
19 0
17 15
18 18
20 19
20 20
18 18
14 13

lists it at salinities above 25% in Florida.
D. discus is common in areas of North
Carolina where the annual salinity range is
from 6-38% but seldom less than 15%
(Norton, 1947). In laboratory experiments
D. discus survived 12 days in 50% seawater
and 15-17 days in 75% seawater (Norton,
1947). Unfortunately, even controls were
dead on the 19th day.

72 CASTAGNA AND CHANLEY

Gemma gemma Totten
(Tables 1,2,13)

This small clam is very common along
the east coast from Labrador to North
Carolina (Sellmer, 1967). In Virginia it
is frequently found in abundance in sand
where salinity ranges from 5-30%o (Wass,
1965).

Gemma gemma responded similarly in
both experiments, adapted well to labora-
tory conditions, and survived for pro-
longed periods even at salinities that
eventually proved lethal.

Clams survived direct transfer to
salinities ranging from 10-30%. When
transferred to 7.5%, all survived for
several days, but then a slow steady
mortality occurred and finally only
22.5% were still alive (Table 13). Salinities
lower than 7.5% eventually proved lethal
to all clams, although 1 clam did survive
51 days at 5%o.

After acclimation to intermediate
salinities, survival of Gemma at 7.5°%0 was.
normal. However, clams transferred to
5.0 °0 suffered a heavy mortality even after
acclimation at 7.5%. All those transferred
to 2.5% or fresh water died. When clams
were moved from 7.5 to 25%o or from

30 to 10%, none died and filtering
and burrowing were normal.

Clams were capable of burrowing after
direct transfer to all salinities of 5%
and higher. However, at least 3 weeks
were required for normal numbers to
burrow at 10%o and only a few burrowed
at 7.5 and 5%o unless first acclimated at
intermediate salinities. Burrowing was
never observed at 2.5%o or in fresh water.

Gemma filtered algae from the water at
all salinities from 2.5-30°%o. However,
filtering was not normal for 5-10 days at
10%o and was reduced and irregular at
7.5% and lower. Normal filtering
occurred at 7.5% if animals were first
acclimated at intermediate salinities, but
was never normal at lower salinities.

When the survivors were discarded at
the conclusion of these experiments,
juvenile Gemma were found in many con-
tainers. Consequently, to determine
reproductive ability at varying salinities,
another experiment was started 23 April
1965, in which 10 Gemma were placed
in salinities ranging from 0-30%o. Оп 20
May, only clams at salinities from 10-30%o
were still alive. Juvenile clams were found
at all these salinities, indicating the ability
to reproduce from at least 10-30%.

TABLE 13. Response of Gemma gemma (Totten) to different salinities. Salinity at collection sites

23.2 and 20.0%.

% Surviving

Salinity After After After
%o direct acclimation direct
transfer transfer
0 0 0 0
9,5 0 0 0
5.0 0 63.9 10.0
10 22/9 100 52.9
10.0 100 98.5 100
125 97.5 99.0 100
15.0 100 100 100
17.5 97.5 100 100
20.0 100 100
22.9 100 100
25.0 100 100 100
РТО 97.5 100 100

Average highest
% burrowing

Feeding (0= попе, R=
reduced, N=normal)

After After After
acclimation direct acclimation
transfer
0 O
0 O R
53.8 O R
98.7 R N
99.4 N N
100 N N
100 N N
100 N N
100 N N
100 N N
100 N N

SALINITY TOLERANCE OF MARINE BIVALVES 73

Family Petricolidae

Petricola pholadiformis | Lamarck
(Tables 1,2,14)

This species is common in peat and
clay from the Gulf of St. Lawrence to the
Gulf of Mexico. Andrews (1956) found it
at salinities from 15-25 % and Wass (1965)
reported it from 20-30%. We have also
collected it in areas where © salinity
exceeds 30 %o.

Although all Petricola pholadiformis
used in the 3 experiments were collected
from the same locality, the salinity toler-
ance varied considerably. The combined
results of all 3 experiments are sum-
marized in Table 14.

When clams were transferred directly
from a salinity of 30-34 %o to experimental
salinities, the minimum salinities at which
they survived in the 3 experiments were
10, 12.5 and 17.5%, respectively, but
mortality was heavy at 10%. The greatest
tolerance range was noted in the experi-
ment conducted at the coolest tempera-
tures.

After acclimation at intermediate
salinities, clams could tolerate a lower
minimum salinity. However, even after
acclimation the minimum salinity at which
clams survived was different in each
experiment (7.9. 10.0% sand # 1275250:
respectively). After acclimation at
minimum salinities, clams were trans-
ferred directly to 30% with virtually no
mortality. Within 1 or 2 days they had
readapted to 30% and were burrowing
and filtering normally. Apparently, slight-
ly greater salinity changes could be
tolerated when the change was toward
30 %o rather than away from it.

At minimum salinities for survival,
comparatively few Petricola burrowed. At
higher salinities virtually all surviving
animals burrowed into the sand sub-
stratum. After acclimation at intermediate
salinities, a few clams burrowed at 5%,
but this salinity was eventually lethal.

Filtering was normal whenever sur-
vival and burrowing were normal. Even
after acclimation, feeding was reduced
at 10%o and lower.

TABLE 14. Response of Petricola pholadiformis (Lamarck) to different salinities. Salinity at collec-

tion site 30-34%.

% Surviving Average highest Feeding (0= попе, R=
% burrowing reduced, N=normal)
Salinity After After After After After After
%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0 O
25) 0 0 O
5.0 0 0 0 5.9 O O
eo 0 67.1 0 51.0 O R
10.0 15) 90.8 10.0 81.8 В В
12.5 67.5 96.2 75.0 95.2 N° N
15.0 75.0 98.5 Го 96.4 № М
ee 95.0 97.0 100 98.4 N N
20.0 97.5 97.1 100 100 N N
29.5 90.0 100 100 100 М М
25.0 85.0 93.6 100 95.0 М М
271.9 92.5 100 N
30.0 82.5 100 N

°Except in 1 experiment where these salinities proved lethal.

Тейта agilis Stimpson (Tables 1,2,-
15)

Tellina agilis is found from the Gulf of
St. Lawrence to North Carolina. It is com-
mon in several areas in Virginia where the
salinity is above 18% (Wass, 1965).

Tellina were collected from an inter-
mediate (20-24%) and а high (33%)
salinity area. Two experiments were con-
ducted with both groups. The results of
all experiments are summarized in Table
15.

Most Tellina Нот 33% died when
transferred directly to salinities below
20%, although a few survived at 17.5%.
Most clams from 20-24% survived direct
transfer to salinities from 12.5-30%о
with a few surviving at 10%. After
acclimation at intermediate salinities, both
groups had similar minimum limits for
survival. A few clams survived at 7.5%o
but mortality was greater at salinities
below 12.5%othan at higher salinities.

Almost all clams burrowed rapidly at
all salinities at which they survived. The
apparent reduction in percent burrowing
(Table 15) after direct transfer to 12.5-
17.5% reflects the failure of high-salinity

CASTAGNA AND CHANLEY

Tellina agilis to burrow at salinities that
were eventually lethal.

Filtering was normal at about 12.5%
and higher. This limit was not appreciably
lowered even when clams were acclimated
to intermediate salinities.

Macoma balthica (L.) (Tables 1,2,16,
17)

This widely distributed species is com-
mon along the eastern coast of North
America from the Arctic Sea to Georgia. It
is apparently euryhaline and is found in
oligohaline as well as oceanic salinities.
This species is abundant in soft substrates
at low salinities (5-15%0) in Chesapeake
Bay and its tributaries (Wass, 1965).

Macoma balthica survived direct trans-
fer from 13-17% to salinities from 2.5-
30%o (Table 16) except in 1 experiment
when the minimum salinity for survival
was 5.0%. After acclimation at inter-
mediate salinities, virtually all clams
survived at 2.5-30%o and did not die
until 8-9 days in fresh water. Clams
that survived 5-6 days in fresh water
before being returned to higher salinities,

TABLE 15. Response of Tellina agilis (Stimpson) to different salinities. Salinity at collection sites

20, 24 and 33%o.

% Surviving

Average highest
% burrowing

Feeding (O=none, R=
reduced, N=normal)

Salinity After After After After After After
%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer

0 0 0 10)

25 0 0 O

5.0 0 0 0 0 O О

Lo 0 10.7 0 76.6 O R
10.0 15.0 66.2 25.0 97.4 R° R
1235 32.5 86.2 50.0 97.9 Re N
15:0 40.0 96.9 50.0 100 N° N
17.0 57.5 95.4 19.0 98.9 N° N
20.0 92.5 100 97.5 100 N N
220 92.5 100 100 100 М М
25.0 95.0 100 100 93.8 М М
97.5 92.5 100 М
30.0 82.5 100 М

“Except for the high salinity groups that died at this salinity.

SALINITY TOLERANCE OF MARINE BIVALVES 75

TABLE 16. Response of Macoma Баса (L.) to different salinities. Salinity at collection sites 13,
15.8 and 16.7%.

% Surviving Average highest
% burrowing

Salinity After After After After
%.o direct acclimation direct acclimation
transfer transfer
0 0 34.9° 0 100
265 60.0 97.0 66.7 100
5.0 96.7 100 100 100
leo 96.7 94.9 96.3 100
10.0 86.7 100 100 100
12.5 96.7 100 100 100
15.0 76.7 96.7
17.9 96.7 100
20.0 86.7 100 100 100
2975 80.0 100 96.7 100
25.0 96.7 100 100 100
27.5 96.7 97.4 100 100
30.0 83.7 95.8 100 100

“These survivors were all from 1 experiment and were exposed to fresh water only 5-6 days. Longer
exposure would probably have been fatal.

TABLE 17: Survival of Macoma balthica after direct transfer between extreme experimental
salinities at which they survived.

Transferred from Transferred to Number Number
(Salinity in %o) (Salinity in %o ) transferred surviving
2.5 30.0 10 0
2.5 279 9 4
5.0 30.0 8 0
5.0 25.0 10 9
7.5 30.0 10 0
10.0 30.0 9 9
10.0 20.0 7 7
20.0 10.0 6 6
22.5 7.9 5 5
25.0 5.0 9 8
27.5 2.5 9 8
30.0 7.5 10 10
30.0 5.0 10 10
30.0 2.9 9 9

would probably have died if they had quickly killed when transferred from
remained in fresh water. salinities of 7.5% and lower to 30%.

Clams were not harmed by sudden Reciprocal changes from 30% to 7.5, 5.0
transfer from 10 to 30%, but they were and 2.5% resulted in no mortality and

76 CASTAGNA AND CHANLEY

clams adapted quickly to the new salinity
(Table 17).

Virtually all surviving clams burrowed.
Even in fresh water all clams burrowed
after acclimation at 2.5%. Within a few
days when clams were dug up, they failed
to burrow again and died.

Масота balthica feeds primarily on
detritus rather than suspended matter and
accurate observations on its feeding or
filtering were not possible.

Macoma mitchelli Dall (Tables
1,2, 19.19)

This species is abundant in many of the

brackish water creeks of Chesapeake Bay
at salinities from 2-20%o (Wass, 1965).

Some Macoma mitchelli survived
direct transfer from field salinities (14.9-
17%) to all salinities from 2.5-30%o.
Mortality at 2.5 and 5% was greater after
such a transfer than at other salinities
(Table 18). Surprisingly, clams taken from
a salinity of 14.9%o were killed by transfer
to 2.5% and only 4 out of 10 survived at
5%. Over 70% of the clams taken from
17%o survived when transferred to these
salinities. After acclimation at inter-
mediate salinities, no unusual mortality
occurred at 2.5-30%. When clams were

TABLE 18. Response of Macoma mitchelli (Dall) to different salinities. Salinity at collection sites

14.9 and 17.0%.

% Surviving

Average highest
% burrowing

Salinity After After After After
%o direct acclimation direct acclimation
transfer transfer
0 0 0 5 1128
225 33:0 95.6 14.3 76.3
5.0 60.0 97.9 72.3 79.3
7.5 90.0 100 72.8 81.4
10.0 100 96.3 85.0 81.7
12.5 90.0 100 1225 88.9
15.0 95.0 90.0
LS 90.0 100
20.0 90.0 100 90.0 100
22.5 100 100 85.0 96.7
25.0 80.0 100 81.6 92.0
С, 95.0 94.5 85.0 94.3
30.0 80.0 90.0 95.0 91.1

TABLE 19. Survival of Macoma тисйей after direct transfer between extreme experimental
salinities to which they had become acclimated.

Transferred to
(Salinity in %o )

Transferred from
(Salinity in %o )

Number transferred

Number surviving

2.5 30.0
5.0 30.0
7.5 30.0
10.0 30.0
30.0 12.5
30.0 10.0
30.0 7.5
30.0 5.0
30.0 2.5

18 0
10 0
1. 0
9 1
6 5
10 10
17 14
10 3
18 0

SALINITY TOLERANCE OF MARINE BIVALVES

moved to fresh water, they eventually
died though some survived for nearly 3
weeks. Rapid salinity increases of 20%o
and more killed most clams (Table 19).
Rapid salinity decreases of 25% resulted
in little mortality and a few clams survived
a rapid salinity decrease of 27.5 % .

Macoma mitchelli burrowed at all
experimental salinities including fresh
water. However, a lower percentage of
clams burrowed after direct transfer to
O and 2.5%. After acclimation there was
little difference in burrowing ability of
clams from 0-30% although clams in
fresh water eventually weakened and died.

Macoma mitchelli did not clear the
water of algae satisfactorily throughout the
experiments. Possibly they are primarily
detritus rather than filter feeders. Some
filtering did occur at 2.5-30%o.

Macoma tenta Say

Macoma tenta is found from Cape Cod
to Florida in a sandy substratum in shallow
water. In Florida it occurs in sandy mud at
salinities above 25% (Menzel, 1964). In
Virginia it is found in silt-clay substrata at

—]
AN

salinities from 20-30% (Wass, 1965).

Family Semelidae

Abra aequalis Say

Abra aequalis is abundant from North
Carolina to Texas. It is found at salinities
above 25%o in Florida (Menzel, 1964). In
Virginia it is rarely encountered (Wass,
1965).

Family Donacidae

Donax variabilis Say (Tables 1,2,20)

Donax variabilis, the colorful toquina of
southern beaches, is common from
Virginia to Florida and Texas. Because of
its unique habitat in the surf zone of sandy
beaches, it is seldom found at salinities
below 30%. In Virginia, D. variabilis is
found on ocean beaches during the
summer and autumn at salinities above
30%o.

Although the 2 experiments involving
this species were conducted under
different temperature regimes and with
clams of different sizes, the results were

TABLE 20. Response of Donax variabilis Say to different salinities. Salinity at collection sites 33-

35%.
% Surviving Average highest Feeding (0=none, r=
% burrowing reduced, N=normal
Salinity After After After After After After
%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0 O
25 0 0 O
5.0 0 0 O
AD 0 0 0 71.9 O R
10.0 0 38.5° 0 94.8 O R
PA) 0 94.6 0 100 O N
15.0 0 100 120 99.3 O N
1725 20.0 99.2 100 100 R N
20.0 60.0 100 100 100 N N
DS 85.0 98.7 100 100 N N
25.0 92.5 100 100 100 N N
PAT) 97.5 100 N N
30.0 92.5 100 N N

“This salinity would probably have eventually killed all.

78 CASTAGNA AND CHANLEY

remarkably similar.

Donax variabilis survived direct trans-
fer to salinities from 17.5-30%, but
heavy mortality was associated with trans-
fers below 22.5% and only 20% survived
direct transfer to 17.5% (Table 20).

The relatively narrow salinity limits
indicated in the first phase of these
experiments were extended appreciably by
acclimating coquinas to intermediate
salinities. After acclimation, clams sur-
vived well and reacted normally at
salinities as low as 12.5 %o.

At the conclusion of the acclimation
phase of the experiments, surviving Donax
variabilis were transferred directly to
30%. Only 1 out of 36 clams died when
transferred from 12.5% (the minimum
salinity at which clams lived) to 30%.
None died when transferred from 15 to
30%o.

Donax variabilis burrowed and filtered
immediately at all salinities at which they
survived. In fact, several dug in and fed
at either 15%o after direct transfer, or
7.5 and 10%o after acclimation even
though these salinities eventually proved

lethal.

Family Sanguinolariidae

Tagelus plebeius Solander (Tables
12.41.22)

This species is listed as common from
Cape Cod to Florida and in the Gulf of
Mexico. It is 1 of the more common
bivalves of Virginia. Andrews (1956)
reports it as euryhaline and common
above 10%o.

Tagelus plebeius were collected from
intermediate salinity areas (about 20%o)
for 3 experiments. These clams survived
direct transfer to salinities from 2.5-30%o,
though only about 1/3 survived at 2.5%.
In the 4th experiment clams were obtained
from nearly oceanic salinities. None of
these clams survived direct transfer to
either 2.5 or 5% and only 10% survived
at 7.5%. Survival from 10-30%
was normal. After acclimation at inter-
mediate salinities, clams from both areas
survived well at 2.5% and higher. None
survived when transferred to fresh water.
The combined results are shown in Table
21. After clams from the intermediate
salinity area were acclimated to a salinity
of 30%, they were transferred directly to

TABLE 21. Response of Tagelus plebeius Solander to different salinities. Salinity at collection sites

14.9, 20.4, 21.8 and 32.4%.

% Surviving

Salinity After After After
%o direct acclimation direct
transfer transfer
0 0 0 0
25 27:5 86.9 19.2
5.0 12.5 81.2 46.4
10 12:0 95.8 56.1
10.0 97.5 95.4 78.9
12.5 97.5 98.8 87.2
15.0 100 91.1 87.5
125 100 83.9 82.5
20.0 97.5 94.] 79.4
22.5 100 89.5 Wed
25.0 97.5 100 91.9
Fico 97.5 100 80.0
30.0 100 95.6 90.0

Average highest
% burrowing

Feeding (0= попе, R=
reduced, N=normal)

After After After
acclimation direct acclimation
transfer
0 O O
81.1 O R
out R N
79.6 R N
85.9 N N
85.2 N N
85.7 N N
81.3 М М
87.6 М М
81.8 М М
78.9 М М
90.0 М М
86.0 М М

SALINITY TOLERANCE OF MARINE BIVALVES 79

TABLE 22. Survival of Tagelus plebeius after direct transfer between the extreme experimental
salinities to which they had become acclimated.

Transferred to
(Salinity in %o)

Transferred from
(Salinity in %o)

2.5 30.0
2.5 27.5
2.5 25.0
5.0 30.0
7.5 30.0

10.0 30.0

12.5 30.0

15.0 30.0

30.0 7.5

30.0 5.0

30.0 2.5

salinities of 7.5 and 5.0% without
appreciable mortality (Table 22). Almost
2/3 survived direct transfer to 2.5%,
whereas clams from the high salinity area
were killed by comparable _ salinity
changes. When clams from both groups
were acclimated to 2.5 and 5% and then
transferred directly to 30%, all died.
Transfer from 7.5 to 30%, 2.5 to 27.5%,
and 2.5 to 25% also resulted in heavy
mortality (Table 22).

Clams burrowed and filtered after
direct transfer to salinities of 2.5-30%o.
However, activity was reduced below 10%o
(Table 21). After acclimation, burrowing
and filtering were not appreciably
increased at salinities from 2.5-30%o.

Tagelus divisus Spengler

This species also is found from Cape
Cod to Florida and in the Gulf of Mexico.
Fraser (1967) studied a Florida population
living in an area where salinity ranged
from 29.1-39.3 %. In Virginia it has been
found only subtidally in moderately
high salinity water.

Family Solenidae
Ensis directus Conrad (Tables 1,2,23)
The common razor clam is found from
Labrador to South Carolina and probably

Florida. In Virginia, Wass (1965) lists it as
an intertidal and subtidal form found

Number transferred

Number surviving

20 0
20 4

9 5
34 0
24 11
15 12
15 14

Y 6
29 29
19 18
38 25

above 20%. In some areas of Chesapeake
Bay it is common at much lower salinities
(Pfitzenmeyer, personal communication).
Under experimental conditions Chanley
(1958) found that E. directus could be
acclimated to survive at 7.5-28%. How-
ever, a rapid salinity change of 15%
within this range was lethal.

Ensis, from nearly oceanic salinities, sur-
vived direct transfer to experimental
salinities of 17.5 and 12.5% in the 2
experiments conducted with this species.
However, mortality was heavy below 20

TABLE 23. Response of Ensis directus Conrad
to different salinities. Salinity at
collection site 32%o.

% Surviving

Salinity After After
%o direct transfer acclimation
0 0
2.5 0 0
5.0 0 80.9
7.5 0 95.3
10.0 0 98.4
12:5 5.0 100
15.0 20.0 100
178 50.0 100
20.0 95.0 98.2
22:9 95.0 100
25.0 95.0 100
27.5 90.0
30.0 95.0

80 CASTAGNA AND CHANLEY

and 17.5% for the 2 experiments (Table
23). Clams were acclimated to survive, at
least for brief periods, at salinities as low as
5%. All clams survived direct transfer
from 12.5 to 30% but transfers from 10%o
and lower to 30% were lethal.

All surviving clams burrowed normally
at salinities of 5%o and higher. Some clams
burrowed at 2.5% but eventually died.
Filtering was slightly reduced below 10%
but otherwise was normal wherever clams
survived.

Solen viridis Say (Tables 1,2)

The green razor clam is fairly common
in shallow water sand flats from Rhode
Island to Florida and in the Gulf states.
In Virginia it is found infrequently in
sand bars of the barrier islands and
therefore only in high-salinity water.

Solen viridis are comparatively rare in
Virginia and enough were found for only
| experiment. Unfortunately, they
survived poorly in the laboratory and the
experiment had to be terminated after 8
days. At this time it seemed likely that
direct transfers from 33-34% to experi-
mental salinities of 17.5 to 20%o could be
tolerated.

Clams were very active and some
burrowed immediately after transfer to all
salinities, including fresh water.

Family Mactridae

Spisula solidissima (Dillwyn) (Tables
1,2,24)

The surf clam, or skimmer, is abundant
from Nova Scotia to Florida and from
Florida to Texas. Under natural conditions
it is not found below 28% but may be
able to tolerate much lower salinities.
Welch (unpublished manuscript) found
the minimum lethal limit between 15 and
20%. He further stated that eggs of this
species do not develop at 22% or lower,
but larvae survive and grow at 16%.
Schechter (1956) places the minimum
tolerance of both eggs and sperm of
Spisula solidissima at “40% sea water”
or about 15%. Eggs in the “polar-body
stage, however, disintegrated at this
salinity.

Some surf clams survived direct transfer
to all salinities from 15-30% (Table 24).
Mortality was heavy at 15%, however,
and in the 2nd experiment clams failed
to survive when transferred to this salinity.

TABLE 24. Response of Spisula solidissima (Dillwyn) to different salinities. Salinity at collection

sites 32-34 %o.

% Surviving

Average highest
% burrowing

Feeding (0= попе, R=
reduced, N=normal)

Salinity After After After After After After
% direct acclimation direct acclimation direct acclimation
transfer transfer transfer

0 0 0 О

2.5 0 0 O

5.0 0 0 O

1.0 0 0 0 60.0 O O
10.0 0 80.3 0 100 О В
12:5 0 96.0 0 100 В М
15.0 25.0 98.4 100 100 К М
5 76.8 100 100 100 N N
20.0 68.9 98.9 100 100 N N
22.0 86.4 100 100 100 N N
25.0 95.0 100 100 100 N N
225 97.5 98.2 N N
30.0 75.0 100 N N

SALINITY TOLERANCE OF MARINE BIVALVES 81

Spisula solidissima failed to remain tightly
closed at lethally low salinities and, con-
sequently, died rapidly. After acclimation
to intermediate salinities, the lower limits
for survival were extended and 75% of
the clams exposed to 10% survived.
Over 90% of those exposed to 12.5% and
higher survived. All clams transferred to
7.5% died. All surviving clams were
transferred directly to 30%. Thirteen of
the 16 moved from 10 to 30%o survived the
change eventually readapted to that salini-
ty. All clams transferred from 12.5%0 and
higher survived and adapted to 30%0
within a few days.

Burrowing was normal at all salinities
at which clams survived, though at
lower salinities there was often a period
of adjustment before normal burrowing
occurred. Some clams burrowed at 7.5%o
before they died.

Clams filtered in all containers in which
they survived. Some limited filtering
occurred at lethal salinities before clams
died (12.5% after direct transfer and
7.5 %o after acclimation).

Mulinia lateralis (Say) (Tables
1.2 95.96)
This small clam is a common to

abundant inhabitant of sandy substrata
in shallow water from Maine to Texas.
Parker (1960) lists it as occurring where
salinity ranges from 18-80%. Ladd (1951)
found few М. lateralis between 4 and 9%o
but many from 10-40%. Nagabhushanam
(1964) found that visceral ganglia of this
species lose their secretory granules at
low salinities.

In Virginia, fluctuating populations
of this species are common above 8%
(Wass, 1965), but less common above
25%.

Two samples of Mulinia lateralis,
collected from an area where the salinity
was between 16 and 17%o, survived direct
transfer to experimental salinities from 5-
30%. Although mortality was heavy in 1
group at 5%, virtually no mortality oc-
curred at higher salinities. When clams
were transferred from environmental
salinities of 20 and 24.6 %, the minimum

TABLE 25. Response of Mulinia lateralis Say to different salinities. Salinity at collection sites 16.5,

16.9, 24.0 and 24.6 “bo.

% Surviving

Average highest
% burrowing

Feeding (0= попе, R=
reduced, N=normal)

Salinity After After After After After After
%o direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0 5.0 20.0 O O
29 0 65.5 WED 75.3 O R
5.0 30.0 87.8 32.5 100 R N
то 60.0 92.0 66.1 100 В М
10.0 97.5 99.1 100 100 М М
119445) 100 98.9 100 100 N N
15.0 100 100 100 100 N N
170) 97.5 100 100 100 N N
20.0 100 100 100 100 N N
22.9 97.5 100 100 100 N N
25.0 100 100 100 100 N N
29 97.5 100 100 100 М М
30.0 100 100 100 100 М М

82 CASTAGNA AND CHANLEY

TABLE 26. Survival of Mulinia lateralis after direct transfer between the extreme experimental
salinities to which they had become acclimated.

Transferred from Transferred to

Number transferred

Number surviving

(Salinity in %o ) (Salinity in %o )

2.5 30.0 20 0

5.0 30.0 2 0

7.5 30.0 18 9
10.0 30.0 10 6
12.5 30.0 10 1
30.0 12.5 10 10
30.0 10.0 18 18
30.0 7.5 40 37
30.0 5.0 19 7
30.0 2.5 20 0

salinities at which they survived were 7.5
and 10%, respectively.

After acclimation at intermediate
salinities, most clams survived at 5%.
Clams from low-salinity areas survived
at 2.5%, a salinity lethal to Mulinia
lateralis from the 2 high-salinity areas
even after acclimation at intermediate
salinities (Table 25). No clams survived
in fresh water. Clams © surviving
at 2.5 and 5.0% were killed when trans-
ferred directly to 30% (Table 26).
Although all clams died in a reciprocal
transfer from 30 to 2.5%0, over 1/3 sur-
vived transfer from 30 to 5%. Fifty per-
cent survived transfer from 7.5 to 30%o but
over 90% survived the reciprocal transfer.
Appreciable mortality occurred even when
clams were transferred from 10 and 12.5%0
to 30%o, but no clams died when transfers
were made from 30 to either 10 ог 12.5%o.

Some clams burrowed after direct trans-
fer to all salinities including fresh water.
The number burrowing was not normal,
however, at salinities that were eventually
lethal. Clams filtered algae from the water
at all salinities at which they survived.

Rangia cuneata (Gray) (Tables
1,227)

Rangia cuneata is a common species in
fresh to brackish water along the coast
from Maryland to Texas (Pfitzenmeyer &
Drobeck, 1964). In Virginia it is common

in low-salinity areas of Back Bay and the
James River (Wass, 1965). Parker (1960)
found R. cuneata in fresh water and in
areas where salinity did not exceed 10%.
Ladd (1951) noted it as abundant where
salinity ranged from 4-9 % but scarce from
13-25%. Parker (1965) observed that
Rangia were found in Texas only where
the average annual salinity was less than
18%. Well-established populations were
studied in Lake Pontchartrain where
salinity varied from 1.5-9.8% annually
(Fairbanks, 1963). Godwin (1967) reported
finding Rangia in Georgia at salinities
from 2.5-11.5%o, with commerical concen-
trations at 3.5-4.5%o. Gunter (1961) noted
that larger Rangia seemed to be found in
areas where salinity was lower.
Pfitzenmeyer & Drobeck (1964) observed
the same phenomenon in Potomac River
populations where they found Rangia at
salinities from 5.7-11.8%o.

In the laboratory, Allen (1961) was able
to keep Rangia alive at several salinities
from fresh water to 25%. He noted that
the concentrations of amino acids in-
creased with salinity to 17% but decreased
with further salinity increase.

Rangia cuneata were collected from
salinities of about 5% and transferred
directly to experimental salinities. In
l experiment mortality was high after
direct transfer to 22.5% and higher. In
the second experiment only 1 clam sur-
vived at salinities of 20% and higher and

SALINITY TOLERANCE OF MARINE BIVALVES 83

TABLE 27. Response of Rangia cuneata (Gray) to different salinities. Salinity at collection site

about 5%o.

% Surviving

Salinity After After

%o direct acclimation

transfer

0 50.0 100
2.5 100

5.0 100

7.5 100
10.0 100 100
1225 100 100
15.0 97.5 100
1723 82.5 100
20.0 47.5 100
2975 15.0 100
25.0 29.5 100
275 2.5 100
30.0 0 100

Highest %

burrowing

After After

direct acclimation

transfer

100 100

100

100

100

100 100

100 100

100 100

100 100

100 100

100 100

100 100

100 100
0 100

several died even at 17.5%. All clams
survived direct transfer to fresh water in
the lst experiment while a similar transfer
was fatal to all clams in the 2nd experi-
ment. These results are summarized in
Table 27.

After acclimation at intermediate salin-
ities, Rangia cuneata survived at all experi-
mental salinities including fresh water and
30%. At the conclusion of the experiments
surviving clams were moved from 30% to
5%0 without mortality.

All Rangia cuneata dug in and filtered
normally at all experimental salinities at
which they survived.

Family Myacidae
Mya arenaria (L. )

The commerically important soft clam is
found from Labrador to North Carolina. It
is known to be a euryhaline form and
has been found at salinities from
6.3-32.4% (Belding, 1930; Kellogg,
1901). Pfitzenmeyer & Drobeck (1963)
found it at salinities as low as 3%. In
Virginia, soft clams are abundant above
10% in Chesapeake Bay and its tributaries
(Wass, 1965). They are also present but

scarce in seaside bays where salinity
may reach 35%. In the laboratory, soft
clams from several different geographical
areas had different minimum salinities
at which they survived but all could be
acclimated to survive at 2.5%o (Chanley,
1958). Stickney (1964) found that about
1% of Mya eggs developed to normal
straight hinge larvae at 8%o. Larvae grew
fairly well at 10%o but optimum salinities
were higher. Salinity requirements of eggs
and larvae were determined by the
environment of the adult.

Family Pholadidae

Barnea truncata (Say) (Tables
1,2,28)
This species occurs from Maine to

Florida and is common from Massachu-
setts south in clay, soft rock or wood
(Turner, 1956). In Virginia it is commonly
found in peat (Wass, 1965) from 16-35%.

Some Barnea survived direct transfer
from 30-34% to 12.5% and 15% but
mortality was greater than after transfer
to salinities above 15% (Table 28). All
clams transferred to salinities of 10%o and
lower died. After acclimation at inter-

84 CASTAGNA AND CHANLEY

TABLE 28. Response of Barnea truncata (Say) to different salinities. Salinity at collection site 33-

35 %o .
% Surviving Feeding (0=none, R=
reduced, N=normal)
Salinits After After After After
%o direct acclimation direct acclimation
transfer transfer
0) 0) O
2.9 0 0 O R
0 0 42.1 O R
То 0 73.8 O R
10.0 () TDA he O R
[225 30.0 99.1 В М
15.0 67.5 100 R N
17.5 95.0 98.0 N N
20.0 90.0 94.5 N N
22:5 95.0 93.8 N N
29:0 92.5 97.4 N N
27.9 95.0 N
30.0 95.0 N

"When clams that survived the direct transfer to 12.5 were moved to 10%, all died. Almost all

0

clams acclimated at other salinities survived when moved to 10%.

mediate salinities, clams survived well at
salinities down to 10%. Some clams sur-
vived at 7.5 and 5.0% but the higher
mortalities at these salinities suggest that
they might eventually be lethal. Direct
transfers of clams from 5, 7.5, and 10% to
30% killed all clams. Thirteen out of 24
clams survived the transfer from 12.5 to
30%, and 14 out of 19 clams survived
transfer from 15 to 30%.

Filtering was normal Нот 17.5-30%o
after direct transfer. No filtering occurred
at 10°%0 and lower and filtering was re-
duced at 12.5 and 15%. After acclimation,
filtering was only slightly reduced at 10%o
and normal at higher salinities. Some
filtering was observed at 2.5% but
filtering was definitely reduced below
10%o.

Barnea truncata are incapable of making
new burrows as adults; consequently,
observations on the effect of salinity on
burrowing were not possible.

Diplothyra smithii (Tryon)

This species is found boring into shell

and, rarely, wood from Massachusetts
to Florida. It is common in the south
but scarce from Virginia north. Menzel
(1964) lists it as occurring at salinities
above 25%o.

Martesia cuneiformis (Say)

Martesia cuneiformis can be found
boring in wood from North Carolina
southwards. It probably does not normally
occur in Virginia (Turner, 1956). Menzel
(1964) lists it at salinities above 25%o.

Cyrtopleura costata (L.) (Tables

152,29)

=,

The angel wing is found in sand
to soft, sticky mud from Massachusetts
to Florida and Texas (Turner, 1956).
Ladd (1951) reports it as occurring from
16-40 %. It is a common Virginia species
in suitable substrata and is found where
salinity is above 10% (Wass, 1965).

Cyrtopleura costata survived direct
transfer from about 20%o to salinities from
7.5-30 %. After acclimation in inter-
mediate salinities, clams survived at

SALINITY TOLERANCE OF MARINE BIVALVES 85

TABLE 29. Response of Cyrtopleura costata (L.) to different salinities. Animals were raised in the

laboratory at a salinity about 20%.

% Surviving

Feeding (0= попе, R=
reduced, N=normal)

Salinity After After After After
%o direct acclimation direct acclimation
transfer transfer

0 0 0 O

2.5 0 0 O R

5.0 0 100 О В

7.0 100 100 R N

10.0 100 100 R N

12.5 100 100 R N

15.0 100 100 N N

17.5 100 100 N N

20.0 100 100 N N

22:5 100 100 N N

25.0 100 100 N N

27.5 100 100 N N

30.0 100 100 N N
2.5% for lengthy periods but eventually salinities.
died and 5% was the minimum salinity Culliney (personal communication)

in which clams survived.

After direct transfer from 20%, the rate
of filtering was reduced at 12.5% and
lower. No clams filtered below 7.5%.
When animals were acclimated in inter-
mediate salinities, feeding was normal
from 7.5-30% but reduced or absent at
lower salinities.

Cyrtopleura costata were incapable of
digging new burrows, so no observations
on the influence of salinity in burrowing
were possible.

Family Teredinidae
Bankia gouldi (Bartsch)

This is a common east coast shipworm
found from New Jersey to Florida.
This species in plentiful in Chesapeake
Bay but is scarce or absent in high-
salinity oceanic water. Clark (1954)
reports its minimum salinity as 10%. This
agrees closely with the observations of
Scheltema & Truitt (1954) who found that
larval B. gouldi set on test panels at
salinities from 9-30%. Within this range,
fewer shipworms were found at lower

reports that Bankia gouldi larvae survive
but are “barely growing” in a constant
salinity of 10%o.

Teredo navalis L.

Teredo navalis has a world wide dis-
tribution and is considered euryhaline. It is
the common shipworm at oceanic salinities
but rare in Chesapeake Bay.

The salinity tolerance of this species
is fairly constant throughout its range and
the minimum salinity for survival has been
listed as 5, 6, 7, and 8% (Blum, 1922;
Miller, 1926; Clark, 1954; Kudinova-
Pasternak, 1960; Soldatova, 1961). These
observations were made over a geographic
range from San Francisco to the Black Sea
and over a period of nearly 40 years, yet
they differ by only 3%. These same
authors report an optimum salinity of 12-
25 or 28% for survival of T. navalis.
Blum (1928) found that activity of
T. navalis was reduced when salinity was
below 7.5% but that they could survive
at 4%o for a month. However, shipworms
eventually died when kept at 4%.
M'Conigle (1927) found activity reduced

86 CASTAGNA AND CHANLEY

at 13% and entirely stopped at 10%.
Both he and Soldatova (1961) reported
that 40%o is the upper lethal salinity.

The minimum salinity for larval devel-

opment has been reported as 9%
(Miller, 1926) and 12% (Kudinova-

Pasternak, 1962). M Conigle (1927) found
some development at 7.5% but lists
this as an “unfavorable” salinity. Culliney
(personal communication) reports that
larval T. navalis were reared to the
pediveliger stage at a constant salinity
of 7.5%. Growth,

however, was very
slow.
Family Lyonsiidae
Lyonsia hyalina (Conrad) (Tables
1,2,30)

Lyonsia hyalina Conrad is common in
shallow water in sandy substrata from
Nova Scotia to Florida. In Virginia it is
found at salinities above 15% (Wass,
1965) and in Florida above 25 % (Menzel,
1964).

Lyonsia hyalina were available for only
l experiment. When transferred directly

from 20% to experimental salinities,
survival was good at salinities from

12.5-30% (Table 30). Four out of 10 sur-
vived at 10%. Salinities lower than 10%
were lethal. Clams could be acclimated
to 7.5% but all died when transferred to
5.0%. Clams began dying from unknown
causes before further transfers could be
made and the experiment was discon-
tinued.

Lyonsia hyalina burrowed actively at all
salinities at which they survived. A limited
amount of filtering was observed at 5%o
though these clams eventually died.
Filtering was also reduced at 10% after
direct transfer and at 7.5% after acclima-

tion to intermediate salinities. Clams
filtered normally at all other salinities.
DISCUSSION

During the course of these experiments
it became apparent that the minimum
salinity tolerated by a species was variable.
Acclimation at intermediate salinities
usually extended tolerance limits.
However, after acclimation, the minimum
salinity in which a species survived
sometimes varied from 2.5-5% between
replicate experiments. Some species
collected from the same location at com-

TABLE 30. Response of Lyonsia hyalina Conrad to different salinities. Salinity at collection site

20%00.

% Surviving Average highest Feeding (0=none, R=
% burrowing reduced, N=normal)
Salinity After After After After After After
%60 direct acclimation direct acclimation direct acclimation
transfer transfer transfer
0 0 0 O
20 0 0 O
5.0 0 0 0 0 O R
139 0 100 0 100 O R
10.0 40.0 100 100 100 R N
12:5 90.0 100 100 100 N N
15.0 90.0 100 100 100 N N
17:5 100 100 N
20.0 100 100 N
22.5 100 100 N
25.0 90.0 90.0 100 100 N N
DO 100 89.9 100 100 N N
30.0 80.0 100 100 100 N N

SALINITY TOLERANCE OF MARINE BIVALVES 87

parable temperatures and salinities but in
different months had different minimum
tolerance limits, indicating a seasonal
variability in salinity tolerance. This
difference was not related to reproductive
condition or to the appearance of the
animals tissues.

Occasionally, minor differences could
be attributed to the different temperatures
at which experiments were conducted.
However, in most cases, the temperature
primarily affected the rate of response
to experimental salinities rather than
changing the tolerance limits. For
example, burrowing, filtering or mortality
usually occurred more rapidly at higher
temperatures, but the salinities at which
these occurred were about the same
regardless of temperature.

In some cases, salinity at the time of
collection appeared to influence the range
of salinity to which bivalves could adapt.
Animals collected when salinity was low
sometimes had higher tolerances at
minimum salinities than those of the same
species collected from high salinity waters.
This difference persisted even after
laboratory acclimation at intermediate
salinities. Perhaps longer and more
gradual acclimation in the laboratory
would have eventually eliminated this
difference.

Some species such as Solemya velum,
Solen viridis and Tagelus plebeius were
not adaptable to laboratory conditions and
their vital activities were reduced or
mortalities increased as experiments

Q

progressed. These 3 species required a
relatively deep substratum for burrowing
and apparently a different food (ie.,
detritus) than the type used. Occasionally,
unusually high mortality not associated
with salinity appeared in some experi-
mental containers but not in others. These
mortalities occurred at all salinities and the
causative agents apparently did not
necessarily exert a synergistic effect at
marginal salinities. On the other hand,
after exposure to several different experi-
mental salinities, some bivalves were
capable of surviving more rapid changes
in salinity than was possible immediately
after collection. In effect, they had
become ‘acclimated,’ and hence more
resistant to physiological stress from salin-
ity changes.

Differences in tolerance limits of the
same species collected from different
localities for this series of experiments
most likely reflect seasonal differences in
temperature, salinity and other
environmental influences and probably
are not due to the occurrence of physiolog-
ically different races.

When bivalves survived in a given
salinity, their activities were generally
normal, except for some arcids and
mytilids which apparently require higher
salinities for byssus formation than for
other activities. Active species did burrow
and filter immediately after being moved
to salinities that eventually proved lethal.
However, there were no salinities at which
animals survived but did not burrow or

TABLE 31. Comparison of the minimum salinity necessary for survival of adults and for survival of

larvae or reproduction.

Approximate

minimum salinity in %o

Species at which adult survives
Bankia gouldi 10
Crassostrea virginica 6

Gemma gemma 10
Mercenaria mercenaria 12.5

Mulinia lateralis 5

Mya arenaria 2.5

Mytilus edulis 8

Spisula solidissima 1255

Teredo navalis 6

Minimum salinity in %o
at which larvae survive
or reproduction occurs

10
5.6
10
15
Who
8 or lower
14
16
1.9

88 CASTAGNA AND CHANLEY

filter.

There appears to be little difference in
the minimum salinity for survival of adult
bivalves and the minimum salinity for
reproduction and larval development
(Table 31). Data are available for only a
few species but in only 1 case did the
salinity tolerance limits for survival of
adults or larvae and occurrence of
reproduction differ by a maximum of 6%.
Small bivalves frequently succumbed
more rapidly to lethal salinities than did

larger individuals of the same species but
there was no difference in the minimum
salinity at which they would survive. Small
bivalves adapted better to experimental
conditions within their individual salinity
tolerance range than the larger in-
dividuals. This could be due to the stress of
overcrowding or increased metabolic
waste accumulation in the larger
specimens.

From the preceding discussion, it is
evident that the minimum salinity for

TABLE 32. Salinity tolerance limits of 36 species of bivalves as determined from natural distribu-

tion and laboratory experiments.

Species Salinity range Experimentally determined
in nature in%o minimum salinity in %o

Argopecten irradians Above 15 15
Amygdalum papyria Above 10 7.5
Anadara ovalis Above 15 12:5
Anadara transversa Above 15 10
Anomia simplex Above 15 12.5
Bankia gouldi Above 10 =>
Barnea truncata Above 15 10
Brachidontes recurvus Above 5 4
Congeria leucophaeta Below 12 0
Crassostrea virginica Above 6 5
Cyrtopleura costata Above 10 5
Donax variabilis Above 30 12.5
Ensis directus Above 10 7.5
Gemma gemma Above 5 7.5
Laevicardium mortoni Above 15 7.5
Lucina multilineata Above 20 7.5
Lyonsia hyalina Above 15 7.5
Macoma balthica Above 5 2.5
Macoma phenax 2-20 2.5
Macoma tenta 20-30 a
Mercenaria mercenaria Above 12.5 12.5
Modiolus demissus Above 8 5
Mulinia lateralis Above 10 5
Mya arenaria Above 3 20
Mytilus edulis Above 8 ==
Noetia ponderosa Above 20 17.5
Nucula proxima Above 20 ==
Petricola pholadiformis Above 15 10
Polymesoda carolininana Below 15 ——
Rangia cuneata Below 15 0
Solemya velum Above 15 15
Spisula solidissima Above 28 12.5
Tagelus plebeius Above 10 2.5
Tellina agilis Above 18 12.5
Teredo navalis Above 6 ——
Yoldia limatula Above 20 ——

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90 CASTAGNA AND CHANLEY

oceanic salinities. D. variabilis, though
living on ocean beaches, undoubtedly
experiences some temporary reductions in
salinity after heavy rains. Juvenile S.
solidissima are frequently found on ocean
beaches and in estuarine waters but are
found as adults only in deeper waters.
In recent laboratory experiments juvenile
Chama congregata, a species normally
found only in oceanic water and not
normally exposed to salinity reductions,
were also discovered to be euryhaline.

About 2/3 of the bivalves which occur
in Virginia's estuarine and inshore
environment occur naturally over the
approximate salinity range they tolerated
in the laboratory (Table 32). This would
indicate ihat salinity is of prime
importance in determining their distribu-
tion. In Virginian waters, Mytilus edulis,
Argopecten irradians, Macoma balthica
and Mya arenaria are not commonly found
over their entire salinity range though they
are in other areas. Virginia is near the
southern limit of the geographical range
for both Mytilus edulis and Mya arenaria.
As mentioned previously, summer water
temperatures limit the distribution of
Mytilus edulis to oceanic waters. Mya
arenaria does not appear to be confined to
low-salinity water by temperature.
However, the unknown factor or factors
which determine the southern range limit
of Mya arenaria may serve to limit this
species to intermediate and low-salinity
areas within the coastal waters of Virginia.

The bay scallop, Argopecten irradians
is rare, and is restricted in Virginia to
high-salinity water. Because this species is
abundant both north and south of Virginia
in a wider range of salinity, its distribu-
tion along the coast of the state must be
limited by other factors, for example,
absence of suitable setting substratum or
protective cover, formerly provided in the
area by the extensive eel grass beds.
Scallops were much more abundant prior
to the disappearance of eel grass (Zostera
marina) in the early 1930's. The absence of
suitable habitat in the eastern shore bays
may prevent scallop populations from
recolonizing those areas of Chesapeake

Bay where salinity is above 15%o and eel
grass, Rupia, or other suitable marine grass
is established. In Virginia Macoma
balthica is limited to low and intermediate
salinity creeks with soft muddy substrata.
This clam is found at higher salinities and
in different substrata elsewhere. Biological
competition for suitable habitats with 3
other tellinids (M. mitchelli, M. tenta, and
Tellina agilis) may account for its distribu-
tion in Virginia.

About 1/3 of the species studied have
never been found naturally over the entire
salinity range tolerated in the laboratory.
Predation could cause this or perhaps
this reflects a lack of adequate sampling in
the cases of Tagelus plebeius, Laevicar-
dium топот, Lyonsia hyalina, Barnea
truncata, and Lucina multilineata. In other

cases (Congeria leucophaeta, Rangia
cuneata, Масота mitchelli, Donax
variabilis, Тейта agilis, and Spisula

solidissima), there can be no doubt that
salinity is, by itself, not a major impor-
tance in limiting distribution. In almost
every instance, these species live in
marginal habitats where species diversity,
and therefore interspecific competition, is
low. Congeria leucophaeta, Rangia
cuneata and Macoma mitchelli are pri-
marily brackish water forms that thrive
at salinities too low for most marine
bivalves and too high for fresh water
bivalves. Donax variabilis inhabits the surf
zone of ocean beaches where few other
species of animals can survive. Tellina
agilis and Spisula solidissima, though not
living in unique habitats, may not inhabit
their potential salinity range because of
biological interaction such as predation
or competition from other species, or
special environmental requirements
(i.e., high oxygen, low levels of suspended
sediments, bottom type, etc. ).

Tellina agilis and Macoma mitchelli are
closely related species, virtually indistin-
guishable except for their hinge structure.
Both exhibited a wide salinity range in
the laboratory (2.5-30%0) yet there is very
little overlap in their distributions.
М. mitchelli is found from 2-20% and
T. agilis from 18-34% (Table 32). It again

SALINITY TOLERANCE OF MARINE BIVALVES 91

appears that some other environmental
requirement determines their distribution.

Spisula solidissima is adapted to the
relatively stable oceanic environment
which supports tremendous beds of this
species. However, when larvae colonize
inshore areas they rarely develop beyond
the juvenile stage because they are
subject to intense predation by a variety
of crabs, carnivorous gastropods and
bottom feeding fish. This predation
rather than salinity prevents establish-
ment of permanent populations of
S. solidissima in estuarine areas.

The relationship, if any, between salin-
ity tolerance and systematic position is
not at all clear. In some taxonomic groups
of closely related species, the separate
species do not occur over the entire
salinity range which the species can
tolerate under experimental conditions.
This could be due to interspecific competi-
tion. Within the Mytilidae and
Pholadidae, the species are separated by
other environmental factors. For example,
in the Mytilidae, Brachidontes recurvus is
epibenthic and subtidal, Amygdalum
papyria benthic intertidally and in shallow
water. Modiolus demissus occurs high in
the intertidal zone. In the Pholadidae
Barnea truncata is found in peat, while
Cyrtopleura costata is found in sand and
soft mud.

In still another group, the Arcacea,
closely related species coexist and inter-
specific competition, if any, has no effect
on salinity distribution. Anadara ovalis
is found with both A. transversa and
Noetia ponderosa. All 3 species of blood
clams had relatively high salinity require-
ments. There was no comparable
taxonomic group with low salinity
requirements.

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SALINITY TOLERANCE OF MARINE BIVALVES 93

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ZUSAMMENFASSUNG

SALZGEHALT-TOLERANZ EINIGER MEERESMUSCHELN VON
LANDNAHEN UND ASTUAR-BIOTOPEN IN DEN GEWASSERN VON
VIRGINIA AN DER WESTKUSTE DES MITTELATLANTIK

M. Castagna und P. Chanley

Viele Arten Brackwasser-Muscheln haben eine Verbreitung, die eng mit dem
Salzgehalt zusammenhangt, was die Wichtigkeit des Salzgehaltes fiir die Verbreitung
zeigt. Die ungefáhre Amplitude der Salzgehalt-Toleranz fiir 36 Arten wird dargestellt.
Die Toleranz-grenzen fiir 29 Arten wurden im Laboratorium experimentell bestimmt.
Die meisten davon sind stark euryhalin. Alle blieben noch bei einem Mindest-Salzgehalt
von 17.5% am Leben, und 25 Arten noch bei 12.5%. Zwanzig Arten ertrugen noch
niedrigeren Salzgehalt.

Die Salzgehalt-Toleranz fiir ein und dieselbe Art ist nicht konstant sondern variiert mit
der Jahreszeit, der Gewóhnung, der Temperatur. Eingraben, Nahrungsaufnahe und
Vermehrung finden bei fast jedem Salzgehalt statt, bei dem die Art am Leben bleibt.
Byssusbildung erfordert einen hóheren Salzgehalt, als er ftir andere Tatigkeiten nótig ist.

In Virginia kónnen etwa zwei Drittel der besprochenen Salzwasser-muscheln in dem
gesamten Salzgehaltis-Bereich gefunden werden, in dem sie im Laboratorium úberlebt
haben. Elf Arten kommen nicht in ihrem gesamten móglichen Salzgehalt-Bereich vor.
Acht davon, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina mul-
tilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis sind nahe
der geographischen Grenze ihres Verbreitungsgebietes; ihre Verteilung kann lokal in
erster Linie durch die Faktoren bestimmt sein, die ihre geographische Verbreitung
bedingen. Die Verbreitung von 5 Arten, Argopecten irradians, Congeria leucophaeta,
Macoma mitchelli, Donax variabilis und Spisula solidissima kann durch Feinde,
Konkurrenz oder besondere ökologische Ansprüche beeinflusst werden. Vier von den 11

SALINITY TOLERANCE OF MARINE BIVALVES

Arten, Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata
kommen an besonderen Biotopen mit geringer Arten-Mannigfaltigkeit vor.

HZ
RÉSUMÉ

TOLÉRANCE A LA SALINITÉ DE QUELQUES
BIVALVES MARINS DES MILIEUX LITTORAUX ET
D'ESTUARIES EN VIRGINIE, CÔTE OUEST MEDIO-ATLANTIQUE

M. Castagna et P. Chanley

Plusieurs bivalves d estuaires ont un type de distribution en corrélation avec la salinité,
ce qui montre l'importance de celle-ci dans le déterminisme de leur distribution. Le
niveau approximatif de tolérance saline pour 36 espèces de bivalves est décrit. La plupart
de ces espèces montre un remarquable degré d'euryhalinité. Toutes survivent à une
salinité minimale de 17,5% et 25 espèces survivent à 12,5 % . Vingt espèces survivent à
diverses salinités plus faibles.

La tolérance saline pour une espèce donnée n'est pas constante, mais varie en fonction
de la saison, du mode expérimental, de la température. Le fouissage, l'alimentation et la
reproduction ont généralement lieu à presque toutes les salinités où la survie est possible.
La formation du byssus réclame une salinité plus forte que celle nécessaire aux autres
activités.

En Virginie, environ les 2/3 des espèces de bivalves étudiées peuvent être trouvées
dans les limites de salinité qu'elles peuvent tolérer au laboratoire. Onze espèces ne se
rencontrent pas jusqu'aux limites qu elles sont capables de supporter au laboratoire. Huit
de ces 11 espèces, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina
multilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis, sont
proches de leurs limites de répartition géographique. Leur distribution localement peut
étre d abord limitée par les facteurs qui déterminent leur répartition géographique. La
distribution de 5 especes, Argopecten irradians, Congeria leucophaeta, Macoma
mitchelli, Donax variabilis, et Spisula solidissima, peut &tre influencée par la prédation,
la compétition et des exigences spéciales d'environnement. Quatre de ces 11 espéces,
Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata, se rencon-
trent dans des habitats spéciaux de faible diversité spécifique.

AE
RESUMEN

TOLERANCIA DE SALINIDAD EN BIVALVOS MARINOS DE AGUAS
COSTERAS Y AMBIENTES ESTUARINOS DE VIRGINIA

M. Castagna y P. Chanley

Muchas especies de bivalvos marinos tienen su distribución correlacionada a la
salinidad, indicando la importancia de tal factor en los patrones distribucionales. Se
estudiaron los limites de tolerancia en 36 especies; 29 fueron determinadas por
experimentos de laboratorio. La mayoría muestran marcada eurihalinidad. Todas
sobrevivieron a una salinidad minima de 17.5% y 25 а tan poca como 12.5% ; 20
sobrevivieron a concentraciones varias, menores.

La tolerancia de una especie dada no es constante sino que varia con la estación y la
temperatura. Excavamiento, nutrición y reproducción ocurren a grado de salinidad en el
que puedan sobrevivir, pero para la formación de biso requieren salinidades más altas.

En Virginia, dos terceras partes de los bivalvos discutidos se pueden encontrar entre los
límites de salinidad que son capaces de resistir en el laboratorio. Once especies no
aparecen en todos sus límites potenciales y ocho de las mismas, Yoldia limatula, Mytilus

95

96

CASTAGNA AND CHANLEY

edulis, Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya
arenaria, Martesia cuneiformis, estan cerca del límite geográfico de tolerancia; sus
distribuciones locales peuden ser limitadas, primariamente por los factores que deter-
minan sus áreas geográficas. La distribución de cinco especies, Argopecten irradians,
Congeria eucophaeta, Macoma mitchelli, Donax variabilis, y Spisula solidissima, pueden
estar influenciadas por predación. Cuatro de las once especies, Congeria leucophaeta,
Macoma mitchelli, Donax variabilis y Rangia cuneata, aparecen en habitats es-
pecializados con diversidad de bajas salinidades.

ИТР:

АБСТРАКТ
ВЫНОСЛИВОСТЬ ПО ОТНОШЕНИК К СОЛЕНОСТИ НЕКОТОРЫХ МОРСКИХ
BIVALVIA ИЗ ПРИБРЕЖНОЙ ЗОНЫ И ЭСТУАРИЕВ ВИРГИНИИ
(ЗАПАЛНО-АТЛАНТИЧЕСКОЕ ПОБЕРЕЖЬЕ)

М. КАСТАНЬЯ И П. ЧЕНЛИ

Особенности распределения ряда видов Bivalvia тесно связано €
распределением солености и имеет для них большое значение.

Описываются пределы выносливости различной солености 36 видов Bivalvia.
ina 29 видов эти пределы были определены экспериментально. Большая
часть изученных видов оказались очень оэвригалинными. Все моллюски
выживали при наименьшей солености в 17.5°/oo, а 25 видов - при 12.507685;

20 видов выживали при различной, HO еще более низкой солености.
Выносливость к солености данного вида не постоянна, а изменяется по
сезонам, при опытах с соленостью и в зависимости от температуры.
Закапывание, питание и размножение моллюсков обычно происходит почти при
всякой солености, при которой только они могут выживать. Образование
биссуса требует более высокой солености, чем другие виды
елеятельности. В районе Виргинии около 2/3 исследованных морских
двустворчатых моллюсков могут встречаться и при более высокой солености,
чем та, которую они выносили в лаборатории. 11 видов не встречаются
при солености, более высокой, чем та, которую они потенциально могут
выдерживать. Восемь видов из одиннадцати - Yoldia limatula, Mytilus edulis,
Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya arenaria,
Martesia cuneiformis находятся здесь почти на границе своего. географического
распространения. Их местная встречаемость может ограничиваться прежде
всего теми факторами, которые определяют их общее географическое
распространение. На распространение пяти видов - Aequipecten irradians,
Congeria leucophaeta, Масота mitchelli, Donax variabilis, Spisula solidissima могут
влиять - хищники, кокуренция или особые потребности моллюсков в условиях
обитания. Четыре из одиннадцати видов - Congeria leucophaeta, Macoma mitchelli,
Donax variabilis, Rangia cuneata - встречаются в особых условиях обитания и
при малом их видовом разнообразии.
Z.A.F.

MALACOLOGIA, 1973, 12(1): 97-113

EFFECTS OF POTASSIUM ON SURVIVAL AND
DISTRIBUTION OF FRESHWATER MUSSELS

Marc J. Imlay
United States Environmental Protection Agency
National Water Quality Laboratory
6201 Congdon Boulevard
Duluth, Minnesota 55804, U.S.A.

ABSTRACT

1. In the laboratory potassium ions were lethal to 4 species of freshwater mussels.
Eleven ppm K was lethal to 90% of Actinonaias carinata, Lampsilis radiata siliquoidea,
and Fusconaia flava in 36-52 days of exposure, and 7 ppm K was fatal to the latter 2
species in about 8 months. Amblema plicata was almost as sensitive as the other species.
Similar K ion concentrations occur naturally in many North American rivers.

2. On the basis of National Water Quality Network data on potassium concentrations
and the concentrations lethal to mussels in the laboratory, it was predicted that certain
rivers would not have mussels and others would. Known distribution of mussels was
generally correlated with the predicted locations. In 1 study the 6 rivers with more than 7
ppm K were not reported to have mussels. Mussels were reported from 28 of 39 rivers
with less than 4 ppm K but from only 2 out of 10 rivers with 4-7 ppm K.

3. On the basis of the laboratory and field data, the predicted maximum safe level for
the continued existence of most freshwater mussels is 4-10 ppm potassium. It is
recommended that the concentration of potassium not be allowed to increase in mussel

producing rivers if the concentration is above 4 ppm.

INTRODUCTION

This investigation owes its origin to the
observation by Koshtoyants & Salanki
(1958) that addition of KC1 to produce a
dissolved potassium ion concentration of
10-*M (39 ppm) exceedingly altered the
“daily activity pattern” of the freshwater
mussel, Anodonta cygnea (Linnaeus)
(Unionidae: Anodontinae)', and by the
knowledge that this concentration was not
much greater than that found in some
rivers. Although mortality of A. cygnea
was not reported, the exposures were for
only about 1 week, and thus it was pos-
sible that longer exposures at lower con-
centrations would be lethal to these
mussels. Ellis, Merrick & Ellis (1931)
studied the effect of potassium on fresh-
water mussels but only at concentrations of
0.1% KCI or more. The purpose of the
present investigation was to study the pos-
sibility that potassium at concentrations
found in some rivers was lethal to North

American mussels. These are rapidly
dwindling in numbers [according to
Stansbery (1970) at least 8 species have
recently become extinct because of Man's
activities], and have considerable commer-
cial importance (Neel & Allen, 1964;
Lopinot, 1967; Isom, 1969).

MATERIALS AND METHODS

A preliminary exposure of mussels to
about 30 ppm potassium and a 2nd ex-
posure to about 9 ppm potassium were
conducted in order to yield a preliminary
indication of the toxic concentrations of
potassium. Two more experiments fol-
lowed each with 4-5 concentrations and a
control.

Testing apparatus

The testing apparatus was effectively
the same in all the experiments and will be
described only for the Ist experiment.
There was a flow of fresh water con-

'The normal active phase lasted 50-100 hours and the rest phase 5-15 hours but after potassium addition both

phases were 3-5 hours.

98 M. J. IMLAY

== = = SS ST — — — STAINLESS HYPODERMIC NEEDLE

FIG. 1. Potassium toxicity testing apparatus.

taining a constant concentration of potas-
sium into the test chamber. A 20 liter
stainless steel chamber contained the test
animals and received 1.0 liter of the test
water at regular (52.5-56.1 min.) in-
tervals. This interrupted flow was ob-
tained by first directing water into a liter
flask which emptied about hourly upon
filling to the level of a siphon tube (Fig.
1). As the water passed down a tygon tube
towards the experimental chamber it
received a precise aliquot of prepared
highly concentrated KCI solution through
a capillary tube because of the venturi
effect. Daily measurements of the volume
of highly concentrated KCI solution re-
moved were used to calculate the actual
diluted concentration in the testing
chamber.

The potassium ion concentration ranged
between 24.4 ppm and 34.4 ppm (x=30.1

il
SNA]

— — —THICK WALLED CAPILLARY TUBE

— —UNDILUTED KCL
SOLUTION

— CONSTANT LEVEL
KCL SOLUTION

CLAM IN TEST
CHAMBER

ppm). The concentration in the 2nd ex-
periment was held at about 9 ppm. This
calculated concentration was verified on 2
occasions by the colorimetric method as
detailed in Standard Methods for the Ex-
amination of Water and Waste Water (cf.
Anonymous, 1967: 240-242). The
measurements were 9.65 ppm and 8.85
ppm.

For the final experiments the cal-
culated potassium ion concentration was
verified throughout each experiments
duration by the flame emission method on
4-5 day composite samples of water from
the testing chambers. Table 1 shows the
mean flame emission concentrations as
well as the range (highest and lowest
measured values). The daily calculated
concentrations were close to the flame
emission composite averages. Note the low
potassium concentration in untreated

POTASSIUM! TOXICITY TO MUSSELS 99

TABLE 1. Water qualities present in the 3rd and 4th experiments on KCI toxicity.

Third experiment (December 19, 1968-January 25, 1969)

Potassium flame emission concentration (ppm)

Mean: DM 99
Rane: 54.0-60.8 32.5-36.4
Water introduced
per hour (liters ) DT 927
Illumination
(foot candles) 22 22

Velocity of water
current (feet
per second) 0.20 0.20

Qt
I
Qt

pH (January 2)

l
24 15 11 (control)
223-250 13.8-15.8 9.9-12.4 0.8-1.0
2.4 DM 2.6 1.9
21 22 19 16
0.20 0.14 0.11 0.20
7.5 Te) ia fs)

Fourth experiment (July 14, 1969-May 14, 1970)

Potassium flame emission concentration (ppm)

Mean: 57
Range: 47-70
Water introduced per
hour (liters) 6.9
Ilumination
(foot candles) 22

(control) test water.

Collection and handling of animals

Three- to six-inch Amblema plicata
(Say), Lampsilis radiata siliquoidea
(Barnes), Actinonaias carinata (Barnes),
Lampsilis ovata ventricosa (Barnes), and
Fusconaia flava (Rafinesque) were chosen
as test species for 2 reasons. They belong
to the clam harvester s commercial 3 ridge,
mucket, pocketbook, and pigtoe forms
respectively (Горшо 1967). Secondly,
they were collected from local rivers
having a calcium content that was
analysed and found to be at most 20%
greater than that of the laboratory test
water (described under “test conditions’)
of 13.5-13.7 ppm. This small difference
minimized calcium content, a major con-
stituent of mollusks, as а difference

37 11 Yi 1
36.3-38.4 9.7-11.9 5.5-8.2 0.5-1.1

4.9 5.6 5.5 4.0

22 22 19 16

between natural and test water. Amblema
plicata is known also as Amblema costata
Rafinesque or Crenodonta costata
(Rafinesque), and Actinonaias carinata as
Actinonaias ligamentina (Lamarck).

For the Ist experiment, 17 mussels were
collected in November 1967 from the Eau
Claire and St. Croix Rivers, Wisconsin,
and maintained at 10-12° C and 5-5.5 ppm
dissolved oxygen until testing which began
on January 28, 1968. These included 4
Lampsilis radiata siliquoidea, 4 Lampsilis
ovata ventricosa, 8 Fusconaia flava, and 1
Amblema plicata. For the 2nd experiment
8 Lampsilis radiata siliquoidea, 9 Lamp-
silis ovata ventricosa, and 6 Fusconaia
flava were collected from the Eau Claire
River and held at 5% C and saturated dis-
solved oxygen until testing began about 2
weeks later, on April 7, 1968. Specimens of
these species from the collection sites on

100 M. J. IMLAY

the St. Croix and Eau Claire Rivers were
identified by Dr. Henry van der Schalie.
For the 3rd experiment each of 6 testing
chambers received 10 Actinonaias carin-
ata on December 11, 1968. Almost all of
these animals were from collections of
equal numbers made on October 28 and
December 6 from Yellow River, Wis-
consin, a few miles above the St. Croix
River. However another collection of what
was believed to be the same species from
the Yellow River was identified by Dr.
David Stansbery as containing about 33%
Lampsilis radiata siliquoidea. He re-
marked (pers. comm.) that “The Yellow
River material was most interesting since
the Lampsilis radiata luteola (Lamarck,
1819) (=siliquoidea Barnes, 1823) are so
very similar in shell characters to the
Actinonaias ligamentina (Lamarck, 1819)
(=carinata Barnes, 1823) from the same
site. Both species are members of the
unionid subfamily Lampsilinae, but there
was no way of knowing which specimens
of each had been included in the experi-
ment. However, the absence of any bimo-
dality in the results makes this experiment
usable. Amblema plicata was collected
from Moose River, Minnesota, near the
city of Sturgeon Lake, on November 25
and 27. The clams were maintained in
water saturated with oxygen at about 10°
C until testing (potassium was introduced
on December 19). There were not enough
Amblema plicata for 10 specimens рег
testing chamber since ice cover prevented
sufficient collecting; each chamber
received only 8 or 9 Amblema plicata.
Lampsilis radiata siliquoidea and
Fusconaia flava were used for the 4th
experiment. Ten mussels of each species
per test concentration were collected from
Ox Creek, Wisconsin (uppermost tributary
of St. Croix River) on July 14, 1969, and
exposure to potassium began the same
day. Conditions at Ox Creek were
potassium, 0.4 ppm; temperature, 28.4°C
(19°C on July 10); alkalinity, 58 ppm; total
hardness, 58 ppm; calcium, 15.6 ppm; and

magnesium, 4.3 ppm.

The exposure extended for over 300
days and the mussels were fed 1 gram of
trout fry commercial feed per test chamber
twice daily. No successful report for
rearing mussels (other than glochidia) in
the laboratory was found in the literature,
although Florkin (1938) studied adult
mussels of Anodonta cygnea in running
tap water without nourishment for 22
months before the mussels succumbed.

The mussels in the 3rd and 4th experi-
ments were examined daily for mortality,
and mussels with gaping valves which re-
mained open after an attempt was made to
close them by hand were considered dead.
For uniformity among the tests at each
potassium concentration, each testing
chamber received 1 mussel from each of 10
size categories.

Testing conditions

Laboratory conditions of temperature,
pH, etc., similar to those in natural con-
ditions, were maintained satisfactorily for
the well-being of the animals. Except for
the 4th experiment which utilized un-
treated water pumped directly to the lab-
oratory from Lake Superior, the test water
was Lake Superior city water dechlor-
inated with carbon filters.

In order to provide lighting similar to
natural conditions, combined fluorescent
(Durotest? optima FS) and incandescent
illumination were used; photoperiod was
automatically adjusted to the local
(Duluth) conditions. Foot candles of illu-
mination at the water surface for the final
experiments are shown in Table 1.

In the Ist experiment (Fig. 1), mixing in
the test chamber was adequate because
the water entered parallel to the channel
of the ellipsoid tank at a high velocity. In
the 2nd experiment, rotating paddle
wheels provided a continuous current of 1
К/Т sec.

Electrical stainless steel stirrers set obli-
quely in each ellipsoid chamber in the 3rd
and 4th experiments provided the flow

Mention of commercial products does not constitute endorsement by the United States Environmental

‚ Protection Agency.

POTASSIUM TOXICITY TO MUSSELS 101

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DAYS OF EXPOSURE

FIG. 2. Number of live mussels (Actinonaias carinata) during exposure to potassium.

rates shown in Table 1; these rates simu-
late stream conditions. Table 1 shows the
amount of water entering each test cham-
ber per hour in the 3rd and 4th experi-
ments. The total volume of a test chamber
was 32.5 liters. From this information one
can calculate turnover rates, if desired.
pH readings taken on January 2 in the
3rd experiment are shown in Table 1. In
the 4th experiment, pH was measured
weekly in all chambers and varied from

7.0-7.7.

Temperature was measured several
times a week in all chambers and in the 1st
experiment ranged from 11-13°C, in the
2nd experiment from 14-18°C, in the 3rd
experiment from 18-19°C and in the 4th
experiment from 16-21°C.

Dissolved oxygen was measured once
weekly in all test chambers with the azide
modification of the Winkler method;
measurements were also made each time

102 M. J. IMLAY

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18 20 22 24 26 28 30 32 34 36

DAYS OF EXPOSURE

FIG. 3. Number of live mussels (Amblema plicata) during exposure to potassium.

more than one mussel died.

Dissolved oxygen, with one exception (1
ppm 2 days in highest concentration of
potassium of 3rd experiment), was always
much greater than that found to be re-
quired for these species of mussels in con-
current experiments and ranged from 4.5-
9.6 ppm.

In the 4th experiment total hardness,
calcium hardness, acidity (as mg/l
CaCO’, Anonymous, 1967) and alkalinity

were measured in all test chambers and
varied from 45-51.5 ppm, 34-40 ppm, 1-2
ppm, and 43.5-45 ppm CaCO’, respec-
tively.

RESULTS

None of the mussels in the Ist experi-
ment (about 30 ppm potassium) died in
the first 17 days of exposure, but more
than half died one by one in the next 15
days. Those which died were 4 Lampsilis

POTASSIUM TOXICITY TO MUSSELS 103

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DAYS OF EXPOSURE

FIG. 4 Number of live mussels
potassium.

out of the initial 8 animals, and 5
Fusconaia flava out of the initial 8.

In the 2nd experiment (about 9 ppm
potassium), 56 days of exposure brought
the death of 6 mussels while 16 mussels
died in the next 31 days of exposure.

Figs. 2, 3, and 4 show the number of
days of exposure required to kill speci-
mens of each species at each potassium
concentration in the 3rd and 4th experi-
ments. Eleven ppm was lethal to 90% of
Actinonaias carinata in 36 days (Fig. 2).
Amblema plicata was not quite as sensi-
tive (Fig. 3). In 36 days 50% had died in 15
ppm K. Lampsilis radiata siliquoidea and
Fusconaia flava were tested at lower con-
centrations and died in about 8 months at
7 ppm K (Fig. 4). Mortality was much
more rapid at 11 ppm. Only 1 of the 40
control animals died while the test animals
were undergoing exposure. Further, on
March 26, 2 months after the last day of
exposure to potassium in the 3rd experi-

(Lampsilis radiata siliquoidea and Fusconaia flava) during exposure to

ment, only 1 of the 20 control animals had
died. Conditions for the 2 months re-
mained the same as during exposure (same
temperature, oxygen, retention time, etc. ),
and consequently it is evident that the
control animals had been in healthy condi-
tion during exposure.

In conclusion 2 species of the amblemid
subfamily Ambleminae (Amblema plicata
and Fusconaia flava) and 2 species of the
unionid subfamily Lampsilinae (Lampsilis
radiata siliquoidea and Actinonaias cari-
nata) are mortally sensitive to very low
levels of potassium.

DISCUSSION
Toxicity and distribution
The laboratory experiments demon-

strated that the 4 species tested from 2 of
the 3 subfamilies of unionid clams were
killed by concentrations of potassium
lower than those found in some rivers of
the United States (cf. National Water

104 M. J. IMLAY

Quality Network, 1962). K* (11 ppm)
killed 90% of Lampsilis radiata siliquo-
idea and Actinonaias carinata in 36-45
days. Eleven ppm was about as lethal to
Fusconaia flava. From the rate of change
of minimum lethal concentration with
time it can be expected that with longer
exposures, lower concentrations would
produce mortality. The chronic test at 7
ppm destroyed laboratory populations of
Fusconaia flava and Lampsilis radiata
siliquoidea in about 8 months. Further-
more, most studies of clams and other
animals show that reproduction and/or
growth are prevented at sublethal con-
centrations of various toxicants. Inhibi-
tion of spawning in fathead minnows
(Mount, 1968) by copper, and reduced
growth of clam and oyster larvae (Hidu,
1965) by detergent, are examples. Re-
production, survival, and growth are, of
course, all necessary for the ultimate exist-
ence of a species. There is evidence that

glochidial larvae of Anodonta may be
more sensitive than adults to KCI. Läbos
& Salánki (1963) found the glochidia to re-
spond by abnormal activity to concentra-
tions as low as 10*M KCI (3.91 ppm К)
and sometimes even lower. Thus it is pos-
sible that 3.91 or about 4 ppm K* is a
maximum safe concentration, and only
rivers with less than 4 ppm K* would con-
tain mussels. The National Water Quality
Network (1962) has measured potassium
from many rivers in the U.S.A., and on the
basis of the Lábos € Salánki report, the
acute results at 11 ppm with rate of change
described above, and the chronic results at
7 ppm, I hypothetically predicted that the
rivers with less than 4 ppm К* would
generally have mussels, and 7 ppm K was
postulated as a predictive indicator that a
river would have no mussels. In addition,
4-7 ppm was considered marginal. Since
the Network data were tabulated for 3-
month composites of weekly samples it

FIG. 5. Prediction of presence of unionid clams (C) (0-4 ppm K), marginal (M) (4-7 ppm K), and no clams (NC)

(7 or more ppm K) based upon National Water Quality Network data of potassium measurements.

POTASSIUM TOXICITY TO MUSSELS 105

CT RS

SN N
NAS
SYS ES Was
SS
SS N
N

SS
AS N

NN N
NN
N
SY
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| i

was felt that any high 3-month value
would be the effective one regardless of
the concentration at another season, and
accordingly the higher value was chosen
where more than one value was pre-
sented. After making these predictions, I
plotted the Network data as shown in Fig.
5. The symbols C (less than 4 ppm), M (4-7
ppm), and NC (greater than 7 ppm) are
predictions of clams, marginal, and no
clams. The symbols are plotted at the

Jame Mail
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fauna as compared to other distinctive mussel assemblages.

N NS

The relatively large area in the United States inhabited by the Mississi
FIG. 6. Reproduction of map published by H. & A. van der Schalie (1950) showing regions of U.S.A. containing

S :
N YI WEST FLORIDA ог APPALACHICOLAN
unionid clams.

y comeentano or CUMBERLANDIAN

Y г ñ
Е I MISSISSIPPI or INTERIOR BASIN

в I ATLANTIC
| М OZARK

@® a Northern
TD b.Southern
8 П PACIFIC

specific sites on the river specified in the
Network data. Comparison of Fig. 5 with a
map published by H. & A. van der Schalie
(1950), Fig. 6, shows a partial correspond-
ence of high potassium concentrations
with the regions of the U.S.A. that are
known to essentially not contain mussels.

The only discrepancy between Figs. 5
and 6 is the North Dakota to Texas zone of
the U.S.A. But the occurrence of
Fusconaia flava, Amblema plicata, Ac-

M. J. IMLAY

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15

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clams from North Dakota to Texas. F

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POTASSIUM TOXICITY TO MUSSELS 107

tinonaias carinata, and Lampsilis radiata
siliquoidea (cf. Murray & Leonard, 1962;
41, 48-49, 110 and 151, respectively),
species tested in the present studies in the
laboratory, as well as the occurrence of the
numerous other species of the Midwest is
limited in significant numbers to only the
eastern fringe of the North Dakota to
Texas zone (Fig. 7). Van der Schalie (pers.
comm.) also notes? that the mussels found
in this zone are few in number; they were
presented on his map (Fig. 6) to show that
the relatively few mussels which are found
here belong to the Mississippi basin
assemblage.

A 2nd method of testing the hypothesis
was to compare the Network data with in-
formation on the presence or absence of
mussels in the Network rivers, some of
which have been sampled for mussels by
the Ohio State Museum (Stansbery, pers.
comm., 1969). None of the 6 streams con-
taining more than 7 ppm K (Colorado at
Yuma, Bear, Big Sioux, North Platte,
Platte, and South Platte) was recognized
by Dr. Stansbery to be reported in the lit-
erature as having mussels. Personnel from
the Ohio State Museum have sampled one
of these rivers (the Colorado River at the
Network Yuma site) and found no mus-
sels. Of the streams with less than 4 ppm
K, Dr. Stansbery was unsure of 2 rivers but
for the others, 28 of 39 were known to have
mussels from reports in the literature or
from Ohio State Museum sampling. In the
marginal category (4-7 ppm K), only 2 of
the 10 rivers were known to have mussels.
For the sake of unbiased interpretation it
should be noted that these 2 rivers were
the only 2 sampled by Ohio State
Museum. The 10 rivers had no known lit-
erature report of mussels. It should be
noted that 28 of 39 is significantly dif-
ferent from 0 of 6, p <0.001, or 2 of 10, p

<0.003 (Croxton & Cowden, 1955: 679-
680).

An interesting case of mussel distribu-
tion was described by Cvancara (1966) for
the Red River of the North and its tribu-
taries. Information on potassium levels in
many of these tributaries appears in Water
Resources Data for North Dakota (1966,
1968, and as yet unpublished data kindly
supplied by the Geological Survey at Bis-
marck, North Dakota and Lincoln,
Nebraska) and in Water Resources Data
for Minnesota (1965, 1966, 1967, and
1968). Potassium was measured in each
tributary close to one of the sites indicated
by Cvancara as having mussels. Average
values were provided or were otherwise
calculated by the author. Several species of
mussels were found by Cvancara in the
following tributaries in Minnesota: South
Branch Two Rivers (4 ppm), Middle River
(4), Red Lake River (4), Wild Rice River,
Minnesota (5), Buffalo River (7), Pelican
River (5-6), Ottertail River (3). In North
Dakota the Pembina River had 8 ppm
potassium but was similarly rich in mus-
sels. This will have to be tolerated as a
slight infringement on the hypothesis that
rivers over 7 ppm will not have mussels.
The Tongue River (4) in North Dakota had
4 species of mussels. The Forest River,
North Dakota, was rich in mussels in the
upper reaches near Fordville (4). At Minto
(6) mussels were also found. Below this
point mussels were not found, but Cvan-
cara (1966) reports that the chloride level
became very high. Suggestive evidence
that potassium was also high will be men-
tioned shortly.

Finally, the Sheyenne River, North Da-
kota, was rich in mussels throughout the
sampled region (lower part). At the lowest
points, West Fargo and Harwood, potas-
sium was 8 ppm. Samples taken slightly

The correlation here is striking and interesting. The basic and widespread “Mississippi” mussel assemblage
usually becomes sparse in such western regions as extend from the Dakotas to Texas, particularly because the
streams are often too intermittent, or, as in the case of the Missouri drainage, the rivers are often too silted to
permit mussel faunas to survive. It should also be emphasized that the mussel distribution patterns as depicted
partially reflect the fish distribution because of the host-parasite relations between larval mussels and their fish
hosts. In any case the correlation as shown is a remarkable one and indicates biological relationships that warrant
further study. Few animals are better suited for studying salt content or mineral relationships than mussels which
often remain active for 25 years and monitor the materials taken into the shell in the growth process.

108 M. J. IMLAY

upstream from mussel sites were found to
have potassium values of 10 ppm. Thus
this river also slightly erodes the pre-
dictive hypothesis.

The following rivers were high in potas-
sium and had few or no mussels. The Wild
Rice River, North Dakota (15 ppm), had
only 1 species and only 1 out of many
sampling stations yielded any mussels at
all The Goose River, North Dakota, at
Portland (8-14) and at Hillsboro (10-12),
was well sampled for both potassium and
mussels but had only 1 species.

Cvancara (1966) found that the upper
reaches of the Park, Turtle, and Forest
Rivers were rich in mussels and had a low
chloride content. The lower reaches were
devoid of mussels and high in chlorides.
He concluded that a correlation “of eco-
logical significance’ appeared to exist be-
tween high chlorides and absence of mus-
sels. Pollution and physical conditions
(bottom type, turbidity, river discharge
rate, or industrial and municipal effluent)
were believed not to be probable causes.
The high chloride content was reported by
Cvancara as being brought in by seepage
from the Dakota group of cretaceous rocks.
Observing that these rocks do contain
potassium (Dole & Wesbrook, 1907), it ap-
peared to me that potassium might be high
where the chloride was high and be the
direct cause of the absence of mussels. The
following data on the Park River sub-
stantiates this explanation. The South
Branch of Park River below Homme Dam
(7 ppm) had mussels. Further down-
stream at Grafton, the Park River proper
had no mussels and the potassium had in-
creased (survey the same day) to 12 ppm.
Finally, another measurement on that day
at Oakwood (still further downstream)
showed 40 ppm and there were no
mussels.

The correlation of potassium con-
centration with mussel distribution is not
necessarily a direct cause-and-effect cor-
relation, but could conceivably be created
by a common variable (carbonate, Mg,
silting, etc.) that causes both the potas-
sium and distribution variation. This is not
considered likely, however, because of the

laboratory demonstration of direct toxicity.
Potassium may enter a stream naturally or
artificially as a pollutant. Potash (K?CO*)
production has been listed as a significant
and steady component of the minerals
industry (Krieger, 1968). KCI occurs in
brines from oil wells and other industrial
wastes (McKee & Wolf, 1963). It is con-
sidered to be a significant component of
paper wastes (Powers, Sacks & Holdaway,
1967: Table 1) and occurs in runoff from
irrigation diversions or excessively fer-
tilized crops. The Green River, Kentucky,
lost most of its former mussel abundance
from brine waste in 1958 with the opening
of the Greensburg, Kentucky oil field
(Williams, 1971).

Other organisms

Low concentrations of potassium may
be toxic to other animals but only rela-
tively short-term studies of potassium ex-
posure ( 1 week) have come to my atten-
tion (McKee & Wolf, 1963). Fig. 3 indi-
cates less than 50% mortality for Amb-
lema plicata for the first 2 weeks of ex-
posure at any concentration tested. Extra-
polation of Fig. 3 indicates the probability
of such a delay in toxicitity of potassium
for concentrations much higher than those
used in the present studies. Thus studies of
only 1 week, while abounding in the litera-
ture, give little evidence of the chronic
effects of potassium.

There is scant evidence that potassium
may be highly toxic to other animals.
Galun € Kindler (1966) found that the
medicinal leech, Hirudo medicinalis
(Linnaeus), would no longer imbibe an
NaCl: glucose solution across a mem-
brance if 7.5 X 102M КС were added,
but this was a rather high K* concen-
tration. Coler, Gunner, & Zuckerman
(1967) substituted sodium for potassium in
the growth medium used with tubificid
oligochaetes because of reports of an effect
of potassium on tubificids, but again con-
centrations were high.

There are indications that high sensi-
tivity to potassium may be unique to
unionaceans or at least certain mollusks. In
a comparison of numerous phyla, (Prosser

POTASSIUM TOXICITY TO MUSSELS 109

& Brown, 1961: 58-63), Anodonta was dis-
tinguished by the lowest blood potassium
along with the other common cations, ex-
cept for calcium. During narcosis,
Anodonta (Bivalvia) and Lymnaea
(Gastropoda: Pulmonata) increase т
weight, and the principal ions become
diluted in the blood, except for potassium
which is released by cells at an even faster
rate than it is diluted (Robertson, 1964:
296). Further studies are necessary to show
whether chronic sensitivity to potassium is
unique or general among aquatic life.
Such studies are underway in this
laboratory and the results to date show
that a freshwater fish, leech, and snail are
at least an order of magnitude less sensi-
tive to chronic potassium exposure than
the mussel.

Effects of other ions

Salanki (1962) found the common
cations K+, Nat, Mgt, Cat to affect
seriously the normal activity of glochidial
and adult Anodonta cygnea, at concentra-
tions which, relative to the actual con-
centrations in streams, would be im-
portant only for the case of potassium in
real river conditions.

Although, it is well known that these
other cations may ameliorate the toxic
effects of potassium, [sodium for Artemia
(Stahl, 1967), and calcium for Tubifex
(Ringer, 1899), to cite representative ex-
amples] the potassium was highly con-
centrated in such studies. There is little
reason to conclude that their addition
would protect organisms from potassium
at the low levels found to be chronically
lethal for mussels. Since KCl was the
vehicle used to introduce K+ in the pre-
sent studies, it is advisable to examine the
possibility that Cl~ contributed to the ob-
served toxicity. The report by Ellis (1937:
Table 7) suggests that C17 is not the toxic
ion in KCl because goldfish show по
apparent injury after 25 days exposure to
the very high concentration of 5,000 ppm
NaCl.

Evidence from data related to mussels,
that C17 is not the toxic ion in KC1, is in
the Water Quality Network data (1962)
which show chlorides to be much higher in
mussel producing streams than in KCl
solutions which killed mussels in the lab-
oratory. Examples are the Allegheny (10-
46 ppm), Escambia (8-100 ppm), Illinois
(9-32, 14-40), Little Miami (9-30), Missis-
sippi (Cape Giradeau, Missouri) (9-21),
Ouachita (14-355), Potomac (8-18), St.
Lawrence (17-36), Wabash (22-132), and
Tombigbee (4-58) Rivers. These are all
rivers specifically stated by Dr. Stansbery
(pers. comm., 1969) as having mussels.

Another line of evidence is the finding
that the threshold of NaCl effect on the
activity of Anodonta cygnea glochidia was
at 100 times greater concentrations than
the KC1 threshold. Further, the effect of
NaCl was short lived (Lábos € Salánki,
1963).* The order of threshold concentra-
tion. (based ion’ molarity was
K<Rb<Cs<Mg<Li<Ca<Na as chlor-
ides, with K* being effective at the lowest
concentration. Only KCI produced a
lasting effect compared to NaCl, MgCl,,
and CaCl? even with very high concen-
trations of chloride (10M NaCl). The
equivalent amount of chloride in 107M
NaCl would be found with КС! solutions
that yield 3910 ppm K. Incidently, since
sodium has been shown consistently to be
about 10 times less toxic than potassium in
the many reports of acute toxicity for
numerous organisms (McKee & Wolf,
1963), it is possible that attention may
usefully be directed to industrial processes
where sodium may simply be substituted
for potassium.

Mode of toxicity of potassium

The specific mode of toxicity of potas-
sium to fresh-water mussels is not known
at the present time. An indication as to
mode of toxicity is provided by the
demonstration by Salänki (1961) that
potassium acts directly upon the receptor

‘Lithium, cesium, and rubidium incidently, had thresholds far greater than concentrations which might be

expected outside the laboratory.

110 M. J. IMLAY

system of Anodonta cygnea since lesion of
siphonal nerves or their paralysis Бу
cocaine abolished the effects of slight
potassium addition on normal activity. He
found, furthermore, that the blood potas-
sium level increased with addition of KC1
but remained constant at the new level
regardless of closed or open phase of
activity rhythm. Since the closed phase
lasted many hours, the animal cannot rid
itself of potassium following any possible
shielding of itself from the environment by
closing. Anodontoides ferussacianus Lea
(Unionidae: Anodontinae) can prevent the
lowering of pH expected under anaerobic
conditions by means of such a shielding
method (Biondi, 1928; Kraft, 1928).

Koshtoyants € Salánki (1958) pre-
sented evidence that functioning of por-
tions of the Krebs cycle may be related to
the effects of potassium, although Lukac-
sovics & Salánki (1964) found the effect of
KCI on activity to be unrelated to tissue
respiration. Cholinergic transmission may
be related to potassium toxicity (Lábos, et
al., 1964).

ACKNOWLEDGEMENTS

I wish to thank Messrs. Edward N.
Leonard and Robert W. Andrew for the
colorimetric and flame emission measure-
ments of potassium, and Mrs. Barbara J.
Halligan for assisting in much of the
laboratory work. Permission from Dr.
Henry van der Schalie (for Fig. 6) and Dr.
Harold Murray (for Fig. 7) to republish
their maps is gratefully acknowledged.
Identifications of species were made by
Dr. van der Schalie, University of Mich-
igan, Ann Arbor, Michigan, and Dr. David
Stansbery, Ohio State University, Colum-
bus, Ohio. The classification of mussels
used here is that of Clarke € Berg (1959).

LITERATURE CITED
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POTASSIUM TOXICITY TO MUSSELS 111

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M. J. IMLAY

ZUSAMMENFASSUNG

BEDEUTUNG DER POTTASCHE FUR LEBEN UND VERBREITUNG VON
SUSSWASSERMUSCHELN

M. J. Imlay

1 Im Laboratorium waren Pottasche-lonen für 4 Süsswassermuschelarten ein
tödliches Gift. Elf Teile pro Million (T.p.M.) K tötete 90% der Arten Actiononaias
carinata, Lampsilis radiata siliquoidea und Fusconaia flava innerhalb von 36-52 Tagen
und 7 T.p.M. К die beiden letzteren Arten in etwa 8 Monaten. Amblema plicata war fast
so emfindlich wie die übrigen Arten. Ähnliche Konzentrationen von K-lonen kommen
von Natur in vielen nordamerikanischen Flüssen vor.

2. Auf Grund der Daten des “National Water Quality Network” betr. Pottaschegehalt
und der obigen Untersuchungsergebnisse wurde geschlossen, dass gewisse Flüsse
Muscheln beherbergen und andere nicht. Die bekannte Verbreitung der Muscheln
wurde allgemein mit der vermuteten Verbreitung verglichen. Von 6 Flüssen mit mehr als
7 T.p.M. К werden keine Muscheln angegeben. In 28 von 39 Flüssen mit weniger als 4
T.p.M. K wurden Muscheln gemeldet, aber nur in 2 von 10 Flüssen mit 4-7 T.p.M. K.

3. Die Laboratoriums- und Gelände-Befunde zeigen, dass die meisten Süsswasser-
muscheln dauernd nur in Gewässen leben können, in denen der Pottaschegehalt nicht
über 4-10 T.p.M. steigt. Es wird empfohlen, die Zunahme des Pottaschegehaltes in
muschelführenden Flüssen nicht zuzulassen, wenn die Konzentration mehr als 4 T.p.M.
beträgt.

HZ
RESUME

EFFETS DU POTASSIUM SUR LA SURVIE ET LA
DISTRIBUTION DES MOULES D'EAU DOUCE

M. J. Imlay

1. Au laboratoire les ions potassium sont léthaux pour 4 espéces de moules d'eau
douce. La dose de 7 ppm K a été léthale pour 90% des Actiononaias carinata, Lampsilis
radiata siliquoidea et Fusconaia flava après 36-52 jours d'exposition, la dose de 7 ppm К a
été fatale aux 2 dernières espèces au bout de 8 mois environ. Amblema plicata est
presque aussi sensible que les autres espèces. De telles concentrations dion К se
rencontrent dans les conditions naturelles dans beaucoup de riviéres nord-américaines.

2. Sur la base des données en concentrations de potassium de la National Water
Quality Network d'une part et des concentrations léthales établies au laboratoire d'autre
part, on a pu prévoir que certaines rivières n'auraient pas de moules, tandis que d'autres
en auraient. La distribution connue des moules a généralement été en corrélation avec
les localisations prévues. Dans une étude sur 6 riviéres avec plus de 7 ppm K, aucune
n avait de moules. Des moules furent trouvées dans 28 rivieres sur 39, ayant moins de 4
ppm K, mais seulement dans 2 sur 10 riviéres ayant 4-7 ppm K.

3. Sur la base des données dans la nature et au laboratoire, le niveau maximum prévu
pour le maintien en vie de la plupart des moules d'eau douce est de 4-10 ppm К. Il est
recommandé de ne pas laisser s accroitre la concentration de potassium dans les rivières
productrices de moules si cette concentration est inférieure & 4 ppm.

ACE,

POTASSIUM TOXICITY TO MUSSELS

EFFECTOS DEL POTASIO EN LA SOBREVIVENCIA Y
DISTRIBUCION DE ALMEJAS DE AGUA DULCE

M. J. Imlay

1. El efecto de potasio fué letal para 4 especies de almejas de agua dulce en el
laboratorio. Once ppm K fué letal para el 90% de Actinonanias carinata, Lampsilis
radiata siliquoidea y Fusconaia flava expuestas durante 36 a 52 dias, y 7 ppm K fué fatal
para los dos ultimas especies en 8 meses. Amblema plicata fué casi tan sensitiva como las
otras especies. Concentraciones similares de iones К se encuentran naturalmente en
muchos ríos de Norte America.

2. En base a los datos de la Red Nacional de Calidad del Agua sobre concentraciones
de potasio, y las concentraciones que fueron letales a las almejas en el laboratorio, se
pronosticó que ciertos ríos pueden contener almejas y otros nó. La distribución conocida
de las almejas, estaba generalmente correlacionada con los locales pronosticados. En un
estudio de 6 ríos con más de 7 ppm K no se registraron almejas, pero fueron encontradas
en 28 de los 39 ríos con menos de 4 ppm K, pero sólo en 2 fuera de los 10 ríos con 4-7 ppm
K.

3. Sobre la base de datos de laboratorio y en la naturaleza, el pronóstico del nivel de
seguridad para la existencia contínua de la mayoría de las especies de almejas, es 4-10
ppm potasio. Se recomienda que la concentracion de potasio no se permita aumentar, si
la concentración es superior a 4 ppm.

Te:

ABCTPAKT

ВЛИЯНИЕ КАЛИЯ HA ВЫЖИВАНИЕ И РАСПРОСТРАНЕНИЕ ПРЕСНОВОДНЫХ
ДВУСТВОРЧАТЫХ МОЛЛЮСКОВ

М. ДЖ. ИМЛЕЙ

1. В эксперименте ионы калия были летальными для 4 видов пресноводных
двустворчатых моллюсков. 1% 10744 к оказались летальными для 90%
Actinonais carinata, о radiata siliquoidea Fusconaia flava при экспозиции
36-52 дня, а 71.107 4% К вызвали летальный исход у двух последних видов
при экспозиции 8 месяцев. Amblema plicata была почти так же
чувствительна, как и другие виды. Естественно, что подобные
концентрации иона К встречаются во многих северо-американских реках.

2. На основании данных Национальной Организации по Регистрации
Качества Воды (National Water Quality Network) по концентрации калия и данных
по концентрациям, оказавшимся летальными для двустворчатых моллюсков при
лабораторных эксперимантах, было предсказано, что в определенных реках

Bivalvia должны жить, а в других - нет. Распределение двустворчатых
моллюсков, имеющее место в действительности, в общем соответствовало
прелсказанному. В 1 исследовании а сведения, что в 6 реках с
концентрацией EOS более, чем 1.10% “+, Bivalvia не обнаружены.

Двустворчатые моллюски найдены в 28 из 39 рек ç концентрацией К меньше,
чем 4.10 te. HO лишь в двух из 10 рек с 4-7.10 %% К.

3. Ва основании полученных в лаборатории и полевых данных
предсказанная максимальная концентрация для продолжительного нормального

сун ee Le большинства пресноводных двустворчатых моллюсков -
4-10.10" tg К. Высказаны пожелания недопустимости повышения уровня
концентрации К в реках, содержащих Bivalvia, если концентрация его там

выше 4.107 4%.
Z.A.F.

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MALACOLOGIA, 1973, 12(1):115-122.

ELECTROPHORETIC STUDIES ON ESTERASES OF SOME
AFRICAN BIOMPHALARIA SPP. (PLANORBIDAE)

Gudrun Wium-Andersen
Danish Bilharziasis Laboratory
Charlottenlund, Denmark

ABSTRACT

Esterases from the hepato-pancreas of African Biomphalaria spp. have been examined
by means of starch-gel electrophoresis. On the basis of esterases it was possible to
separate the following species determined from their morphological characters: B.
pfeifferi (Krauss), B. alexandrina (Ehrenberg), B. camerunensis (C. R. Boettger) and B.
sudanica tanganyicensis (Smith). В. alexandrina wansoni Mandahl-Barth is identical with
B. camerunensis' in regard to the esterase pattern.

The esterases emphasize the conformity found in shell morphology between
Biomphalaria alexandrina from Ismailiya and В. sudanica tanganyicensis. In В.
alexandrina esterases varied from one population to another while they were completely
constant in all B. pfeifferi populations examined. This variability parallels a great
variation in susceptibility to infection with Schistosoma mansoni Sambon found in the
populations of В. alexandrina examined, and a constant susceptibility to infection with 5.
mansoni in the populations of B. pfeifferi examined.

INTRODUCTION

African Biomphalaria spp. show great
variation in shell morphology and anat-
omy, which impedes a classification of
species on these characters. Examinations
of esterases might possibly contribute
towards a better understanding of the
taxonomy within the genus and give some
information as to whether the differences
in susceptibility to Schistosoma mansoni
within a certain species can be correlated
to different forms occurring within the
now accepted species.

MATERIALS

The following species of Biomphalaria
were used in the experiments (see Figs. 1,
2):

1. Biomphalaria pfeifferi from Sendafa in
Ethiopia, Lubumbashi in the Congo,
Pakwach in Uganda and Gwebi in Rho-
desia.

2 В. alexandrina populations from the fol-

lowing localities: Alexandria, Tanta,

Qalyub, Abu Rawaash, Giza, El Min-

ya, Khartoum, Suez and Ismailiya, all

Egypt, except Khartoum in the Sudan.
3. B. camerunensis from the following

Congolese localities: Lubudi, Mam-

peza, Makelele, Basoko, all near Kin-

shasa.

4. В. alexandrina wansoni from Kisan-
gani and from Kabondo near Kis-
angani in the Congo.

5. B. sudanica tanganyicensis from Mwan-
za in Tanzania.

The Biomphalaria alexandrina speci-
mens used for electrophoresis are off-
spring from the snails examined by
Cridland (1968) for experimental infec-
tion. Infection experiments have also been
carried out with the other above men-
tioned species (Cridland, 1970).

METHODS

The snails were kept in aquaria under

'When Biomphalaria alexandrina wansoni and B. camerunensis manzadica were described, the typical B.
camerunensis was only known from the original description by Boettger. Since then quite a number of
camerunensis samples as well as samples of wansoni have been received and examined by the WHO Snail
Identification Centre at Charlottenlund, and there is no doubt about wansoni being related more closely to
camerunensis in morphological respect than to alexandrina. It should be considered an inland form of B.

camerunensis (Mandahl-Barth pers. comm.)

116 G. WIUM-ANDERSEN
Biomphalaria anode
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species

identical laboratory conditions and fed on
scalded oven-dried lettuce.

Preparation

Hepato-pancreas is removed from the
live snail and placed in a micro test tube
with a drop of distilled water. After homo-
genization with a rotating glassrod the
specimens are centrifuged at a tempera-
ture of 5°C and 12000 g for 2 minutes.

1. The esterase bands found in African Biomphalaria species by electrophoresis of hepato-pancreas.

localities for the African Biomphalariae examined and the geographic distribution of the

Each specimen contains hepato-pancreas
from only one animal, so that the esterase
pattern is determined for individual snails.

Electrophoretic procedure

The horizontal starch-gel electro-
phoresis is carried out in a rectangular
plexiglass frame (0.6 x 15 x 28 cm) using a
gel composed of 12.5% starch dissolved in
a 1:14 dilution of a 0.341 M boric acid

ESTERASES OF BIOMPHALARIA

buffer with a value of pH 9.0 (21.1 g boric
acid and 5.32 g NaOH in 1 litre H,O).
Concentrated buffer is placed in the buffer
containers. Four pieces of filter-paper
Whatmann No. 1 serve as a bridge be-
tween the gel and the buffer. The super-
natant from each centrifugated hepato-
pancreas is sucked up in a piece of What-
mann No. 4 filterpaper 6 x 3 mm and
placed in a slit 3 - 4 cm from the edge of
the gel at a distance of about 2 mm from
each other. This arrangement makes space
for approximately 20 specimens. During
electrophoresis the gel is placed between 2
cooling plates of the same size as the gel.
Plastic-foil is placed between the gel and
the cooling plates, which maintain a tem-
perature of 0°C to 2°C. Best results are ob-
tained with a voltage of 290 У сог-
responding to 70 mA in 2 hours.

Methods of staining

To obtain the clearest staining of the
bands, the gel is split lengthwise. For the
specific staining of esterases 50 mg fast
blue salt RR (Michrome) was used, dis-
solved in 100 ml buffer, to which was
added 2 ml 1% 1-naphthyl acetate in ace-
tone and water in the ratio of 1:1. The es-
terases are stained for approximately half
an hour.

RESULTS
Biomphalaria pfeifferi
In this species I found 6 esterase bands
(see Fig. 1), out of which 2 move towards

the cathode and the remaining to the
anode. The bands are called a', a?, b', b?, с!

117

and &@. The number of animals examined
from each locality and the bands occuring
are shown in Table 1.

The individuals from Sendafa, Lubum-
bashi and Pakwach were identical, and all
the bands appeared with a frequency of
100%. The Gwebi individuals were similar
to the 3 populations mentioned except that
band a! was lacking. Unfortunately only 2
specimens from this population were avail-
able.

Biomphalaria alexandrina

The maximum number of esterase
bands found in this species was 11, desig-
nated: Al A2 А BiB В. С EICHE:
and С° (see Fig. 1). However, with the
technique used, Biomphalaria alexandrina
from Ismailiya did not show bands Nos. В',
В? and В? but instead 2 more powerful ones
with a quite thin band in between (see Fig.
1) moving a little faster towards the anode.
These 3 bands almost merge. In all the
other B. alexandrina populations bands B',
В? and B® were always present. The fre-
quency of the bands А', A’, Аз, C!, C?, C?,
C* and С? is given in Table 2. It can be
seen that the variation in the esterase pat-
tern in B. alexandrina is very great from
one population to another. The only bands
always found in the A and С series are A!
and C? Apart from the B-series, the
Ismailiya population can always be dis-
tinguished from the others by the pres-
ence of С'. The Suez population is rec-
ognizable by the presence of С? and С? and
the lack of C'. The Abu Rawaash popula-
tion showed the greatest variation. The

TABLE 1. Total number and frequency of esterase bands in 4 populations of Biomphalaria

pfeifferi.
Localities No. Esterase bands
a! а? b! b? c! с? a! а? b! b? c! с?
Sendafa 10 10 10 10 10 10 10 100 100 100 100 100 100
Lubumbashi 14 14 14 14 14 14 14 100 100 100 100 100 100
Gwebi 2 0 2 2 2 2 2 O 100 100 100 100 100
Pakwach 8 8 8 8 8 8 8 100 100 100 100 100 100

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ESTERASES OF BIOMPHALARIA 119

pattern of the Giza and Tanta individuals
was almost alike.

Biomphalaria camerunensis

Eight esterase bands are always present
(see Fig. 1 and Table 3).

Biomphalaria alexandrina wansoni

This species is identical to B. cam-
erunensis (see Fig. 1 and Table 3).

Biomphalaria sudanica tanganyicensis

Unfortunately only a limited amount of
material (6 specimens) was at my disposal.
The middle bands (b series) of
Biomphalaria sudanica tanganyicensis (see
Fig. 1) are identical with those of B. alex-
andrina from Ismailiya.

DISCUSSION

The division of the African Biompha-
laria species has caused many problems.
Mandahl-Barth (1958) described con-
chological and anatomical differences for a
division of species, but drew attention to
the fact that a separation based on these
characters was doubtful because, in re-
spect of both characters “almost every
intermediate stage has been found, so that
it seems reasonable to collect them into
one species, as some authors have actually
done.’ He continues: “However, in na-
ture some of them behave as separate
species, for they have been found living in
the same small place without inter-
breeding.”

As a help for a systematic examination of
African species of Biomphalaria and Bul-
inus electrophoresis has previously been
applied by Wright (1963, 1965, 1966),
Coles (1970) and Burch € Lindsay (1967).
Wright (1966) conjectured that esterases
from the hepato-pancreas might be useful
for further examination of the taxonomy
when mature snails are kept on a standard
diet (lettuce), a method which has been
followed in this work. Coles (1970), on the
other hand, doubted that esterases could
be of any value in distinguishing between
species. Burch € Lindsay (1967) showed
that 2 species groups in the genus Bulinus
that are difficult to distinguish by

morphological characters could be
characterized by their esterase patterns.
My results show that the Biomphalaria
pfeifferi, B. alexandrina, B. sudanica
tanganyicensis and B. camerunensis
diagnosed on morphological characters,
have different esterases and therefore also
different genes. The morphological
characters can thus be used in identifica-
tion of the snail populations in question.
According to Dr. Mandahl-Barth's per-
sonal comments, В. “alexandrina” wan-
soni is related more closely to B.
camerunensis than to B. alexandrina. His
views are supported by the present work,
which shows that B. camerunensis and B.
“alexandrina” wansoni have identical es-
terases. B. wansoni can be considered an
inland form of B. camerunensis (see Fig.
2):

The electrophoretic technique em-
ployed in this study reveals great varia-
tion in the populations of Biomphalaria
alexandrina examined. In contrast the
populations of B. camerunensis and B.
pfeifferi examined showed hardly any
variation in the esterase pattern although
the geographical distance between the
populations of B. pfeifferi was much
greater than that between the different B.
alexandrina populations (see Fig. 2).

Cridland (1968) showed that different
Egyptian populations of Biomphalaria
alexandrina vary in their susceptibility to
infection with Egyptian strains of S. man-
soni, whereas B. pfeifferi from geo-
graphically widely separated localities all
have the same high susceptibility widely
separated localities all have the same high
susceptibility to infection. The results ob-
tained in this work thus demonstrate a
correlation with (1) the lack of variation in
the esterase pattern and the uniform sus-
ceptibility to infection in B. pfeifferi, and
(2) a corresponding variation of both fea-
tures in B. alexandrina. The populations
from Giza and Tanta have almost the same
esterase pattern and same susceptibility to
infection, but apart from this finding it has
not been possible to observe a direct rela-
tion between the occurrence of certain
esterases and susceptibility in B. alex-

120

С. WIUM-ANDERSEN

TABLE 4. Mean measurements of shell and rachidian of 10 fully grown Biomphalaria alexandrina
from each of the 8 Egyptian localities, carried out by Dr. G. Mandahl-Barth.

Localities Shell
A D H
X $ X $
Ismailiya 6.0 129 0.13 3.4 0.06
Giza 5:3 I3100:18 41 0.05
Alexandria 5.6 13.3 0.36 4.1 0.13
Suez Sac TELS 20:07 3.9 0:04
El Minya 55 13.8 ? 43 ?
Qalyub 5.3 11.5 0.09 3.3 0.04
Tanta 5.4 13:35 0:94. 4:37. 40.08
Abu Rawaash 5.8 12.8 0.23 4.4 0.07

Central tooth
U Ux 100 Hx 100

X $ Н D length ши
5.3 0.11 156 26.4 10-11
46 0.12 112 31.3 12
5.5 0.16 134 30.8 12
40 0.07 103 34.5 12
4.9 ? 114 31.2 14
4.8 0.06 146 28.7 14
5.0 0.09 116 32.3 15
44 0.08 100 34.4 15

A = number of whorls
D = greatest diameter of shell in mm
H = height of last whorl behind aperture

in mm

U = greatest diameter of umbilicus in mm
A

s = standard error of the mean

X = mean

TABLE 5. Mean measurements of shell and rachidian of 10 fully grown Biomphalaria from each of
5 species, carried out by Dr. G. Mandahl-Barth.

Biomphalaria sp. Shell Central tooth
(Localities) D H U Ux 100 H x 100
A X 5 X 5 X 5 H D length in u
wansoni (Kisangani) 5.3 14.2 0.10 42 002 55 0.14 131 29.6 13
camerunensis (Lubudi) 5.5 14.6 0.18 4.9 0.07 5.8 0.09 118 33.6 15
sundanica tanganyicensis 6.0
(Mwanza) 6.0 15 0.20 4.4 0.04 5.6 0.13 127 27.6 11
pfeifferi (Katanga) 50 131 0.22 50 0.02 43 0.06 86 38.2 17
typical sudanica
(Sudan) 6.0 14.4 0.27 3.8 0.14 5.7 0.18 150 26.4 10
A = number of whorls U = greatest diameter of umbilicus in mm
D = greatest diameter of shell in mm s = standard error of the mean
H = height of last whorl behind aperture X = mean
in mm
andrina. length of the central radular tooth and ex-

The Biomphalaria alexandrina popu-
lation from Ismailiya shows similarity with
В. sudanica tanganyicensis as regards the
B-series. The Ismailiya population is the
only В. alexandrina population having C*,
while the remaining esterases in the
Ismailiya population are identical with
those of the other 3 populations of B. alex-
andrina. Esterase band No. A? in B. alex-
andrina occurs in B. pfeifferi and band A!
in B. sudanica.

Dr. Mandahl-Barth has measured the

amined the shape of the shell (see Tables 4
and 5). The central tooth in Biomphalaria
pfeifferi was 17 и, in В. sudanica tanganyi-
censis Ши and in В. alexandrina it varied
from 10 to 15 a. The ratio 410 had a
value of 86 in B. pfeifferi from Katanga
and of 150 in typical B. sudanica, it varied
from 100 to 156 in populations of B. alex-
andrina. In the length of the central tooth
and in shell shape the Ismailiya popula-
tion showed great conformity with B.
sudanica. The question therefore arises

ESTERASES OF BIOMPHALARIA 121

whether this population should not be con-
sidered as an isolated population of B.
sudanica.

The esterase pattern shows a great
genetic polymorphism within and be-
tween populations in Biomphalaria alex-
andrina, as the other characters used
(susceptibility, length of central teeth,
ratio of umbilicus to height of the shells)
have also shown. B. alexandrina is prob-
ably a species in evolution.

ACKNOWLEDGEMENTS

I am greatly indebted to Drs. G.
Mandahl-Barth and C. C. Cridland for
much good advice and inspiration. My
thanks are also due to Dr. T. Bennike who
collected the material.

This study was supported by a grant
from the WHO Snail Identification Cen-
tre, Charlottenlund.

LITERATURE CITED

BURCH: TB... & LINDSAY, С.К., 1967,
Electrophoretic analysis of esterases in
Bulinus. Amer. malacol. Union ann. Reps.,
34:39-40.

COLES, G.C., 1970, Enzyme electrophoresis
and speciation of Schistosoma intermediate
hosts. Parasitology, 61: 19-25.

CRIDLAND, C.C., 1968, Results of exposure
of batches from highly susceptible and less-
susceptible strains of Biomphalaria alex-
andrina from Egypt to strains of Schistosoma
mansoni from Cairo and Alexandria. Bull.
Wild. Hlth. Org., 39: 955-961.

CRIDLAND, C.C., 1970, Susceptibility of the
snail Biomphalaria alexandrina alexandrina
from the UAR and the Sudan to infection
with a strain of Schistosoma mansoni from
Tanzania. Bull. Wid. Hlth. Org., 43: 809-
815.

MANDAHL-BARTH, G., 1958, Intermediate
hosts of Schistosoma. World Health
Organization, Geneva, Monograph Series
No. 37. p 46.

WRIGHT, C.A. € ROSS, G.C., 1963, Electro-
phoretic studies of blood and egg proteins
in Austrolorbis glabratus, (Gastropoda,
Planorbidae). Ann. trop. Med. Parasitol.,
57: 47-51.

WRIGHT, C.A. € ROSS, G.C., 1965, Electro-
phoretic studies of some planorbid egg pro-
teins, Bull. Wid. Hlth. Org., 32: 709-712.

WRIGHT, CA, FILE, 5.К. & ROSS. СЕ.
1966, Studies on the enzyme systems of
planorbid snails. Ann. trop. Med. Parasitol.,
60, 4: 522-525.

ZUSAMMENFASSUNG

UNTERSUCHUNGEN MIT HILFE DES ELEKTROPHORS
AUF ESTERASEN BEI EINIGEN AFRIKANISCHEN
BIOMPHALARIA-ARTEN (PLANORBIDAE)

G. Wium-Andersen

Esterasen aus dem Hepato-Pankreas afrikanischer Biomphaoarien-Arten wurden
mittels Stärkel-Gel-Elektrophorese untersucht. Auf Grund der Esterasen war es möglich,
die folgenden nach ihren morphologischen Charakteren bestimmten Arten ebenfalls zu

unterscheiden: Biomphalaria pfeifferi

(Krause). B. alexandrina (Ehrenberg), B.

camerunensis (C. R. Boettger) und B. sudanica tanganyicensis (Smith). B. alexandrina
wansoni Mandahl-Barth ist in Bezug auf die Esterase-Zusammensetzung identisch mit B.

camerunensis.

Die Esterasen bestätigen die Ähnlichkeit, die zwischen Biomphalaria alexandrina von
Ismailia und B. sudanica tanganyicensis auch in der Morphologie der Schale festgestellt
wurde. Bei B. alexandrina variieren die Esterasen zwischen den einzelnen Populationen,
während sie bei allen Populationen von В. pfeifferi gleich blieben. Mit dieser Variabilität
ist eine stark unterschiedliche Empfänglichkeit für die Infektion mit Schistosoma
mansoni Sambon in den untersuchten Populationen von B. alexandrina verbunden, und
eine konstante Empfänglichkeit für Infektion mit diesem Parasiten bei den untersuchten

Populationen von B. pfeifferi.

H. 2.

bo
bo

G. WIUM-ANDERSEN

RESUME
ETUDES PAR ELECTROPHORESE SUR LES ESTERASES
DE QUELQUES ESPECES AFRICAINES
DU GENRE BIOMPHALARIA (PLANORBIDAE)

G. Wium-Andersen

Les estérases de l'hépato-pancréas d'espèces africaines de Biomphalaria ont été
examinées au moyen de |’ électrophorése sur gel d'amidon. Sur la base des estérases il a
été possible de séparer les espèces suivantes déterminées d'après leurs caractères
morphologiques: B. pfeifferi (Krauss), B. alexandrina (Ehrenberg), B. camerunensis (C.
R. Boettger) et B. sudanica tanganyicensis (Smith). B. alexandrina wansoni Mandahl-
Barth est identique à B. camerunensis en ce qui concerne les données en estérase.

Les estérases accentuent la conformité, déjà reconnue par la morphologie de la
coquille, entre Biomphalaria alexandrina de Ismailiya et B. sudanica tanganyicensis.
Chez В. alexandrina les estérases varient d'une population à l'autre tandis qu'elles sont
tout-ä-fait constantes dans toutes les populations examinées de В. pfeifferi. Cette
variabilite est a mettre en parallele avec une grande variation de la susceptibilité à
l'infection par Schistosoma mansoni Sambon envers les populations examinées de В.
alexandrina et la constante susceptibilité à l'infection par 5. mansoni dans les populations
examineés de B. pfeifferi. AL

RESUMEN

ESTUDIOS ELECTROFORETICOS SOBRE ALGUNAS BIOMPHALARIA
SPP. AFRICANAS (PLANORBIDAE)

G. Wium-Andersen

Esterasas del hepato-pancreas de Biomphalaria spp. de Africa fueron examinadas por
medio de almidón-gel-electrofóresis. Sobre tal base fue posible separar las siguientes
especies determinadas por $us caracteres morfológicos: B. pfeifferi (Krauss), B. alexan-
drina (Ehrenberg), B. camerunensis (C. R. Boettger), y B. sudanica tanganyicensis
(Smith). B. alexandrina wansoni Mandahl-Barth es idéntica a B. camerunensis en lo que
respecta al patrón de esterasa.

Las esterasas acentúan la conformidad encontrada en la morfología conchológica entre
Biomphalaria alexandrina de Ismailiya y B. sudanica tanganyicensis. En B. alexandrina
las esterasas varian de una población a otra, mientras que fueron completamente
constantes en todas las poblaciones observadas de B. pfeifferi. Esta variabilidad es
paralela a la gran variación en susceptibilidad a la infección con Schistosoma mansoni
Sambon constatada en las poblaciones de B. alexandrina examinadas, y una suscep-
tibilidad constante a la infección con S. mansoni en las poblaciones de B. pfeifferi.

Te

ABCTPAKT

ЭЛЕКТРОФОРЕТИЧЕСКОЕ ИЗУЧЕНИЕ ЭСТЕРАЗЫ НЕКОТОРЫХ АФРИКАНСКИХ
ВИЛОВ BIOMPHALARIA (PLANORBIDAE)

Г. ВИУМ- АНДЕРСЕН

одом крахмально-гелевого электрофореза изучалась эстераза из
о-панкреаса видов Biomphalaria. На основании изучения эстеразы
3 лось возможным разделение следующих видов моллюсков, определенных
по их морфологическим признакам: В. pfeifferi, (Krauss), В. alexandrina (Ehren-
berg), В. camerunensis (Boettger) и В. sudanica tanganyicensis (Smith). По своей
эстеразе В. alexandrina wansoni Mandal-Barth оказалась идентичной В. сатетипеп-
515.

Эстераза подтверждает сходство, найденное по морфологии раковины у
В. alexandrina из Исмаилии и В. sudanica tanganyicensis. У В. alexandrina acTepa3a
изменялась от одной популяции к другой, ау всех изученных популяций
В. pfeifferi она была совершенно постоянной. Эта вариабильность оказалась
параллельной большим колебаниям в восприимчивости к инфекции Schistosoma

№

mansoni Sambon, найденной B исследованных популяциях В. alexandrina.
Наблюдается ПОСТОЯНСТВО в восприимчивости к инфекции S. mansoni E

изученных популяциях В. pfeifferi.

Z.A.F.

MALACOLOGIA, 1978, 12(1): 123-150

EMBRYONIC DEVELOPMENT AND ORGANOGENESIS
IN THE SNAIL MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE)

I. GENERAL OUTLINES OF DEVELOPMENT!
Emile 5. Demian? and Fouad Yousif?
ABSTRAGT

The present series of embryological investigations is an extension of the basic
morphological, biological and ecological studies currently in progress on the aquatic
gastropod Marisa cornuarietis (Linnaeus), а snail of potential importance in the
biological control of schistosome-transmitting snails. This part is concerned with the
early cleavage, gastrulation and general outlines of embryogenesis in Marisa.

The egg undergoes total spiral cleavage, which was followed up till the 24-cell stage.
The first 2 divisions are equal; the 3rd is unequal and dexiotropic. Gastrulation is
epibolic, and the blastopore closes by the end of that process. Embryogenesis takes 8 days
at 25-30°C and 20 days at 15-20°C. The blastula is fully developed in 14 hours, and
gastrulation is completed in 22 hours at the former temperature range. Torsion occurs
through the differential growth of the 2 sides of the embryo; it starts about 3% days after
egg-deposition and lasts for about 2 days.

Twelve distinct embryonic stages were distinguished during embryonic development
after gastrulation. The age, dimensions and distinctive anatomical features of each of
these embryonic stages are given, together with an outline of the development of the
different organ systems, except for the reproductive system which develops mainly after
hatching. Findings partly diverge from earlier reports for related ampullariid snails, in
particular as regards the origin and development of the mantle, mantle cavity,

pericardium, heart, kidney, ureter, renal vestibule and digestive gland.

INTRODUCTION

The freshwater snail Marisa cornuarietis
(Linnaeus) has recently attracted con-
siderable attention as a potential antagon-
ist of some snail vectors of schistosomiasis
and fascioliasis. The present series of in-
vestigations is another contribution to the
basic morphological, biological and eco-
logical studies currently undertaken at Ain
Shams University, Cairo, with the main
objective of gaining as much fundamental
knowledge about this snail as possible, be-
fore any attempt is made to introduce it as
a biological control agent against
schistosome-transmitting snails into areas
outside its present range of distribution in
the neotropics.

The Ampullariidae (syn. Pilidae: Meso-

gastropoda, Architaenioglossa), to which
Marisa cornuarietis belongs, are lower pro-
sobranchs specialized for an amphibious
existence in a way unparallelled by any
other prosobranch. Among other char-
acteristics, they possess a lung in addition
to a monopectinate gill, and have 2 func-
tional excretory chambers. The develop-
ment of the lung of the Ampullariidae, the
origin of their 2 renal chambers and the
homologies of some of their organs have
been so far variously interpreted and dis-
puted by many authors. The homologies of
their right gill with the left gill of the
Mesogastropoda, and of their 2 renal
chambers with the single left kidney of
other mesogastropods are still question-
able. The points which have remained un-
decided in the ontogeny of the Am-

This investigation was supported in part by research grants (AI 04906 and Al 07696) from the National Institute
of Allergy and Infectious Diseases, U.S. Public Health Service.

"Department of Zoology, Faculty of Science, Ain Shams University, Cairo.

3Laboratory of Bilharziasis Research, National Research Centre, Cairo.

124 DEMIAN AND YOUSIF

pullariidae are perhaps more numerous
than in any other prosobranch family.
The present paper is the first in a series
that deals with the embryonic develop-
ment of a member of the ampullariid
genus Marisa (syn. Ceratodes), the devel-
opment of which has hitherto not been ex-
amined. In this paper, a description is
given of the early cleavage, the gastrula-
tion and the outline of ontogeny in M.
cornuarietis before hatching. Details on
the origin and organogenesis of the dif-
ferent organ systems, excepting the repro-
ductive system which develops mainly
after hatching, are dealt with in sub-
sequent parts of this series. The bearing of
our results on the various ontogenetic
problems and on the phylogenetic rela-
tions in the family Ampullariidae are dis-
cussed in the relevant parts of this series.

HISTORICAL

The literature pertaining to the embry-
onic development of freshwater proso-
branchs is generally limited and mostly
concerned with a few familiar forms such
as Paludina (=Viviparus). Marine pro-
sobranchs as well as opisthobranchs and
pulmonates were subject to more
numerous and elaborate embryological
investigations. A detailed review of the
literature on molluscan development is be-
yond the scope of the present report.
Extensive historical reviews are included
in the works of Fretter € Graham (1962)
and Hyman (1967). Moreover, a general
survey of the present state of knowledge of
descriptive and experimental molluscan
embryology was given by Raven (1966),
with special emphasis on cytological and
cytochemical aspects of development.

Comparatively little work has been done
on the embryonic development of the
Ampullariidae. The earliest of these
studies are probably those made by
Semper (1862) on Ampullaria polita De-
shayes, and by Ryder (1889) on A. de-
pressa Say. These were brief reports mostly
concerned with cleavage divisions. Scott
(1934) gave a somewhat more detailed
account of the development of A. canali-
culata Lamarck wnich, however, was

limited to an external description of some
embryonic stages. The most elaborate in-
vestigation was probably that of Ranjah
(1942) which included a detailed descrip-
tion of the embryonic development of Pila
globosa (Swainson) and an extensive dis-
cussion of the older literature dealing with
the embryology of the Gastropoda.
Studies largely concerned with specific
ontogenetic problems of the Ampul-
lariidae are those by Brooks € McGlone
(1908) on the origin of the lung in Ampul-
laria depressa Say, by Fernando (1931) on
the ontogeny of the kidney in A. gigas
Spix, by Nagaraja (1943) on the develop-
ment of the alimentary canal in Pila virens
(Lamarck), and by Raja (1943) on the
formation of the shell gland in P. globosa
(Swainson). The observations made by
these earlier authors are discussed in the
relevant sections of the present series.

MATERIAL AND TECHNIQUES

Marisa cornuarietis used in the present
study were reared in the laboratory from an
original Puerto Rican stock. A large colony
was maintained in 3- and 10-gallon glass
aquaria filled with continuously aerated
tap water. The snails were liberally fed on
fresh romaine lettuce every other day.

Egg masses were carefully scraped off
the side walls of the aquaria immediately
after deposition and isolated in Petri dishes
in dechlorinated tap water. The water was
changed every other day, and a daily
record was kept of the maximum and min-
imum water temperatures in these dishes.

Since temperature is undoubtedly a
major factor affecting the rate of develop-
ment, embryogenesis was followed up
twice, under 2 different temperature con-
ditions: once during June and July when
the water temperature in the incubating
dishes ranged between 25 and 30°C, and
also during the following January and Feb-
ruary at a temperature range of 15-20%C.
Each time observations on the developing
eggs were made in more than 100 egg
masses.

To follow up embryonic development,
eggs were successively separated from the
egg mass, 2 at a time, at intervals ranging

EMBRYOLOGY OF MARISA

from % to 12 hours according to the age of
the egg mass. Each egg was immediately
dissected with a pair of sharply pointed
needles in saline solution under a stereo-
microscope. The embryo was carefully
taken out of the egg capsule and freed
from the surrounding albumen. Some em-
bryos were examined fresh, while others
were fixed, stained and mounted whole, or
infiltrated with paraffin wax and sec-
tioned. Drawings were made of both fresh
and stained embryos with the aid of a
camera lucida.

Several fixatives were used with varying
degrees of success. The best results were ob-
tained with the Duboscq-Brazil modification
of Bouin s fluid (Gatenby € Beams, 1950)
which was therefore largely used. The
material was washed in 70% ethanol for at
least 48 hours after fixation then stained for
1-3 hours in alcoholic borax carmine solution
(Grenacher, 1879), dehydrated in ascending
grades of ethanol, cleared in xylol or cedar
wood oil, and mounted in canada balsam.

Embryos fixed in the above mentioned
way, but stained only very lightly with
alcoholic borax carmine for 15 minutes,
were infiltrated with paraffin wax and sec-
tioned to the thickness of 54. The light
borax carmine staining facilitated rapid
orientation of the embryo in the paraffin
block, under a stereomicroscope. Several
sets of serial transverse and sagittal sec-
tions were cut in every embryonic stage
and stained mainly with Delafield's
haematoxylin and eosin or with Mallory $
triple stain. Graphic reconstructions of the
embryo and of its internal organs were
made in each stage with the help of these
series of serial sections.

OBSERVATIONS

The egg, egg mass, egg laying and
mating behaviour of Marisa cornuarietis
have been described in a previous paper
(Demian & Ibrahim, 1970/71). The ferti-
lized ovum (Fig. 1A) is spherical, opaque,
light brownish and measures about 110 in
diameter. The first indication of polar dif-
ferentiation in the ovum can be noted a
few minutes after oviposition, when 2 clear

. I. GENERAL DEVELOPMENT 12:

QU

polar bodies (PB) are extruded, one after
the other, at one end of the ovum, which
represents the animal pole. These bodies
remain attached to the segmenting ovum
during early cleavage until the 16-cell
stage is reached.

Two hours after the appearance of these
polar bodies and before the first cleavage,
a small translucent area becomes con-
spicuous at the animal pole, and the nucle-
us migrates into this region from the
centre of the ovum. The rest of the cyto-
plasm remains opaque and condensed with
yolk, whereby the animal and vegetative
poles become well-differentiated. More or
less similar processes of polar differentia-
tion have been recognized before the on-
set of the Ist cleavage in the eggs of
Ampullaria canaliculata and Pila globosa
by Scott (1934) and Ranjah (1942) respec-
tively.

1. Cleavage

The egg undergoes the typical total
spiral cleavage common to the Gastro-
poda. In eggs maintained at temperatures
of 25-30°C, the Ist cleavage (Fig. 1B,C)
takes place 2%-3 hours after egg-deposi-
tion. It starts at the animal pole and pro-
ceeds meridionally towards the vegetative
pole, dividing the ovum into 2 equal
spherical blastomeres. These blastomeres
soon lose their regular spherical form as
they become pressed against each other.

The 2nd cleavage is also meridional and
passes at right angles to the 1st cleavage. It
starts about 1 hour after the completion of
the 1st cleavage, and results in the forma-
tion of 4 equal spherical blastomeres or
quadrants (A, B, C, D, Fig. 1D) enclosing
a narrow central cleavage cavity in be-
tween them. However, these blastomeres
soon press against each other, lose their
spherical form and the cavity between
them consequently disappears.

The first indication of the spiral char-
acter of this cleavage appears about 45
minutes after the commencement of the
2nd division, when the cleavage planes
cease to be strictly meridional and make an
angle with the polar axis of the egg. In
consequence, at the animal pole, the

126 DEMIAN AND YOUSIF

FIG. 1. Early cleavage divisions: A, Fertilized ovum. В, Beginning of Ist cleavage. С, 2-cell stage. D,E, 4-cell
stage as seen from the side and from the vegetative pole. F,G, 8-cell stage as seen from the side and from the
animal pole. H,I,J, 12-, 16- and 24-cell stages as seen from the animal pole.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 127

KEY TO LETTERING ON FIGURES

(All drawings are of Marisa cornuarietis (L.))

A auricle

AM _ aortic ampulla

ANP anal cell-plate

APP apical cell-plate

AT archenteron

BL blastocoel

BV buccal vestibule

CG cerebral ganglion

CM cerebral commissure

CML. columellar muscle

CN ctenidium

COP crop or mid-oesophagus

DGA anterior lobe of digestive gland
DGP posterior lobe of digestive gland
В еуе

EN — endoderm

ET ectoderm

F foot

GZS — sorting area of gizzard

СИТ cuticularized region of gizzard

H head

HP head plate
1 intestine
K kidney

JE lung

LAB labial palp

LGS left gastric streak

LOC lateral odontophoral cartilage
ES larval stomach

M mouth

MS mesoderm or mesenchyme cells
MT mantle

MTC mantle cavity

MTE mantle edge

OE _ oesophagus

OER pro-oesophagus

blastomeres B and D move apart while A
and C approach one another, a deep polar
furrow developing along the line of con-
tact between them (Fig. 1E); whereas, at the
vegetative pole, the blastomeres A and C
move apart while B and D touch each other
and a polar furrow, comparable but at right
angles to that formed at the animal pole,
appears between them.

The 8rd cleavage (Fig. 1F) is lati-
tudinal, but passes nearer to the animal
pole so that the egg may be considered
moderately telolecithal. It occurs about 5
hours after egg-deposition and results in
the formation of 8 blastomeres of 2 dif-
ferent sizes. The upper tier of 4 blasto-
meres, ог lst quartette of micromeres (la-
14), is considerably smaller than the set of

OET post-oesophagus

OP operculum

ОРГ. opercular lip

OS osphradium

Р pericardium

PB polar bodies

PDGR pedal groove

PDGL pedal gland

РОМ pedal commissure

PDP _ pedal cell-plate

PHK common primordium for pericardium, heart
and kidney

ES peristome

РТ prototroch

RC radular collostyle
RGS right gastric streak

RI rudimentary intestine
RNV renal vestibule

RS radular sac

RT rectum

SD stomodaeum

SDB _ buccal region of stomodaeum
SDO_ oesophageal region of stomodaeum
SH shell (protoconch)

SHG shell gland

SHGR rudimentary shell gland

SLG | salivary gland

SOR subradular organ

SS style sac

STC statocyst

TN tentacle

U ureter

V ventricle

УГ. velum

VS visceral sac

macromeres below (1A-1D). The spindle
axis of cleavage soon becomes oriented
obliquely to the polar axis of the seg-
menting ovum as the micromeres shift
slowly and come to lie over the angles
formed by the contiguity of the macro-
meres below them (Fig. 1G). In other
words, the micromeres rotate clockwise
through approximately 45% above the
macromeres, clearly indicating that the
3rd cleavage is dexiotropic.

The 4th cleavage (Fig. 1H) starts about
6 hours after egg-deposition. It is again
latitudinal, but anti-clockwise or laeo-
tropic and cuts the 4 macromeres into 8
cells of 2 different sizes. The 4 smaller ones
constitute the 2nd quartette of micro-
meres (2a-2d); the rest are labelled 2A-2D.

128 DEMIAN AND YOUSIF

The Ist quartette of micromeres divide about
half an hour later (Fig. 11), also laeotropical-
ly; thus 4 small cells (la'-1d') are cut off
towards the animal pole, the remainder (1a?-
1d?) lie below them, and the 16-cell stage is
established.

Right after the completion of the 3rd
and of 4th cleavage divisions, the dividing
cells are yet spherical; between them there
is a narrow irregular cleavage cavity. But
these cells soon get pressed against one an-
other, losing their regular spherical form,
and the cavity in between them dis-
appears before the commencement of the
succeeding cleavage.

The 5th cleavage (Fig. 1]) takes place
about 7% hours after egg-deposition. At
this cleavage, a 3rd quartette of micro-
meres (3a-3d) is cut off by a dexiotropic
division from the macromeres, the ге-
mainder of which are labelled 3A-3D. The
2nd quartette of micromeres divide al-
most simultaneously, in a similar dexio-
tropic direction, into 2a'-2d' and 2a?-2d?,
and the 24-cell stage is thus reached.
cleavage cavity appears at this stage nearer
to the animal pole and persists throughout
subsequent stages as the blastocoel.

The following divisions of the macro-
and micromeres are rapid, and the regular
pattern of the spiral cleavage is soon lost.
The dividing cells are pressed against each
other after every division, the cell bound-
aries become vague, while the egg re-
tains its regular spherical form. The
blastula is fully developed about 14 hours
after oviposition. It is spherical, about
110 y in diameter, and has its cells ar-
ranged in a single layer enclosing a rela-
tively large segmentation cavity.

2. Gastrulation

Gastrulation is mainly epibolic, not em-
bolic as described for Pila globosa by
Ranjah (1942). It is completed about 22
hours after egg-deposition. Shortly after
the formation of the blastula, the embryo
becomes slightly flattened at both poles.
The smaller micromeres overgrow and en-
close the larger yolk-laden macromeres,
while the latter simultaneously become
elongated and protrude into the segmenta-

tion cavity; these will form the future
endoderm. A widely open rounded blasto-
pore is thus formed at the vegetative pole,
but it gradually shifts towards the other
pole and simultaneously narrows by the
gradual approach of its lateral lips until it
completely closes by the end of gastrula-
tion. Meanwhile, a narrow irregular space,
the archenteron (AT, Fig. 2), makes its
appearance in between the dividing mega-
meres.

Since cell-lineage was not followed up in
detail beyond the 24-cell stage, the origin
of the mesoderm could not be determined
with certainty in the present study. How-
ever, there is good indication, derived
from repeated preliminary observations on
live and sectioned embryos, that the meso-
derm in Marisa is teloblastic in origin, as in
Pila globosa (Ranjah, 1942) and several
other prosobranchs (Raven, 1966). It is
most probably derived from micromere 4d
which is cut off from macromere 3D
during the 6th cleavage, and which later
propagates 2 loose strands of small ovoid
or polygonal mesoblastic cells, with a
densely granular cytoplasm and large
spherical nuclei, in the segmentation cavi-
ty.

The fully formed gastrula (Fig. 2)
ovoid in outline. The ectodermal cells (ET)
are transparent, range from short cuboi-
dal to tall columnar and have a granular
and deeply stainable cytoplasm and rela-
tively large spherical nuclei. The endo-
derm (EN) forms a spheroidal inner mass
of cells which are even more varied in form
and size. They are opaque, heavily loaded
with yolk granules and impart a distinct
yellowish colour to the gastrula.

3. General outlines of embryonic develop-

ment after gastrulation

Development in Marisa cornuarietis is
direct, as in most other freshwater gas-
tropods. Twelve distinct embryonic stages
have been distinguished from the end of
gastrulation till hatching. Before going in-
to the details of the origin and develop-
ment of the different organ systems, it will
be expedient to give a brief general out-
line of the whole process of embryonic

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 129

o вед SHGR
: Fed
Se

2 e ©
“= 5 So

alge > - ANP

FIG. 2. Sagittal section of the gastrula.

FIG. 3. The embryo in Stage I: A, Left lateral view. B, Dorsal view.

FIG. 4. Median sagittal section of the embryo in Stage I.

FIG. 5. The embryo in Stage II: A, Left lateral view. B, Dorsal view. C, Ventral view.
FIG. 6. Median sagittal section of the embryo in Stage II.

130

TABLE

Stage

IT]

\

VI

VII

VIII

IX

days days

14

X

- Es

he days

28

DEMIAN AND YOUSIF

Embryonic stages of Marisa cornuarietis

9

34 a
40 5
48 6
56 7
70 9
82 10
90 11

2

Age at
eve 30 15-2 0

Dimensions

Length Breadth

Diagnostic characters

ee А

120

160

190

240

300

450

970

630

100 12% 650

670

100

130

160

180

200

300

310

330

450

Bilaterally symmetrical, with distinct prototroch; apical, pedal and anal
cell-plates; stomodaeum in early stage of differentiation.

Bilaterally symmetrical; with invaginated rudimentary stomodaeum;
rudiments of shell gland and ureter in early stage of differentiation; 2
rudimentary aggregates of mesoderm cells differentiated on either side of
endodermal sac.

Bilaterally symmetrical externally, but asymmetrical internally; with
prominent rudimentary foot and visceral sac on lower side; stomodaeal in-
vagination communicating with archenteron; rudiments of shell gland and
ureter invaginated; a single right rudimentary mesodermal vesicle
representing a common primordium for pericardium, heart and kidney.

Bilaterally asymmetrical both externally and internally; with shell gland
rudiment shifted left of median line; pericardium and kidney differen-
tiated from common primordium; rudimentary ureter communicating
with rudimentary kidney.

Pear-shaped with well-developed velum; cup-shaped rudimentary shell
gland opening widely on left side of visceral sac; rudiments of ctenidium
and osphradium, and those of cerebral, pedal, pleural and intestinal
ganglia in early stage of differentiation; endodermal sac differentiated into
larval stomach and rudimentary intestine.

Foot cone-shaped; rudimentary shell gland everted and cap-like;
rudiments of sorting and cuticularized regions of gizzard differentiated in
wall of larval stomach; rudiments of auricle and ventricle differentiated
and inter-communicating; ureter U-shaped; rudiments of statocysts in-
vaginated, and rudiments of most nerve ganglia delaminated from ec-
toderm.

Torsion is first noticeable; visceral sac slightly rotated anti-clockwise;
foot elongated with flattened creeping sole; statocysts form closed vesicles
below ectoderm; reno-pericardial tube developed; rudiments of hepatic
vestibule, buccal ganglia and visceral ganglion differentiated.

Visceral sac makes an angle of 30° with longitudinal head-foot axis;
mantle cavity first noticeable as shallow depression on right dorsolateral
side of visceral sac; pericardium, kidney and osphradium displaced to left
side; ureter oriented transversely to longitudinal axis of body; style sac and
intestine differentiated.

Visceral sac makes an angle of 45° with longitudinal axis of head and foot;
mantle cavity enlarged and bowl-shaped; ctenidium has 3 ctenidial
lamellae and projects, with osphradium, at opening of mantle cavity; oper-
culum, tentacles and eye rudiments differentiated; anus first recognized,
opening together with renal vestibule in mantle cavity.

Torsion completed; visceral sac cone-shaped, with apex pointing
downwards; mantle cavity deep, opening widely behind head vesicle;
ctenidium and osphradium enclosed within mantle cavity, lung rudiment
differentiated between them; about 7 ctenidial lamellae developed; heart
chambers beating rhythmically; tentacles stumpy, eyes form closed

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT

131

vesicles below ectoderm; 2 rows of teeth developed within radular sac; all
nerve commissures and connectives established.

Visceral sac showing early signs of spiral coiling, with apex pointing
forwards; mantle thin, mantle cavity has assumed definitive form and posi-
tion; ctenidium elongated with about 12 ctenidial lamellae; ureter and
heart projecting on roof of mantle cavity; velum diminished; foot with
well-differentiated operculum, pedal gland and columellar muscle; 5 rows
of teeth developed within radular sac; gizzard U-shaped and fully formed;

XI 6 16 750 600
intestine long and W-shaped.

mm mm

ХИ т» 18 1.3 0.9

Minature of adult; head, tentacles, eyes, labial palps and nuchal lobes
well-developed; pedal cell-plate has disappeared; visceral sac makes 1%
coils; ctenidium stretched far in front of ureter, with about 20 ctenidial
lamellae; 6-7 rows of teeth developed within radular sac; oesophageal
pouches and anal gland differentiated; lateral odontophoral cartilages,
jaws and buccal muscles well-recognizable; rudiments of 2 lobes of
digestive gland elongated and approximated to one another at rear of lar-
val stomach; aortic ampulla well-differentiated and lodged below pericar-
dium; kidney dorso-ventrally flattened and stretched transversely behind
ureter; all nerve ganglia at definitive locations.

development and to characterize each of
the 12 embryonic stages recognized. The
distinctive anatomical features of each
stage, its dimensions and approximate age
(as developed at 2 different temperature
ranges of 25-30 and 15-20%C) are sum-
marized in Table 1.

Stage I (Figs. 3A,B, 4)

The embryo is spheroidal, bilaterally
symmetrical both externally and т-
ternally and about 1204 long. It shows a
marked advance over the gastrula stage as
evidenced by the development of the pro-
totroch and the differentiation of the
apical, pedal and anal cell-plates.

The prototroch (PT), or preoral ciliated
band, shows as a slightly projecting, trans-
lucent, circular band located nearer to the
upper‘ (dorsal) side. It consists of a double
row of large pyramidal cells which carry
short cilia on their free edges and present a
vacuolated and highly acidophilic cyto-
plasm.

A few large transparent ectodermal cells
on the dorsal surface of the embryo con-
stitute the apical cell-plate (APP). These
cells are narrower than those of the proto-
troch, but they similarly carry short cilia

and have a markedly acidophilic, vacuo-
lated cytoplasm. Ventrally 2 other groups
of more or less similar, large, transparent,
ciliated ectodermal cells also become con-
spicuous: the anterior pedal and posterior
anal cell-plates (PDP and ANP re-
spectively). (Terminology after Conklin,
1897, and Ranjah, 1942.)

The ectoderm, in a small circular area
just below the prototroch, thickens form-
ing the rudiment of the stomodaeum
(SD). This rudiment is situated just in
front of the site of closure of the blasto-
pore which has shifted forward to the
opposite pole by the end of gastrulation.
The endoderm (EN) forms a central
spheroidal mass which still encloses a small
irregular archentric cavity (AT, Fig. 4); its
wall is still more than one cell thick.

Stage II (Figs. 5A-C, 6)

The embryo is considerably elongated,
measures about 160 и in length and starts
rotating actively inside the egg capsule
with the help of its cilia. The pedal (PDP)
and anal (ANP) cell-plates become more
prominent as their cells further enlarge.
The rudiment of the stomodaeum (SD)
deeply invaginates, but does not yet con-

‘The dorso-ventral axis of the embryo at this stage is at right angles to the animal-vegetative polar axis.

FIG.
FIG.
FIG.
FIG.

DEMIAN AND YOUSIF

E
($)
$)

ay
qe
A

Pe
&

. The embryo in Stage Ш: A, Left lateral view. В, Dorsal view. С, Ventral view.

8. Median sagittal section of the embryo in Stage III.

9. The embryo in Stage IV: A, Left lateral view. B, Right lateral view. C, Dorsal view.
10. Median sagittal section of the embryo in Stage IV.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 133

nect with the archenteron.

The ectoderm, in a small circular area
on the posterior side, thickens forming the
rudimentary shell gland (SHGR). Another
smaller and less conspicuous thickened
ectodermal plate is also differentiated to
the right side of the anal cell-plate:
the rudiment of the renal vestibule and
ureter (U).

The endodermal sac (EN, Fig. 6) en-
larges and assumes an ovoid outline; its
cells become somewhat flattened and are
arranged in a single layer surrounding a
relatively wide archenteron (AT). Two
compact masses of mesenchyme cells (MS,
Fig. 5A) of unequal size become con-
spicuous in the posterior region of the
embryo, on both sides of the endodermal
sac. The right mass is slightly larger and a
little posterior to the left one. The latter
will soon disappear, while the former per-
sists and represents a common primordium
for the pericardium, heart and kidney.

Stage Ш (Figs. 7A-C, 8)

The embryo is slightly more elongated,
bilaterally symmetrical externally but
asymmetrical internally, and measures
about 190 и in length. It has developed 2
rounded prominences on the ventral side
which represent the rudiments of the foot
(F, Fig. 7A) and visceral sac (VS). Two
new ectodermal cell-plates, the head
plates (HP, Figs. 7B, 8), have dif-
ferentiated anteriorly, above the level of
the prototroch. They consist of densely
granular, columnar cells with central
spherical nuclei. These cells will later de-
velop into the tentacles, eyes and cerebral
ganglia.

The stomodaeum invagination (SD)
deepens further, its cavity communicates
with the archenteron (AT, Fig. 8), and the
cells in its roof develop short cilia. The
anterior opening of the stomodaeum, or
mouth (M), is rounded and faces antero-
ventrally. The rudimentary shell gland
(SHGR) is enlarged and forms а сир-
shaped median invagination on the
posterior side. The rudiment of the renal
vestibule and ureter (U, Fig. 7A) becomes
invaginated.

The left aggregate of mesoderm cells
has disappeared. The right mass, a com-
mon rudiment for the pericardium, heart
and kidney (PHK, Fig. 7A), enlarges in
this stage, shifts a little upwards and hol-
lows out, forming an ovoid vesicle with a
small central cavity, the coelom.

Stage IV (Figs. 9A-C, 10)

The embryo measures about 240 и in
length. It starts to lose its external sym-
metry as the rudimentary shell gland
(SHGR) further enlarges and slightly shifts
towards the left side. The stomodaeal tube
is now roughly divisible into an anterior
buccal region (SDB) and a narrower pos-
terior oesophageal part (SDO). The rudi-
ment of the radular sac (RS, Fig. 10) be-
comes noticeable as a small evagination in
the floor of the oesophageal region. The
endodermal sac (EN) is pear-shaped, with
the narrower end pointing postero-
ventrally. No clear differentiation of parts
is yet visible in this sac. The archenteron
(AT) is filled with the albuminous fluid
that apparently reaches it through the
mouth opening (M).

The common rudiment for the peri-
cardium, heart and kidney (PHK, Fig. 9B)
becomes incompletely divided by a con-
striction into 2 parts: a larger and thinner-
walled anterior portion that will develop
into the pericardium and heart, and a
smaller, thicker-walled posterior part that
represents the rudiment of the kidney. The
invaginated rudiment of the renal vesti-
bule and ureter (U) deepens and connects
with the cavity of the rudimentary kidney.

Stage V (Figs. 11A-D, 12)

The embryo has grown pear-shaped
with a broader anterior region, and
measures about 300 и in length. The foot
rudiment (F) juts out more prominently; it
tapers ventrally so that its transverse sec-
tion is V-shaped. The cells of the pedal
cell-plate (PDP) are further enlarged and
are now arranged in a median longi-
tudinal double row on the lower edge of
the foot. The prototroch protrudes more
markedly on either side of the head vesicle
forming a conspicuous larval velum (VL).

DEMIAN AND YOUSIF

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FIG. 11. The embryo in Stage V: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.
FIG. 12. Sagittal section of the embryo in Stage V passing to the left of the median line.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 135

The rudimentary shell gland (SHGR) is
considerably enlarged and entirely shifted
to the left side. It forms a large, deep, cup-
shaped depression that is lined with a thin
cuticular secretion, the protoconch or lar-
val shell (SH, Fig. 12). The cells found at
the periphery of this depression thicken in
subsequent stages and form the shell gland
of the adult.

Rudiments of the ctenidium (CN) and
osphradium (OS, Fig. 11B) differentiate as
thickened oval areas of the ectoderm on
the right dorso-lateral wall of the visceral
sac. Rudiments of the cerebral, pedal,
pleural and intestinal ganglia, as well as
the rudiments of the statocysts (STC), all
also start to differentiate at this stage as
small ectodermal thickenings.

A tubular evagination develops postero-
ventrally from the rear of the endodermal
sac which thus becomes differentiated into
an anterior larval stomach (LS, Fig. 11A)
and a posterior rudimentary intestine (RI).
The former is ovoid, much larger, thicker-
walled and has a wider lumen than the
latter. It presumably serves in absorbing
and digesting the albuminous fluid of the
egg throughout embryonic life. Only small
parts of it will contribute to the formation
of the adult s stomach; the rest will be re-
placed by the digestive gland a short while
after hatching. The rudimentary intestine
is short, tubular, points downwards and
ends blindly.

The rudiment of the pericardium and
heart (P, Fig. 11B,D) enlarges further and
shifts backwards behind the larval
stomach. The rudimentary kidney (K, Fig.
11B) acquires a tubular form and lies be-
hind the pericardial rudiment, with which
it still widely communicates. Rudiments of
several blood vessels and sinuses start to
differentiate at this stage as irregular
spaces or as parts of the segmentation
cavity surrounded by mesenchyme cells.

Stage VI(Figs. 13A-D, 14)

A considerable growth in length has
taken place so that the embryo is 450 u
long. The foot (F) has further enlarged and
assumed a conical form; its antero-ventral
edge starts flattening, thus marking the

beginning of the formation of the creeping
sole. The visceral sac (VS) is also much en-
larged and rounded in outline, but some-
what laterally compressed. The skin
around the mouth forms a thickened rudi-
mentary lip in the form of an incomplete
ring, and the radular sac evagination (RS)
enlarges.

The rudimentary shell gland is further
enlarged and thickened at the periphery,
while its central part, formerly concave,
thins and bulges outward so that the whole
rudiment assumes a cap-like shape. The
thickened periphery (SHG, Fig. 13A)
represents the actual rudiment of the
adult’s shell gland, while the thin central
part will subsequently form the skin of the
visceral mass and will also contribute to
the formation of the mantle fold. Close
around the thickened periphery, the ecto-
derm is slightly raised so as to form a pro-
jecting circular fold (MTE) which will
form the mantle edge of the adult.

Rudiments of the cerebral, pedal,
pleural and intestinal ganglia become de-
laminated from the ectodermal layer and
form compact cellular masses below it, and
rudiments of the statocysts (STC) become
invaginated.

The larval stomach (LS) has grown con-
siderably in size and its cells are much en-
larged (Fig. 14). A narrow longitudinal
streak, referred to here as the right gastric
streak (RGS, Fig. 13B), makes its appear-
ance on the right dorso-lateral side of the
larval stomach. The cells in this streak will
develop into the cuticularized portion of
the adults gizzard. The cells in a small
oval area on the left wall of the larval
stomach also start differentiating at this
stage, eventually developing into the sort-
ing area of the adult's gizzard. The rudi-
mentary intestine (RI) is sharply bent
downwards and still ends blindly.

The rudiment of the pericardium and
heart elongates in the antero-posterior
direction; its wall becomes deeply in-
vaginated at 2 points, 1 on the left side and
the other on the postero-dorsal side. The 2
chambers thus formed communicate and
represent the ventricle (V) and auricle (A)
respectively (Fig. 13B). The opening be-

136 DEMIAN AND YOUSIF

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CAE age ES
q RDA y

FIG. 13. The embryo in Stage VI: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.
FIG. 14. Median sagittal section of the embryo in State VI.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 137

FIG. 15. The embryo in Stage VII: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.
FIG. 16. The embryo in Stage VIII: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.

138 DEMIAN AND YOUSIF

tween the pericardial cavity and the rudi-
mentary kidney (К) becomes simul-
taneously more constricted (Fig. 14). The
posterior portion of the kidney has dilated
and shifted up and to the left towards the
median line. The rudimentary ureter (U,
Fig. 13B,C) is more elongated and bent in
the shape of a U with 2 unequal arms. The
shorter dorsal arm communicates anterior-
ly with the rudimentary kidney, while the
ventral arm opens into the renal vestibule
(RNV). The 2 arms are thick-walled; they
communicate by a cross connection in the
form of a thin double lamella.

The spaces between the different inter-
nal organs are now almost completely
occupied by scattered stellate mesen-
chyme cells (MS, Fig. 14).

Stage УП (Fig. 15A-D)

Torsion begins as the embryo reaches
this stage, after about 82 hours of incuba-
tion at 25-30°C, and as it attains a length
of about 570 и. The process of torsion
takes about 2 days, i.e. until the embryo
passes through Stage X. It is apparently
due to differential growth of the 2 sides of
the embryo, since no distinct muscles have
as yet been developed.

In this stage, the foot (F) appears more
elongated and its apex points backwards,
making an acute angle with the longi-
tudinal axis of the body. It has developed a
broad flattened sole which is now used for
creeping on the inner surface of the egg
capsule.

The rudiment of the adult's shell gland
(SHG) is further enlarged. The visceral sac
(VS) also enlarges and is more laterally
compressed so that it assumes the form of a
thick circular disc. The first sign of torsion
is manifest by the position this sac now
assumes relative to head and foot. It is no
longer parallel to the longitudinal axis of
these organs, but has started rotating anti-
clockwise: its postero-ventral part has
slightly moved to the right and upwards,
while its antero-dorsal part has shifted to
the left and downwards. The anal cell-
plate (ANP) is consequently displaced to
the right side of the median line.

The rudiments of the ctenidium (CN)

and osphradium (OS) are further
thickened and shifted forwards (Fig. 15B).
Rudiments of the buccal ganglia and the
visceral ganglion become differentiated,
and each pedal ganglion fuses with the
pleural ganglion of its respective side. The
2 intestinal ganglia appear rotated anti-
clockwise around the larval stomach; the
left ganglion thus becoming sub-intestinal
and the right one supra-intestinal. Nerve
commissures and connectives start to dif-
ferentiate as thin extensions from the
nerve ganglia. The statocysts (STC, Fig.
15B) separate from the ectoderm and form
2 closed vesicles below it.

The larval stomach (LS) enlarges and
extends further backwards in the lumen of
the visceral sac. A 2nd longitudinal streak,
referred to here as the left gastric streak
(LGS, Fig. 15A), is seen running along the
entire length of the left ventro-lateral side
of the larval stomach. The cells in this
streak will develop into the hepatic vesti-
bule of the adult. The still closed tip of the
rudimentary intestine (RI) is shifted to the
right as a result of the slight rotation of the
visceral sac.

The heart chambers within the peri-
cardial cavity start to show some irregular
contractions. The kidney (K) becomes
ovoid and communicates with the peri-
cardial cavity through a narrow reno-peri-
cardial tube. The 2 arms of the U-shaped
ureter (U) come to lie so close to each
other that the space between them is re-
duced to a mere furrow. The afferent and
efferent ureteral veins, which supply and
drain the ureter, become conspicuous at
this stage. The renal vestibule (RNV) shifts
a little upwards, thus coming to open near
the center of the right face of the visceral
sac.

Stage VIII (Fig. 16A-D)

The embryo appears more asym-
metrical due to further torsion and
measures about 630 и in length. The foot
is now well-demarkated from both the
head and visceral sac. The sole assumes a
triangular outline. А thickened circular
area projects on the postero-dorsal side of
the foot: the rudiment of the opercular lip

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 139

(OPL, Fig. 16A), which will later secrete
the operculum. Some glandular cells
appear within the foot, marking the begin-
ning of differentiation of the pedal gland.

The visceral sac is more twisted and lies
at an angle of 30° to the longitudinal axis
of the head and foot. As a result of this
twisting, a broad shallow depression forms
on the right side of the visceral sac near its
dorsal edge, marking the beginning of de-
velopment of the mantle cavity (MTC,
Fig. 16B).

As torsion proceeds during further
development, the rudimentary shell gland
enlarges gradually until it covers the whole
of the visceral sac, then prolongs forward
to form the mantle skirt. In other words,
the skin now found on the left side of the
visceral sac, which is covered by the shell
(SH) and encircled by the adults shell
gland (SHG), will grow enormously so as
to form the whole of the outer covering of
the future visceral mass, as well as the
outer epithelium of the mantle fold in
front. Meanwhile, the mantle edge
thickens, the mantle cavity enlarges, and
the skin which now covers the right side of
the visceral sac is gradually enfolded in-
side the deepening mantle cavity, to form
its inner lining as well as the inner
epithelium of the mantle fold. The
ctenidium (CN) and osphradium (OS),
which have already been differentiated on
this skin, on the right dorso-lateral side of
the visceral sac, will accordingly pass in-
side the mantle cavity in subsequent
stages.

In Stage VIII, and as a result of torsion,
the kidney (K, Fig. 16A,B) comes to lie
postero-dorsally to the pericardium (P),
and both become displaced leftwards. The
aperture of the renal vestibule (RNV, Fig.
16B) now points forwards; the ureter (U,
Fig. 16C,D) lies almost transversely to the
longitudinal axis of the body; it takes from
the right side of the kidney.

The rudimentary intestine becomes dif-
ferentiated into a proximal funnel-shaped
style sac (SS, Fig. 16A) and a distal tubu-
lar intestine. All nerve ganglia are con-
siderably enlarged, and the sub-intestinal
ganglion shifts forwards close to the right

pleuro-pedal ganglionic mass.

Stage IX (Figs. 17A-D, 18)

The embryo is slightly more elongated,
measuring about 650 и in length. Torsion
is more pronounced. The visceral sac now
lies at an angle of 45° to the longitudinal
axis of the head and foot.

The foot (F) assumes its definitive shape
and position; the opercular lip (OPL) be-
comes more prominent and secretes a thin
cuticular covering, the operculum (OP,
Fig. 18). The tentacles (TN) develop on
the head plates as 2 small conical pro-
tuberances, and the eyes become dif-
ferentiated on the same plates as 2 slightly
invaginated circular discs lying close be-
hind the tentacles.

The deepening mantle cavity (MTC,
Fig. 17B) grows bowl-shaped and is thus
better recognized. The mantle opening is
semi-lunar and the mantle edge (MTE) is
considerably thickened. The ctenidium
(CN) and osphradium (OS) become en-
closed in the mantle cavity, and now hang
down from its roof close behind the mantle
edge. The ctenidium shows 3 transverse
epithelial folds, the first 3 ctenidial lamel-
lae to develop.

The tubular radular sac evagination (RS,
Figs. 17A, 18) becomes much elongated
and S-shaped. Rudiments of the odon-
tophoral cartilages and some buccal mus-
cles differentiate as 2 symmetrical aggre-
gates of mesenchyme cells below the radu-
lar sac, and the salivary glands start to
develop as 2 small tubular evaginations
from the roof of the buccal region of the
stomodaeum.

The rudiments of the adult's digestive
gland are first noticeable in this stage as 2
narrow circular bands located close above
and below the rudiment of the sorting area
of the gizzard (GZS), which has already
differentiated in Stage VI on the left wall
of the larval stomach (LS). The style sac
(SS, Fig. 17A,D) is further enlarged and
shifted to the left due to the enlargement
of the larval stomach. The intestine (1) is
much elongated; leading from the style sac
at the rear of the larval stomach, it bends
and runs anteriorly along its right side. It

140 DEMIAN AND YOUSIF

FIG. 17. The embryo in Stage IX: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.
FIG. 18. Median sagittal section of the embryo in Stage IX.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 14]

SHG

FIG. 19. The embryo in Stage X: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view.
FIG. 20. Median sagittal section of the embryo in Stage X.

142 DEMIAN AND YOUSIF

now opens in the mantle cavity by the
anus, a new perforation first seen in this
stage.

The ventricle (V, Fig. 17A) is pear-
shaped, and there appear irregular in-
ternal folds projecting into its lumen. The
opening between the auricle and ventricle
has become much constricted. The rudi-
ment of the aortic ampulla differentiates as
a compact aggregate of mesoderm cells
lying below the pericardium. The opening
of the renal vestibule (RNV, Fig. 18) is
now pushed inside the mantle cavity, and
the greater part of the U-shaped ureter (U)
lies in front of the kidney (K, Fig. 17C).

Stage X (Figs. 19A-D, 20)

Torsion is completed at this stage of de-
velopment, when the embryo is about
670 и long. The tentacles (TN) are further
elongated and finger-like. The eyes (E)
form 2 ovoid closed vesicles below the
ectoderm. The opercular lip (OPL) is more
clearly marked off from the foot, the
operculum (OP) more distinct, and the
columellar muscle (CML, Fig. 20) is dif-
ferentiated within the substance of the
foot.

The visceral sac is cone-shaped, with a
downward pointing apex, and is entirely
covered by a thin yellowish shell (SH). The
mantle (MT) has grown to the fore, and
the ctenidium (CN) and osphradium (OS)
have been engulfed inside the mantle
cavity and are no longer visible externally.
The ctenidium has further enlarged, is J-
shaped and presents about 7 transverse
ctenidial lamellae. The lung (L, Fig. 19C)
starts to differentiate at this stage as a
thickened concave area of the inner
epithelium of the mantle, lying between
the ctenidium and osphradium.

Two transverse rows of radular teeth are
now visible within the distal end of the
radular sac (RS, Fig. 20) The rudi-
mentary salivary glands (SLG, Fig. 19A)
are elongated and extend on either side of
the oesophagus (OE). As the anterior part
of the larval stomach (LS) starts to
diminish in size, the opening of the
oesophagus into it shifts to the rear. The
rudiments of the anterior and posterior

lobes (DGP, Fig. 20) of the digestive gland
enlarge at the expense of the epithelium in
the wall of the larval stomach.

The heart is now oriented antero-
posteriorly (Fig. 19A), with the auricle (A)
lying in front of and a little dorsal to the
ventricle (V); both chambers beat rhyth-
mically. The kidney (K) is further en-
larged, and the ureter (U, Figs. 19B,C, 20)
extends along the mantle skirt parallel
with the intestine (1) and ctenidium (CN).
It connects with the kidney through a
short tube lying a little in front of the
opening of the ureter into the renal vesti-
bule. All nerve commissures and connec-
tives are now established.

Stage XI (Figs. 21A-C, 23)

The embryo is about 750 u long. The
velum has diminished considerably in size.
The head (H) begins to acquire its
definitive form. The tentacles (TN) are
further elongated and the eye vesicles (E)
appear enlarged and are carried on 2 short
ectodermal projections, the eye stalks. A
retina and a lens are now differentiated in
each eye. The opening of the pedal gland
(PDGR) is noticeable as a transverse slit
running across the anterior edge of the
foot. The operculum (OP), opercular lip
(OPL) and columellar muscle (CML, Fig.
23) are all well-recognizable. The stato-
cysts (STS) become spheroidal, shift from
their original locations to lie on either side
of the foot, and a few statoconi appear in-
side them.

The mantle (MT) has become thinner
and is prolonged anteriorly, forming a con-
tinuous cloak around the body, behind the
head. The visceral mass is also much en-
larged and starts to show signs of spiral
coiling as its apex runs forwards and a little
to the right. The ctenidium (CN) is more
elongated and shows about 12 ctenidial
leaflets. It has shifted forwards along with
the forward extension of the mantle so that
it comes to lie in front of the heart, and ex-
tends obliquely along the mantle (Fig.
21A,C). The osphradium (OS) also shifts
forwards and presents 2 small folds on its
free surface. The rudiment of the lung (L,
Fig. 21C) becomes further invaginated.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 143

FIG. 21. The embryo in Stage XI: A, Left lateral view. В, Right lateral view. С, Dorsal view.
FIG. 22. The embryo in Stage XII: A, Left lateral view. В, Dorsal view.

144 DEMIAN AND YOUSIF

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ES

K

AD ES
2 Sy a) E

E

В

A eine »]

А
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a RT AS Later NS e)

DGP

FIG. 23. Median sagittal section of the embryo in Stage XI.
FIG. 24. Median sagittal section of the embryo in Stage VII.

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 145

The pallial fold or epitaenia starts to de-
velop as a small epithelial fold projecting
horizontally across the right posterior cor-
ner of the floor of the mantle cavity.

Five transverse rows of teeth are now
conspicuous inside the radular sac (RS,
Fig. 23), and the subradular organ (SOR)
starts differentiating on the floor of the
buccal cavity. The gizzard ( GZT, GZS,
Fig. 21A) becomes fully formed and
assumes its characteristic U-shape. The
intestine (1) is further elongated, W-
shaped; the anus opens at the right an-
terior end of the mantle cavity.

The heart now lies in front of the style
sac (SS), embedded in the left posterior
corner of the roof of the mantle cavity. The
aortic trunk, aortic ampulla and cephalic
aorta as well as the cephalopedal and vis-
ceral haemocoelic sinuses are well-
established. The kidney (K, Fig. 21C) has
grown into a spacious chamber which lies
to the right side of and behind the heart,
and a few inner folds project from its roof.
The afferent and efferent renal veins
supplying the kidney are also well-
differentiated. The ureter (U) has become
almost as long as the ctenidium and runs
obliquely along the roof of the mantle
cavity. The renal vestibule (RNV) assumes
its definitive position, opening at the right
posterior corner of the mantle cavity. The
opening of the ureter into the renal
vestibule lies behind and to the right side
of the short tubular passage connecting the
ureter with the kidney.

Stage XII (Figs. 22A,B, 24)

The embryo is now almost a miniature
of the adult. It measures about 1.3 mm in
length. It has a somewhat dorso-ventrally
compressed head (H), with 2 short conical
labial palps (LAB) projecting anteriorly on
either side of the ventral mouth opening.
The right and left nuchal lobes are also de-
veloped as 2 projecting ectodermal ridges
on either side of the head. The eyes (E)
have developed dense black pigment, and
the inner and outer cornea have become
differentiated in each. The pedal cell-plate
has disappeared, while the anal cell-plate
still exists. The visceral sac is further

coiled, showing about 1% spiral coils.

Six to seven rows of teeth are developed
inside the radular sac (RS, Fig. 24). The
jaws, lateral odontophoral cartilages
(LOC), and most of the buccal muscles are
well-recognizable. The oesophageal
pouches start to differentiate in this stage
as 2 lateral tubular evaginations from the
roof of the buccal mass.

The anterior portion of the larval
stomach, formerly within the head vesicle,
has disappeared. The oesophagus con-
sequently is much elongated. It opens pos-
teriorly on the left ventro-lateral side of
the gizzard. The 3 main regions of the
oesophagus, namely the pro-oesophagus
(OER), crop (COP) and post-oesophagus
(OET), are histologically differentiated
(Fig. 24). The posterior portion of the lar-
val stomach (LS), however, is still large
and fills the greater part of the visceral sac.
The intestine (1) has greatly increased in
length, and the anal gland has begun to
differentiate as a narrow tubular evagina-
tion from its distalmost part, or rectum
(RT, Fig. 22B). The rudiments of the an-
terior (DGA, Fig. 22A,B) and posterior
(DGP, Figs. 22A, 24) lobes of the diges-
tive gland are also further enlarged and
meet behind the gizzard.

The aortic trunk and aortic ampulla
(AM, Fig. 22A) are now lodged below the
pericardium. The kidney (K) becomes
dorso-ventrally flattened, extending almost
transversely behind the ureter (U);
numerous inner folds appear projecting
from its roof. The ctenidium (CN)
stretches far in front of the ureter and pre-
sents about 20 ctenidial lamellae. How-
ever, the greater portion of this organ still
lies to the left side of the median line. No
further changes take place in the lung
rudiment (L) until the embryo hatches.

All nerve ganglia have now attained
their definitive shapes and positions. The
osphradium has developed much more
and shows 4 transverse folds on its free
surface.

The embryo is now capable of re-
tracting within its shell, and the egg albu-
men is almost completely utilized. Rudi-
ments of the genitalia are not yet recogniz-

146 DEMIAN AND YOUSIF

able, and no new structures appear until
the embryo hatches. The egg increases in
average diameter from 2.5 to 4.8 mm
during this embryonic life.

DISCUSSION

Early cleavage divisions in Marisa cor-
nuarietis are basically similar to those de-
scribed by Scott (1934) in Ampullaria
canaliculata and by Ranjah (1942) in Pila
globosa in that the first 2 divisions are
equal and the 3rd cleavage is unequal. The
relative inequality in the size of the re-
sulting micro- and macromeres is com-
parable to that noted in P. globosa, while a
less marked difference between the size of
the corresponding micro- and macro-
meres seems to exist in the case of Ampul-
laria canaliculata, the eggs of which may
have a relatively smaller amount of yolk.

As is the general rule in dextral gas-
tropods, the 3rd cleavage is dexiotropic,
and subsequent cleavages follow according
to the law of alternating cleavages. Sinis-
trality is associated with reversed 3rd and
subsequent cleavages such as have been
observed in Physa (Crampton, 1894;
Wierzejski, 1905) and Planorbis (Rabl,
1879: Holmes, 1900). Narrow recurrent
cleavage cavities, which probably serve as
a mechanism for osmotic regulation
(Raven, 1966), appear between the
dividing blastomeres following the 3rd and
4th cleavage divisions, but they soon dis-
appear. It is the cleavage cavity that
develops during the 5th cleavage that per-
sists as the blastocoel in Marisa.

Gastrulation was found to be epibolic, as
in the majority of gastropods with yolk-
rich eggs (Raven, 1966), and not embolic
as described in Pila globosa by Ranjah
(1942). Gastrulation occurs by embolic in-
vagination in certain prosobranchs with
microlecithal eggs such as
Paludina (= Viviparus) (Erlanger, 1891;
Otto & Ténniges, 1906), while in other
prosobranchs, such as Crepidula (Conklin,
1897), Littorina (Delsman, 1914) and
Patella (Smith, 1935), epiboly and emboly
seem to be of equal importance in gas-
trulation.

While there is a general agreement in

the literature as to the origin of the ecto-
derm and endoderm in the Pro-
sobranchia, some dispute still exists as re-
gards the origin and development of the
mesoderm, of which extensive reviews are
given by Ranjah (1942), Fretter & Graham
(1962), Raven (1966) and Hyman (1967).
Although the details of cell-lineage were
not followed up in Marisa beyond the 24-
cell stage, preliminary observations made
during the present study would indicate
that the mesoderm in this snail is most
probably teloblastic, or entirely derived
from micromere 4d, as in Pila globosa
(Ranjah, 1942). Although Smith (1935),
Crofts (1938) and Creek (1951) have
claimed that the mesoderm in Patella,
Haliotis and Pomatias, respectively, is not
derived from micromere 4d, but from
macromere 4D, this contention, according,
to Raven (1966), can hardly be accepted as
yet.

Development beyond the gastrula stage
follows the general pattern described in
other ampullariids (Semper, 1862; Scott,
1934; Ranjah, 1942). The 12 embryonic
stages recognized here are readily com-
parable to those described by Ranjah
(1942) for Pila globosa, yet the present
observations are not in complete agree-
ment with those made by that author.
Apart from some minor differences as
regards the differentiation of certain
organs in relation to age, there are other
more important differences concerning the
origin and development of a number of
organs. Ranjah states that, in P. globosa: a)
the blastopore persists after gastrulation
and forms the anus; b) the mantle cavity
develops at a very early stage as a mid-
ventral ectodermal invagination; c) the
pericardium develops from 2 symmetrical
mesodermal masses which later approach
each other and shift together to the right
side of the body; d) the kidney arises by 2
rudiments from the pericardial
epithelium; e) the ureter develops as an in-
vagination from the lining of the mantle
cavity; f) the rudimentary stomach trans-
forms early into the adults digestive
gland; g) the mantle skirt develops as 2
ectodermal folds which approach one

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 147

another at a late stage and meet to form
the roof of the mantle cavity; and h) the
statocysts develop relatively late. Similar
observations were made by Fernando
(1931) on the origin and development of
the pericardium, heart, kidney, ureter and
mantle cavity in Ampullaria gigas. These
observations conflict with the present fin-
dings in Marisa cornuarietis. The dif-
ferences between these earlier accounts
and the present observations will be dis-
cussed in detail in the relevant sections of
the present series of studies.

The average period for embryonic
development in M. cornuarietis was 8
days at a temperature range of 25-30°C,
and 20 days at 15-20°C. For other ampul-
lariids, the corresponding incubation
period was reported as less than 14 days for
Ampullaria polita (Semper, 1862), 2-6
weeks for A. gigas (Kohler, 1905), 28 days
in the natural environment in the shade for
A. canaliculata (Scott, 1934), and 10-14
days at 90-100°F or 3 weeks at 70-80°F for
Pila globosa (Ranjah, 1942).

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the
valuable contribution of Dr. K. Mansour,
Emeritus Professor of Zoology, Faculty of
Science, Ain Shams University, Cairo, in
the supervision of the present series of
studies, his enthusiastic support and help-
ful criticism. The writers are also highly in-
debted to Dr. B. Hubendick, Director of
the Natural History Museum in
Gothenberg, Sweden, for directing this re-
search project and for his continuous help
during the course of the work.

LITERATURE, CITED

BROOKS, W.K. & McGLONE, B., 1908, The
origin of the lung of Ampullaria. Carnegie
Inst. Publ., 102: 95-104.

CONKLIN, E.G., 1897, The embryology of
Crepidula, a contribution to the cell lineage
and early development of some marine
gastropods. J. Morphol., 13: 1-226.

CRAMPTON, H.E., 1894, Reversal of cleavage
in a sinistral gastropod. Ann. N.Y. Acad.
Aci., 8: 167-170.

CREEK, G.A., 1951, The reproductive system

and embryology of the snail Pomatias
elegans (Muller). Proc. zool. Soc. Lond.,
121: 599-640.

CROFTS, D.R., 1938, The development of
Haliotis tuberculata, with special reference
to organogenesis during torsion. Phil. Trans.
Roy. Soc. Lond., В, 228:219-268.

DELSMAN, H.C., 1914, Entwicklungs-
geschichte von Littorina obtusata. Tijdschr.
ned. dierk. Ver., 13: 170-340.

DEMIAN, E.S. & IBRAHIM, A.M., 1970/71,
The egg mass, egg laying and mating
behaviour of the snail Marisa cornuarietis
(L.). Bull. zool. Soc. Egypt, 23: 1-12.

ERLANGER, R. von, 1891, Zur Entwicklung
von Paludina vivipara. 1. Morph. Jb., 17:
337-379.

FERNANDO, W., 1931, The development of
the kidney in Ampullaria (Pila) gigas. Proc.
2001. Soc. Lond., 62: 745-750.

FRETTER, V. & GRAHAM, A., 1962,
British prosobranch molluscs, their func-
tional anatomy and ecology. Ray Soc., Lond.,
755 p.

GATENBY, J.B. & BEAMS, H.W., 1950, The
microtomist s vade-mecum. Churchill Ltd.,
Lond., 118 Ed.,755'p.

GRENACHER, H., 1879, Einige Notizen zur
Tinctionstechnik besonders zur Kernfär-
bung. Arch. mikrosk. Anat., 16: 463-471.

HOLMES, 5.]., 1900, The early devel-
opment of Planorbis. J. Morphol., 16: 369-
458.

HYMAN, L.H., 1967, The Invertebrates, Vol.
VI, Mollusca I. McGraw Hill, Inc., 792 p.

KÖHLER, W., 1905, Über Laichgeschäft und
Geschlechtsunterschiede bei Ampullaria
gigas Spix. Blätt. Aquar. Terrar.-Kunde,
16: 438-439.

NAGARAJA, S., 1943, A note on the devel-
opment of the alimentary canal in Pila.
Proc. Indian sci. Congr., 30: 59.

OTTO, H. & TÖNNIGES, C., 1906,
Untersuchungen über die Entwicklung von
Paludina vivipara. Zt. wiss. Zool., 80: 411-
514.

RABL, C., 1879, Uber die Entwicklung der
Tellerschnecke. Morph. Jb., 5: 562-660.

RAJA, S.N., 1943, A preliminary account of the
development and disintegration of the shell
gland in Pila globosa. Proc. Indian sci.
Congr., 29: 154.

RANJAH, A.R., 1942, The embryology of the
Indian apple-snail, Pila globosa (Swainson)
(Mollusca, Gastropoda). Rec. Indian Mus.,
44: 217-322.

RAVEN, C.P., 1966, Morphogenesis: The

148 DEMIAN AND YOUSIF

analysis of molluscan development. Pergamon

Press, 2nd Ed., 365 p.

RYDER, J.A., 1889, Notes on the development
of Ampullaria depressa Say. Amer. Natur.,
23: 735-737.

SCOTT, M.I.H., 1934, Sobre el desarrollo
embrionario de Ampullaria canaliculata.
Rev. Mus. La Plata, 34: 373-385.

geschichte der Ampullaria polita Deshayes.
Naturkund. Verh. provinc. Kunsten.
Wetensch., Utrecht, 1: 1-20.

SMITH, F.C.W., 1935, The development of
Patella vulgata. Phil. Trans. Roy. Soc. Lond.,
B, 225: 95-125.

WIERZEJSKI, A., 1905, Embryologie von
Physa fontinalis L. Zt. wiss. Zool., 83: 502-

SEMPER, Es

1862, Entwicklungs- 706.

ZUSAMMENFASSUNG

EMBRYONALENTWICKLUNG UND ORGANOGENESE BEl DER SCHNECKE
MARISA CORNUARIETIS (MESOGASTROPODS: AMPULLARIIDAE)

I. ALLGEMEINE GRUNDZUGE DER ENTWICKLUNG
E. S. Demian und F. Yousif

Die vorliegende Serie embryologischer Untersuchungen schliesst an die
grundlegenden morphologischen, biologischen und ökologischen Studien an, die zur Zeit
uber die Wasserschnecke Marisa cornuarietis (Linnaeus), durchgeführt werden. Die Art
ist möglicherweise wichtig für die biologische Kontrolle der Schistosoma-Zwischenwirte.
Dieser Teil behandelt die ersten Zellteilungen, Gastrulation und allgemeine Grundzuge
der Embryogenese bei Marisa.

Das Ei unterliegt der Spiralfurchung bis zur Erreichung des 24-Zellen-Stadiums. Die
ersten zwei Teilungen erfolgen zu gleichen Teilen, die dritte ist ungleich und dexiotrop.
Die Gastrulation ist epibolisch, und der Blastoporus schliebt sich am Ende des Prozesses.
Die Embryogenese dauert 8 Tage bei 25-30°C und 20 Tage bei 15-20°C. Die Blastula
entwickelt sich vollständig innerhalb 14 Stunden, und die Gastrulation ist in 22 Stunden
bei den obigen Temperaturen beendet. Die Torsion erfolgt durch das verschiedene
Wachstum der beiden Seiten des Embryos; sie beginnt 3% Tage nach Eiablage und
dauert etwa 2 Tage.

Zwölf verschiedene Stufen der Embryonalentwicklung nach der Gastrulation werden
unterschieden. Alter, Masse und wesentliche anatomische Merkmale jeder dieser
Entwicklungsstufen werden gegeben, dazu ein Überblick uber die Entwicklung der
verschiedenen Organsysteme, ausgenommen das Genitalsystem, das sich hauptsächlich
nach dem Schlüpfen entwickelt. Die Betunde weichen teilweise von früheren Berichten
über verwandte Ampullariiden ab, besonders in bezug auf Ursprung und Entwicklung
des Mantels, der Mantelhohle, des Pericardiums, des Herzens, der Niere, des Ureters,
des Nierenvorhofes und der Verdauungsdrüse.

HZ:
RESUME

DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGENESE
CHEZ MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE)

I. ESQUISSES GENERALES DU DEVELOPPEMENT
E.S. Demian et F. Yousif
La présente série d investigations embryologiques est une extension aux études
fondamentales qui progressent actuellement sur la morphologie, la biologie et l'écologie

du gastropode aquatique Marisa cornuarietis (L.). Cette espece a une importance
potentielle dans le controle biologique des mollusques vecteurs de la bilharziose. La

EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT

présente partie envisage la segmentation, la gastrulation et les grandes lignes de
l'embryologie de Marisa.

Les oeufs subissent une segmentation totale et spirale, qui a été suivie jusqu au stade
24-cellules. Les 2 premiéres divisions sont egales; la 3e est inégale et dexiotropique. La
gastrulation se fait par épibolie et le blastopore se bouche à la fin de ce processus.
L'embryogenèse dure 8 jours à 25-30°C et 20 jours à 15-20°C. La blastula est
complétement développée en 14 heures et la gastrulation terminée en 22 heures a 25-30°C.
La torsion s'établit par suite d'une croissance différentielle entre les 2 côtés de
l'embryon; elle débute environ 3 jours et demi après la ponte et dure pendant environ 2
jours.

On a distingué 12 stades embryonnaires après la gastrulation. La durée, les dimensions
et les caractères anatomiques distinctifs de chacun de ces stades embryonnaires sont
décrits ainsi que l’esquisse du développement de chaque appareil, à l'exception de
l'appareil reproducteur qui se développe principalement après l'eclosion. Les résultats
sont partiellement différents des précédents rapports établis sur des Ampallariides
voisins, en particulier en ce qui concerne le manteau, la cavité palleale, le péricarde, le
coeur, le rein, l'uretére, le vestibule rénal et la glande digestive.

ALE:
RESUMEN

DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN
MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE)

I. DESARROLLO GENERAL
E. S. Demian y F. Jousif

Esta serie de investigaciones embriológicas es una extensión de los estudios básicos-
morfológicos, biológicos y ecológicos-que se estan realizando sobre el gastrópodo
acuatico Marisa cornuarietis (Linnaeus), de importanica potencial en el control biologico
de los caracoles transmisores de Schistosoma. Esta primera parte trata de la división tem-
prana, gastrulación y aspectos generales de la embriogenesis.

El huevo experimenta una division celular espiral que se continúa hasta la 24-célula.
Las primeras dos divisiones son iguales; la tercera es desigual y dexiotropica. La
gastrulación es epibólica y el blastoforo se cierra al terminar el proceso. La embriogenesis
tarda 8 días a 25-30°C y 20 días a 15-30°C. La blastula se desarrolla completamente en
14 horas y la gastrulación se completa en 22 horas a las mismas temperaturas. La torsión
se produce a través del crecimiento diferencial de los dos lados del embrión: empieza
después de tres días y medio de la ovoposición y dura dos días.

Se distinguieron estados embrionarios diferentes después de la gastrulación. La
edad, dimensiones, y aspectos anatómicos diferenciales de cada uno se dan conjun-
tamente con las líneas generales de desarrollo en los varios sistemas organicos. Los
resultados obtenidos en la investigación difieren en parte con los conocidos para otros
ampularidos, particularmente en los orígenes y desarrollo del manto y cavidad paleal,
pericardio, corazón, riñón, uretra, vestibulo renal y glándula digestiva.

JE

149

|

0

DEMIAN AND YOUSIF

ABCTPAKT

ЭМБРИОЛОГИЧЕСКОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS

(MESOGASTROPODA, AMPULLARIIDAE)
1. ОБЩЕЕ РАЗВИТИЕ

Э.С. ДИМИЭН, ©. ЮЗИФ

Настоящая серия эмбриологических работ представляет собой развитие
основных морфологических и экологических исследований по моллюскам -
гастроподам Marisa cornuarietis (L.), имеющим большое потенциальное значение
для биологического контроля над моллюсками-переносчиками шистозомиазиса.
Эта часть работы касается ранних стадий дробления, гаструляции и общего
эмбриогенеза у Marisa. Яйцо проходит полное спиральное дробление,
которое прослеживается до стадии 24 клеток. Первые два деления -
равные, 3-e - неравное и декситропическое. Гаструляция эпиболическая,
бластопор замыкается в конце этого процесса. При температуре 25-30°C
эмбриогенез занимает 8 дней, а при 15-2096 - 20 дней. Бластула,
полностью развивается за 14 часов, гаструляция завершается за 22 часа
(при указанных выше температурах). Торсия происходит во время ростовой
дифференциации с обеих сторон эмбриона, начинается примерно через 3.5
дня после откладки яиц и длится около 2 дней. Во время эмбриогенеза
после гаструляции различаются 12 различных стадий развития. Возраст,
размеры и отдельные анатомические черты каждой из этих стадий
рассматриваютея вместе с общим развитием систем различных органов, за
исключением половой системы, которая развивается, главным образом, после
вылупления. Обнаруженные факты частично расходятся с ранее известными
для родственных Форм моллюсков Ampullariidae, особенно с точки зрения
происхождения и развития мантии, мантийной полости, перикардия, сердца,
почек, уретры, почечной вестибулы и пищеварительной железы.

Z.A.F.

MALACOLOGIA, 1973, 12(1): 151-174

EMBRYONIC DEVELOPMENT AND ORGANOGENESIS
IN THE SNAIL MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE)

Il. DEVELOPMENT OF THE ALIMENTARY SYSTEM!
Emile S. Demian? and Fouad Yousif?
ABSTRACT

The alimentary system of Marisa cornuarietis (Linnaeus) comprises: a) an ectodermal
stomodaeum from which the radular sac, oesophageal pouches and salivary glands are
developed, and b) an endodermal mesenteron differentiated into a gizzard, digestive
gland, style sac and intestine.

The stomodaeum develops early as an ectodermal invagination that later opens into
the endodermal sac, then differentiates into an anterior buccal region and a posterior
oesophageal one. The mouth is a new perforation, arising close to the site of blastopore
closure.

The radular sac develops as a mid-ventral evagination from the buccal region of the
stomodaeum. The radular teeth are secreted by successive transverse bands of
odontocytes, which are produced by cell proliferation from a mass of odontoblasts
located at the distal end of the radular sac, and are continuously added to the subradular
epithelium. Successive bands of odontocytes are separated by transverse bands of weakly
secretory cells which produce the radular membrane. The supraradular epithelium is also
developed by cell proliferation from a mass of cells located in front of the odontoblasts,
the supraradular plug. It contributes to the formation and shaping of the radular teeth.
The jaws are secreted shortly before hatching within a differentiated mandibular region
of the buccal cavity.

The salivary glands and oesophageal pouches develop relatively late as tubular
evaginations from the roofing epithelium of the buccal mass. The entire oesophagus is
ectodermal in origin. It starts differentiating into pro-, mid- and post-oesophagus before
hatching.

The odontophoral cartilages, radular collostyle and buccal muscles are all mesodermal
in origin and develop from mesenchyme cells which aggregate in early stages below the
rudimentary stomodaeum.

The endodermal sac differentiates early into a larval stomach and a rudimentary
intestine. The former serves in absorbing and digesting the albuminous material during
embryonic life. Only small portions of its wall take part in the formation of the adult s
stomach and digestive gland. The rest diminishes during late embryonic development
and disappears shortly after hatching, when it is replaced by the digestive gland. The
gizzard develops from certain differentiated cells which line a distinct longitudinal streak
on the right wall of the larval stomach and a small oval area on the left wall. Cells which
line another streak on the left wall of the larval stomach give rise to the hepatic vestibule.
The digestive gland arises by 2 rudiments on the left posterior wall of the larval stomach.

The intestine is entirely endodermal in origin, develops as a posterior tubular
prolongation of the endodermal sac, and opens into the mantle cavity by the anus at a
relatively late stage. No proctodaeal ectodermal invagination is developed. The anus
forms as a new perforation independently of the blastopore, which closes by the end of
gastrulation.

This investigation was supported in part by research grants (AI 04906 and AI 07696) from the National Institute
of Allergy and Infectious Diseases, U.S. Public Health Service.

"Department of Zoology, Faculty of Science, Ain Shams University, Cairo.

Laboratory of Bilharziasis Research, National Research Centre, Cairo.

151

152 DEMIAN AND YOUSIF

INTRODUCTION

The present investigation is the second
in a series dealing with the embryonic de-
velopment and organogenesis of Marisa
cornuarietis (L.), a snail of potential im-
portance in the biological control of schis-
tosomiasis. These studies also aim at clari-
fying certain ontogenetic problems and
phylogenetic relations in the family Am-
pullariidae.

In the first part of the series (Demian &
Yousif, 1972), a description was given of
the early cleavage, gastrulation and gen-
eral outlines of the process of embryonic
development of M. cornuarietis. The ap-
proximate age, dimensions and distinctive
anatomical features were given for each of
the 12 stages distinguished during the
embryonic life of this snail, and the de-
velopment of the different organs through-
out these stages was briefly described.

The present report comprises a detailed
description of the origin and embryonic
development of the alimentary system of
M. cornuarietis. Observations were made
on the same material and sets of serial sec-
tions which furnished the basis for all other
parts of the series. The material and tech-
niques employed have already been de-
scribed in the lst part of the series. Ref-
erence may be made to that part also for
the age, dimensions and diagnostic char-
acters of the different embryonic stages
which are frequently referred to below.

The terminology adopted in the present
account is based on the works of Demian
(1964) and Lutfy & Demian (1964a,b,
1967) on the gross and microscopic
anatomy of the alimentary system of adult
M. cornuarietis.

OBSERVATIONS

1. Early stomodaeum and
endodermal sac

By the end of gastrulation, the blasto-
pore has shifted from the vegetative pole
towards the opposite pole. In the Ist
embryonic stage, the rudiment of the
stomodaeum starts to differentiate just in
front of the site of blastopore closure. This
rudiment shows as a thickened circular
ectodermal plate just below the level of the

prototroch. The cells in this plate appear
taller and stain darker than neighbouring
ectodermal cells, and show а distinctly
granular cytoplasm and spherical central
nuclei.

The endoderm in this stage forms a
yellowish spheroidal opaque mass which
occupies the greater part of the blastocoel
and encloses a narrow irregular archentric
cavity. The endodermal cells are mostly
cuboidal and have a lightly acidophilic
cytoplasm. Their nuclei are large,
spheroidal, central in position and relative-
ly rich in chromatin; each presents a
conspicuous nucleolus.

As development proceeds, the rudi-
mentary stomodaeal plate invaginates for-
ming a simple narrow blind tube which ex-
tends backwards until in Stage II its distal
tip comes to touch the endodermal sac.
The wall of this tube is single-layered; its
cells range from tall columnar at the
proximal end of the tube, to cuboidal at
the distal end. Meanwhile the endo-
dermal cells proliferate and arrange them-
selves in a single layer, enclosing a rela-
tively wide archenteron.

In Stage III, the stomodaeal tube
further elongates and opens distally in the
endodermal sac. The archenteron thus
communicates with the outside through
the anterior opening of the stomodaeal
tube, the mouth. This opening is rela-
tively wide and faces antero-ventrally.

In Stage IV, the stomodaeum becomes
funnel-shaped and thus roughly divisible
into 2 regions: a wider anterior buccal
region, and a tubular posterior
oesophageal one. A slight median evagina-
tion shows on the floor of the former
region, marking the beginning of forma-
tion of the radular sac. Meanwhile the
endodermal sac becomes much enlarged
and pear-shaped. Reference may be made
to figs. 3-10 of Part I of this series (Demian
& Yousif, 1972) to follow up these early
steps in the development of the
stomodaeum and endodermal sac.

2. Radular sac and radula
As development proceeds beyond Stage
IV, the radular sac evagination grows into

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 153

FIG. 1. Part of a median sagittal section of the embryo in Stage V.
FIGS. 2-4. Median sagittal sections of the radular sac of the embryo in Stages VI, VIII and IX respectively.

154 DEMIAN AND YOUSIF

KEY TO LETTERING ON FIGURES

(All drawings are of Marisa cornuarietis (L. ))

A auricle
AB albuminous material
ALP alary process of radula
AM aortic ampulla
ANP anal cell-plate
AT archenteron
BC buccal cavity
BL blastocoel
BML buccal muscles
BRI inner region of dorsal
buccal ridge
BRO outer region of dorsal
buccal ridge
BV buccal vestibule
CG cerebral ganglion
CH collostylar hood
CML columellar muscle
CN ctenidium
COP стор or mid-oesophagus
CT cuticle
ОСА anterior lobe of digestive gland
DGC digestive cell
DGP posterior lobe of digestive gland
EXC excretory cell
F foot
FC food channel
FGC fusiform gland cell
GB goblet cell
GZS sorting area of gizzard
СИТ cuticularized region of gizzard
HV _ hepatic vestibule
I intestine
И jaw
K kidney
LOC lateral odontophoral cartilage
LGS left gastric streak
ES larval stomach
M mouth
MN _ mitotic nucleus
MS mesoderm or mesenchyme cells
MT mantle
MTC mantle cavity

a long tube (RS, Figs. 1-6), which gradual-
ly flattens out in the dorso-ventral direc-
tion, starting from its anterior (proximal)
end backwards. This flattening is ас-
companied by a gradual upward reflec-
tion of the 2 lateral edges of the tube, pro-
ducing a crescent-shaped transverse зес-
tion (Fig. 6B). The distal third of the tube,
however, retains its tubular form and wide
lumen. It curves upwards, though, so that
the radular sac eventually assumes an S-
shape.

The cells in the wall of the tube be-

MTE mantle edge

OC! Ist band of odontocytes
ОС? 2nd band of odontocytes
OD — odontoblastic cushion
ОЕ — oesophagus

OEP oesophageal pouch
OER pro-oesophagus

OET post-oesophagus

IR pericardium

PDP pedal cell-plate

PRL post-radular ledge

PS peristome

R radula

RC radular collostyle
RGS right gastric streak

RI rudimentary intestine
RM radular membrane
RS radular sac

SDB buccal region of stomodaeum
SDO__ oesophageal region of stomodaeum
SE subradular epithelium

SH shell (protoconch)

SHG shell gland

SLD | salivary duct

SLG | salivary gland

SMB subradular membrane

SNC sublingual cavity

SOC | superior odontophoral cartilage
SOR subradular organ

SPE supraradular epithelium

SPP supraradular plug

SS style sac

STC statocyst

TL’,- lateral tooth of 2nd

TL’ and 5th rows

TM” marginal tooth of 5th row
TR',- rachidian or median

TR’,- tooth of Ist,

ТК’ 2nd and 5th rows

V ventricle

VL velum

come considerably differentiated as these
developments take place. Thus, in a sagit-
tal section of the tube in Stage VIII (Fig.
3), the wall in the proximal third of the
tube is formed of narrow columnar cells
with densely granular cytoplasm and oval,
basal or central nuclei. This part of the
tube will not form part of the future
radular sac, but will later be pushed for-
wards and incorporated in the lining
epithelium of the buccal cavity. The rest of
the tube constitutes the actual rudiment of
the radular sac (RS). Its roof is formed of

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 155

broad columnar cells with relatively large,
ovoid, central or apical nuclei. The floor
consists of much narrower columnar cells
which decrease gradually in height
anteriorly and present ovoid or elliptical,
basal nuclei. The odontoblasts (OD) start
to differentiate in this stage at the distal
end of the floor as remarkably tall colum-
nar cells which have dense spheroidal
nuclei located at different levels within
their basal halves. The differentiation of
these odontoblasts marks the beginning of
formation of the odontoblastic cushion de-
scribed in the radular sac of the adult snail
by Lufty & Demian (1964а).

In Stage IX, the radular sac (RS, Fig. 4)
appears further enlarged; its distal globu-
lar portion curves more pronouncedly.
Thus the odontoblasts come to lie at the
posterior wall of the sac, where they form a
distinct crescent-shaped odontoblastic
cushion. The odontoblasts in this cushion
proliferate actively, giving rise to suc-
cessive transverse bands of teeth-
producing cells, or odontocytes, which
gradually pass forward and are added to
the subradular epithelium in the floor of
the radular sac.

The Ist band of odontocytes (OC') is
produced late in Stage IX. It consists of 6
adjacent transverse rows of cells which are
distinctly shorter and narrower than the
odontoblasts, and have smaller basal
nuclei and a more acidophilic cytoplasm.
Numerous acidophilic secretory granules
and fibrillae appear in the apical regions of
these odontocytes, indicating that they
have become engaged in active secretion:
they produce the basic chitinous material
of which the earliest row of teeth is
formed. The Ist row actually consists of a
single rachidian or median tooth (TR')
which is secreted directly above the odon-
tocytes. A 2nd transverse band of odonto-
cytes (OC?, Fig. 5A,B) is developed in
Stage X and secretes a row of 3 teeth above
it, 1 median (TR?) and 2 laterals (TL?). The
3rd band of odontocytes appears early in
Stage XI. It is longer than the first 2 bands
and is curved like a horse-shoe, following
the curvature of the odontoblastic cushion.
This band secretes a 3rd row of 5 radular

teeth, 1 median, 2 laterals and only 2
marginals. Five bands of odontocytes and
5 transverse rows of teeth are developed by
the end of Stage XI (Fig. 6A). The 5th
band is the first to produce a full row of the
usual 7 teeth, i.e. 1 median ( TR’, Fig. 6B),
2 laterals (TL*), and 2 inner and 2 outer
marginals (TM).

When first formed, the teeth of each
row stand up almost vertically over the
band of odontocytes which secretes them.
But as they are conveyed forwards along
the radular sac, the lateral edges of the
radular ribbon are gradually reflected up-
wards so that the marginals are directed
horizontally (Fig. 6C).

The bands of odontocytes are separated
from one another by narrower bands of
taller and somewhat broader cells which
carry no teeth, have a less acidophilic cyto-
plasm and are apparently not engaged in
as much active secretion as the odonto-
cytes (Fig. 6A). These cells secrete a thin
layer of a similar nature and staining reac-
tions as the substance elaborated by the
odontocytes, but their secretion only con-
tributes to the formation of the radular
membrane (RM) which binds successive
rows of teeth together at their bases. The
difference in height between the alternate
bands of odontocytes and of these weakly
secretory cells will account for the irregu-
larity in thickness of the subradular
epithelium of the adult which has been re-
ported by Lutfy & Demian (1964а).

The secretory activity of the odonto-
cytes and of the other weakly secretory
cells decreases gradually as they move for-
wards towards the open end of the radular
sac. However, mitotic figures continue to
appear within these cells, especially in the
weakly secretory cells, which apparently
proliferate at a faster rate causing suc-
cessive rows of teeth to be more widely
separated from each other as they grow
older.

As successive bands of odontocytes are
formed at the odontoblastic cushion and
are added to the subradular epithelium,
other cellular elements are seen pro-
liferating at the rear of the radular sac
adding to the supraradular epithelium

156 DEMIAN AND YOUSIF

Loc dl | 7

SPE
RC

MEA

Se
PLE

SOR

FIG. 5. A, Part of a median sagittal section of the embryo in Stage X. B. Transverse section of the radular sac,

same stage.
FIG. 6. A, Part of a median sagittal section of the embryo in Stage XI. B,C, Transverse sections of the radular sac
at the same stage, passing at the level of the 5th row of radular teeth (B), and near the proximal end of the sac

(C).

EMBRYOLOGY OF MARISA. Il. ALIMENTARY SYSTEM 157

(SPE, Fig. 6A-C) in the roof of the sac.
These cells form a compact mass that lies
above and in front of the odontoblastic
cushion and constitutes what has been re-
ferred to in the adult as the supraradular
plug (SPP) by Lutfy & Demian (1964a).
The cells of this plug are remarkably tall,
narrow, have relatively large nuclei lo-
cated at different levels, and present
numerous mitotic figures. Newly formed
cells of the supraradular epithelium gain
gradually in breadth and their nuclei be-
come basal as they move forwards, away
from the supraradular plug. Meanwhile
several vesicles of different sizes appear in
their cytoplasm so that they stain lighter
with routine histological stains than any
other cells in the radular sac. Later on their
apices project into the spaces found be-
tween the teeth so that the supraradular
epithelium becomes serrated at its free
surface.

The supraradular epithelium 15 ар-
parently moved forwards at the same pace
as the subradular one. Thus when a row of
teeth is secreted and shifted forwards, the
overlying cells of the supraradular
epithelium are moved forwards along with
it. With this continuous movement of the
radula, the tooth first formed reaches the
opening of the radular sac in Stage XII. By
that time 6-7 rows of teeth have already
developed in the radular sac, and the
anteriormost part of the growing supra-
radular epithelium has become reflected
backwards so as to form a cap, the col-
lostylar hood (CH, Fig. 6A), covering an
aggregate of mesenchyme cells which lies
within a median furrow shaped on the
dorsal side of the radular sac. These cells
represent the precursor of the radular
collostyle (RC) As development pro-
ceeds, the radula is pushed further for-
wards so as to project outside the opening
of the radular sac and extend on the an-
terior surface of the odontophoral mass as
far as the subradular organ (SOR).

As mentioned above (p. 154), the anterior
third of the original radular sac evagina-
tion does not take part in the formation of
the radular sac proper, but is pushed for-
wards in Stage XI, beyond the opening of

the radular sac. The epithelium in its floor
thus spreads over the rudiments of the
odontophoral cartilages (LOG, Fig. 6A),
and a median stripe of it will later be sur-
mounted by the radula as it protrudes from
the opening of the radular sac. This
epithelium produces a thin cuticular secre-
tion, the subradular membrane, below the
radular ribbon. The roofing epithelium, on
the other hand, thins out and contributes
to the formation of the post-radular ledge
(PRE):

Contrary to what has been reported by
Ranjah (1942) for Pila globosa, the cells of
both sub- and supraradular epithelia ap-
parently contribute to the secretion and
shaping of the radular teeth. The teeth in
the youngest 2 rows always stain uni-
formly red with haematoxylin and eosin
(H-E) and blue after Mallory’s triple stain,
just as the radular membrane. In the next
row in front, the apices of the teeth start to
acquire a bluish colour with H-E and stain
deep blue after Mallory’s stain. In the fol-
lowing 2 rows of older teeth, the cor-
responding apices of the teeth stain deep
blue and reddish-violet after H-E and
Mallory's stain respectively, but no change
takes place in the staining property of the
basal parts of the teeth. This may add
further support to the suggestion made by
Lutfy & Demian (1964a) that the supra-
radular epithelium elaborates certain sub-
stances which diffuse into the basic
material of the teeth originally laid down
by the subradular epithelium, thus
modifying the chemical nature and con-
sistency of the teeth.

Two narrow longitudinal strands of tall
columnar cells start differentiating along
the 2 dorso-lateral edges of the radular sac
at Stage XI. These cells secrete a dense
globular secretion (ALP, Fig. 6C) that
stains blue with H-E and red with Mal-
lory's stain, and accumulates in the angles
between the sub- and supraradular
epithelia ( SE and SPE) on both sides. This
secretion later on forms the 2 chitinous
rods which extend on either side of the ex-
posed radular ribbon, and also contributes
to the formation of the upper layer of the 2
alary processes of the radula (ALP, Fig.

158 DEMIAN AND YOUSIF

SA).

3. Peristome and lining epithelium of
buccal cavity

The epithelial covering of the peristome
is first differentiated in Stage IV in the
form of a few tall, narrow, non-ciliated
ectodermal cells which lie below the
mouth opening, have a densely granular
cytoplasm and contain spherical basal
nuclei. These cells increase in number in
subsequent stages (PS, Figs. 1, 5A, 6A, for
Stages V, X and XI respectively). They
gradually extend upwards on either side of
the mouth opening, until they form an in-
complete circle around it. After Stage X,
the nuclei in these cells become topped
each with a small elongated cone of dense
cytoplasm, and their ground cytoplasm
becomes distinctly vacuolated. The
rounded mouth opening simultaneously
acquires an oval outline, and finally
assumes the shape of a vertical slit in Stage
AL.

The epithelium of the buccal vestibule,
or the anteriormost part of the buccal
cavity, also starts to differentiate in Stage
IV as a few tall ciliated columnar cells,
readily recognized in the roof and floor of
the mouth opening (BV, Figs. 1, 5A, 6A).
As the stomodaeum enlarges during
further development, the buccal vestibule
gradually elongates while its cells become
highly vacuolated and their cilia markedly
longer.

The region of the buccal cavity right be-
hind the vestibule will enclose the jaws
and is therefore described as the man-
dibular region (Lutfy & Demian, 1967).
This region becomes laterally compressed
during late embryonic development, and a
small evagination from it passes below the
developing odontophore to form the sub-
lingual cavity (SNC, Figs. 5A, 6A).

The 2 jaws (J, Fig. 7A) are not secreted
until the embryo reaches Stage XI, when
the mandibular region of the buccal cavity
becomes so much compressed that it
appears as an inverted T in transverse sec-
tion. The epithelium on both sides of the
vertical limb of this T-shaped cavity con-
sists of narrow columnar cells with central,

ovoid to elliptical, dense nuclei and a
highly acidophilic cytoplasm loaded with
fine acidophilic secretory granules (Fig.
7B). The granules are elaborated by the
cells in the form of narrow columns
staining pink with H-E and orange-red
with Mallory 5 stain, and appear regularly
arranged parallel to the longitudinal axes
of the underlying secretory cells. These
columns, which represent the main com-
ponent of the jaws, gradually gain in
height after hatching. The rest of the
epithelium lining the mandibular region of
the buccal cavity secretes a thin homo-
geneous cuticular layer (CT, Fig. 7A) that
stains red with H-E and blue with Mal-
[огу $ stain.

The mandibular region is followed Бу
the odontophoral region of the buccal
cavity (Fig. 8A). The latter becomes dorso-
ventrally compressed during late embry-
onic development as a result of the enor-
mous growth of the odontophoral mass
below it. А mid-dorsal longitudinal food
channel (FC), lined with ciliated cuboid
cells, becomes conspicuous in the roof of
this cavity as early as Stage X. The
epithelium on either side of this channel
gradually thickens so as to form the 2
dorsal buccal ridges. A longitudinal fur-
row appears on each ridge in Stage XII,
dividing it into an inner medial region
(BRI) and an outer lateral one (BRO). Two
types of cells become well-differentiated in
the epithelium of the former region in this
stage: ordinary ciliated columnar
epithelial cells with relatively large, ovoid,
central nuclei and vacuolated cytoplasm;
and much narrower, non-ciliated fusiform
gland cells (FGC, Fig. 8C) with densely
granular cytoplasm and small oval nuclei.
Two other types of cells can also be recog-
nized in the epithelial covering of the
outer region of each dorsal buccal ridge.
The first consists of non-ciliated columnar
cells with vacuolated cytoplasm and ovoid
nuclei, and the second comprises large,
pear-shaped or saccular secretory cells
with basal, ovoid nuclei and a cytoplasm
filled with numerous secretory spherioles,
which stain purple with H-E and faint
blue with Mallory's stain.

[ag
GR

i
[7

32

MO

FIG. Т.А, Transverse section of the head region of the embryo in Stage XII, passing across the mandibular region
of the buccal cavity. B, Enlarged portion of the same section showing the jaw and its secretory epithelium.
FIG. 8. A, Transverse section of the head region of the embryo in Stage XII, passing across the odontophoral
region of the buccal cavity. B,C, Enlarged portions of the same section showing the cells of the lateral
odontophoral cartilage (B), and the epithelium of the inner region of the dorsal buccal ridge.

FIG. 9. Transverse sections of the pro-oesophagus (A), crop (B) and post-oesophagus (C) of the embryo in Stage
XO:

160 DEMIAN AND YOUSIF

The subradular organ (SOR, Fig. 6A)
becomes conspicuous in Stage XI as a
rounded prominence that projects on the
floor of the buccal cavity in front of the
opening of the radular sac. The glandular
nature of the covering epithelium of this
organ becomes apparent in Stage XII,
when large saccular gland cells, similar to
those found in the outer regions of the
dorsal buccal ridges, start to differentiate
in it.

4. Odontophoral cartilages and

buccal muscles

The 2 pairs of odontophoral cartilages
and all buccal muscles are mesodermal in
origin. They develop from mesoderm cells
(MS, Fig. 1) which in early stages are
arranged in thin longitudinal strands
below the stomodaeum. As development
proceeds, these cells proliferate actively
and form distinct aggregates of
mesenchyme cells around the developing
radular sac. At least 10 of these masses can
be recognized in Stage IX. The largest 3 of
them lie 1 below and 2 on either side of the
radular sac. The 2 lateral masses form the
lateral odontophoral cartilages and some
associated muscles, while the ventral mass
develops mainly into the infraventral carti-
lage tensor muscle. Three other smaller
aggregates of mesenchyme cells lie above
the radular sac, of which the median one
forms the radular collostyle, whereas the 2
lateral masses develop mainly into the sus-
pensor muscles of the radular sac. Two
more strands of mesoderm cells lie below
the rear of the radular sac, and 2 others lie
dorsal to the buccal region of the
stomodaeum. These cells contribute to the
formation of various other buccal muscles.

More aggregates of similar mesoderm
cells become conspicuous during further
development, until, when the embryo
reaches Stage XII, the rudiments of most
of the buccal muscles (as described in the
adult snail by Demian, 1964) become
easily identifiable in the embryo.

The majority of the cells in these rudi-
mentary mesodermal masses are stellate or
spindle-shaped. They have a_ highly
acidophilic cytoplasm and oval or ellipti-

cal nuclei relatively rich in chromatin
material, with 1 or 2 nucleoli each.

The 2 lateral odontophoral cartilages
(LOC, Fig. 8A) develop somewhat earlier
than the 2 superior ones (SOC). However,
both pairs of cartilages are easily dis-
tinguishable in Stage XII. The cells of
these cartilages (Fig. 8C), as well as those
of the radular collostyle, are considerably
enlarged and assume various shapes. They
have a highly vacuolated, lightly
acidophilic cytoplasm, and relatively
small, oval or spheroidal, peripheral
nuclei.

5. Oesophageal pouches

The 2 oesophageal pouches (OEP, Fig.
9A) start to develop late in Stage XII as
tubular evaginations from the dorso-lateral
walls of the buccal mass, close behind the
2 dorsal buccal ridges. The cells in these
evaginations are columnar, non-ciliated
and have basal spherical nuclei. They
show no further differentiation until the
embryo hatches.

6. Salivary glands

These glands first appear in Stage IX as
2 small outpocketings from the roof of the
odontophoral region of the buccal cavity.
These rudiments grow rapidly into 2 long
tubular evaginations (SLG, Fig. 13) which
run backwards on either side of the
oesophagus (OE). In Stage XI, the distal
portions of these tubes become pro-
nouncedly dilated, and develop small
lateral diverticula, thus acquiring a
digitate form. Their cells enlarge and
become cuboidal and their nuclei become
basal and denser, while large secretory
spherioles form in their cytoplasm. How-
ever, the proximal parts of these rudi-
mentary tubes retain their narrow tubular
form and simple walls formed of cuboid
cells with spherical central nuclei. These
portions will form the salivary ducts.

As development proceeds to Stage XII,
the rudiments of the salivary glands
further enlarge and their lateral diverti-
cula increase in size and number (Fig.
16A). The diverticula develop secondary
branches and continue to ramify until the

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 161

2 glands eventually assume their com-
pound acinar structure after hatching.
Meanwhile the surrounding mesenchyme
cells form connective tissue strands which
ensheath the developing salivary glands
and bind their acini together.

The secretory cells in these glands in-
crease in number, and numerous secre-
tory globules accumulate in them. There-
fore, the ground cytoplasm becomes con-
fined to thin peripheral strands. A few
secretory cells of the same nature make
their appearance in the walls of the sali-
vary gland ducts. At the same time some
fusiform gland cells (FGC, Fig. 9A) as well
as ordinary ciliated columnar epithelial
cells appear wedged in between the secre-
tory elements of both the salivary glands
and their ducts. The 2 ducts open in the
buccal cavity through 2 minute apertures
located near the middle of the dorsal buc-
cal ridges.

7. Oesophagus

The oesophageal region of the
stomodaeum (SDO, Fig. 10A) differ-
entiates early in Stage V. As development
continues, this oesophageal rudiment (OE,
Figs. ПА, 12A, 13) gradually elongates
until it attains а length of 200 и in Stage X.
Until then, its walls present a uniform
histological picture. The floor is formed of
ciliated columnar cells with granular cyto-
plasm and spherical to ovoid nuclei, and the
roof is mostly composed of broader cells
having vacuolated cytoplasm and spheri-
cal basal nuclei.

By the time the embryo reaches Stage
XII, the oesophagus attains a length of
420 и and has 3 morphologically differen-
tiated regions corresponding to the pro-,
mid- and post-oesophagus of the adult
snail (Lutfy & Demian, 1967). The most
anterior region (OER, Fig. 16A) is much
shorter and narrower than the other 2
parts. It is laterally compressed and sur-
rounded on both sides by the salivary
glands (SLG, Fig. 9A). Its cells develop
long cilia and attain different heights, thus
forming a few longitudinal internal folds.
A few fusiform gland cells (FGC), loaded

with minute acidophilic secretory glo-

bules, make their appearance among these
cells.

The middle and longest region, the crop
or mid-oesophagus (COP, Fig. 16A), is
almost regularly cylindrical and its wall is
composed of cuboid to columnar cells with
short cilia, vacuolated cytoplasm and
spherical basal nuclei (Fig. 9B).

The posterior region, or post-
oesophagus (OET, Figs. 9C, 16A), has a
somewhat dorso-ventrally compressed
lumen and presents 2 longitudinal ridges
on one side. The epithelium on these
ridges is formed of relatively large ciliated
cells, the cytoplasm of which encloses
numerous secretory vesicles, and their
basal nuclei have corrugated nuclear
membranes. The rest of the wall is lined
with much narrower and shorter ciliated
columnar to subcolumnar cells with less
vacuolated cytoplasm. No part of the
endoderm shares in the formation of the
oesophagus which is thus entirely ecto-
dermal in Marisa cornuarietis.

8. Gizzard and hepatic vestibule

Starting with Stage V, the endodermal
sac becomes clearly divisible into 2 por-
tions: a much more dilated and thicker-
walled anterior larval stomach (LS, Fig.
10A,B), and a short tubular posterior rudi-
mentary intestine (RI). The cells of the
larval stomach are relatively large, have
spherical basal nuclei and their cytoplasm
encloses globules of albuminous material
(AB). The globules stain red with H-E and
blue with Mallory's stain, as does the
albuminous fluid that fills the archen-
teron (АТ).

The larval stomach apparently func-
tions in absorbing and digesting the albu-
men reserve of the egg during embryonic
life since only small portions of it take part
in the formation of the adult s stomach.
The rest diminishes gradually until it dis-
appears shortly after hatching and is re-
placed by the digestive gland. As develop-
ment proceeds after Stage V, the larval
stomach continues to enlarge (LS, Fig.
12A-C, for Stage VIII); it becomes pear-
shaped, with a wider anterior part and a
smaller posterior one. Meanwhile its wall

DEMIAN AND YOUSIF

2063

[

625

FIG. 10. А. Reconstruction of the alimentary system of the embryo in Stage У. В, Transverse section of the
embryo, same stage; plane of section indicated by a stippled line in A.
FIG. 11. A, Reconstruction of the alimentary system of the embryo in Stage VI. В, Transverse section of the

embryo, same stage; plane of section indicated by a stippled line in A.

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 163

FIG. 12. A, Reconstruction of the alimentary system of the embryo in Stage VIII. B,C, Transverse sections of the
embryo, same stage; planes of sections indicated by stippled lines in A.
FIG. 13. Reconstruction of the alimentary system of the embryo in Stage X.

164 DEMIAN AND YOUSIF

further thickens and its cells become
gradually saccular, with elongated oval
peripheral nuclei. The posterior portion
grows faster and projects more and more
backwards within the cavity of the visceral
sac rudiment, so that by the time the
embryo reaches Stage X, the anterior and
posterior regions of the larval stomach
become equal in size (Fig. 13). There-
after, the anterior region starts to diminish
in size (Fig. 16A) until it disappears shortly
before hatching. Meanwhile the posterior
region continues to enlarge. It persists for
a short while after hatching, when it
becomes replaced by the growing diges-
tive gland.

A conspicuous longitudinal streak, here
referred to as the right gastric streak (RGS,
Fig. 11A,B), makes its appearance on the
wall of the larval stomach in Stage VI. It
runs along the entire length of the right
dorso-lateral side of the organ. The cells
lining that streak will develop into the
cuticularized part of the adults gizzard.
They differ markedly from neighbouring
cells as they are narrow columnar, smaller,
have basal spheroidal nuclei and their
cytoplasm is devoid of albuminous
globules.

Together with the appearance of the
right gastric streak, the epithelium in a
small oval area (GZS) on the left posterior
side of the larval stomach becomes dif-
ferentiated. In this area also, there develop
narrow columnar cells with spheroidal sub-
basal nuclei and a granular cytoplasm de-
void of albumen globules. These cells com-
prise the rudiment of the sorting region of
the adult's gizzard.

As the larval stomach is rotated anti-
clockwise during torsion, the right gastric
streak is gradually shifted upwards and
then over to the left until it comes to lie on
the left wall of the larval stomach in Stage
XI (RGS, Fig. 14A,B.). Meanwhile its cells
start to secrete a thin surface layer of
cuticle (CT, Fig. 14B). With the dis-
appearance of the anterior portion of the
larval stomach in the following stage, this
streak becomes much shortened, widened
and confined to the left wall of the
remaining posterior part of the larval

stomach, where its cells develop gradually
to form the cuticularized portion of the
gizzard (СИТ, Fig. 16А).

The rudiment of the sorting area of the
gizzard (GZS, Fig. 12A,C) simultaneously
enlarges and its epithelium thins out and
forms a broad evagination on the left pos-
terior side of the larval stomach. This rudi-
ment shifts gradually upwards during tor-
sion until, in Stage XI, it comes to lie on
the left dorso-lateral side of the larval
stomach (Fig. 14A,B). Its epithelium con-
nects posteriorly with that of the right
gastric streak. These 2 differentiated
epithelial sheets gradually enfold as the
rest of the wall of the larval stomach
diminishes in size, eventually forming a U-
shaped tubular sac, the gizzard.

A second streak, the left gastric streak
(LGS, Fig. 12A,B.), lined with narrow
columnar cells having a highly acidophilic
cytoplasm and sub-basal nuclei, starts to
differentiate on the left ventro-lateral side
of the larval stomach (LS) in Stage VII.
The epithelium in this streak represents
the rudiment of the hepatic vestibule
through which the digestive gland leads
into the gizzard. Its posterior half is
gradually shifted downwards and then to
the right during torsion, until it comes to
lie on the right side of the larval stomach
in Stage XI (Fig. 14A,B). As the larval
stomach diminishes in size during later
development, this rudiment shifts gradual-
ly nearer to the cuticularized portion of the
gizzard, and enfolds to form the hepatic
vestibule (HV, Fig. 16B).

9. Digestive gland

The 2 lobes of the digestive gland
develop from 2 unequal bands of columnar
epithelial cells, with densely granular cyto-
plasm and large ovoid basal nuclei, which
differentiate in the wall of the larval
stomach in Stage IX. These bands (DGA
and DGP, Fig. 13) lie immediately above
and below the rudiment of the sorting area
of the gizzard (GZS); the lower band is
longer and broader than the upper one.
The 2 bands enlarge considerably in the
following stage (Fig. 14A, for Stage X) at
the expense of the epithelium in the wall

EMBRYOLOGY OF MARISA. П. ALIMENTARY SYSTEM 165

DGA

625

FIG. 14. A, Reconstruction of the alimentary system of the embryo in Stage XI. В, Transverse section of the
embryo, same stage; plane of section indicated by a stippled line in A.

FIG. 15. A-D, Transverse sections of the pro-intestine (A), mid-intestine (B), post-intestine (C) and rectum (D) of
the embryo in Stage XI.

166 DEMIAN AND YOUSIF

of the larval stomach.

In Stage XII (Fig. 16A), the 2 bands
meet behind the rudimentary gizzard
(GZS and GZT). Meanwhile 2 types of cells
become differentiated among their or-
dinary columnar cells. The first type
(EXC, Fig. 16D) consists of cone-shaped
cells with a granular and highly chromo-
philic cytoplasm and large spherical sub-
basal nuclei. The second type (DGC) con-
sists of narrower and taller columnar cells
with broad corrugated apices and ovoid
central or basal nuclei; their cytoplasm
contains small vesicles enclosing globules
of the albuminous fluid. These cell types
correspond to the excretory and digestive
cells described in the adults digestive
gland by Lutfy & Demian (1967).

The epithelium in the 2 rudiments of
the digestive gland starts to show small
inner foldings about the time of hatching.
By that time, a considerable portion of the
wall of the larval stomach is still existing. It
consists of large vacuolated cells loaded
with albuminous globules. But shortly
after hatching, these cells are rapidly re-
placed by the increasing cells of the diges-
tive gland, the 2 types being morpho-
logically quite distinct from each other. At
the same time, the inner folds of the diges-
tive gland epithelium increase in size and
number and develop secondary folds, so
that the lumen of the larval stomach is
largely obliterated soon after hatching.

10. Style sac and intestine

As mentioned above (p 161), the endo-
dermal sac becomes differentiated in Stage
V into an anterior larval stomach (LS, Fig.
10) and a short tubular posterior rudi-
mentary intestine (RI). The latter region
has a thinner wall composed of short
columnar cells with central ovoid nuclei
and a granular cytoplasm devoid of
albumen globules. This rudimentary intes-
tine gradually elongates and bends sharply
downwards during further development
until, in Stage VIII, it becomes differen-
tiated into 2 parts: a proximal funnel-
shaped style sac (SS, Fig. 12A) which
widely connects with the larval stomach,
and a distal tubular intestine (1). With sub-

sequent enlargement of the posterior
region of the larval stomach and torsion of
the visceral mass, the style sac gradually
shifts upwards and forwards until it comes
to occupy its definitive position anterior to
the sorting area of the gizzard (Fig. 14).
Meanwhile the intestine is displaced to the
right and carried upwards to run on the
right side of the body.

In Stage X, the opening between the
larval stomach and the style sac (SS, Fig
13) comes to lie above the rudiment of the
sorting area of the gizzard (GZS). Its wall
then appears formed of sub-columnar cells
with short cilia, granular cytoplasm and
large ovoid nuclei. The intestine (Г) is
much elongated and courses from the style
sac to the right around the rear of the
larval stomach, then forwards along its
right side to open by the anus in the
mantle cavity. The anus first appears in
Stage IX as a new perforation in the ecto-
dermal layer lining the mantle cavity,
close behind the anal cell-plate. No trace
of a proctodaeal ectodermal invagination
was noticed. Therefore the whole of the
intestine is endodermal in origin in Marisa
cornuarietis.

As development proceeds, the intestine
becomes more elongated and curves in the
shape of a W. Serial cross sections of the
embryo at Stage XI show that the 4 regions
of the adults intestine start differen-
tiating in this stage. The most proximal
region next to the style sac, or the pro-
intestine (Fig. 15A), shows a single inner
longitudinal ridge on the dorsal side. The
following part, or mid-intestine (Fig. 15B),
is slightly longer and presents 2 main inner
longitudinal ridges. The 3rd region, or
post-intestine (Fig. 15C) is the widest and
shows a single inner longitudinal ridge,
while the most distal and narrowest por-
tion, or rectum (Fig. 15D), presents no
internal ridges. The cells in the walls of
these 4 regions of the intestine do not show
any appreciable differences at this stage,
and seem to be mostly columnar with an
acidophilic granular cytoplasm and ovoid
basal or sub-basal nuclei.

In Stage XII, 2 adjacent longitudinal
inner folds develop on the ventral side of

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 167

FIG. 16. A, Reconstruction of the alimentary system of the embryo in Stage ХИ. В, Transverse section of the
embryo, same stage; plane of section indicated by a stippled line in A. C-E, The epithelia of the pro-intestine (C),
digestive gland (D) and style sac (Е) of the embryo in Stage ХИ.

168 DEMIAN AND YOUSIF

the style sac. They correspond to the major
and minor typhlosoles of this region. The
rest of the wall of the style sac (Fig. 16D) is
formed of remarkably tall columnar cells
carrying long cilia. The intestine further
elongates at this stage, and the cells in its 2
proximal regions (Fig. 16C) develop cilia
and a few goblet cells (GB), while the cells
in the 2 distal regions аге relatively
shorter, non-ciliated and exhibit a more
acidophilic cytoplasm. A small tubular
evagination, which represents the rudi-
ment of the anal gland, develops in this
stage also from the wall of the rectum, a
little behind the anal aperture.
DISCUSSION

The present study has revealed that the
stomodaeum develops very early in Marisa
cornuarietis as an ectodermal invagina-
tion, and that the mouth arises as a new
perforation just in front of the site of blas-
topore closure. Marisa more or less con-
forms in this respect with Achatina (Ghose,
1962), but differs from such prosobranchs
as Littorina (Delsman, 1914), Patella
(Smith. 1935) and Pomatias (Creek, 1951)
in which the blastopore persists as the
mouth opening, and from Crepidula
(Conklin, 1897) and Melania
(Ramamoorthi, 1955) in which the mouth
opens at the same spot where the blas-
topore was located.

The radular sac in M. cornuarietis arises
by a single evagination in the floor of the
stomodaeum. It starts to differentiate only
after the connection between the
stomodaeum and endodermal sac has been
established, a condition similar to that ob-
served in Ampullaria canaliculata by Scott
(1934) and in Pila globosa by Ranjah
(1942). These authors, however, did not
indicate when the radula was first secreted
or noticed. Ranjah only stressed that the
lateral teeth are the first to develop in each
transverse row of the radula in P. globosa,
the inner marginals developing next, fol-
lowed by the outer marginals and the
median tooth. In contrast, the present
study indicates that, in Marisa сот-
nuarietis. the median tooth is secreted
first, and that the Ist row of the radula is

composed of a single median tooth. The
inner and outer marginals are secreted
next, and the laterals appear last in each
transverse row.

An extensive review is given by Raven
(1966) of the previous literature per-
taining to the development of the radular
sac in various molluscs. It seems that no
differentiation has been made before be-
tween the cells actually involved in tooth
secretion, here called odontocytes, and
those which produce the tooth-secreting
cells, or odontoblasts. Both cell types are
commonly referred to in the literature as
the odontoblasts and generally considered
responsible for tooth production.

The so-called oesophageal pouches
proved to be buccal structures which arise
as tubular evaginations from the roofing
epithelium of the buccal mass shortly be-
fore hatching. They are thus quite distinct
from the mid-oesophageal glands de-
veloped in some other gastropods
(Graham, 1939). The oesophagus is en-
tirely ectodermal in origin, as is the case in
Pila (Ranjah, 1942; Nagaraja, 1943) and
the majority of the Gastropoda (Raven,
1966). It is neither wholly nor even partly
endodermal as reported for Pomatias
(Creek, 1951) and Limax (Meisenheimer,
1898).

In most ampullariids, as in other
prosobranchs with yolk-rich eggs, the
originally uniform endodermal cells of the
so-called primitive or larval stomach dif-
ferentiate during development into some
large yolk-filled cells and some other small
ones. The former cells act as a larval liver
and usually disappear at the end of em-
bryonic life, while the latter cells form the
epithelium of the definitive stomach
(Biitchli, 1877; Erlanger, 1891; Delsman,
1914; Scott, 1934; Ranjah, 1942; Nagaraja,
1943; Raven, 1966). In Marisa, the
epithelium of the greater part of the
adults stomach develops from similar
small-celled regions which differentiate in
the wall of the larval stomach, forming 2
distinct longitudinal streaks on that wall,
recognized here as the right and left
gastric streaks. Earlier investigations of
embryonic development in various am-

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 169

pullariids, however, did apparently not
follow up the development of the stomach
closely enough to suggest with any рге-
cision which regions of the primitive
stomach give rise to the different com-
ponents of the organ in the adult. Ranjah
(1942) recognized 2 longitudinal bands of
small cells in the primitive stomach of Pila
globosa, which are comparable to the right
and left gastric streaks here described.
However, he simply referred to these
streaks as the rudiment of the alimentary
canal proper, and did not relate them
exactly to the cuticularized region of the
adult gizzard and hepatic vestibule, as was
ascertained in the present work. He also
noticed an area in the wall of the primi-
tive stomach of Pila which he defined as
the rudiment of the true stomach, but
which corresponds to the rudiment of the
sorting area of the gizzard in Marisa.
Semper (1862), Scott (1934) and Nagaraja
(1943) all described a single streak in the
primitive stomach of the different am-
pullariids they examined, corresponding to
the right gastric streak of M. cornuarietis,
but they did not relate it to the adult's
gizzard.

There seems to be general agreement in
the literature that the digestive gland in
the Prosobranchia develop from 1 or 2
rudiments in the wall of the primitive
stomach (Erlanger 1891, Drummond,
1903; Otto € Tónniges, 1906; Delsman,
1914; Crofts, 1938; Creek, 1951). In M.
cornuarietis, the 2 lobes of the digestive
gland arise from 2 rudiments differen-
tiating early on the left posterior side of
the larval stomach. The greater part of the
larval stomach diminishes gradually
during late embryonic development while
it is replaced by the developing digestive
gland until it disappears after hatching.
These observations are not in agreement
with those made for Pila globosa by Ran-
jah (1942) who suggested that the large
cells in the wall of the primitive stomach
passed directly into the digestive gland of
the adult. According to this author they
enlarged and became vacuolated during
late embryonic development, as a result of
the absorption and deposition of ingested

albumen, and thereby transformed into
the digestive gland. This interpretation is
presumably erroneous, and may explain
why Ranjah considered the digestive gland
of Pila as formed of only one lobe. Naga-
raja (1943) also denied that the so-called
primitive stomach persists and transforms
into the adults digestive gland in P.
globosa. He considered it an embryonic or
larval organ that disappears during em-
bryonic life. However, he assumed that the
disappearance of this larval organ was due
to the activity of certain phagocytic nuchal
cells, similar to those characteristic of the
embryos of pulmonates; an assumption
which is not confirmed by the present
observations.

The intestine arises as a posterior pro-
longation of the endodermal sac which
meets the ectoderm of the body wall,
breaking through it to open by the anus;
no ectodermal proctodaeum is developed.
The intestine is, therefore, entirely endo-
dermal in origin as in other ampullariids
(Semper, 1862; Scott, 1934; Ranjah, 1942)
and most gastropods (Conklin, 1897;
Wierzejski, 1905; Smith, 1935; Carrick,
1939; Creek, 1951; Ghose, 1962; Raven,
1966). The anus in M. cornuarietis forms
as a new perforation, independently of the
blastopore. This observation conflicts with
Ranjah's (1942) in Pila globosa, that the
blastopore persists after gastrulation and
forms the anus.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the
valuable contribution of Dr. K. Mansour,
Emeritus Professor, Faculty of Science,
Ain Shams University, Cairo, in the super-
vision of the present work. Thanks are also
due to Dr. B. Hubendick, Director of the
Natural History Museum in Gothenberg,
Sweden, for directing this research project
and for his continuous help during the
course of the work.

LITERATURE CITED

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geschichtliche Beiträge. I. Zur Entwicklungs-
geschichte von Paludina vivipara Müller.

170 DEMIAN AND YOUSIF

Zt. wiss. Zool., 29: 216-254.

CARRICK, R., 1939, The life history and
development of Agriolimax agrestis L., the
grey field slug. Trans. Roy. Soc. Edinb.,
59: 563-597.

CONKLIN, E.G., 1897, The embryology of
Crepidula, a contribution to the cell lineage
and early development of some marine
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CREEK, GA. 1951, The reproductive
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CROFTS, D.R. 1938, The development of
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DELSMAN, H.C., 1914, Entwicklungs-
geschichte von Littorina obtusata. Tijdschr.
ned. dierk. Ver., 13: 170-340.

DEMIAN, Е.5., 1964, The anatomy of the
alimentary system of Marisa cornuarietis
(L.) Medd. Géteborgs Mus. Zool. Avd. 138
(Göteborgs К. Vetensk.-Vitterh.-Samh.
Handl., Ser. В, 9: 1-75).

DEMIAN,. E.S., € YOUSIF, F., 1972,
Embryonic development and organogenesis
in the snail Marisa cornuarietis (Mesogas-
города: Ampullariidae). I. General outlines
of development. Malacologia, 12(1): 123-149.

DRUMMOND, I.M., 1903, Notes on the devel-
opment of Paludina vivipara, with special
reference to the urino-genital organs and
theories of gastropod torsion. Quart. J.
microsc. Sci., 46: 97-143.

ERLANGER, R. von, 1891, Zur Entwicklung
von Рашата vivipara. П. Morph. Jb.,
17: 636-680.

GHOSE, K.C., 1962, Origin and development
of the digestive system of the giant land
snail Achatina fulica Bowdich. Proc. Roy.
Soc. Edinb., B, 68: 186-207.

GRAHAM, A., 1939, On the structure of the
alimentary canal of style-bearing proso-
branchs. Proc. zool. Soc. Lond., В, 109:
75-112.

LUTFY, В.С. & DEMIAN, E.S., 1964a, The
histology of the radula and the radular sac
of Marisa cornuarietis (L.). Ain Shams Sci.
Bull., 10: 97-118.

LUTFY, В.С. & DEMIAN, E.S., 1964b, On the
histology of the odontophoral cartilages of
Marisa cornuarietis (L.). Ain Shams Sci.
Bull., 10: 119-129.

LUTFY, В.С. & DEMIAN, E.S., 1967, The
histology of the alimentary system of
Marisa cornuarietis (Mesogastropoda:
Ampullariidae). Malacologia, 5: 375-422.

MEISENHEIMER, J., 1898, Entwicklungs-
geschichte von Limax maximus L. Zt. wiss.
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NAGARAJA, S., 1943, A note on the devel-
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OTTO, Н. € TÖNNIGES, C., 1906,
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melaniid snails. J. zool. Soc. India, 7: 25-34.

RANJAH, A.R., 1942, The embryology of the
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embrionario de Ampullaria canaliculata.
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706.

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM

ZUSAMMENFASSUNG

EMBRYONALENTWICKLUNG UND ORGANOGENESE
BEI DER SCHNECKE MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE)

Il. ENTWICKLUNG DES ERNAHRUNGSSYSTEMS
Е. $. Demian und Е. Yousif

Der Ernährungstrakt von Marisa cornuarietis (Linnaeus) umfasst: a) ein ektodermales
Stomodaeum, von dem die Radula-Tasche, Schlundtaschen und Speicheldrusen
entwickelt werden, und b) ein entodermales Mesenteron, das in Magen, Verdau-
ungsdriise, Stielsack und Darm unterteiltist.

Das Stomodaeum bildet sich frúhzeitig als eine Einstulpung des Ektoderms, die sich
später in den entodermalen Sack öffnet und sich dann in eine vordere Mundregion und
eine hintere Schlundregion differenziiert. Der Mund ist eine neue Offnung, die nahe bei
dem geschlossenen Blastoporus entsteht.

Der Radula-Sack bildet sich als eine Ausstülpung mitten auf der Unterseite der
Mundregion des Stomodaeums. Die Radulazáhne werden von aufeinanderfolgenden
Querreihen von Odontocyten ausgeschieden, die aus den Odontoblasten am Distalende
des Radulasackes hervorsprossen und laufend dem Epithel unter der Radula angefugt
werden. Aufeinanderfolgende Reihen von Odontocyten werden voneinander durch
guerbänder schwach sezernierender Zellen getrennt, die die Radula-Membran bilden.
Das Epithel über der Radula wird ebenso durch Zell-Sprossung aus einer Zellmasse vor
den Odontoblassen gebildet, dem Supraradula-Zapfen. Er trägt bei zur Bildung und
Formung der Radula-Zähne. Die Kiefer werden kurz vor dem Schlüpfen in einer
besonderen mandibularen Region der Mundhöhle gebildet.

Die Speicheldrusen und Schlundtaschen entwickeln sich verhältnismässig spät als
schlauchförmige Ausstülpungen des Deck-Epithels der Buccalmasse. Der ganze
Oesophagus ist von ektodermaler Herkunft. Er beginnt, sich vor dem Schlüpfen in
Vorder-Mittel- und Hinter-Oesophagus zu unterteiln.

Die zahntragenden Knorpel der Radula-Collostyle und die Mundmuskeln sind
sämtlich mesodermalen Ursprungs und entwickeln sich aus Mesenchym-Zellen, die sich
in fruhen Entwicklungsstufen unter dem rudimentären Stomodaeum sammeln.

Der Entodermsack differenziiert sich früh in den larvalen Magen und einen
rudimentären Darm. Der erste dient zur Aufnahme und Verdauung von Eiweiss während
des Embryonalstadiums. Nur kleine Teile seiner Wand haben an der Bildung des
endgültigen Magens und der Verdauungsdrüse teil. Der Rest nimmt während der
späteren Embryonalentwicklung ab und verschwindet kurz nach dem Schlüpfen, er wird
dann durch die Verdauungsdrüse ersetzt. Der Magen entwickelt sich aus gewissen
differenziierten Zellen, die einen abgegrenzten Längsstreifen an der rechten Wand des
Larvenmagens bedecken und einem kleinen ovalen Feld an der linken Wand. Zellen, die
einen anderen Streifen an der linken Wand bedecken, werden zum Leber-Vorhof. Die
Verdauungsdruse bildet sich aus 2 Resten an der linken Hinterwand des larvalen
Magens.

Der Darm ist ganz und gar entodermaler Herkunft, er entwickelt sich als eine hintere
schlauchförmige Verlangerung des Entodermalsackes und offnet sich erst in einer
verhaltnismässig spaten Stufe mit dem Anus in die Mantelhöhle. Von diesem Ende aus
findet keine Einstülpung des Ektoderms statt. Der After bildet sich als neue Kör-
peröffnung unabhängig vom Blastoporus, der sich am Ende der Gastrulation schliesst.

HZ:

al

17:

DEMIAN AND YOUSIF

RÉSUMÉ

DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGÉNÈSE
CHEZ MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE)

Ik DEVELOPPEMENT DE L’APPAREIL DIGESTIF
Е. $. Demian et Е. Yousif

L'appareil digestif de Marisa cornuarietis (Linnaeus) comprend: a) un stomodeum
ectodermique.a partir duquel se developpent le sac radulaire, les poches oesophagiennes
et les glandes salivaires, b) un mésenteron endodermique différencié en gésier, glande
digestive, sac du stylet et intestin.

Le stomodeum se développe tót sous forme d'une invagination ectodermique qui, plus
tard, s ouvre dans la cavité endodermique et qui, ensuite, se différencie en une région
buccale antérieure et une oesophagienne postérieure. La bouche est une nouvelle
perforation, apparaissant tout près de l'emplacement de | occlusion du blastopore.

Le sac radulaire se développe comme une évagination de la région buccale du
stomodeum. Les dents radulaires sont sécrétées par des bandes transversales successives
d'odontocytes, qui sont produits par multiplication cellulaire d'une masse d odon-
toblastes, localisés à l'extrémité distale du зас radulaire. Les bandes successives
d odontocytes sont séparées par des bandes transversales de fines cellules secrétrices qui
produisent la membrane radulaire. L'épithélium supraradulaire se développe aussi par
multiplication cellulaire d'une masse de cellules, le bouchon” supraradulaire, localisée
en avant des odontoblastes. П contribue 4 la formation et au modelage des dents
radulaires. Les mächoires sont secrétées un peu avant | éclosion dans une région
mandibulaire différenciée dans la cavité buccale.

Les glandes salivaires et les poches oesophagiennes, se développent relativement tard
sous forme d' évaginations tubulaires à partir de |’ épithélium supérieur de la masse
buccale. L'oesophage est en entier d'origine ectodermique. I] commence a se différencier
еп pro-, méso- et post-oesophage avant I éclosion.

Les cartilages odontophoraux, le collostyle radulaire et les muscles buccaux sont tous
d'origine mésodermique et se développent à partir de cellules mésenchymateuses qui
5 accumulent dès les premiers stades au-dessous du stomodeum rudimentaire.

La cavité endodermique se différencie tôt en un estomac larvaire et un intestin
rudimentaire. Le premier sert à absorber et digérer les substances albuminoïdes pendant
la vie embryonnaire. Seulement de petites portions de sa paroi prennent part dans la
formation de l'estomac de l'adulte et de la glande digestive. Le reste diminue durant la
fin du developpement embryonnaire et disparaît peu après l'éclosion. Le gésier se
développe à partir de certaines cellules différenciées qui tapissent un sillon longitudinal
distinct sur la paroi droite de l'estomac larvaire et une petite aire ovale sur la paroi
gauche. Les cellules qui tapissent un autre sillon de la paroi gauche de l'estomac larvaire
donnent naissance au vestibule hépatique. La glande digestive se forme à partir de 2
rudiments sur la paroi postérieure gauche de l'estomac larvaire.

L'intestin, entièrement d'origine endodermique, se développe comme un prolonge-
ment tubulaire postérieur de la cavité endodermique et $ souvre dans la cavité palléale
par l'anus, à un stade relativement tardif. Aucune invagination proctodéale ectoder-
mique ne se développe. L'anus se forme comme une nouvelle perforation indépendante
du blastopore, qui s est fermé vers la fin de la gastrulation.

Apt?

EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM

RESUMEN

DESARROLLO EMBRIONARIO Y ORGANOGENESIS
EN MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE)

II. DESARROLLO DEL SISTEMA DIGESTIVO
Е. $. Demian у F. Jousif

El sistema digestivo comprende: a) un stomodeum ectodermico del cual se desarrollan
los sacos radular y esofágico, y glándulas salivares; b) un mesenterón endodermico en el
que se distinguen la molleja, saco del estilete, glándula digestiva e intestino.

El stomodeum se desarrolla primero como una invaginación ectodermica, se abre en
un saco endodermal, diferenciándose después en una región bucal anterior y una
posterior esofágica. La boca es una abertura nueva cerca del sitio del cierre blastogórico.

El saco radular crece como una invaginacion medio-central, de la región bucal del
stomadeum. Los dientes radulares son secretados por bandas transversales y sucesivas de
odontocitos, los cuales se producen por proliferación celular de una masa de odon-
toblastos localizada al término distal del saco radular, y se van agregando continuamente
al epitelio subradular. Las sucesivas bandas de odontocitos estan separadas por otras
transversales de células secretoras débiles las cuales producen la membrana radular. El
epitelio supraradular tambien se desarrolla por proliferación celular de una masa de
células ubicadas frente a los odontoblastos, la espita u obturador supraradular. Esto con-
tribuye a la formación de los dientes radulares y a sus configuraciones. Las mandíbulas
son secretadas poco antes del nacimento del embrión dentro de una región mandibular
diferenciada de la cavidad bucal.

Las glándulas salivares y sacos esofágicos se desarrollan relativamente tarde como
evaginaciones tubulares del epitelio en el techo de la masa bucal. El esófago entero es de
origen ectodermico; empieza diferenciándose entre pro-medio- y post-esófago antes de la
eclosión.

Los cartílagos odontoforicos, colostilo radular y músculos bucales, son todos de origen
mesodermico y se desarrollan de células mesenquimales, que se aglomeran en las
primeras fases debajo del stomodeum rudimentario.

El saco endodermal comienza una diferenciación temprana entre un estómago larval
rudimentario y un intestino. El primero sirve para absorber y digerir las materias
albuminoideas durante la vida embrionaria. Sólo pequeñas prociones de sus paredes
toma parte en la formación del estómago del adulto y la glándula digestiva. El resto se
reduce durante el desarrollo embrionario posterior y desaparece poco antes de la eclo-
sión, siendo reemplazado por la glándula digestiva. La molleja es creada por ciertas
células diferenciadas que forran una faja longitudinal distinta sobre la pared derecha del
estómago larval y una pequeña area oval de la pared izquierda. Células que forran otra
banda de la pared izquierda dan desarrollo al vestíbulo hepatico. La glándula digestiva se
forma de 2 rudimentos sobre la pared izquierda posterior del estómago larval.

El intestino es totalmente de origen endodermico, se desarrolla como una prolongación
tubular posterior del saco endodermico y se abre, en un estado larval tardío, en la región
anal de la cavidad paleal. No hay invaginación ectodermica proctodeal. El ano se forma
como una nueva perforación independiente del blastofore, el cual se cierra al final de la
gastrulación.

те

173

174

DEMIAN AND YOUSIF

ABCTPAKT

ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗУ

MARISA CORNUARIETIS (MESOGASTROPODA, AMPULLARIDAE)
П. РАЗВИТИЕ ПИЩЕВАРИТЕЛЬНОЙ СИСТЕМЫ

Э.С. IMM3H И 0. ЮЗИФ

Пищеварительная система Marisa cornuarietis включает В себя: a)
эктодермальный стомодеум, из которого развиваются радулярный мешок,
карманы пищевода и слюнные железы и 6) эндодермальный мезентерон,
дифференцирующийся в 306, пищеварительную железу, мешок стебелька и
кишку.

Стомодеум развивается рано, как эктодермальное впячивание, которое
затем открывается в оэндодермальный мешок, потом дифференцируется в
переднюю буккальную и заднюю пищеводные области. Рот является новым
отверстием, возникающим близко от места закрытия бластопора.

Радулярный мешок развивается как выпячивание в середине нижней части
буккальной области стомодеума. Зубы радулы секретируются
последовательными поперечными рядами одонтоцитов, которые возникают в
результате пролиферации клеток из массы одонтобластов, расположенных на
дистальном конце радулярного мешка, и непрерывно добавляются к
субрадулярному эпителию. Последовательные ряды одонтоцитов разделяются
поперечными рядами слабо секретирующих клеток, производящих радулярную
мембрану. Супрарадульный эпителий так же развивается за счет пролиферации
клеток из массы клеток, расположенных впереди одонтобластов -
супрарадулярной пробки. Он способствует образованию и Формированию
радулярных зубов. Челюсти секретируются незадолго перед вылуплением
внутри дифференцированной мандибулярной области буккальной полости.

Слюнные железы и карманы пищевода развиваются относительно поздно в
виде трубчатых выпячиваний эпителия крыши буккальной массы. Весь
пищевод по происхождению эктодермальный. Он начинает дифференцироваться
в передний, средний и задний отделы пищевода перед вылуплением.

Хрящи одонтофора, радулярный коллостиль и буккальные мускулы -
мезодермального происхождания и развиваются из тех клеток мезенхимы,
которые аггрегируются на ранних стадиях под рудиментарным стомодеумом.

Эндодермальный мешок рано дифференцируется в ларвальный желудок и
рудиментарную кишку. Первый служит для всасывания и переваривания
белкового материала в течение эмбриональной жизни. Лишь небольшие части
его стенки принимают участие в формировании желудка взрослой особи и

пищеварительной железы. Остальная его часть уменьшается во время
позднего эмбрионального развития и исчезает вскоре после вылупления,
когда ларвальный желудок замещается пищеварительной железой. Зоб

развивается из определенных дифференцированных клеток, выстилающих в
виде продольной полоски правую стенку личиночного желудка и небольшую
овальную область на левой стенке. Клетки, выстилающие другую полоску на
левой стенке личиночного желудка, дают начало преддверию печени.
Пищеварительная железа возникает в виде 2 рудиментов на левой задней
стенке ларвального желудка.

Кишка, по происхождению полностью оэндодермальна, возникает как
трубчатое продолжение эндодермального мешка и на относительно поздней
стадии открывается в мантийную полость анусом. Эктодермального

выпячивания проктодеума не возникает. Анус образуется назависимо от
бластопора, закрывающегося к концу гаструляции.

Z.A.F.

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Vol. 12, No. 1 MALACOLOGIA

CONTENTS

В. Н. POHLO

Feeding and associated functional morphology in Tagelus
californianus and Florimetis obesa (Bivalvia: Tellinacea)............

E. G. DRISCOLL and D. E. BRANDON

Mollusc-sediment relationships in northwestern Buzzards Bay, ha
Massachusetts, USA iat Со ОО ene fear!

M. CASTAGNA and P. CHANLEY

Salinity tolerance of some marine bivalves from inshore and
estuarine environments in Virginia waters on the western

| Midatlantic coasts os ae 0e и A AE AAN Oy
2 M.J. IMLAY À
| Effects of potassium on survival and distribution of freshwater |
mussels SEATS О РН NEE ИННА AD AO EN RE. Е fé
G. WIUM-ANDERSEN АИТ |
Electrophoretic studies on esterases of some African Biomphalaria
+ spp. (Planorbidae) Be ANA ER RATES Lu
E S. DEMIAN aad в. YOUSIF (otha tee A te у
| р _ Embryonic development and organogenesis in the snail Marisa
nf Bar cornuarietis (Mesogastropoda: Ampullariidae) AR ae Sea
Дер i) у ñ I. General outlines of development ..... RUBI be
| LE $ DEMIAN and F. YOUSIF ВНИИ
i Embryonic development and organogenesis in the snail Marisa. |

cornuarietis (Mesogastropoda: Ampullariidae)
Tey he II. Development of the alimentary. system

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MALACOLOGIA

Editor-in-Chief
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*

VOL. 12 NO. 2 1973

MALACOLOGIA

International Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie
Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

In Memoriam

G. P. Kanakoff
N. H. J. Odhner

R. V. Seshaiya

MALACOLOGIA EDITORS

MALACOLOGIA, 1973, 12(2): 175-194

EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL
MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE).
Ш. DEVELOPMENT OF THE CIRCULATORY AND RENAL SYSTEMS!

Emile $. Demian? and Fouad Yousif?

ABSTRACT

The pericardium, heart and kidney of Marisa cornuarietis arise from a single common
mesodermal anlage which differentiates early (Stage IT) on the right side of the embryo.
This common rudiment develops a central cavity, the coelom, by the separation of its
cells, then divides by a constriction into an anterior pericardial sac and a posterior
kidney. A corresponding left rudiment soon disappears, disintegrating into mesenchyme.
Thus the 2 rudiments do not fuse to form a single sac, as previously reported for some
ampullariids.

The auricle and ventricle do not develop as a single tube which later constricts in the
middle, but as 2 separate invaginations from 2 opposite sides of the rudimentary pericar-
dial sac. They subsequently inter-communicate (Stage VI), forming a tubular heart
which initially lies almost fransversely. Torsion later shifts the pericardium to the left
dorso-lateral side and brings the auricle in front of the ventricle.

Haemocoelic sinuses and blood vessels develop independently of the pericardium and
heart from irregular spaces in the mesenchyme within the blastocoel. Most of these
become well-established during embryonic life, connecting with the heart at a late stage.
The aortic ampulla was shown to develop as a haemocoelic sinus below the pericardium
and later not to lie within the pericardial sac, but to be lodged in a deep inward bulge of
the thin floor of that sac.

The anterior part of the rudimentary kidney transforms into a short ciliated reno-
pericardial tube. The remainder forms the kidney which, first tubular, then saccular,
develops a thick plexus of blood vessels in its roof. Torsion shifts the kidney dorso-
laterally to the left.

The ureter, a fully functional excretory organ previously thought to be another kidney,
is ectodermal in origin and arises by a tubular invagination on the right side only of the
embryo. It later communicates with the mesodermal kidney (Stage IV). Its proximal part
forms a funnel-shaped renal vestibule, first described here. The walls of the ureter
develop transverse internal foldings which become richly vascularized, serving an ex-
cretory function. The ureter shifts in front of the kidney during torsion, coming to lie in
the roof of the mantle cavity, while the excretory opening and the renal vestibule
become deeply enclosed in the mantle cavity.

By demonstrating that the kidney is homologous with the topographically left kidney
of the Archaeogastropoda and that the ureter is not homologous with their right kidney
but with the ureter of other Mesogastropoda, this study contributes to the clarification of
the controversial homologies of these organs in the Ampullariidae.

INTRODUCTION |, naeus), an ampullariid snail which has

recently gained considerable importance

This is the 3rd paper in a series dealing as a biological control agent against
with the embryonic development and schistosome-transmitting snails. These
organogenesis of Marisa cornuarietis (Lin- studies are meant to contribute to a better

! This investigation was supported in part by research grants (AI 04906 and AI 07696) from the National Institute
of Allergy and Infectious Diseases, U.S. Public Health Service.

2 Department of Zoology, Faculty of Science, Ain Shams University, Cairo.

3 Laboratory of Bilharziasis Research, National Research Centre, Cairo.

(175)

176 DEMIAN AND YOUSIF

knowledge of this species, and to clarify
certain ontogenetic problems and
phylogenetic relations in the family Am-
pullariidae to which the snail belongs.

The Ist part of the series (Demian &
Yousif, 1973a) included a description of
the early cleavage, gastrulation and the
general outlines of the process of em-
bryonic development of Marisa сот-
nuarietis during the 12 embryonic stages
recognized and described. The 2nd part
(Demian & Yousif, 1973b) was concerned
with the embryogenesis of the alimentary
system.

The present paper comprises a detailed
description of the origin and embryonic
development of the circulatory and renal
systems of Marisa cornuarietis. These 2
systems are here treated together since
their main organs arise from a common
primordium. Findings are compared with
earlier information on other Am-
pullariidae.

Observations were made on the same
material and sets of serial sections which
were used in all other parts of the series.
The material and techniques employed
have been described in the Ist part of the
series, to which reference should also be
made for the age, dimensions and
diagnostic features of the different em-
bryonic stages which are frequently
referred to below.

KEY TO LETTERING ON FIGURES!

A auricle
AM aortic ampulla
ANP anal cell-plate

APP apical cell-plate
ARV - afferent renal vein
AT archenteron

АСУ afferent ureteral vein

BE blastocoel

С coelom

CN ctenidium

CON - excretory concretions

DGP _ posterior lobe of digestive gland
EN endoderm

ET ectoderm

EUV | efferent ureteral vein

FR lateral furrow on ureter

GZS sorting area of gizzard

I intestine

K kidney

LS larval stomach

MS mesoderm or mesenchyme cells

MT mantle

МТС mantle cavity
MTE mantle edge
MYB myoblasts

E pericardium

E pericardial cavity

PDP _ pedal cell-plate

РНК common primordium for pericardium,
heart and kidney

PT prototroch

RGS right gastric streak

RENO external renal opening

RNV renal vestibule

RPT reno-pericardial tube

RT rectum

SD stomodaeum

SH shell (protoconch)

SHG shell gland

SHGR rudimentary shell gland

SS style sac

U ureter

V ventricle
OBSERVATIONS

1. Early rudiments

The pericardium, heart and kidney of
Marisa cornuarietis are all mesodermal in
origin and arise from a single common
primordium; the ureter is ectodermal.
Rudiments of all these organs start to
differentiate early, in Stage II of the em-
bryo, which generally corresponds to the
free trochophore larva of marine
prosobranchs. Two small compact masses
of mesoderm cells (MS, Fig. 1A,B) make
their appearance at that stage on either
side of the endodermal sac (EN), nearer to
the posterior end? of the embryo. These
masses most probably arise by cell
proliferation from 2 teloblasts derived
from the micromere 4d (Demian & Yousif,
1973a). They consist of ovoid or polygonal

ЗАП drawings are of Marisa cornuarietis (L.). The general views are reconstructions of the circulatory and renal
organs made from serial transverse and sagittal sections.

"The antero-posterior axis of the embryo at this stage corresponds to the animal-vegetative polar axis.

EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 177

ANP
0.1mm B

0.1mm

FIG. 1. A, Embryo in Stage II, left lateral view.
B, Transverse section of the embryo, same stage; plane of section indicated by stippled line
in A.
FIG. 2. A, Embryo in Stage III, left lateral view.
B, Transverse section of the embryo, same stage; plane of section indicated by stippled line
in A.
FIG. 3. A, Embryo in Stage IV, left lateral view.
B, Part of a sagittal section of the embryo (same stage) passing through the common
primordium of pericardium, heart and kidney.

178 DEMIAN AND YOUSIF

cells with highly chromophilic granular
cytoplasm and large spherical nuclei. The
left mass is somewhat smaller, lies a little
anterior to the right one and remains con-
spicuous for only a short period. It then
diminishes gradually in size until it dis-
appears completely in the following em-
bryonic stage (Fig. 2A), disintegrating into
mesenchyme. The right mass, on the other
hand, persists and constitutes a common
rudiment for the pericardium, heart and
kidney (PHK).

The rudiment of the ureter (U, Fig.
1A,B) also differentiates in Stage II as a
small thickened circular plate in the ec-
toderm, to the right of the anal cell-plate
(ANP).

The common rudiment of the pericar-
dium, heart and kidney (PHK, Fig. 2A,B)
slightly enlarges in Stage Ш, shifts a little
upwards and transforms into an ovoid vesi-
cle that measures about 35 и in length. Its
cells move apart and arrange themselves in
a single layer, surrounding a small central
cavity (C, Fig. 2B) which is the sole
coelomic cavity to develop in the embryo;
the coelom is thus a schizocoel.

This rudimentary mesodermal vesicle
becomes further enlarged in Stage IV. A
distinct constriction develops nearer to its
posterior end, dividing it incompletely into
2 parts which communicate freely with
one another. The anterior part is larger,
thinner-walled, measures about 50 w in
diameter and represents a rudimentary
pericardial vesicle (P, Fig. 3A,B) from
which the heart will also develop later.
The posterior part measures only 20 u in
diameter and constitutes the rudiment of
the kidney (K); it communicates posterior-
ly with the rudimentary ureter (U) by the
end of Stage IV.

2. Pericardium and heart

The rudimentary pericardial vesicle (P,
Fig. 4A,B) shifts a little backwards in Stage
V, and its wall thins out all over except in 2
small areas on the left and the postero-
dorsal sides from which the ventricle (V,
Fig. 4C) and auricle (A), respectively,
develop. The cells in these 2 thickened
areas are cuboid, rhomboidal or polygonal,

with large spherical nuclei. The rest of the
wall of the rudimentary vesicle consists of
more or less flattened cells and develops
into the future pericardium (P).

The rudiment of the auricle starts in-
vaginating late in Stage V. It gradually
forms a pouch-like invagination (A, Fig.
5A-C) that projects into the rudimentary
pericardial vesicle (P), and some
mesenchyme cells (MS) from the
blastocoel or segmentation cavity (BL)
migrate into it. This process of invagina-
tion is immediately followed by a similar
invagination of the rudimentary ventricle
(V). The latter forms a narrower and
thicker-walled tubular invagination which
projects diagonally to the right and up-
ward into the pericardial cavity (PC) until
it touches the invaginated auricle; the
cavities of the 2 invaginations then com-
municate. Thus a rudimentary tubular
heart becomes well-established in Stage
VI, extending almost transversely, with the
auricle lying to the right side and a little
dorsal to the ventricle. The cavity of this
heart communicates widely at both ends
with the primary body cavity (BL, Fig.
5C). At this stage, the pericardium (P) is
thin and formed by a single layer of
squamous cells with elliptical nuclei. The
wall of the auricle (A) consists of less
flattened cells with thickened central por-
tions enclosing large spherical nuclei,
while that of the ventricle (V) is made up
of columnar to sub-columnar cells with
ovoid nuclei and darkly stainable granular
cytoplasm.

In Stage VII, the pericardial sac (P, Fig.
6A) has further enlarged, measuring about
100 u in diameter. It has moved a little to
the left, coming to lie medially above the
rear of the larval stomach (LS). The heart
stretches obliquely inside it and begins to
show some irregular pulsations.

Torsion causes the pericardial sac (P,
Fig. 7) to shift further to the left in Stage
VIII. Meanwhile, the ventricle (V) begins
to lose its tubular form, becomes saccular
and some minute internal projections
appear on its wall. In Stage IX, the pericar-
dial sac (P, Fig. 8) attains a length of 140 u.
The heart pulsates rhythmically; the ven-

EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 179

>, A —
es 5 zent
4 VAIO
¿OY
RS,

=

m
0.1mm 4

ger CS El
| Ez Le «< ~ , de
QT ee

N

FIG. 4. A,B, Embryo in Stage У, in left lateral (A) and dorsal (В) views.
С, Part of a sagittal section of the embryo (same stage) passing through the primoridia of
the pericardium, kidney and ureter.
FIG. 5. A,B, Embryo in Stage VI, in left lateral (A) and dorsal (B) views.
С. Part of a transverse section of the embryo, same stage; plane of section indicated by
stippled line in A.

180 DEMIAN AND YOUSIF

tricle (V) has become pear-shaped and
shows numerous inner processes pointing
in various directions. The opening
between the auricle and ventricle becomes
more constricted, and 2 inner septal
processes develop close to it, representing
2 rudimentary auriculo-ventricular valves.

As the pericardial sac continues to
enlarge in subsequent stages (P, Figs. 9A;
10A), it is gradually pushed forwards along
with the forward extension of the mantle
skirt (MT). The auricle (A) and ventricle
(V) broaden at their junction, and the cells
in their walls flatten more and more (Fig.
9D).

In Stage XII, 2 types of cells become
well-differentiated in the walls of the auri-
cle (A, Fig. 10C) and ventricle (V):
squamous endothelial cells with small
elliptical nuclei, and larger irregularly-
shaped myoblasts (MYB) with spherical or
ovoid nuclei. The latter cells have highly
acidophilic attenuated ends and thick cen-
tral portions containing numerous
basophilic granules of different sizes.
Some of these cells extend to various direc-
tions within the cavities of the heart
chambers, especially in the ventricle (V).
They increase gradually in number after
hatching, developing into numerous
irregular crossing and anastomosing mus-
cle strands which run within the cavities of
the heart chambers in the adult.

3. Blood vessels and sinuses

Blood vessels and sinuses develop, in-
dependently of the pericardium and heart,
from scattered irregular spaces or portions
of the primary body cavity which are left
in between the propagating mesenchyme
cells. In early embryonic stages, these
spaces are surrounded by loose
mesenchyme cells of different shapes.
During development, they gradually
assume a tubular form, acquire a lining of
simple endothelium of flattened
mesenchyme cells, with ovoid or elliptical
nuclei, arid finally connect with the heart.

At least 8 such rudimentary blood spaces
can be recognized in Stage V of the em-
bryo. One of these sinuses, which lies
below the stomodaeum, and another,

which develops on the left side of the lar-
val stomach, will join in Stage VII to form
the anterior or cephalic aorta. Two other
sinuses, one on either side of the
stomodaeum, constitute the rudiment of
the cephalopedal haemocoelic sinus. The
remaining 2 pairs of sinuses will unite in
later stages of development to form the
visceral haemocoelic sinus: the Ist pair lies
to the right and below the larval stomach, |
and the 2nd to the right and behind the
pericardium.

In Stage IX, some mesenchyme cells
aggregate below the pericardium,
representing the rudiment of the main aor-
ta and aortic ampulla. These cells enclose a
small space which is in open communica-
tion with the cavity of the ventricle. The
aortic ampulla (AM, Fig. 9B,C) becomes
well-established in Stage X, appearing as a
thin-walled sac that lies just below the
pericardium (P), on the left dorso-lateral
side of the larval stomach (LS). As the
stomach greatly enlarges during subse-
quent development, the aortic ampulla is
gradually pushed upwards and pressed
against the pericardium (P) until in Stage
XII, it becomes entirely lodged within a
deep concavity in the floor of the pericar-
dial sac.

The pallial and renal blood vessels and
sinuses develop relatively late and will be
considered below, in connection with the
development of the kidney and ureter.

4. Kidney

The kidney of Marisa cornuarietis is un-
paired from the beginning. After being
differentiated from the persisting (right)
common rudiment of the pericardium,
heart and kidney in Stage IV (p 178), the
rudimentary kidney (K, Fig. 3A,B)
gradually elongates and assumes a tubular
form. It attains a length of 40 u in Stage У
(K, Fig. 4A-C) and has relatively thick
walls formed by columnar cells with
densely granular cytoplasm and spherical
to ovoid nuclei.

The posterior part of this tubular rudi-
ment dilates rapidly during further
development so that, as the embryo
reaches Stage VII, 2 morphologically dis-

EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 181

tinct regions are differentiated in the
rudimentary kidney: а sbort tubular
anterior or proximal part which measures
12 и in length and will develop into the
reno-pericardial tube (RPT, Fig. 6A,B),
and a much more dilated ovoid distal part,
which measures 40 u in length and 55 u at
its greatest width, and will form the kidney
proper (К). The wall of the latter part con-
sists of cuboid to columnar cells with
vacuolated cytoplasm and basal spherical
nuclei (Fig. 6B). By the end of Stage VII,
the rudimentary kidney has curved about
the reno-pericardial tube.

In Stage VIII, the kidney (К, Fig. 7)
becomes displaced to the left as a conse-
quence of torsion. The ureter (U) now
opens into the right side of the kidney. The
reno-pericardial tube (RPT) is slightly
elongated and its cells have acquired short
cilia.

In the following embryonic stage, the
kidney (K, Fig. 8) is more enlarged and
projects further forward around the reno-
pericardial tube (RPT). Thus, by the end
of Stage IX, the reno-pericardial tube is
surrounded on all but its right side by the
growing saccular kidney. The opening of
the tube simultaneously comes to lie near
that found between the kidney and the
ureter (U). At the same time a few
mesenchyme cells begin to aggregate
within the primary body cavity to the right
side of the reno-pericardial tube. These
cells become so arranged in the following
stage as to form a narrow tubular sinus, the
afferent renal vein (ARV, Fig. 9C), which
will later communicate with the
cephalopedal haemocoel.

The kidney (K, Fig. 9A) continues to
enlarge in Stage X while gradually shifting
to the right. It is now V-shaped, with the
dorsal and ventral limbs (K, shown
transversely in Fig. 9B,C) embracing the
reno-pericardial tube (RPT), and projec-
ting further forwards to embrace the rear
of the pericardial sac (P, Fig. 9A,B). The
wall of the kidney (K, Fig. 9C) consists
largely of cuboid cells with distinctly
vacuolated cytoplasm and basal or
peripheral dense nuclei, while that of the

reno-pericardial tube (RPT) is composed
of tall ciliated columnar cells with densely
granular cytoplasm and basal ovoid nuclei.

During further development, the ven-
tral limb of the kidney and the afferent
renal vein are both pushed upward as a
consequence of continued torsion and
further enlargement of the larval stomach
below them. Thus, in Stage XI, the lower
limb of the kidney comes to lie to the right
of, and on the same horizontal plane with,
the other limb. The 2 limbs of the kidney
are now so close to each other that the
afferent renal vein becomes lodged in a
deep longitudinal groove running dorsally
between them.

Another narrower tubular sinus, the
efferent renal vein, also differentiates in
Stage XI, dorsal to the left limb of the
kidney, and later communicates with the
auricle.

The kidney attains its definitive shape
and position and apparently starts func-
tioning in Stage XII (K, Fig. 10A). It then
appears covered dorsally by a thin layer of
ectoderm (ET, Fig. 10B); its roof consists
of cuboid and club-shaped cells with
spherical basal nuclei and highly
vacuolated cytoplasm. The latter is dis-
tinctly more acidophilic towards the
apices of the cells and contains numerous
vesicles enclosing minute excretory con-
cretions (CON). The floor, on the other
hand, consists of a thin layer of much more
flattened cells.

In Stage XII, the roof of the kidney
starts to show some inner foldings.
Mesenchyme cells (MS, Fig. 10B) from the
primary body cavity migrate into these
folds and haemocoelic cavities appear
between them. The folds increase steadily
in number and size after hatching and
produce secondary folds which press
against each other so that the roof gradual-
ly acquires the spongy structure
characteristic of the adult's kidney. A com-
plex network of blood sinuses develops
within these folds and connects with the
afferent and efferent renal veins. The floor
of the kidney, however, remains thin and
unfolded.

182 DEMIAN AND YOUSIF

0.Imm

7 K 8 OMA

FIG. 6. A, Embryo in Stage VII, dorsal view.
B, Transverse section of the kidney, same stage.
C, Transverse section of the ureter, same stage.
FIG. 7. Embryo in Stage VIII, dorsal view.
FIG. 8. Embryo in Stage IX, dorsal view.

EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 183

5. Ureter and renal vestibule

The rudiment of the ureter (U, Fig.
1A,B), as mentioned above (p 178),
differentiates early in Stage II as a small
thickened circular plate in the ectoderm
(about 6 cells in diameter), to the right side
of the anal cell-plate (ANP). The cells in
this rudiment are taller and narrower than
neighbouring ectodermal cells (ET, Fig.
1B) and show a more chromophilic
cytoplasm and relatively smaller, ovoid,
central nuclei.

In Stage III, this rudimentary ectoder-
mal plate (U, Fig. 2A,B) starts in-
vaginating, thus projecting deeply inwards
below the common rudiment of the
pericardium, heart and kidney (PHK). The
invagination enlarges during further
development and gradually assumes a
tubular form. Its distal tip comes to touch
the posterior wall of the rudimentary
kidney (K, Fig. 3A), into which it opens by
the end of Stage IV. It is the distal portion
of this tube that constitutes the rudiment
of the ureter proper (U); the proximal
narrower part forms what is referred to
here as the renal vestibule (RNV). No trace
of a comparable rudimentary structure or
invagination is seen on the opposite or left
side of the embryo, i.e., the ureter is un-
paired from the beginning. Nothing is
developed in the embryo that can be
regarded as a 2nd or left rudimentary
ureter.

In Stage V, the rudimentary renal
vestibule (RNV, Fig. 4A,B) further
enlarges and shifts a little upwards so as to
lie below the pericardial sac (P).
Meanwhile, the much more dilated
rudimentary ureter (U) becomes laterally
compressed.

During subsequent development (Stage
VI), the ureteral tube (U, Fig. 5A,B)
further elongates. Its walls become pinch-
ed centrally along the longitudinal axis so
that, in cross section, the lumen appears
dumbbell-shaped. Viewed in its entirety,
the lumen of the organ essentially consists
of a U-shaped peripheral canal, surround-
ing a narrow central compressed portion.
The dorsal limb of the “U” connects
anteriorly with the kidney (K), while the

ventral limb leads, also anteriorly, into the
renal vestibule (RNV). The wall of the
ureter consists of tall columnar cells with
vacuolated cytoplasm and sub-basal ovoid
nuclei.

In the same embryonic stage (Stage VI),
2 tubular sinuses become differentiated in
the segmentation cavity alongside the
ureter. The Ist sinus extends along the
right dorso-lateral edge of the organ, while
the 2nd runs along its left ventro-lateral
side. These sinuses give rise later (Stage X)
to the 2 efferent ureteral veins (EUV, Fig.
OBI):

In Stage VII, the renal vestibule (RNV,
Fig. 6A) has shifted further upward and
now touches the floor of the kidney (K). At
the same time, a longitudinal furrow (FR,
Fig. 6C) is shaped on the left side of the
ureter (U). Two further longitudinal
haemocoelic sinuses become established at
this stage, one within the furrow and the
other along the right face of the ureter.
These sinuses will later form the dorsal and
ventral branches, respectively, of the
afferent ureteral vein (AUV, Fig. 9B,C, for
Stage X).

The renal vestibule (RNV, Fig. 7) is
further enlarged and appears cone-shaped
in Stage VIII. Its external opening now
faces forward as a result of torsion and lies
within a broad concavity that represents
the incipient mantle cavity (MTC). The
ureter (U) has also been rotated, due to
torsion, so that its longitudinal axis comes
to lie transversely to the longitudinal axis
of the body, and the lateral furrow (FR)
faces backwards.

As torsion proceeds through Stage IX,
the ureter (U, Fig. 8) becomes con-
siderably elongated and further rotated so
that its greater part extends along the
mantle roof anterior to the kidney (K), and
its lateral furrow (FR) comes to face to the
right. In the meantime, the opening of the
renal vestibule has been completely
enclosed within the developing mantle
cavity.

By the end of torsion in Stage X, the
ureter (U, Fig. 9A-C) is about 220 u long.
Its longitudinal lateral furrow (FR) faces
dorso-laterally. The connection between

184 DEMIAN AND YOUSIF

FIG. 9. A, Embryo in Stage X, dorsal view.
B, C, Transverse sections of the embryo, same stage;
stippled lines in A.
D, Part of a sagittal section of the embryo (same stage) passing through the pericardium

and heart.
Е, Transverse section of the ureter, same stage (enlarged from В).

planes of sections indicated by

EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 185

FIG. 10. A, Embryo in Stage XII, dorsal view.
B, Part of a transverse section of the kidney (same stage) showing folded roof (left) and thin
floor (right).
C, Part of a longitudinal section of the embryo (same stage) passing through the pericar-
dium and heart.

186 DEMIAN AND YOUSIF

the ureter and the kidney (K) is formed by
a short narrow tube. Two types of cells
become differentiated in the wall of the
ureter (U, Fig. 9B,E) at this stage. The Ist
type comprises large sub-columnar
secretory cells with narrow apices, ovoid
peripheral nuclei, and a highly vacuolated
cytoplasm in which excretory concretions
(CON) start to accumulate. The 2nd type
consists of columnar cells with ovoid cen-
tral nuclei and lightly acidophilic
cytoplasm free of excretory material. The 2
branches of the afferent ureteral vein
(AUV, Fig. 9B,C) connect posteriorly with
the afferent renal vein (ARV).

The renal vestibule attains its definitive
shape and position in Stage XI when it
appears as a small funnel-shaped invagina-
tion at the right posterior corner of the
mantle cavity. The ureter grows con-
siderably, attaining lengths of 0.4 mm in
Stage XI and 0.55 mm in Stage XII (U,
Fig. 10A). Numerous inner folds project
transversely from its wall. Mesenchyme
cells and blood lacunae make their
appearance within these folds and subse-
quently connect with the afferent and
efferent ureteral veins serving the organ.
Thus the kidney and ureter become well-
established towards the end of embryonic

life.

DISCUSSION

Among the chief peculiarities of the
mesogastropod family Ampullariidae is the
possession of a peculiar ureter which is
structured and functions as a kidney, with
2 symmetrical rows of transverse excretory
lamellae arising on either side of 2 central
longitudinal vessels: the 2 branches of the
afferent ureteral vein. Two lateral efferent
ureteral veins drain into the afferent
ctenidial vein.

Posteriorly the ureter communicates
with the far more spacious saccular
kidney, which has a thick spongy roof with
numerous pinnately branched folds. The
afferent and efferent renal veins run
longitudinally within the roof and branch
profusely in its inner folds. The kidney
communicates with the pericardial sac by a
fine ciliated reno-pericardial tube. This

arrangement is essentially similar in all
ampullariids (Andrews, 1965).

These 2 inter-communicating and struc-
turally very distinct excretory organs of the
Ampullariidae have for long been thought
to be 2 kidneys and were commonly
referred to as either the anterior and
posterior kidneys, renal chambers or renal
lobes (Bouvier, 1888; Burne, 1898;
Sachwatkin, 1920; Hagler, 1923; Prashad,
1925; Scott, 1934, 1957; Demian, 1954;
Michelson, 1956, 1961; Fretter € Graham,
1962; Andrews, 1965; Starmühlner, 1969).
The origin of these 2 functional excretory
organs and their homologies with the
single kidney of other Mesogastropoda (=
Monotocardia or Pectinibranchia) as well
as with the 2 kidneys of the
Archaeogastropoda (= Diotocardia or
Aspidobranchia) were the subject of exten-
sive discussions by many authors.

The earliest investigators of the
morphology of the Ampullariidae only saw
the anterior renal chamber (= ureter),
which they took to be the kidney
(Troschel, 1845; Jourdain, 1879; Sabatier,
1879). Bouvier (1888) was the first to
describe “2 kidneys” in Ampullaria ра,
an anterior lamellar kidney and a posterior
saccular one, but did not mention any
reno-pericardial tube. By comparing the
blood vessels supplying these 2 kidneys
with those supplying the 2 kidneys of an
archaeogastropod like Haliotis, Bouvier
conjectured that the anterior and posterior
kidney chambers of Ampullaria are,
respectively, homologous with the right
and left kidneys of Haliotis, and of the
Archaeogastropoda in general. And since
Bouvier was of the opinion that the single
kidney found in most Mesogastropoda cor-
responded to the topographically right
kidney of the Archaeogastropoda, he
assumed that the anterior renal chamber
(= ureter) of Ampullaria was homologous
with the single kidney of other
mesogastropods, while the posterior renal
chamber (= kidney) of Ampullaria cor-
responded to the topographically left
kidney of the Mesogastropoda, which dis-
appeared during development.

After reviewing the then existing

EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 187

hypotheses on the homologies of the
kidney of the Mesogastropoda, Perrier
(1889) surmised that the single kidney of
most mesogastropods originated by fusion
of what corresponded to the right and left
kidneys of archaeogastropods. And since
the Ampullariidae retained 2 inter-
communicating kidneys, he considered
them to represent an evolutionary link
between the Mesogastropoda and the
Archaeogastropoda.

Erlanger (1892) inverted the homology
suggested by Bouvier (1888) by con-
sidering the anterior renal chamber (=
ureter) of Ampullaria, and also the single
kidney of other mesogastropods, to be
homologous with the topographically left
kidney of the Archaeogastropoda, while
the posterior chamber was homologous
with their right kidney. In most
mesogastropods the rudiment of that
organ disappeared during development or
became incorporated in the gonoduct. Ac-
cordingly, he theorized that if a reno-
pericardial connection was present at all in
the Ampullariidae, it should be found
between the anterior renal chamber and
the pericardium, a prediction proved
wrong by Burne (1898). Upon discovering
a reno-pericardial tube between the
posterior renal chamber and the pericar-
dium in A. urceus, Burne rejected
Erlanger's interpretation and reverted to
Bouvier's (1888) original suggestion that
the posterior renal chamber of Ampullaria
corresponded to the topographically left
kidney of the Archaeogastropoda.

Sachwatkin (1920), after surveying
earlier evidence, believed that both renal
chambers of Ampullaria correspond to the
topographically ieft kidney of the
Archaeogastropoda, while the right kidney
of the Mesogastropoda was modified to
form the gonoduct, as suggested by
Erlanger.

This view subsequently gained general
acceptance, although Fernando (1931),
who studied the embryonic development
the excretory organs in Ampullaria gigas,
refuted all previous hypotheses on the
homologies of the 2 excretory organs of
Ampullaria. He showed that those 2

organs were markedly different in origin
and therefore could be neither 2 kidneys
nor 2 parts of a single kidney, as suggested
by earlier authors. He supplied evidence
that only the posterior renal chamber was
of mesodermal origin, retained com-
munication with the pericardium
throughout development, and was
therefore а kidney proper.
Morphologically it was the right kidney
of the embryo, which assumed a position
on the left side after torsion. The so-called
anterior renal chamber, on the other hand,
was ectodermal in origin, opened in the
mantle cavity, and was therefore
homologous with the ureter of other
mesogastropods. Thus Fernando was the
first to recognize the ureter and to
differentiate between it and the kidney
proper in any ampullariid.

Ranjah (1942) provided further
evidence in support of Fernando's (1931)
findings from an extensive embryological
study of Pila globosa. He, however, added
that a rudimentary left kidney and a left
ureter did also develop in the early embryo
of Pila, but later became incorporated in
the gonoduct, a statement which is neither
supported by Fernando's observations in
Ampullaria nor by the present findings in
Marisa.

In spite of the embryological evidence
provided by Fernando (1931) and later
confirmed by Ranjah (1942),
morphologists either ignored Fernando s
data (e.g., Starmühlner, 1969) or were hesi-
tant to accept them (Scott, 1934, 1957; De-
mian, 1954; Michelson, 1956), while some
have rejected them outright (Fretter €
Graham, 1962; Andrews, 1965); thus the
homologies of the excretory organs in the
Ampullariidae have remained in dispute.
According to Fretter & Graham (1962), the
“anterior renal chamber” of Ampullaria
should be regarded as being homologous
with the dorsal wall of the kidney of other
mesogastropods, and not with the ureter,
because it has inner folds covered by ex-
cretory tissue and vascularized by vessels
connected with the ctenidium. Andrews
(1965) also did not accept the idea that the
“anterior renal chamber’ in Pomacia

188 DEMIAN AND YOUSIF

canaliculata and in other ampullariids
represented an ectodermal ureter and, on
the basis of its excretory nature and its
nerve and blood supply, she suspected it to
be a mesodermal contribution to the
kidney.

The present study vindicates Fernando ’s
(1931) theory as regards the origin and
homologies of the kidney and ureter in the
Ampullariidae. Evidence here brought
forward for Marisa indicates that this am-
pullariid indeed has a single kidney—its
so-called posterior renal cham-
ber—corresponding to that of other
mesogastropods. It is homologous with the
topographically left kidney of the
Archaeogastropoda. The so-called anterior
renal chamber, although lamellated and
apparently excretory in function, is un-
questionably homologous with the ureter
of other mesogastropods, for which reason
it has been so termed in this paper.

Also, in accordance with the present fin-

dings, the terminology commonly used by
previous authors (Prashad, 1925; Demian,
1954: Michelson, 1956; Andrews, 1965;
Starmühlner, 1969, and others) for the
blood vessels supplying the 2 excretory
organs in various ampullariids is here
changed. The terms afferent and efferent
renal veins are now restricted to those
blood vessels which have so far been
referred to as the “posterior” afferent and
efferent renal veins. The terms afferent
and efferent ureteral veins are here in-
troduced to replace the previous terms
“anterior” afferent and efferent renal
veins.
‚ The particulars in which the present
observations diverge from earlier reports
on the origin and development of the cir-
culatory and renal organs in related am-
pullariids are discussed below.

In most molluscs, except perhaps the
Cephalopoda, the pericardium, heart and
kidney, and often also the gonad, are
mesodermal in origin and arise from a
common primordium, which may be
either paired or unpaired at the beginning
(Raven, 1966). In the few Ampullariids, in
which the development of the pericar-

dium, heart and kidney was examined in
detail, it has been asserted that these
organs arise from 2 mesodermal
rudiments. Both Fernando (1931) and
Ranjah (1942), working on Ampullaria
gigas and Pila globosa respectively, have
correctly described 2 rudimentary
aggregates of mesoderm cells, like those
described here for Marisa, differentiating
in the early embryo on either side of the
endodermal sac. However, those 2 masses
were then said to grow equally up to a cer-
tain stage, then the right mass grew larger.
Both masses acquired cavities, thus being
transformed into 2 coelomic vesicles
referred to as the “right and left rudimen-
tary pericardia. The smaller, left, vesicle
was stated to shift to the right, coming to
lie just beside or below the right vesicle.
The 2 vesicles communicated later with
each other to form a single sac, within
which the heart subsequently developed.

In contrast, the present study revealed
that only the right mesodermal mass grows
and develops into the pericardium, heart
and kidney; the left one diminishes quick-
ly in size and finally disintegrates into
mesenchyme. Marisa thus conforms in this
respect with such prosobranchs as Calyp-
traea (Salensky, 1872), Bithynia (Erlanger,
1891), Littorina (Delsman, 1914), Patella
(Smith, 1935) and Pomatias (Creek, 1951);
and with such pulmonates as Arion
(Heyder, 1909), Limax (Hoffmann, 1922),
Ariophanta (Balsubramaniam, 1953) and
Achatina (Ghose, 1963).

Fernando (1931) and Ranjah (1942)
described 2 rudimentary kidneys develop-
ing as 2 evaginations from the so-called
“right and left rudimentary pericardia,”
before the latter united into а single
pericardial sac. Both authors also agreed
that the right rudimentary kidney
developed into the post-torsional left
definitive kidney. But, while Fernando
stated that the left rudimentary kidney dis-
appeared at an early stage, Ranjah asserted
that it persisted, to become later incor-
porated in the gonoduct. Semper (1862),
however, had described but а single
kidney rudiment in Ampullaria polita, and
Scott (1934) similarly made no mention of

EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 189

a left rudimentary kidney in A.
canaliculata.

The present observations indicate that
the kidney of Marisa is unpaired from the
beginning. The kidney rudiment is con-
stricted off the common primordium of the
pericardium, heart and kidney formed on
the right side of the early embryo. No trace
of a corresponding left rudimentary kidney
was recognized throughout development.

Fernando (1931) and Ranjah (1942)
moreover spoke of a reno-pericardial
“pore” by which the cavity of the kidney
communicated with that of the pericardi-
um in the ampullariids they examined.
They made no mention of а гепо-
pericardial tube forming that connection,
as did Burne (1898) for Ampullaria urceus,
Sachwatkin (1920) for A. gigas, and An-
drews (1965) for Pomacea canaliculata. In
Marisa, the kidney communicates with the
pericardial sac through a distinct reno-
pericardial tube which differentiates from
the same kidney rudiment and later is
enclosed in the cavity of the definitive
kidney.

Ranjah (1942) not only reported 2
rudimentary kidneys, but also described 2
rudimentary ureters for Pila globosa; the
right rudiment developing into the
definitive ureter, while the left one con-
tributed to the formation of the gonoduct.
Fernando (1931) described only a right
rudimentary ureter in Ampullaria gigas.

The present findings, although agreeing
with those of Fernando in as much as they
show that the ureter of Marisa is single
from the start, conflict with the reports
made by both Fernando and Ranjah as
regards the details of formation and
development of these rudimentary organs.
Fernando considered the rudimentary
ureter to have developed, in Ampullaria,
as a constricted portion of the mantle cavi-
ty, and Ranjah described the 2 rudimen-
tary ureters of Pila globosa as arising from
the mantle cavity by evagination. It is
clear from the present report, however,
that in Marisa the rudiment of the ureter
and renal vestibule arises as an invagina-
tion of the ectoderm on the right side of
the embryo, long before the mantle cavity

has started differentiating. What was con-
sidered as the mantle cavity by Fernando
and Ranjah corresponds to the renal
vestibule here described for the Ist time.
The vestibule starts to develop in Marisa as
early as Stage IV and becomes later
engulfed in the mantle cavity.

No trace of a rudimentary gonad, such
as that described by Ranjah (1942) for Pila,
was recognized in the embryo of Marisa.
The gonad as well as the gonoduct have a
largely post-embryonic development in
Marisa, as in Ampullaria gigas (Fernando,
1931).

The present observations also conflict
with those of Ranjah (1942) as regards the
development of the heart rudiment. Accor-
ding to that author, the heart of Pila arises
as a single tubular invagination from the
wall of the united rudimentary pericardia.
That invagination deepens gradually until
it meets the opposite wall and perforates
it; the heart is then divided by a constric-
tion into an auricle and ventricle. But, in
Marisa, the rudimentary auricle and ven-
tricle are separate at the beginning. They
arise as 2 invaginations from 2 nearly op-
posite sides of the rudimentary pericardial
sac and communicate with each other
later. This is somewhat similar to what ob-
tains in Achatina (Ghose, 1963).

Another characteristic of the Am-
pullariidae—the feature from which this
family has derived its name—is the posses-
sion of a thick-walled,capacious and highly
expandable aortic ampulla found on the
anterior aorta, almost immediately after it
leaves the main aortic trunk. This ampulla
is believed to accommodate the blood
which may be forced out of the highly
vascularized mantle skirt during retraction
of the snail into the shell (Andrews, 1965).
Morphologists have generally agreed that
the aortic ampulla lies within the pericar-
dial cavity, directly below the heart
(Troschel, 1845; Bouvier, 1888; Prashad,
1925: Scott, 1934; Andrews, 1965). The
present investigation, however, has shown
that the aortic ampulla lies outside the
pericardium from the start. It develops as a
haemocoelic sinus below the pericardial
sac. Later it is pressed against the floor of

190 DEMIAN AND YOUSIF

the pericardial sac until it becomes deeply
lodged in it, bulging into the pericardial
cavity. The pericardial floor, however, is so
thin that upon dissection the ampulla
appears to be contained within the pericar-
dial cavity.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the
valuable contribution of Dr. K. Mansour,

Emeritus Professor of Zoology, Faculty of

Science, Ain Shams University, Cairo, in

the supervision of the present work.

Thanks are also due to Dr. B. Hubendick,

Director of the Natural History Museum

in Gothenberg, Sweden, for his continuous

interest and support.
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216.

ZUSAMMENFASSUNG

EMBRYONALE ENTWICKLUNG UND ORGANOGENESE
IN DER SCHNECKE MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIIDAE).

Ш. ENTWICKLUNG DES KREISLAUF-AUD NIERENSYSTEMS

E. S. Demian und F. Yousif

Perikard, Herz und Niere von Marisa cornuarietis entwickeln sich aus einer einzigen
mesodermalen Anlage, die schon früh (Stadium II) auf der rechten Seite des Embryos
erkennbar ist. Dieses gemeinsame Rudiment bildet durch Spaltung seiner Zellen einen
zentralen Hohlraum, das Coelom, und teilt sich dann durch Abschnürung in einen
vorderen Herzbeutel und in eine hintere Niere. Die entsprechende linke Anlage
verschwindet bald, indem sie sich in Mesenchymzellen auflöst. Die beiden Anlagen
verschmelzen also nicht zu einem einzigen Sack, wie für einige Ampullariiden
angegeben.

Auch Vor- und Herzkammer entwickeln sich nicht aus einem einzigen Schlauch, der
sich später in der Mitte abschnürt, sondern aus 2 getrennten Einstülpungen an
entgegengesetzten Seiten des rudimentären Herzbeutels. Diese treten erst später
(Stadium VI) in Verbindung und bilden ein schlauchförmiges Herz, das anfänglich fast
quer liegt. Durch die Drehung des Eingeweidesacks verlagert sich das Perikard nach
links, so dass Vorkammer vor Herzkammer zu liegen kommt.

Blutlakunen und Blutgefässe entstehen unabhängig vom Perikard und Herzen aus un-
regelmässigen Räumen im Mesenchym des Blastocoels. Sie sind grösstenteils schon
während der embryonalen Entwicklung gut ausgebildet; der Anschluss ans Herz jedoch
erfolgt erst spät. Es zeigt sich, dass die Aortenampulle unterhalb des Perikards als Sinus
in Hoemocoel entsteht und auch später nicht innerhalb des Herzbeutels liegt, sondern
in einer tief ins Perikard hineinragenden Einsackung des dünnen Perikardbodens.

Der vordere Teil der Urniere verwandelt sich in einen kurzen bewimperten
Renoperikardialgang. Der resliche Teil, zuerst schlauchförmig, dann sackförmig, bildet
die Niere, in deren Dach sich ein starkes Netzwerk von Blutgefässen entwickelt.
Drehung des Eingeweidesackes verlagert die Niere dorsolateral nach links.

Der Ureter, ein ebenfalls exkretorisches Organ, das früher für eine zweite Niere
gehalten wurde, ist ektodermalen Ursprungs, und bildet sich aus einer schlauchförmigen
Einstülpung an der rechten Seite des Embryos. Die Verbindung mit der mesodermalen
Niere wird erst später, im IV. Stadium, hergestellt. Der proximale Teil des Ureters
besteht aus einem trichterförmigen, hier zum ersten Mal beschriebenen Vestibül. An den
Ureterwänden bilden sich stark vaskularisierte innere Querfalten aus, die der
Ausscheidung dienen. Durch die Torsion kommt der Ureter vor der Niere zu liegen.

192

DEMIAN AND YOUSIF

Beide Organe befinden sich nun im Mantelhöhlendach; Vestibül und Aussenmündung
liegen tief in der Mantelhöhle.

Dadurch, dass erwiesen wurde, dass die Niere homolog mit der topographisch links
gelegenen Niere der Archaeogastropoden ist und dass der Ureter nicht mit deren rechter
Niere homolog ist, sondern mit dem Ureter anderer Mesogastropoden, trägt diese
Unterschung zur Klärung der in den Ampullariiden strittigen Homologien dieser Organe
bei.

А.С.

RESUME

DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGENESE
CHEZ MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE).
Ш. DEVELOPPEMENT DES APPAREILS CIRCULATOIRE ET EXCRETEUR

Е. 5. Demian et Е. Yousif

Le péricarde, le coeur et le rein de Marisa cornuarietis apparaissent á partir d'un seul
feuillet mésodermique commun qui est différencié trés tot (Stade II) sur le cóté droit de
l'embryon. Cette ébauche commune développe une cavité centrale, le coelome, par
clivage de ses cellules puis se devise а la suite d'une constriction en un péricarde
antérieur et un rein postérieur. Une ébauche correspondante du cóté gauche disparait tót
en se transformant en mésenchyme. Ainsi les deux ébauches ne fusionnent pas pour
former un sac unique, comme cela a été décrit pour certains Ampullariidés.

L oreillette et le ventricule ne se développent pas comme un unique tube qui plus tard
subirait une constriction médiane, mais comme deux invaginations séparées provenant
des deux cótés opposés du sac péricardique initial. Elles entrent en communication plus
tard (Stade VI), formant un coeur tubulaire qui, initialement, est placé presque transver-
salement. Une torsion ultérieure déplace le péricarde vers le cóté dorso-latéral gauche et
méne l'oreillette en face du ventricule.

Des sinus hémocoeliens et des vaisseaux sanguins se développent indépendamment du
péricarde et du coeur, а partir de lacunes du mésenchyme dans le blastocoele. La plupart
de ceux-ci s élaborent pendant la vie embryonnaire et se mettent en relation avec le coeur
au stade final. On a montré que Гатроше aortique se développe comme un sinus
hémocoelique placé sous le péricarde, qui plus tard, ne se situe pas dans le sac péricar-
dique mais se loge dans un profond renflement interne du plancher de ce sac.

La partie antérieure du rein rudimentaire se transforme en un court tube réno-
péricardique cilié. Le reste forme le rein qui, d'abord tubulaire, puis sacculaire,
développe un épais plexus de vaisseaux sanguins dorsalement. La torsion déplace le rein
dorsolatéralement sur la gauche.

L uretére, organe excréteur entierement fonctionnel, précédemment considéré comme
étant un autre rein, est d’origine ectodermique et apparaît sous forme d'une invagination
tubulaire sur le seul côté droit de l'embryon. Il communique plus tard avec le rein
mésodermique (Stade IV); sa partie proximale forme un vestibule rénal en forme d'en-
tonnoir, pour la premiere fois décrit ici. Les parois de l'uretére développent des replis in-
ternes transversaux qui se vascularisent abondamment. L'uretére se déplace en face du
rein pendant la torsion, venant se placer dans la partie dorsale de la cavité palléale, tandis
que le pore excréteur et le vestibule rénal sont profondément enfermés dans la
cavité palléale.

En démontrant que le rein est homologue du rein gauche topographique des
Archaeogastropodes et que l'uretére n'est pas l'homologue de leur rein droit mais de
l'uretére des autres Mésagastropodes, cette étude contribue à clarifier les homologies
controversées de ces organes chez les Ampullariidae.

ASE.

EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 193

RESUMEN

DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN
MARISA CORNUARIETIS (MESOGASTROPODA:
AMPULLARIIDAE). III. DESARROLLO DE LOS

SISTEMAS CIRCULATORIO Y RENAL

E. S. Demian y F. Yousif

El pericardio, corazón y riñón de Marisa cornuarietis nacen de una masa de células
mesodermales, simple, que se diferencian temprano (II estado) sobre el lado derecho del
embrión. Este rudimento común desarrolla una cavidad central, el celoma, por el
desdoblamiento de sus células, dividiéndose después por constricción en un saco pericar-
dial anterior y un riñón posterior. Un rudimiento izquierdo, correspondiente, desaparece
enseguida, desintegrándose en mesenquima. De tal manera, los dos rudimentos no se
fusionan para formar un saco único, como se habia registrado para algunos ampularidos.

La aurícula y ventrículo no se desarrollan como un tubo único para contraerse en el
medio, sino como 2 invaginaciones separadas de 2 lados opuestos del saco pericardial
rudimentario. Después se intercomunican (VI estado) para formar un corazón tubular el
cual, al principio, descansa casi transversalmente. La torsión luego lleva el pericardio al
lado dorso-lateral y trae la auricula frente al ventrículo.

Senos homocélicos y vasos sanguíneos desarrollanse independientemente del pericar-
dio y corazón, de los espacios irregulares de la mesenquima dentro del blastocelo.
Muchos de estos quedan bien establecidos durante la vida embrionaria, conectandos al
corazón en un estado posterior. La ampolla aórtica ha mostrado la formación de un seno
homocélico debajo del pericardio, pero no se ubica más tarde dentro del saco pericardial,
sino en una profunda comba hacia adentro del techo del saco.

La parte anterior del riñón rudimentario se transforma en un tubo reno-pericardial,
corto y ciliado. El resto forma el riñón, el cual siendo primero tubular y después sacular,
produce en su techo una gruesa red vasos sanguíneos. La torsión lleva el riñón dorso-
lateralmente a la izquierda.

La uretra, un órgano excretor funcional completo, (se habia considerado previamente
como otro riñón), es de orígen ectodermico y se forma por una invaginación tubular sólo
en el lado derecho del embrión. Más tarde se comunica con el riñón mesodermal (IV es-
tado); su parte proximal forma un vestibulo renal como un embudo, que se describe aquí
por primera vez. Las paredes de la uretra desarrollan pliegues internos transversales, los
cuales se vascularizan en manera abundante. La uretra se muda frente al riñón durante la
torsión, viniendo a colocarse en el techo de la cavidad paleal, mientras que la abertura de
excresión y el vestibulo renal quedan profundamente envueltos en la cavidad del manto.

Al demonstrar que el riñón es homólogo con el, topograficamente, riñón izquierdo de
los Archaeogastropoda, y que la uretra no es homóloga con el riñón derecho sino con la
uretra de otros Mesogastropoda, este estudio contribuye a la clarificación en la controver-
sia sobre homologías de tales órganos en los Ampullariidae.

J.J.P.

194

DEMIAN AND YOUSIF

АБСТРАКТ

ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIDAE)
Ш. РАЗВИТИЕ ЦИРКУЛЯЦИОННОЙ И ПОЧЕЧНОЙ СИСТЕМ

9. ДИМЬЯН И Ф. KCH

Перикардий, сердце и почки у Marisa cornuarietis происходитя от одного
общего мезодермального образования, которое диференцируется довольно рано
(на П стадии) на правой стороне эмбриона. Этот общий рудимент образует
центральную полость, целом, путем расщепления его клеток, а затем
разделяется путем стягивания их и образования переднего перикардиального
мешка и задней почки. Соответственно, левый рудимент вскоре исчезает,
перерождаясь в мезенхиму. Таким образом, в данном случае 2 рудимента не
сливаются, чтобы образовать единый мешок, как это наблюдалось раньше у
некоторых Ampullariidae.

Предсердие и желудочек не представляют собой единой трубки, которая позже
образует перетяжку посредине, HO образована двумя отдельными
инвагинациями e двух противоположных сторон рудиментарного
перикардиального мешка. Позже они образуют внутренние коммуникации (на
У1 стадии) и сердечную трубку, первоначально расположенную почти
поперечно. Наступающая позднее торсия смещает перикардиум налево и
дорзо-латерально, предсердие оказывается перед желудочком. Синусы
гемоцёля и кровеносные сосуды развиваются независимо от перикардия и
сердца от неправильно-расположенных лакун внутри бластоцёля. Большая их
часть хорошо развивается втечение эмбрионального периода жизни,
соединяясь с сердцем на поздних стадиях развития. Было показано, что
ампула аорты развивается как синус гемоцёля, под перикардием; позже он
уже находится не внутри перикардиального мешка, а помещается в глубокой
вдавленности, имеющейся в тонкой стенке этого мешка.

Передняя часть рудиментарных почек трансформируется в короткую
реснитчатую почечно-перикардиальную трубку. Остальная часть - сначала
- трубчатая, затем мешковидная, образует почки, которые развивают на
своей стенке толстое сплетение кровеносных сосудов. Торсионный процесс
сдвигает почки дорзо - латерально и налево.

Уретра - это полноценно-функционирующий выделительный орган прежде
считавшаяся другой почкой, имеет эктодермальное происхождение и
возникает с правой стороны эмбриона, ввиде трубчатой инвагинации. Позже
она связывается с мезодермальной почкой (стадия 1У); её проксимальная
часть образует воронковидную почечную вестибулу, впервые описанную в
настоящей статье. Стенки уретры образуют поперечные внутренние складки,
пронизанные большим количеством кровеносных сосудов. Торсионный процесс
сдвигает ‘уретру кпереди от почки так, что она лежит в стенке
мантийной полости, в то время как экскреторное отверстие и почечная
воронка оказываются глубоко погруженными в мантийную полость.

В статье показано, что в данном случае почка по местоположению
гомологична левой почке Archaeogastropoda, но что ypeTpa не является
гомологом их правой почки, а соответствует уретре других Mesogastropoda.
Изложенные в статье материалы выясняют противоречивость суждений об этих
органах у Ampullariidae.

Z.A.F.

MALACOLOGIA, 1973, 12(2): 195-211

EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL
MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE).
IV. DEVELOPMENT OF THE SHELL GLAND, MANTLE AND
RESPIRATORY ORGANS!

Emile 5. Demian? and Fouad Yousif?
ABSTRACT

A “rudimentary shell gland” starts differentiating at the aboral end of the early em-
bryo as a median thickened ectodermal plate. It invaginates to form a cup-shaped
hollow, shifts to the left and secretes a delicate cuticular larval shell. Its central part then
bulges up and its epithelium flattens. Together with the larval shell, it spreads circularly
over the visceral sac rudiment, extending beyond it. Ultimately it forms the outer
epithelium of the visceral mass and mantle. A peripheral epithelial rim remains thicken-
ed, and will form the definitive shell gland. The larval shell persists as a layer of the adult
shell.

Contrary to earlier reports on related ampullariids, the mantle cavity develops relative-
ly late, only after the onset of torsion. Starting as a depression or groove on the right
dorso-lateral wall of the visceral sac rudiment, it gradually transforms into a deep cavity
as it becomes overgrown by the mantle. The ectoderm, engulfed by that cavity, forms its
internal lining and the inner mantle epithelium. During torsion the mantle opening
shifts to face forwards.

The ctenidium was shown to be ontogenetically older than the mantle cavity. Its rudi-
ment starts differentiating early as a thickened ectodermal plate in the right wall of the
visceral sac rudiment. It secondarily passes into the mantle cavity during torsion when it
shifts to the left side, extending forwards as the mantle grows anteriorly. Transverse
epithelial folds develop on it to later form the ctenidial lamellae.

The lung, a structure peculiar, within the prosobranchs, to the Ampullariidae, starts
developing shortly before hatching as a broad invagination in the roofing epithelium of
the mantle cavity, between the ctenidium and osphradium. The epithelial rim edging the
invagination grows centrad from the periphery to form the floor of the lung cavity, leav-
ing open a narrow slit which persists as the pneumostome. The lung grows enormously
after hatching, displacing the ctenidium to the right side. These findings indicate that
the lung is a new acquisition in the Ampullariidae. It is not a modified 2nd ctenidium
and does not seem to have any direct ancestral relationship with the lung of pulmonates.

The accessory breathing organs, i.e., the pallial fold or “epitaenia” and the 2 nuchal
lobes (siphons) also develop late, as folds of the epithelium in the floor of the mantle cavi-
ty. They attain their definitive shapes and positions after hatching.

INTRODUCTION

The present investigation is the 4th in a
series of embryological studies carried out
on Marisa cornuarietis (L.), a freshwater
ampullariid gastropod of potential impor-
tance in the biological control of
schistosome-transmitting snails.

The Ist part of the series (Demian &
Yousif, 1973a) included a description of
the early cleavage, gastrulation and the
general outlines of the process of em-
bryonic development. Twelve embryonic
stages were distinguished. The 2nd part
(Demian & Yousif, 1973b) covered the em-

1 This investigation was supported in part by research grants (Al 04906 and Al 07696) from the National
Institute of Allergy and Infectious Diseases, U.S. Public Health Service.

2 Department of Zoology, Faculty of Science, Ain Shams University, Cairo.

3 Laboratory of Bilharziasis Research, National Research Centre, Cairo.

(195)

196 DEMIAN AND YOUSIF

bryogenesis of the alimentary system, and
the 3rd part (Demian & Yousif, 1973c) that
of the circulatory and renal systems.

In the present report, a detailed descrip-
tion is given of the origin and embryonic
development of the shell gland, mantle,
mantle cavity and respiratory organs. Fin-
dings are compared with earlier informa-
tion on other Ampullariidae. The gross and
microscopic anatomy of the mantle and
respiratory organs of adult Marisa cor-
nuarietis have been described in previous
publications (Demian, 1965; Lutfy & De-
mian, 1965) which may be consulted for
details of structure and function of these
organs.

The present observations were made on
the same material and sets of serial sec-
tions that furnished the basis for all other
parts of the series. The material and
techniques employed have already been
described in the Ist part of the series, to
which reference should also be made for
the age, dimensions and diagnostic
features of the different embryonic stages
which are frequently referred to below.

KEY TO LETTERING ON FIGURES!

1 auricle

afferent ctenidial vein
ANP anal cell-plate

СИ. ciliated ridge

CN ctenidium

DGP posterior lobe of digestive gland
E eye

ECV — efferent ctenidial vein

EN endoderm

EPT _ pallial fold or “epitaenia”

ET ectoderm

Е foot

СВ goblet cell
GZS sorting area of gizzard

Н head

I intestine

K kidney

I lung or pulmonary sac

LGS left gastric streak

LNL | left nuchal lobe

LPPG left pleuro-pedal ganglionic mass
LS larval stomach

MS mesoderm or mesenchyme cells

MT mantle

МТС mantle cavity

MTE mantle edge

OS osphradium

В pericardium

PG pericardial cavity
PDP _ pedal cell-plate

PO pulmonary opening
EN prototroch

RGS right gastric streak
ENL right nuchal lobe

ENV renal vestibule

RT rectum

SD stomodaeum

SH shell (protoconch)
SHG shell gland

SHGR rudimentary shell gland
SPG supraintestinal ganglion
STC statocyst

TN tentacle

l ureter
V ventricle
VS visceral sac

1. Shell gland and mantle

A “rudimentary shell gland’ (SHGR,
Fig. 1A,B), which is in fact the common
rudiment of the mantle and the shell
gland, differentiates early in the ectoderm
(ET, Fig. 1B) at the aboral or “posterior”
side of the embryo in Stage II. It appears
as a thickened median circular plate of a
single layer of tall columnar cells with sub-
basal ovoid nuclei and a densely granular
cytoplasm. This rudimentary structure
considerably enlarges in the following
stage and simultaneously invaginates, for-
ming a cup-shaped median depression
(SHGR, Fig. 2A,B) about 60 u in diameter
and 40 u deep.

As the invaginated rudiment con-
tinues to enlarge in subsequent stages, it
gradually shifts to the left until it comes to
lie left of the median line in Stage V
(SHGR, Fig. 3A). Meanwhile, its cells
(SHGR, Fig. ЗВ) have produced a thin
cuticular secretion of uniform thickness,
the larval shell or protoconch (SH), which
lines the whole invaginated rudiment. The
epithelium around the opening of the in-
vagination forms a slightly projecting fold

ЗАП drawings are of Marisa cornuarietis (L.). The general views are reconstructions of the shell gland, mantle
and respiratory organs made from serial transverse and sagittal sections.

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 197

that will develop into the free mantle edge
(MTE) of the adult.

As development proceeds, the т-
vaginated rudiment further enlarges. Its
central part bulges up, gradually rising out
of the opening of the invagination. The
rudiment thus acquires a cap-like form in
Stage VI (Fig. 4A). The cells at the
periphery remain tall, forming a circular
marginal thickening (SH +, Fig. 4B) which
eventually will develop into the definitive
shell gland. The epithelium in the central
part of the bulge, on the other hand, grows
thinner.

The mantle first appears at the onset of
torsion (Stage VII) as a consequence of the
rapid growth of the epithelium of the cap.
This epithelium further thins as it grows
and spreads over the left half of the vis-
ceral mass (VS, Fig. 5A) in Stage VIII.
Its flattened cells (Fig. 5B) harbour ellip-
tical nuclei in their thickest central por-
tions. This epithelium continues to grow
until it covers the whole visceral sac; it
then extends beyond the sac to form the
outer epithelium of the mantle (MT, Figs.
6C, 8B) which has now become con-
spicuous. The thin cuticular secretion
elaborated by this epithelium
simultaneously spreads on the outer sur-
face of the visceral sac and mantle forming
a cup-shaped thin larval shell (SH, Figs.
5A,B; 6A-C; 7; 8A,B) that reflects the
shape of these organs.

As these developments take place, the
thickened margin (SHG, Fig. 4A,B) of the
original rudiment, which represents the
actual anlage for the definitive shell gland,
further thickens and enlarges (Fig. 5A,B).
The circular ectodermal fold, which will
form the future mantle edge (MTE),
projects around the rudiment of the shell
gland (SHG), the 2 being separated by a
conspicuous mantle groove. In subsequent
stages, the shell gland (SHG, Figs. 6A,B;
7) and the mantle edge (MTE) are
gradually carried forward, as a result of the
forward prolongation of the mantle (MT),
until they come to occupy their definitive
positions around the head in Stage XI (Fig.
SA). The shell gland at that stage consists
of narrow columnar cells with ovoid nuclei

and a highly chromophilic cytoplasm.
Mesenchyme cells aggregate below its
cells, and unicellular glands make their
appearance among them shortly before
hatching.

The larval shell remains part of the adult
shell. Secretions added to it from the shell
gland and the outer epithelium of the
mantle contribute later to the formation
and growth of the definitive shell.

2. Mantle cavity

The mantle cavity also develops
relatively late in Marisa cornuarietis, i.e.,
only after torsion has begun (Stage VII).
When the visceral sac starts rotating anti-
clockwise as a result of torsion, a con-
spicuous depression or groove shows on its
right dorso-lateral side marking the begin-
ning of formation of the mantle cavity
(MTC, Fig. 5A,B). This groove gradually
deepens as it becomes overgrown in sub-
sequent stages by the developing mantle,
being finally transformed into a deep cavi-
ty whose wide external opening 15 рег-
manently retained and serves as the man-
tle opening.

During torsion, as mentioned above, the
ectoderm, which in Stage VIII is on the
left side of the visceral sac rudiment (VS,
Fig. 5A) and which is originally derived
from the epithelium of the “rudimentary
shell gland,” grows rapidly so as to cover
the whole visceral sac rudiment (VS, Fig.
6A,B) and to project as a thick lobe (MT)
over and a little beyond the mantle cavity
in Stage IX (MTC, Figs. 5A,B; 6A-C).
While the visceral sac bulges out on the
left side, the ectoderm, which was situated
on the right side of the visceral sac rudi-
ment up to Stage VIII, caves in, coming to
lie inside the mantle cavity and now for-
ming its inner lining as well as the inner
epithelium of the mantle growing over it.
Certain structures, such as the rudimen-
tary ctenidium (CN, Figs. 3A,B; 4A,B),
which has already started differentiating
in that ectoderm in earlier stages, are
similarly engulfed in the developing man-
tle cavity (Figs. 5B, 6B).

The mantle (MT, Figs. 6A,C; 7)
gradually prolongs anteriorly during sub-

198 DEMIAN AND YOUSIF

FIG. 1. A, Embryo in Stage И showing the rudimentary shell gland, left lateral view.

B, Part of a sagittal section of the embryo (same stage), passing through the rudimentary
shell gland.

A, Embryo in Stage III, left lateral view.

B, Part of a sagittal section of the embryo (same stage), passing through the rudimentary
shell gland.

FIG. 3. A, Embryo in Stage У, dorsal view.

B, Transverse section through visceral sac of embryo, same stage; plane of section in-
dicated by stippled line in A.

FIG.

bo

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 199

es |
0.1mm

FIG. 4. A, Embryo in Stage VI, dorsal view.
B, Transverse section through visceral sac of embryo, same stage; plane of section in-
dicated by stippled line in A.
FIG. 5. A, Embryo in Stage VIII, dorsal view.
В, Transverse section through visceral sac of embryo, same stage; plane of section in-
dicated by stippled line in A.

200 DEMIAN AND YOUSIF

sequent development, arching over the
head vesicle, until it attains its definitive
shape and position in Stage XI (MT, Fig.
ЗА, В). By this same process, the mantle
cavity (MTC, Figs. 6A-C; 8B) has grown
conspicuously larger and deeper. Its wide
external opening, originally facing to the
right (Fig. 5A), shifts during torsion so as
to face forwards (Stage X, Fig. 7), and on
account of the simultaneous growth of the
mantle and mantle cavity it lies close
behind the head in Stage XI (Fig. 8A).

3. Ctenidium

Marisa, like all other ampullariids,
possesses a single monopectinate
ctenidium. In the adult the organ consists,
on the average, of 350 thin flattened
triangular lamellae hanging from the man-
tle roof with their apices pointing into the
mantle cavity. The 2 free lateral edges of
each lamella are unequal in length, the
right or afferent edge being shorter than
the left or efferent edge (Demian, 1965).

The rudiment of the ctenidium (CN,
Fig. 3A.B) first differentiates in Stage У as
a thickened oval ectodermal plate on the
right side of the visceral sac rudiment (VS,
Fig. 3A). This plate measures about 40 u
across. Its cells (CN, Fig. 3B) are tall,
columnar and have a densely granular
cytoplasm and ovoid sub-basal nuclei
relatively rich in chromatin material. They
proliferate rapidly, giving rise to a mul-
titude of elliptical, polygonal and irregular
cells which aggregate below the ctenidial
rudiment (CN, Fig. 4B).

When torsion begins, the rudimentary
ctenidium, along with the ectoderm
covering the right side of the visceral sac
rudiment, is gradually drawn inside the
developing mantle cavity. In Stage IX, the
whole rudiment (CN, Fig. 6A,B) has been
enclosed within the mantle cavity (MTC),
i.e., it now lies on the inner epithelium of
the mantle (MT, Fig. 6C) just behind the
mantle opening. It has also elongated,
shifted a little to the left, and has acquired
the shape of a J, with the longer and
broader right limb projecting ahead of the
left limb (CN, Fig. 6B). Meanwhile,
transverse epithelial folds, which will later

form ctenidial leaflets or lamellae, started
developing at the broader anterior end of
the organ. Two or 3 of these rudimentary
ctenidial lamellae are conspicuous in Stage
IX, where the organ measures about 0.2
mm in length.

As the mantle stretches forward in Stage
X, the ctenidium (CN, Fig. 7) further
elongates and shows new transverse
epithelial folds behind the older ones, with
a total of 7 ctenidial lamellae at that stage.
Each rudimentary lamella is a double-
walled flattened fold with an epithelial
covering of cuboid cells that have a
vacuolated cytoplasm and relatively large
spherical nuclei. Mesenchyme cells from
the segmentation cavity migrate inside
these lamellae, leaving irregular
haemocoelic lacunae in between them.

In Stage XI, the ctenidium (CN, Fig.
ЗА, В) shifts further forward, coming to lie
in front of the heart (A,V) and kidney (K).
It is now about 0.35 mm long and extends
obliquely along the roof of the mantle
cavity, parallel with the ureter (U, Fig.
SA). The afferent and efferent ctenidial
veins (ACV, ECV) become conspicuous
along the 2 lateral edges of the organ.
Twelve ctenidial lamellae are developed at
this stage and project considerably into the
mantle cavity (MTC, Fig. 8B). Transverse
sections of these lamellae show that each
has developed a narrow ciliated ridge on
its anterior and posterior surfaces, running
near to and parallel with its left or efferent
edge.

As development proceeds through Stage
XII, the ctenidium further lengthens and
now projects far in front of the anterior tip
of the ureter. It is about 0.7 mm long at
this stage and carries 20 ctenidial lamellae.
The largest of these lie near the anterior
end of the organ, their sizes decreasing
gradually towards both ends. The
epithelial cells covering the lamellae have
already started differentiating (Fig. 9).
Numerous basophilic granules accumulate
within their apical ends and a few goblet
cells (GB) differentiate between them, es-
pecially near the bases of the lamellae. The
cells in the ciliated ridges (CIL) carry long
cilia and have a vacuolated cytoplasm. The

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 201

FIG. 6. A,B, Embryo in Stage IX, in right lateral (A) and dorsal (B) views, showing the mantle
(MT) enclosing the developing mantle cavity (MTC). The ctenidial lamellae are shown
in transparency as dark bands in B.
C, Transverse section through visceral sac of embryo, same stage; plane of section in-
dicated by stippled line in B.

202 DEMIAN AND YOUSIF

FIG. 7. Embryo in Stage X, dorsal view.
FIG. 8. A, Embryo in Stage XI, dorsal view.
B, Transverse section of the embryo, same stage; plane of section indicated by stippled line
in A.
FIG. 9. Transverse section of a ctenidial lamella from the embryo in Stage ХИ passing parallel to
the afferent edge and showing ciliated ridges on efferent edge.

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 203

narrow inner space found within each
lamella is filled with mesenchyme cells
(MS) of various forms and encloses
irregular haemocoelic sinuses.

At the time of hatching, the greater por-
tion of the ctenidium still lies on the left
side of the mantle roof. After hatching, the
organ is displaced to the right side as a
result of the enormous development of the
lung on the left side. New ctenidial
lamellae are continuously added at the
posterior end of the organ. Thus there are
30, 50 and 75 lamellae, respectively, in
snails 1, 3 and 5 weeks old (CN, Figs. 11-

SI)

4. Lung or pulmonary sac

Although essentially aquatic and
breathing with a ctenidium, the Am-
pullariidae have also developed a lung by
means of which they use atmospheric air,
apparently an adaption to life in habitats
with foul water conditions and periodic
droughts. Adult Marisa cornuarietis
possesses a more or less rectangular,
spacious, pouch-like lung or pulmonary
sac hanging from the roof of the mantle
cavity on the left side. The roof of this sac
is formed by the thin mantle. Its floor is
thick, highly vascularized and perforated
near its left anterior corner by a small
ovoid pulmonary opening ог
pneumostome (Demian, 1965).

The lung, as the ctenidium, is ectoder-
mal in origin, but develops much later.
The lung rudiment (Г, Fig. 7) starts
differentiating in Stage X as a small oval
disc of cuboid to flattened cells in the
epithelium lining the roof of the mantle
cavity, between the ctenidium (CN) and
osphradium (OS). This rudimentary disc
becomes invaginated in Stage XI (L, Fig.
8A,B); the invagination then enlarges,
without any further differentiation, until
the embryo hatches. The epithelium
around the edge of the invagination thus
forms a thick projecting continuous fold,
which gradually grows over the concavity
and towards the center, thus separating
the lung cavity from the mantle cavity.
The floor of the lung rudiment does not
close entirely; a narrow slit-like opening is

spared out and persists as the
pneumostome in the adult.

In a snail 1 week old (about 2 mm
diameter) the lung (L, Fig. 11) shows as an
elongated dorso-ventrally compressed sac,
0.7 mm in length and 0.1 mm in maximum
width, with a slit-like pneumostome (PO),
about 0.6 mm long.

Thereafter the lung gradually increases
in size, displacing the ctenidium to the
right side. It attains a length of about 1
mm and a width of 0.4 mm in snails 3
weeks old (L, Fig. 12), and measures 1.7
by 1.4 mm in snails 5 weeks old (L, Fig.
13); the pneumostome (PO) has widened
and assumed a triangular outline. The in-
crease in floor area thereafter is more
pronounced to the right of and behind the
pneumostome, which therefore retains a
position near the anterior left corner of the
pulmonary sac.

5. Pallial.fold and nuchal lobes

The chief accessory respiratory organs in
the Ampullariidae are the pallial fold, or
“epitaenia of Ihering (1887), and the 2,
right and left, nuchal (neck) lobes or
siphons.

In adult Marisa (Demian, 1965), the
epitaenia is a prominent ciliated
longitudinal fold running along the entire
length of the floor of the mantle cavity un-
derneath the strip of the roof separating
the ctenidium from the lung. It plays a
major role in creating the respiratory water
current that flows inside the mantle cavity
and bathes the ctenidium, and in shutting
off the cavity around the ctenidium during
aerial respiration. It also separates from
the rest of the mantle cavity a narrow
channel on the right side of the mantle
floor, along which excretory and waste
products are passed out with the exhalant
stream. The nuchal lobes are 2 highly
muscular, flattened, flaps which project
anteriorly from the floor of the mantle
cavity, one on either side of the head.
Unlike aquatic pulmonates, ampullariids
are unable to bring the pulmonary
opening directly to the water surface. Thus
during pulmonary respiration, their
pneumostome is moved forward only a lit-

204 DEMIAN AND YOUSIF

FIG. 10. Part of a transverse section of the embryo in Stage XII, passing through the epitaenia.

FIGS. 11-13. Mantle cavity and respiratory organs of juvenile snails 1 week (11), 3 weeks (12) and 5
weeks (13) after hatching. The shell is removed and the mantle is cut along the right
edge of the ctenidium and reflected to the left so as to expose the mantle cavity.

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 205

tle and apposed to the base of the left
nuchal lobe which rolls itself into a tube or
siphon that reaches to the surface film. At-
mospheric air passes in and out of the lung
cavity through that siphon. The right
nuchal lobe aids in aquatic respiration by
forming a shallow gutter that directs the
exhalant water current from the mantle
cavity away from the head.

The epitaenia first appears in Stage XI
of the embryo as a small epithelial fold
which projects transversely on the floor of
the mantle cavity. Its epithelium consists
of columnar to cuboid cells with relatively
large ovoid nuclei. It gradually increases in
length and height in subsequent stages,
while 2 types of cells (EPT, Fig. 10)
become differentiated in its epithelium.
The majority of the cells are ciliated,
columnar, with highly acidophilic granular
cytoplasm and central or apical ovoid
nuclei. The 2nd type consists of non-
ciliated narrow columnar cells with less
acidophilic cytoplasm and small elliptical
nuclei located at various levels within
these cells.

The epitaenia elongates after hatching
(EPT, Figs. 11-13), but does not assume its
definitive form and its complete course
along the floor of the mantle cavity until 4-
5 weeks after hatching. ;

The left and right nuchal lobes are first
seen in Stage XII as 2 small ectodermal
folds on either side of the head. These 2
folds (LNL, RNL, Fig. 11) grow forward
and expand laterally after hatching,
reaching from behind the 2 eyes to the free
mantle edge, while 2 types of cells
differentiate in their epithelial covering.
Some cells are ciliated and have a marked-
ly acidophilic cytoplasm, while others are
glandular and goblet-like.

The histology of the fully-developed
ctenidium, lung, epitaenia and nuchal
lobes has been described in a previous
publication (Lutfy € Demian, 1965).

DISCUSSION

A so-called “rudimentary shell gland,”
more or less similar to that here described
for Marisa cornuarietis, seems to be com-
mon to all gastropods and to develop

similarly into the shell gland of the adult
and the outer covering epithelia of the
visceral mass and the mantle (Ghose, 1963;
Raven, 1966).

The present account of the early
differentiation and course of development
of the “rudimentary shell gland” in Marisa
generally agrees with observations made
by some earlier authors on the correspond-
ing structure in other ampullariids, i.e., in
Ampullaria depressa by Brooks &
McGlone (1908), in A. gigas by Fernando
(1931), in A. canaliculata by Scott (1934)
and in Pila globosa by Ranjah (1942).
There is considerable disagreement,
however, as regards the development of
the mantle cavity and the method by
which the rudimentary shell gland con-
tributes to the formation of the mantle.
According to both Fernando (1931) and
Ranjah (1942), the mantle cavity develops
as a mid-ventral invagination of the ec-
toderm of the visceral sac rudiment at a
very early embryonic stage. The invagina-
tion grows into a tubular structure from
which the ureter takes origin on the right
side. This tube, the rudimentary mantle
cavity, is shifted to the right side of the
visceral sac during torsion, is constricted
off from the ureter, and is finally moved to
the dorsal side by the end of torsion. The
sequence of events during torsion, as out-
lined by those 2 authors, is not clear.
Brooks € McGlone (1908) and Scott
(1934), on the other hand, made no men-
tion of such an invaginated mantle cavity
rudiment in the early embryos of the am-
pullariids they examined, and did not see a
mantle cavity before the beginning of tor-
sion.

The present study revealed that, in
Marisa, the mantle cavity does not arise at
an early stage but only at a relatively late
stage, after the onset of torsion. It does not
start as a ventral tubular invagination, but
as a depression or groove on the right
dorso-lateral side of the visceral sac rudi-
ment, as a consequence of torsion. This
depression becomes later overgrown by
the mantle, by which process it is
transformed into a deep mantle cavity.
Marisa is not unique in this respect. The

206 DEMIAN AND YOUSIF

mantle is known to start in various other
gastropods as a groove or a pair of grooves
in the wall of the visceral sac rudiment,
and to become secondarily overgrown by
the mantle, as described for Paludina
(Drummond, 1903), Haliotis (Crofts, 1938)
and Pomatias (Creek, 1951) among the
Prosobranchia; and for Planorbis (Rabl,

1879), Arion (Heyder, 1909), Agriolimax
(Carrick, 1939), Ariophanta

(Balsubramaniam, 1952) and Achatina
(Chose, 1963) among the pulmonates.
The conflict between the present obser-
vations and those made by Fernando
(1931) and Ranjah (1942) is doubtlessly
due to a misinterpretation: from their il-
lustrations and descriptions it is clear that
they must have taken the rudiment of the
ureter and renal vestibule, such as here
observed in Marisa, for a rudimentary
mantle cavity. The former rudiment arises
as a tubular ectodermal invagination in the
early embryo, its opening shifts to the
right during torsion and is then drawn into

the mantle cavity (Demian & Yousif,
1973с).
Earlier authors dealing with the

development of the ctenidium in the Am-
pullariidae generally agreed that this
organ started to differentiate at a late em-
bryonic stage from a thickening in the ec-
toderm lining the mantle cavity. Brooks &
McGlone (1908) and Scott (1934), in the
embryos of the Ampullaria spp. they in-
vestigated, did not recognize the
ctenidium until the mantle cavity was
developed. Fernando (1931) asserted, for
A. gigas, that the organ did not start
differentiating until torsion was com-
pleted, and Ranjah (1942) reported that in
Pila it developed at a late stage, com-
parable to our embryonic Stage VIII.
The descriptions given by those earlier
authors suggest that they probably
overlooked the early anlage of the
ctenidium and failed to distinguish the
organ until it had developed a few
ctenidial lamellae. That Fernando (1931),
Scott (1934) and Ranjah (1942) observed
and figured a number of well-defined
lamellae on the rudimentary ctenidium,
right after the completion of torsion, im-

plies that the rudiment must have started
differentiating a few stages earlier. Ranjah
(1942) did describe a rudimentary thicken-
ing in the right wall of the visceral sac of
the early embryo of Pila, but apparently
mistook it for the rudiment of the visceral
ganglion; the thickening, however, evi-
dently corresponds to the rudiment of the
ctenidium here described in Marisa.

The present investigation has clearly
shown that the ctenidium, in Marisa, is on-
togenetically older than the mantle cavity.
Its early rudiment starts differentiating on
the right wall of the visceral sac rudiment
before either torsion begins or the mantle
cavity forms. It later passes inside the
mantle cavity, and ctenidial lamellae
begin to develop on it. In some other
prosobranchs such as Crepidula, Fulgur
and Fasciolaria (Raven, 1966), the
ctenidium similarly differentiates at a very
early embryonic stage and is secondarily
taken into the mantle cavity.

It may be worthy of note that the
ctenidium of Marisa, which originates on
the right side of the embryo and corre-
sponds morphologically to the right cteni-
dium of the Archaeogastropoda, comes

lie on the left side of the advanced
embryo after torsion, and that, as a result
of the development of the voluminous
lung on the left side after hatching, it then
again becomes displaced to the right side.

The Ampullariidae are the only
prosobranchs which have a well- developed
lung in addition to the ctenidium. Such a
peculiar development has raised much
speculation and several important
questions which have long been discussed
and disputed by general morphologists
and systematists. Among these questions
are: How has this lung appeared? Is it a
modified ctenidium or a new acquisition?
Has it any ancestral connection with the
lung of pulmonates?

Brooks € McGlone (1908) were
probably the first to advance some

answers, basing themselves on an em-
bryological study of the respiratory organs
in Ampullaria depressa. They reported
that the ctenidium, osphradium and lung
developed simultaneously or nearly so

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 207

from the inner epithelium of the mantle,
the ctenidium and osphradium developing
as 2 parallel ridges on that epithelium, and
the lung arising as an infolding of the
epithelium between them. They conclud-
ed therefrom that, in Ampullaria, the
ctenidium, osphradium and lung con-
stituted a series of homologous structures,
specialized in differing directions, and that
the lung might be regarded as represen-
ting one or more modified gill lamellae.
Prashad (1925), who agreed to that view,
further suggested that the lung might be a
modified part of a 2nd ctenidium which, in
response to a need for aerial respiration,
has been developed in close association
with the Ist ctenidium. Ranjah (1942), ша
study of the embryonic development of
Pila, confirmed that the lung arose as an
infolding of the mantle epithelium, almost
simultaneously with the ctenidium and os-
phradium. However, Brooks & McGlone
as well as Ranjah described only the early
rudiments of the ampullariid lung, and did
not follow up the full development of the
organ as was done in the present study.

Evidence derived from the present in-
vestigation indicates that in Marisa:

1. The lung does not arise simultaneous-
ly with the ctenidium and osphradium as
claimed by Brooks & McGlone (1908) and
Ranjah (1942) for other ampullariids. It
starts to differentiate much later than the
ctenidium, and develops principally after
hatching.

2. The lung is not a modified 2nd
ctenidium as suggested by Prashad (1925)
for Pila, but a new structure, developing as
a modification of the mantle epithelium.
The ctenidium arises from a single ec-
todermal rudiment which starts differen-
tiating on the right wall of the visceral sac
rudiment before the mantle or mantle
cavity have developed, and no trace of a
2nd ctenidial rudiment is observable at
that time, or later. Moreover, there is no
reason to believe that the lung represents
one or more modified gill lamellae derived
from the Ist ctenidium, as suggested by
Brooks & McGlone (1908).

3. The probability of an ancestral con-
nection between the lung of the Am-

pullariidae and that of pulmonates
suspected by some authors is remote, be-
cause the lung, as observed in Marisa, is
derived in a way that is basically different
from that most commonly met with in the
pulmonates. The pulmonate lung usually
arises, prior to and independent of the
mantle cavity, as an ectodermal invagina-
tion on the ventral or right posterior wall
of the visceral sac rudiment in the early
embryo. It becomes secondarily engulfed
into the mantle cavity to become a non-
separable part of it, the edges of the 2
cavities growing together so that they ul-
timately open to the exterior by a common
opening, the pneumostome, as has been
described for Helix (Fol, 1880), Limax
(Meisenheimer, 1898), Arion (Heyder,
1909), and Achatina (Ghose, 1963).

The pallial fold and the 2 nuchal lobes,
in Marisa, were shown, through this study,
to be pallial structures developed as folds
of the epithelium lining the mantle cavity.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the
valuable contribution of Dr. K. Mansour,
Emeritus Professor of Zoology, Faculty of
Science, Ain Shams University, Cairo, in
the supervision of the present work.
Thanks are also due to Dr. B. Hubendick,
Director of the Natural History Museum
in Gothenberg, Sweden, for his continuous
interest and support.

REFERENCES

BALSUBRAMANIAM, T.S., 1952, Develop-
ment of Ariophanta bristrialis Beck. J. An-
namalai Univ., 17: 94-100.

BROOKS, W.K. & McGLONE, B., 1908, The
origin of the lung in Ampullaria. Carnegie
Inst. Publ., 102: 95-104.

CARRICK, R., 1939, The life history ‚and
development of Agriolimax agrestis L., the
grey field slug. Trans. Roy. Soc. Edinb., 59:
963-597.

CREEK, G.A., 1951, The reproductive system
and embryology of the snail Pomatias
elegans (Müller). Proc. Zool. Soc. Lond., 121:
599-640.

CROFTS, R.R., 1938, The development of
Haliotis tuberculata, with special reference

208

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DEMIAN, E.S., 1965, The respiratory system
and the mechanism of respiration in Marisa
cornuarietis (L.). Ark. Zool., Ser. 2, 17: 539-
560.

DEMIAN, E.S. € YOUSIF, F., 1973a, Em-
bryonic development and organogenesis in
the snail Marisa cornuarietis
(Mesogastropoda: Ampullariidae). I. General
outlines of development. Malacologia, 12:
123-150.

DEMIAN, E.S. € YOUSIF, F., 1973b, Em-
bryonic development and organogenesis in
the snail Marisa cornuarietis
(Mesogastropoda: Ampullariidae). II.
Development of the alimentary system.
Malacologia, 12: 151-174.

DEMIAN, E.S. € YOUSIF, F., 1973c, Em-
bryonic development and organogenesis in
the snail Marisa cornuarietis
(Mesogastropoda: Ampullariidae). III.
Development of the alimentary system.
Malacologia, 12: 175-194.

DRUMMOND, LM., 1903, Notes on the
development of Paludina vivipara with
special reference to the urino-genital organs
and theories of gastropod torsion. Quart. J.
microsc. Sci., 46: 97-143.

FERNANDO, W., 1931, The development of
the kidney in Ampullaria (Pila) gigas. Proc!
zool. Soc. Lond., 62: 745-750.

FOL, H., 1880, Études sur le développement
des mollusques. III. Sur le développement

DEMIAN AND YOUSIF

des gastéropodes pulmonés. Arch. Zool. exp.
gén., 8: 103-232.

GHOSE, K.C., 1963, Morphogenesis of the
shell gland, lung, mantle and mantle cavity
of the giant land snail Achatina fulica. Proc.
malacol. Soc. Lond., 35: 119-126.

HEYDER, P., 1909, Zur Entwicklung der Lun-
genhóhole bei Arion. Nebst Bemerkungen
über die Entwicklung der Urniere und Niere,
des Pericards und Herzens. Zt. wiss. Zool.,
93: 90-156.

IHERING, H. von, 1887, Giebt es Or-
thoneuren? Zt.wiss. Zool., 45: 499-531.

LUTFY, В.С. & DEMIAN, E.S., 1965, The
histology of the respiratory organs of Marisa
cornuarietis (1). Ark. Zool., Ser. 2, 18: 51-71.

NEISENHEIMER, J., 1898, Entwicklungs-
geschichte von Limax maximus L. Zt. wiss.
Zool., 63: 573-664.

PRASHAD, B., 1925, Anatomy of the common
Indian apple-snail, Pila globosa. Mem. In-
dian Mus., 8: 91-152.

RABL, C., 1879, Uber die Entwicklung der
Tellerschnecke. Morph. Jb., 5: 562-660.

RANJAH, A.R., 1942, The embryology of the
Indian apple-snail, Pila globosa (Swainson)
(Mollusca, Gastropoda). Rec. Indian Mus.,
44: 217-322.

RAVEN, D.P., 1966, Morphogenesis: The
analysis of molluscan development.
Pergamon Press, 2nd Ed., 365 р.

SCOTT, M.LH., 1934, Sobre el desarrollo em-
brionario de Ampullaria canaliculata. Rev.
Mus. La Plata, 34: 373-385.

ZUSAMMENFASSUNG

EMBRYONALE ENTWICKLUNG UND ORGANOGENESE
IN DER SCHNECKE MARISA CORNUARIETIS (MESOGASTROPODA:
AMPULLARIIDAE).
IV. ENTWICKLUNG DER SCHALENDRUSE, DES MANTELS UND DER
ATMUNGSORGANE

Е. S. Demian und Е. Yousif

Die Schalendriisenanlage lässt sich schon früh am aboralen Ende des Embryos als eine
mediane Ektodermalplatte unterscheiden. Diese vertieft sich becherartig, wandert nach
links und sondert eine zarte, kutikulare, larvale Schale ab. Der mittlere Teil der Ver-
tiefung wölbt sich dann empor, während seine Epithelzellen verflachen. Zusammen mit
der Schale wächst dieses Epithel kreisförmig über den Proto-Eingeweidesack, und dann
allein darüber hinaus, und bildet so schliesslich das äussere Epithel des
Eingeweidesackes und des Mantels. Der wulstartige Epithelkranz am Mantelrand wird
zur endgültigen Schalendrüse. Die Schale der Larve bleibt in einer Schicht der
endgültigen Schale erhalten.

Im Gegenstaz zu früheren Berichten über Ampullariiden, entsteht die Mantelhöhle
erst spät, nach Drehung des Eingeweidesacks. Anfänglich eine Vertiefung oder Furche

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 209

in der rechten dorsolateralen Wand des Proto-Eingeweidesackes, verwandelt sie sich
allmählich, sährend sie vom Mantel überdeckt wird, in eine tiefe Höhle. Das
einbezogene Ektoderm bildet ihre innere Auskleidung und das innere Mantelepithel.

Die Kieme erwies sich als ontogenetisch älter als die Mantelhöhle. Die Kiemenanlage
hebt sich schon früh, als verdickte Ektodermplatte, an der rechten Wand des Proto-
Eingeweidesacks ab. Durch die Torsion gelangt die Urkieme sekundär in die
Mantelhöhle. Sie verschiebt sich nach links und verlängert sich mit dem wachsenden
Mantel nach vorn. Epitheliale Querfalten, die späteren Kiemenblättchen, werden
angesetzt.

Die Lunge ist ein unter den Prosobranchiern den Ampullariiden eigentümliches
Organ, das sich erst kurz vor dem Ausschlüpfen als eine breite Einsenkung des
Mantelhöhlendaches, zwischen Kieme und Osphradium, auszubilden beginnt. Der
Epithelsaum um die Vertiefung wächst vom Rande her nach innen und bildet so den
Boden der Lungenhöhle. Ein schmaler Spalt bleibt offen, der als Pneumostom erhalten
bleibt. Nach dem Ausschlüpfen wächst die Lunge enorm und verlagert dadurch die
Kieme nach rechts. Die Lunge der Ampullariiden ist demnach eine Neuentwicklung und
keine modifizierte Kieme. Ein direkter stammesgeschichtlicher Zusammenhang mit der
Pulmonatenlunge ist nicht ersichtlich.

Die akzessorischen Atmungsorgane, d.h. die Pallialfalte (Epitaenia) und die 2
Nackenlappen (Siphos), werden als Falten des Mantelbodenepithels ebenfalls spät
ausgebildet. Sie erlangen ihre endgültige Gestalt und Lage erst nach dem Ausschlüpfen.

А.С.

RESUME

DEVELOPPEMENT EMBRYONNAIRE ET
ORGANOGENESE CHEZ LE MOLLUSQUE
MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE).
IV. DEVELOPPEMENT DE LA GLANDE COQUILLIERE,
DU MANTEAU ET DES ORGANES RESPIRATOIRES

E. S. Demian et F. Yousif

Une glande coquilliere rudimentaire commence à se différencier au pôle aboral du
jeune embryon sous forme d'un disque ectodermique épaissi en position médiane. I] s'in-
vagine pour constituer une cavité en forme de coupe, s étend sur la gauche et sécréte une
délicate coquille larvaire cuticulaire. Par la suite sa partie centrale s épaissit et son
épithélium s aplanit. En même temps que la coquille larvaire, il s'étend circulairement
par-dessus le rudiment de sac viscéral en le débordant et en s'étendant plus avant. A la
fin, il forme les épithéliums externes de la masse viscérale et du manteau. Un bourrelet
épithélial circulaire et périphérique demeure épaissi, c'est lui qui formera la glande
coquilliére définitive. La coquille larvaire persiste dans une couche de la coquille adulte.

Contrairement aux résultats des premiers travaux sur des Ampullariidés apparentés, la
cavité palléale ne se développe que relativement tard, apres le choc de la torsion. Elle
débute comme une dépression ou une gouttiére sur la paroi dorso-latérale droite de
l'ébauche de sac viscéral, puis se transforme graduellement en une cavité profonde tandis
que le manteau la déborde. L'ectoderme enfoncé dans cette cavité forme sa doublure in-
térieure et l'épithélium interne du manteau.

Il a été prouvé que la cténidie est ontologiquement plus ancienne que la cavité
palléale. Son ébauche commence à se différencier primitivement comme un disque ec-
todermique épaissi, sur la paroi droite de l’ébauche de sac viscéral. Secondairement, elle
passe dans la cavité palléale pendant la torsion lorsqu elle se déplace sur le cóté gauche,
s'étendant plus en avant quand le manteau s'accroît antérieurement. Des replis
épithéliaux transversaux se développent sur elle pour former plus tard les lamelles
cténidiales.

Ге poumon qui, chez les Prosobranches, est une structure particuliére aux Ат-
pullariidae, commence а se développer, peu avant l'éclosion, sous forme d'une large in-

210

DEMIAN AND YOUSIF

vagination dans le toit de l'épithélium de la cavité palléale, entre la cténidie et
losphradie. Le bourrelet épithélial bordant l'invagination s'accroît à partir de la
périphérie pour former le plancher de la cavité pulmonaire, laissant ouverte une fissure
étroite qui persistera en tant que pneumostome. Le poumon s accroit énormément aprés
l'éclosion, déplaçant la cténidie sur le côté droit. Ces découvertes prouvent que le
poumon est une nouvelle acquisition chez les Ampullariidae. Ce n'est pas une cténidie
modifiée et il ne semble pas avoir la moindre parenté ancestrale avec le poumon des
Pulmonés.

Les organes palléaux accessoires de la respiration c’est-à-dire les ““epitaenia” et les 2
lobes nucaux (siphons), se développent aussi tardivement, sous forme de replis
épithéliaux qui apparaissent sur le plancher de la cavité palléale. Ils atteignent leurs
formes et leurs positions définitives aprés | éclosion.

A.L.

RESUMEN

DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN
MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE).
IV. DESARROLLO DE LA GLANDULA CONCHIFERA,
MANTO Y ORGANOS RESPIRATORIOS

E. S. Demian y F. Yousif

Una gländula de la concha rudimentaria comienza por differenciarse en el polo aboral
del temprano embriön, como una placa media, ectodermal, engrosada. Al envaginarse
forma cavidad como una taza, se traslada a la izquierda y segrega una delicada conchilla
larval cuticular. La parte central se comba hacia arriba y su epitelio se aplana. La glän-
dula se extiende, junto con la concha larval, circularmente y sobrepasando el saco visceral
rudimentario. Ultimamente se forman el epitelio externo de la masa visceral y el manto.
Un anillo periferico epitelial permanece engrosado, y luego formarä la gländula
definitiva. La conchilla larval persiste en una capa de la adulta.

Contrariamente a lo que se habia indicado en otros informes sobre los ampularidos, la
cavidad del manto se desarrolla relativamente tarde, después que la torsión ha comen-
zado. Iniciándose como una hendidura en la pared derecha dorso-lateral del saco visceral
rudimentario, gradualmente se transforma en una profunda cavidad al ser superada por
el desarrollo del manto. El ectoderma engolfado dentro de la cavidad forma su forro in-
terior y el epitelio del interior del manto.

La ctenidia mostro ser de una edad ontogeneticamente mayor que la cavidad paleal.
Su rudimento se diferencia temprano como una placa ectodermal engrosada en la pared
derecha del saco visceral rudimentario. Secundariamente pasa dentro de la cavidad
paleal durante la torsión, cuando se mueve al lado izquierdo, extendiéndose hacia
adelante en medida que el manto crece anteriormente. El pliegue epitelial transversal
desarrolla por encima, más tarde, las lamelas de la branquia.

El pulmón—una estructura peculiar dentro de los Prosobranquios de los Am-
pullariidae, comienza muy poco antes de la eclosión, como una invaginación ancha en el
techo del epitelio de la cavidad paleal, entre las branquias y el osfradio. El anillo epitelial
que rodea la invaginación crece de la periferia para formar el piso de la cavidad paleal o
pulmón, dejando una estrecha ranura que persiste como el penumostoma. El pulmón
crece enormemente después de la enclosión, desplazando la branquia hacia el lado
derecho. Esto indica que el pulmón es una adquisición nueva entre los Ampullariidae, No
es una branquia modificada y no parece tener ninguna relación ancetral directa con el
pulmón de los pulmonados.

Los órganos respiratorios accesorios, como el pliegue paleal (o “epitaenia”) y los dos
lóbulos nucales (sifones), tambien se desarrollan tarde como pliegues del epitelio en el
piso de la cavidad del manto. Estos alcanzan sus formas definitivas después de la
eclosión.

J.J.P.

EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS

ДБСТРАКТ

ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS
(MESOGASTROPODA: AMPULLARIDAE)
1V. РАЗВИТИЕ РАКОВИННОЙ ЖЕЛЕЗЫ, МАНТИИ И ДЫХАТЕЛЬНЫХ ОРГАНОВ

D. ДИМЬЯН И ©. ЮСИХФ

Рудимент раковинной железы начинает дифференцироваться на ранней
стадии развития эмбриона, на аборальной его стороне, как срединное
утолщение эктодермальной пластинки. Она — вдавливается, образуя
чашковидную впадину, сдвигается налево и выделяет нежную кутикулярную
личиночную раковину. Ee центральная часть затем становится выпуклой, a

эпителий уплощается. Вместе с личиночной раковиной она окружает
рудимент висцерального мешка, разрастаясь над ним. Наконец, она
образует эпителий висцеральной массы и мантии. Периферическая

эпителиальная кайма остается утолщенной и впоследствии образует
окончатальную раковинную железу. МЛичиночная раковина сохраняется и в
раковине взрослого моллюска.

В противоположность более ранним данным о развитии родственных форм
Ampullariidae, было найдено, что мантийная полость у них развивается
сравнительно поздно, после начала процесса торсии. Начинается это с
образования вдавленности или желобка на правой дорзо- латеральной стенке
рудимента висцерального мешка; постепенно он превращается в глубокую
полость, когда она обрастает мантией. Эктодерма, вдающаяся в эту
полость, образует её внутреннюю выстилку и внутренний эпителий мантии.

В статье доказано, что ктенидии и онтогенетически старше, чем
мантийная полость. Их рудимент начинает дифференцироваться рано, ввиде
утолщения эктодермальной пластинки В правой стенке рудимента
висцерального мешка. Вторично он входит в мантийную полость во время
процесса торсии, когда он сдвигается на левую сторону, выдаваясъь вперед,

во время роста мантии спереди. Ha нем развиваются поперечные
эпителиальные складки, которые позже служат началом образования
пластинок ктенидиев. Легкие, образование необычное для Prosobranchia

Ampullariidae, начинают развиваться незадолго до вылупливания личинок,
ввиде широкой инвагинации, выстилающего мантийную полость эпителия,
между ктенидием и осфрадием. Эпителиальная кайма, опоясывающая эту
инвагинацию, растет от центра к периферии, образуя выстилку легочной
полости, оставляя открытой узкую щель, которая остается, образуя
пневмотостом. Легкие растут очень сильно после выклевывания личинок,
вытесняя ктенидии к правой стороне. Эта особенность указывает Ha TO,
что легкие являются HOBHIM образованием У Ampullariidae. Это не
модифицицированные ктенидии, и они, видимо, не имеют какого-либо прямого
предкового родства с легкими Pulmonata.

Добавочные дыхательные органы, т.е. мантийные складки или "эпитении" и
2 нукальных лопасти (сифоны) также развиваются позже, из складок
эпителия, выстилающего мантийную полость. Они достигают свое го
окончательного вида и расположения после выклева личинок.

Z.A.F.

211

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MALACOLOGIA, 1973, 12(2): 213-223

REGULATION OF APICAL CILIA DEVELOPMENT BY THE POLAR
LOBE OF ILYANASSA (GASTROPODA: NASSARIIDAE)!

James N. Cather

Department of Zoology, The University of Michigan
Ann Arbor, 48104, U.S.A.

ABSTRACT

Ilyanassa passes through a stage comparable to the trochophore within the egg cap-
sule. The typical structures of the trochophore are reduced, but apical cilia appear on the
apical cells la!!! - Id!!! and are therefore homologous with the apical tuft of the
trochophore. Lateral tufts of cilia on la?! and |b?! are the only vestiges of the prototroch.

Removal of the first or second polar lobe or the D quadrant macromere results in the
development of cilia over most of the pretrochal region; thus cells which remain un-
ciliated in the normal embryo develop cilia in operated embryos. It is proposed that the
polar lobe normally inhibits ciliation in those cells whose prospective fate is to form un-
ciliated cephalic plate cells.

The regulation of apical cilia development in Ilyanassa is compared to that of other
spiralians.

Ciliation has been shown by others to occur in the absence of DNA-dependent RNA
synthesis as well as in the absence of RNA-dependent protein synthesis. It appears that
regulation might occur at a post-translational level in the apical cilia-polar lobe system

and possibly at the time of the assembly of tubulin into cilia.

INTRODUCTION

The relationship of the polar lobe to the
formation of the apical tuft was one of the
first embryological phenomena т-
vestigated experimentally. Wilson (1904a)
found that the pretrochal region of the
trochophore of the scaphopod mollusc
Dentalium is covered with short vibratile
cilia, while the apex bears a long non-
vibratile ciliary tuft on a circumscribed
apical thickening, the apical organ.
Removal of the Ist polar lobe, the non-
nucleate vegetal extrusion of the Ist
cleavage, resulted in larvae lacking an
apical tuft, probably the apical organ, and
the post-trochal region. The vibratile cilia
were unaffected by this and subsequent
operations. After removal of the 2nd polar
lobe, the apical tuft was formed normally
but the post-trochal region was missing.
Partial embryos which developed from

isolated blastomeres, or combinations of
blastomeres, only developed the apical tuft
when the D quadrant, the recipient of the
polar lobe material, was present. Wilson
found that about half the Ist polar lobe
was required for apical tuft formation
while Geilenkirchen, Verdonk & Timmer-
mans (1970) found that the apical tuft
would form after removal of 60% but not
80% of the vegetal side of the Ist polar
lobe. Verdonk, Geilenkirchen & Timmer-
mans (1971) found that removal of 70% of
the volume of the polar lobe from the
vegetal pole of fertilized or unfertilized
eggs had no detrimental effect on apical
tuft formation. They then found the factor
responsible for tuft formation to be localiz-
ed in the animal half of the Ist polar lobe,
in the vegetal half of the CD blastomere at
the 2-cell stage, and in the animal portion
of the D blastomere at the 4-cell stage.
Verdonk (1968a) showed that centrifuga-

Supported in part by Institutional Research Grant No. IN-40M to the University of Michigan from the

American Cancer Society

(213)

214 J. N. CATHER

tion did not affect the development of the
apical tuft in intact or operated eggs, thus
indicating a cortical rather than a general
cytoplasmic influence. Timmermans,
Geilenkirchen & Verdonk (1970) originally
proposed that DNA-containing granules in
the vegetal cortex served as
morphogenetic factors for the apical tuft;
but the later study of Verdonk, Geilen-
kirchen € Timmermans (1971) showed
that removal of these granules has no
effect on the apical tuft, although they
might still serve as post-trochal
morphogenetic determinants. The mussel,
Mytilus, is much like Dentalium in that
lobeless embryos or those lacking the D
quadrant lack an apical tuft (Rattenbury &
Berg, 1954). Removal of the 2nd polar lobe
does not affect tuft formation. As in
Ilyanassa there is a general appearance of
ectodermization in lobeless embroyos but
this is due to the reduction of endodermal
volume rather than an actual enhance-
ment of ectodermal development.

Other species have not been as
thoroughly investigated. In Patella,
Wilson (1904b) found that the apical tuft
would form in any Y embryo and is not
dependent on the D quadrant. The polar
lobe is not present in this species. In the
annelid, Sabellaria, Novikoff (1938 a,b)
found that the apical tuft formed only in
the presence of the C macromere when the
Ist polar lobe was present. Removal of the
2nd polar lobe had no effect on the tuft.
Thus it appears the lobe has made its con-
tribution to CD at the 2-cell stage just as in
Dentalium, but the final site is in the C
blastomere rather than the D blastomere.
Pretrochal cilia in Sabellaria are depen-
dent on the presence of A or B. In the
fresh-water prosobranch, Bithynia, the
apical cilia appear to be normal in AB or
CD halves or C or D quarters but are ab-
sent in total exogastrulae (Hess, 1971).

In another annelid Nereis (Costello,
1945) the apical tuft is derived from Та! -
1d! as it is in Patella, while in Dentalium
only Id! contributes to the apical tuft
(Wilson, 1904b). The apical plate in Lym-
naea (Verdonk, 1965) and Biomphalaria
(Camey & Verdonk, 1970) has a similar

cellular origin; in these cases the cell
lineage has been worked out in detail.
Cather (1971) reported that, in Ilyanassa,
progeny from isolated la! - lc! had a
single cluster of cilia while those of 1d! had
2 ciliary clusters suggesting an origin of
the apical cilia similar to that of the tuft of
Dentalium.

Conklin (1897) found that a distinct
apical sense organ was formed in
Crepidula from the 4 apical cells la!!! -
Id!!! and that in addition a few of their
progeny proliferated into the head vesicle.
Posterior to the apical organ is the head
vesicle which is covered by the large
ciliated cells of the posterior cell plate in
the veliger. These cells are the progeny of
the posterior turret cells Ic? and Id? and of
the basal сей (1d!2!) and the middle cell
(1d122) of the posterior arm of the
molluscan cross.

The term apical plate was used by
Conklin to refer to the 7 large ciliated cells
derived from the anterior arm of the cross
which extend from the apical organ to the
velum. Their progeny make up 13 cells in
the young veliger. Verdonk (1965) in-
cludes the 4 apical cells in the apical plate
in Lymnaea thus including all of the large

cells between the small-celled cephalic

plates, which are the sites of origin of the
tentacles, eyes and cerebral ganglia. Even
though Ilyanassa is much more like
Crepidula than like Lymnaea, 1 will use
apical plate to include all the large cells
between the cephalic plates including the
apical organ, and restrict the use of apical
organ to the apical cells at whatever stage
they are considered. The apical plate is a
structure of the veliger in Ilyanassa while
the apical organ is a vestige of the
trochophore which is subsequently
morphologically if not functionally incor-
porated into the apical plate of the veliger.

The following observations were made
and experiments were done to determine
the character and mode of regulation of
the apical cilia in Ilyanassa.

METHODS

The experiments were performed on
eggs and embryos of the prosobranch gas-

APICAL CILIA REGULATION IN ILYANASSA 215

tropod, Nassarius obsoletus Say, common-
ly referred to as Ilyanassa by em-
bryologists. Animals were obtained from
the Marine Biological Laboratory, Woods
Hole, Mass., U.S.A., and were raised in
Instant Ocean (Aquarium Systems Inc.) at
The University of Michigan.

All embryos were maintained at 20 +
1°C. At this temperature full differentia-
tion of the veliger requires about 3 weeks.
The details of handling eggs and embryos
and of performing operations are given by
Clement (1952, 1962, 1971) and Cather
(1967). Analysis of ciliary patterns was
done with a Zeiss Nomarski Differential
Interference Contrast Microscope on liv-
ing embryos. These were then fixed in 10%
formalin-sea water on the slide,
photographed, and made into permanent
preparations by mounting the unstained
embryos in diaphane (Clement & Cather,
1957). Several staining procedures were
tried to enhance visibility of both the cell
boundaries and the ciliary patterns, but
none of the stained specimens was com-
parable in quality to the unstained em-
bryos in diaphane. The latter though were
less satisfactory for observation of ciliary
patterns than living embryos. Fixation and
staining often resulted in the loss of cilia
from positions where they had been
observed on living embryos.

RESULTS

In Ilyanassa and other neogastropods
the stage comparable to the trochophore is
passed within the egg capsule, and typical
ciliation is markedly reduced. There is no
apical tuft comparable to that of forms
with free-living trochophores such as Den-
talium, Patella, Sabellaria, and Mytilus.
The apical tuft of Nereis is distinct but the
cilia are short and more motile than in
those species previously noted. Short
motile cilia do appear on the 4 apical cells
of Ilyanassa (la!!! - 1b!!!) about 36 hours
after the Ist cleavage (Fig. 1). At this time
the cells still occupy an apical position over
the furrow between the macromeres. The
cells are relatively large and temporarily
flattened when compared to the surroun-
ding micromeres at this stage. The apical

cells are delimited from the surrounding
cells by a slight groove visible in section.
Since the 4 cells that become ciliated
shortly after gastrulation are the same cells
which form the apical tuft in other
annelids and molluscs, these apical cilia of
Ilyanassa are homologous with the apical
tuft of the trochophore. The apical cells
which are formed within 8 hours of the for-
mation of the mesentoblast cell do not
divide again, at least through the early
veliger stage shown in Fig. 11. The apical
cells remain distinct through the
developmental period due to their prox-
imity to the posterior turret cells 1c? and
ld? which remain very large until the head
vesicle of the veliger begins to form. The
same ciliary pattern persists as the
stomodeum is formed and the mesoblast
bands continue their elaboration (Fig. 2).

RESULTS

Normal Post-Gastrula Ciliation

Although only the 4 apical cells are in-
itially ciliated 3 additional cells become
ciliated by the 5th or 6th day of develop-
ment to give the ciliated area a Y or cross
shape, with the arms slightly off the sagit-
tal and transverse planes of the em-
bryo. Judging from Conklin's (1897) il-
lustrations of the cell pattern around the
apical cells in Crepidula, which is very
similar to Ilyanassa, these later ciliated
cells appear to be derivatives of the
anterior arm of the cross, which form the
apical plate cells in Crepidula. It has been
possible to follow the formation and fate of
1b1112 in Ilyanassa, due to its size and posi-
tion, until the time of ciliation. In the
veliger of Ilyanassa, as in Crepidula, all of
the cells of the apical plate and the
posterior cell plate are ciliated. From the
stage comparable to the trochophore until
the early veliger there is a shift in the posi-
tion of the apical cells from the original
animal pole to an anterior position.

By the 6th day the anterior wall of the
stomodeum is ciliated (Fig. 3) and the
lateral trochoblast derivatives la?! and 1b?!
which have remained very large become
ciliated (Fig. 4). The early differentiation

216 J. N. CATHER

FIGS. 1-8. Drawings of normal (Figs. 1-4) and experimental (Figs. 5-8) embryos of Ilyanassa grown
at 20°C. The animal pole is uppermost in each drawing.

FIG. 1. 36-hr control embryo, lateral view.
FIG. 2. 48-hr control embryo, lateral view.
FIG. 3. 6-day control embryo, lateral view.
FIG. 4. 6-day control embryo, front view.

FIGS. 5-7 are from operated embryos at a stage of development comparable to Figs. 3 and 4.

FIG. 5. 6-day embryo after Ist polar lobe removal.

FIG. 6. 7-day embryo after 2nd polar lobe removal.

FIG. 7. 6-day embryo after D macromere removal.

FIG. 8. 9-day embryo after Ist polar lobe removal showing complete development of ciliation. x
125.

FIGS. 9-14. Photomicrographs of normal and experimental embryos of Ilyanassa grown at 20°C.
(All x 220.)

FIG. 9. 4-day control embryo, lateral view.

FIG. 10. 9-day embryo after Ist polar lobe removal.

FIG. 11. 9-day control embryo, dorsolateral view.

FIG. 12. 11-day 1/4 embryo.

FIG. 13. 4-day control, front view.

FIG. 14. 9-day embryo after removal of the 1st polar lobe. The animal pole is at upper left.
Abbreviations Used: a = apical cilia of apical cells; ac = apical cilia of all first quartet
micromeres; f = foot; h = head cilia of head vesicle and apical plate; p = prototroch vestige
of la2!: 5 = stomodeum: sc = stomodeal cilia; sh = shell; у = velar lobe; ус = velar cilia.

APICAL CILIA REGULATION IN ILYANASSA

218 |. Nt CATHER

of these cells and the fact that they remain
the only lateral ciliated cells for almost 1/3
of the developmental period, suggest that
they represent vestiges of the prototroch.
The other velar rudiments appear much
later.

The development of the velum and of

the ciliated bands anterior and ventral to
the shell gland and on the foot and mantle
occur much later; they have not been well

worked out, but as structures of the veliger

they are beyond the stages to be con-
sidered here.

Ciliation in Lobeless Embryos

The ciliary pattern was studied in 44 liv-
ing embryos from which the first polar
lobe had been removed. Lobeless embryos
complete gastrulation slightly more rapid-
ly than eel embryos, but no apical cilia
develop until the embryos are ap-
proximately 48 hours old, a lag of about 12
hours behind the controls. Ciliation usual-
ly extends ventrally somewhat farther than
the lateral trochoblast position in tontrol
embryos. This is apparently due to the fact
that the first quartet derivatives cover
relatively more of the lobeless embryo
than of the control. Most or all of the
derivatives of the first quartet appeared to
be ciliated (Figs. 5, 10, 14) in 39 embryos;
4 embryos had unciliated patches in the
region of the first quartet derivatives and 1
embryo had a single broad band of cilia
across its apex. There was little variation in
the basic pattern of ciliation through the
stage comparable to the trochophore,
although it is known that some variation is
present in later stages (Clement, 1952;
Atkinson, 1971). The pattern of cellular
distribution was also studied an ad-
ditional 24 fixed lobeless embryos and it
was found to be quite uniform through the
stage comparable to the trochophore.

Although a detailed cell lineage has not
been carried out on lobeless embryos,
some observations have been made which
are important in the interpretation of the
pattern of ciliation lobeless embryos.
Clement (1952) has shown that the pattern
of cleavage is modified lobeless ет-
bryos, but Davidson et al. (1965) and

Cather and Mirkes (Cather, 1971) have
shown that the total cell number is not ap-
preciably modified. The total number of
Ist quartet derivatives, including those of
the turret cells, increases from 38 to 52 in
the trochophore stage in both normal and
lobeless embryos. The turret cells remain
large and distinctive in lobeless embryos
just as in control embryos and clearly mark
the equatorial boundaries of ciliation in
the trochophore stage. The apical cells in
delobed embryos are similar in size to
those in normal embryos and are equally
distinctive. Velar cilia develop at the same
equatorial position and ventral to the
turret cell derivatives but later than the
apical cilia (Fig. 8).

The early formation of the stomodeal in-
vagination acentric to the vegetal pole in
lobeless embryos may indicate an aspect of
polarity which is not lobe dependent (see
Clement, 1952; Atkinson, 1971).

An analysis of 12 living embryos and an
additional 16 fixed embryos with the 2nd
polar lobe removed indicated that there
are no appreciable differences in the
ciliary patterns between embryos with the
Ist or 2nd polar lobe removed (Fig. 6). In
cases where portions of the pretrochal
areas remain unciliated, following either
operation, the ciliated area could be
observed to shift toward 1 side (Fig. 6).
Such a shift cannot be detected when all of
the pretrochal region is ciliated, even if it
takes place. This may represent the normal
shifting of the apical plate to an anterior
position, but there is no way to determine
the anterior-posterior axis in lobeless em-
bryos due to the absence of ‘landmarks.’

Deletion of the D Quadrant Macromere

The CD macromere was deleted in 20
cases to form AB half embryos; D was
deleted in 7 cases to form ABC embryos;
ABD, ACD and BCD were deleted in 2
cases each to form C, B and A quarter em-
bryos respectively (Fig. 12). Following
these operations the pattern of ciliation
was essentially the same as in lobeless em-
bryos, so that a cap of ciliated cells more or
less covered the upper % of the embryo.
The velar cilia develop later from the ven-

APICAL CILIA REGULATION IN ILYANASSA 219

trolateral area and may be interspersed
with additional short cilia from cells which
by their position are probably 2nd quartet
derivatives.

DISCUSSION

In lobeless embryos of Ilyanassa the
ciliary pattern of the stage comparable to
the trochophore is considerably different
from the pattern in spiralians previously
studied, when comparing the tuft of the
trochophore with the development of
apical cilia. Removal of the Ist polar lobe
does not result in the absence of apical
cilia in Ilyanassa, but rather in the absence
of morphogenetic regulation of apical
cilia. The same results follow the removal
of the 2nd polar lobe. Certain cells of the
Ist quartet, normally unciliated in early
development, now develop cilia. Some of
the cells under consideration would be ex-
pected to develop cilia much later, but
others are the cells which normally give
rise to the eyes and cerebral ganglia, which
remain unciliated normally.

Atkinson (1971) has pointed out the dif-
ficulty of making comparisons between
lobeless forms of species such as Ilyanassa,
lacking a free-living trochophore, and
those species with a free-living
trochophore, such as Dentalium, Mytilus
and Sabellaria. Both Clement (1952, 1962)
and Atkinson (1971), who have done the
most complete analyses of lobeless em-
bryos, have focused on the completely
differentiated form comparable to the
veliger. Because of the excellence of these
works it is possible to direct attention to
the intermediate stages for a more com-
plete analysis of the steps leading to
differentiative changes.

Atkinson found that the normal veliger
of Ilyanassa was essentially the same as
Crepidula as far as the apical plate and
surrounding area is concerned. He further
found that the pre-velar epidermis of
lobeless larvae was often non-ciliated
cuboidal epithelium, though such larvae
often had an area of ciliated ectoderm,
usually opposite the posterior protrusion.

In this study, each of the 130 lobeless or
D-less embryos examined in detail at a

stage comparable to the trochophore had
an apical area with motile cilia covering
most of the pretrochal ectoderm. This
observation supports the wisdom of Atkin-
son s statement concerning the difficulty
of attempting comparisons between
different larvae following the same opera-
tion, and also illustrates the importance of
sequential developmental analysis.

Investigations thus far have shown that
the polar lobe may influence development
sequentially through: 1) modification of
cleavage pattern (Clement, 1952); 2)
material contribution to structures in the
D quadrant cell lineage (Clement, 1952,
1956, 1962); 3) induction of specific organs
(Clement, 1952, 1956, 1962, 1967; and
Cather, 1967); and 4) inhibition (Cather,
1967; Atkinson, 1971). Results of the pre-
sent study appear to fall in the last
category. Polar lobe derivatives somehow
influence certain cells of the first quartet
so that the potential to form cilia is not
realized. Removal of the lobe, or of the
early blastomeres into which it is incor-
porated, evidently releases this inhibition
so that not only the normally ciliated
apical cells form cilia, but all the Ist
quartet derivatives become ciliated. This is
consistent with the view of Verdonk
(1968b) on radialized embryos of Lym-
naed.

Alternative hypotheses—the stimulation
of apical cell division to cover the apical
ciliated region in lobeless embryos, or a
precocious appearance of velar cilia—do
not appear to be tenable. In the Ist case,
the apical cells of lobeless embryos are ap-
proximately the same size as in normal em-
bryos, which indicates that there has not
been a significant increase in progeny
from these cells. Furthermore, the total
number of cells derived from the Ist
quartet is similar in delobed and control
embryos. In the 2nd case, velar cilia
develop ventrally and equatorially to, and
include the turret cell derivatives. The
velar cilia appear subsequently to the
development of the rest of the apical
ciliated region, which persists without be-
ing involved in velar lobe formation in
lobeless embryos.

220 J. ¿Ni CATHER

The formation of cilia in lobeless em-
bryos by cells which are unciliated in nor-
mal embryos is particularly interesting in
light of recent work indicating that cilia
can form in the absence of DNA-
dependent RNA synthesis in Ilyanassa
(Collier, 1966; Feigenbaum & Goldberg,
1965; Mirkes, 1970) and in the sea urchin
(Auclair & Siegel, 1966). It has also been
shown (Iverson, 1971) that the sea urchin
can regenerate cilia without RNA-
dependent protein synthesis by utilizing
an intracellular pool of tubulin, formed
originally on maternally derived mRNA.
Repeated deciliation and regeneration
does require new synthesis. Amemiya
(1971) further found that while isolated
cells of the sea urchin cannot regenerate
cilia, those in reaggregates under the same
conditions can. He attributes this to inhibi-
tion of the biosynthesis of precursor
proteins or to an inhibition of the associa-
tion of subunits in isolated cells. The in-
vestigations cited above present evidence
in favor of the later alternative, but in
either case, the role of the cell surface as a
regulatory agent is indicated.

In Ilyanassa, an interesting and testable
hypothesis, although still highly
speculative, is that subunits for ciliary syn-
thesis are present in ectodermal cells of at
least the Ist quartet. However the associa-
tion of such subunits is inhibited in all
non-apical cells by the polar lobe. The
cells of lobeless Ilyanassa embryos which
are added to the ciliated apical group are
cephalic plate cells which go through ap-
parently the normal number of divisions
prior to their abnormal ciliation.

It is not known how tubulin utilization is
regulated for cell division or ciliation, but
it is interesting to consider how the
ancestral apical tuft might be reduced in
length to be the apical cilia in those forms
with a reduced trochophore.

Shell inhibition in the A, B and C
quadrants (Cather, 1967) is similar to the
ciliary inhibition in that only certain cells
respond to the inhibition while others
proceed to form shell and carry out their
prospective fates. Multiple lobes of the
velum and multiple stomodea in lobeless

embryos of Ilyanassa (Atkinson, 1971)
suggest another case of inhibitory in-
fluence by the polar lobe in normal
development.

The regulatory mechanisms are un-
known in all these cases but the regulation
of ciliation may be most amenable to fruit-
ful further investigation because of the re-
cent advances in our knowledge of the
biochemistry of cilia formation.

LITERATURE CITED

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ATKINSON, J. W., 1971, Organogenesis in
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CAMEY, T. & VERDONK, М. H., 1970, The

early development of the snail Biomphalaria
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¡ATHER, J. N., 1967, Cellular interactions in
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CLEMENT, A. C., 1956, Experimental studies
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CLEMENT, A. C., 1967, The embryonic value
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CLEMENT, А. C., 1971, Ilyanassa. In, “Ех-
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M

ra

lan

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ZUSAMMENFASSUNG

REGULIERUNG DER APIKALZILIENBILDUNG DURCH
DEN POLLAPPEN BEI ILYANASSA (GASTROPODA: NASSARIIDAE)

J.N. Cather

Ilyanassa durchläuft in der Eikapsel ein Entwicklungsstadium, das der Trochophora
vergleichbar ist. Die typischen Trochophora-Strukturen sind zuriickgebildet, doch
bilden sich Apikalzilien auf den Apikalzellen la!!! bis 1411; sie sind daher mit dem
apikalen Biischel der Trochophora homolog. Laterale Wimpernbiischel auf Та?! und 1b?!

sind die einzigen Rudimente des Prototrochs.

Entfernung des ersten oder zweiten Pollappens oder der Makromere des D-
Quadranten führt zur Zilienentwicklung auf dem größten Teil der Prätrochalregion. So

222

J. N. CATHER

entwickeln Zellen, die im normalen Embryo unbewimpert bleiben, bei operierten Em-
bryonen Zilien. Der Pollappen inhibiert, wie zur Deutung vorgeschlagen wird, die Zilien-
bildung in denjenigen Zellen, deren prospektive Bestimmung es ist, unbewimperte
Scheitelplatten-Zellen zu bilden.

Die Regulierung der Apikalzilienentwicklung bei Ilyanassa wird mit der anderer
Spiralier verglichen.

Andere Autoren konnten zeigen, daß Zilienbildung beim Fehlen DNS-abhängiger
RNS-Synthese vorkommt wie auch beim Fehlen RNS-abhängiger Protein-Synthese. Es
scheint, daß die Regulierung auf der Posttranslationsstufe im Apikalzilien-Pollappen-
System stattfiden kann, möglicherweise zur Zeit der Ansammlung von Tubulin in den
Zilien.

C.M.-B.

у RESUME

REGULATION DU DEVELOPPEMENT DES CILS APICAUX PAR
LE LOBE POLAIRE CHEZ ILYANASSA (GASTROPODA: NASSARIIDAE)

J. N. Cather

Ilyanassa atteint un stade comparable а la trochophore а l'intérieur de la capsule de
l'oeuf. Les structures typiques de la trochophore sont réduites, mais cependant des cils
apicaux apparaissent sur les cellules apicales la!!! - 1d!!! et sont homologues de la touffe
apicale de la trochophore. Des touffes latérales de cils sur la?! et 1b?! sont les seuls
vestiges de la prototroque.

Si Гоп enléve le premier ou second lobe polaire ou le macromere D du stade 4, il en
résulte le développement de cils sur la plus grande partie de la région prétrochale; ainsi
les cellules qui demeurent non-ciliées sur l'embryon normal développent des cils sur les
embryons opérés. On suppose que le lobe polaire inhibe normalement la ciliation dans
ces cellules dont la destinée future est de former des cellules céphaliques de revêtement,
non-ciliées.

La régulation du développement des cils apicaux chez Ilyanassa a été comparée à celle
des autres spiralias.

D'autres auteurs ont montré que la ciliation se produit en l'absence de synthèse de
RNA dépendante du DNA, aussi bien que de l'absence de synthèse de proteines dépen-
dantes du RNA. Il semble que la régulation pourrait se manifester au niveau post-
translationnel dans le système cils apicaux—lobe polaire et peut-être au moment de
l’ajustage des tubules dans les cils.

А.Г.

RESUMEN

REGULACION DEL DESARROLLO DE CILIAS APICALES POR
EL LOBULO POLAR DE ILYANASSA (GASTROPODA: NASSARIIDAE)

J. N. Cather

Dentro de la cápsula ovigera, Пуапазза pasa por un estado comparable al de trocosfera.
Las estructuras apicales de la trocosfera estan reducidas, pero las cilias estan presentes
sobre las células apicales la!!! - Id!!! siendo asi homólogas a los penachos apicales
trocosfóricos. Los únicos vestigios de la prototrocosfera son los penachos laterales de cilias
en la?! y 1b21

Extirpación del primer o segundo lóbulo polar, o del cuadrante D macromero, resulta
en el desarrollo de cilias; por esto, células que en un desarrollo normal permanecerían no
ciliadas, tienen cilias en los embriones operados. Se sugiere que el lóbulo polar nor-

APICAL CILIA REGULATION IN ILYANASSA 223

malmente inhibe la ciliación en aquellas células cuyo destino es formar placas celulares

cefálicas no ciliadas.
La regulación en el desarrollo de las cilias espirales en Ilyanassa es comparada con las

de otros con desdoblamiento espiral.

J.J.P.

АБСТРАКТ

РЕГУЛЯЦИЯ РАЗВИТИЯ АПИКАЛЬНЫХ РЕСНИЧЕК ПОЛЯРНОЙ ЛОПАСТЬК
ILYANASSA

ДЖ. КЭТЕР

Пуапазза проходит через стадию развития, сравнимую с трохофорой, внутри
яйцевой капсулы. Типичное строение трохофоры редуцировано, но апикальные
реснички появляются на апикальных клетках la Wl - аш | и поэтому
гомологичны апикальному пучку трохофоры. Латеральные пучки ресничек на
la! и 162 являются единственными следами прототроха. Удаление первой
или второй полярной лопасти или Д-квадранта макромеры имеет своим
результатом развитие ресничек на большей части претрохальной области;
таким образом у клеток нормального эмбриона, не имеющего ресничек,
таковые развиваются у оперированного эмбриона.

Предполагается, что полярная лопасть нормально не имеет ресничек на
тех клетках, дальнейшее назначение которых состоит в образовании
безресничных клеток цефалической пластинки.

Регуляция развития апикальных ресничек у Пуапазза в статье сравнивается
с другими спиральными формами.

Ранее было показано, что образование ресничек встречается при
отсутствии DNA - зависимого компонента при синтезе RNA, как и в случае
отсутствия ВМА - зависимого компонента протеинового синтеза.

По-видимому, эти регуляции может встречаться на пост-трансляционном
уровне в системе "апикальные реснички - полярная лопасть" и, возможно,
во время накопления тубулина в ресничках.

Z.A.F.

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MALACOLOGIA, 1973, 12(2): 225-245

MORPHOGENESE, DE „ГА, CHARNIERE. CHEZ, 5 1ESPECES DE

VENERIDAE!

Marcel L. M. Le Pennec

Laboratoire de Zoologie, Université de Bretagne Occidentale
29 N. Brest, France

RESUME

L'élevage au laboratoire de 5 représentants des Veneridae des côtes de Bretagne a
fourni des renseignements sur la morphogenése des charnieres. Le stade de la
métamorphose a été dépassé pour toutes les espéces. L'observation journalière des со-
quilles larvaires a permis de suivre en détail l’évolution de la charnière: d’abord les
crénelures de la prodissoconque, puis la formation des lames primitives chez la dis-
soconque, enfin la régression des crénelures. Parallélement nous avons noté la formation
et la position du ligament. Les résultats sont traduits sous forme d'une clé de détermina-
tion pour les 5 espéces de Veneridae. Le genre Venerupis est caractérisé, des la fin de la
premiere semaine, par des crénelures bien formées et dénombrables alors qu elles restent
indistinctes chez le genre Venus. A l'intérieur du genre Venerupis la variation du nombre
des crénelures permet de différencier les espéces : de 8 4 10 pour Venerupis pullastra,
généralement 12 pour Venerupis aurea. A la fin de la deuxiéme semaine des formations
latérales apparaissent chez Venus fasciata. Les stries trés marquées de la coquille de
Venus striatula aident а reconnaítre cette espéce. Aucun caractére morphologique par-
ticulier n'a pu être retenu pour Venus verrucosa. Il ressort de cette étude que l'examen de
la charniére des coquilles larvaires est un des critéres les plus sûrs pour établir l'identité
des larves de bivalves récoltées dans le plancton. Cependant la détermination des larves,
au moyen de cette méthode, reste impossible avant la constitution des crénelures qui а

lieu ä la fin de la premiere semaine.

INTRODUCTION

L'élevage au laboratoire permet
d’obtenir les différents stades larvaires de
la plupart des mollusques et le probléme
de la récolte et de la détermination est ain-
si résolu. Il est désormais possible de suivre
la morphogenese de la coquille larvaire et
de déterminer les critéres qui aideront а
résoudre le probléme de la détermination
spécifique des larves de bivalves du planc-
ton, récolté en mer.

Au cours d'une étude précédente (Le
Pennec, 1970; Le Pennec € Lucas, 1970)
nous avons retenu 5 critéres qui sont: les
dimensions de la larve, la forme générale
de la coquille, la proéminence de ГитБо,
les détails de la charniére et la position du
ligament.

L'examen de la charniére et la position
du ligament nécessitent l'ouverture de la
coquille larvaire, mais les résultats obtenus
montrent que ce sont les 2 meilleurs
critéres pour la reconnaissance spécifique
des larves. Ils font l'objet de ce present
travail.

Depuis Bernard, en 1895, peu d auteurs
ont étudié les charniéres de mollusques.
Werner (1939), Sullivan (1948), et Rees
(1950) ont suggéré que Гехатеп des char-
niéres serait un bon critere pour l'iden-
tification des larves dans le plancton.
Leurs observations, bien que super-
ficielles et effectuées sur des échantillons
récoltés en mer, leur ont permis d'établir
une classification simplifiée des larves de
bivalves.

! Etude réalisée dans le cadre des contrats 70/170 et 71/292 passés entre le Professeur Lucas et le C.N.E.X.O.

(225)

226 M. L. M. LE PENNEC

L'obtention des différents stades lar-
vaires en laboratoire permet de suivre de
maniére certaine l’évolution d'une char-
nière de la prodissoconque jusqu à
l'adulte.

Partant de ces données nouvelles,
Chanley (1965, 1969) decrit la
morphologie de nombreuses larves de bi-
valves et différencie les especes prin-
cipalement d’apres la structure de leur
charniére (crénelures et dents juvéniles).
Malheureusement on ne trouve dans ses
publications aucun schéma (ou photo)
montrant une évolution complète de la
charnière larvaire et post-larvaire.

La premiére classification des bivalves
basée sur la charnière, et la systématisa-
tion de la plupart des types (Cryptodontes,
Taxodontes, Hétérodontes, etc.) sont dues
au paléontologiste Neumayr (1891). De
plus, la division des bivalves en famille et
en genre est fondée en grande partie sur le
caractére des dents et du ligament.

Bernard (1895) a proposé de traduire la
disposition respective des dents et des
fossettes par des formules cardinales. Les
dents se forment aux dépens de lames
primitives. Des chiffres romains indiquent
le rang de la lame primitive à laquelle elles
appartiennent. Si cette lame se divise, on
utilise la notation en chiffre arabe 2a, 2b:
3a, 3b, etc. Les chiffres sont impairs pour
la valve droite, pairs pour la valve gauche.

Chez les Hétérodontes, auxquels appar-
tiennent les Veneridae, les dents sont dis-
semblables avec généralement 3 cardinales
semblant rayonner des umbos et
divergeant plus ou moins vers le bord in-
férieur du plateau cardinal.

La prodissoconque a une charniére rec-
tiligne dépourvue de dent. Les 2 valves
sont maintenues jointes le long du cété rec-
tiligne grace au périostracum qui se con-
tinue d'une valve sur l’autre.

Au bout de quelques heures le plateau
cardinal s épaissit et la prodissoconque
présente des dents qui apparaissent com-
me des crénelures encore peu marquées.
Cette charniére embryonnaire est appelée
provinculum (Bernard, 1895). Les
crenelures grandissent à mesure que
s épaissit le plateau qui les porte. Elles sont

paralléles entre elles et perpendiculaires a
la ligne dorsale. Puis les crénelures pren-
nent une direction moins rigoureusement
parallele, ce qui est en relation avec le fait
que le bord cardinal extérieur prend une
direction plus arquée sous la poussée de
l'umbo.

D'une maniére générale, c'est à peu pres
pendant le stade de transition entre la
prodissoconque et la dissoconque que les
premiéres dents apparaissent chez les
Hétérodontes. Aprés la métamorphose les
crénelures larvaires disparaissent а mesure
que se développent les dents définitives.

Dans la présente étude la morphogenése
de la charniére a été étudiée sur 5 espéces
de Veneridae vivant sur les cótes de
Bretagne; ce sont: Venus striatula, Venus
verrucosa, Venus fasciata, Venerupis
pullastra et Venerupis aurea.

METHODES

Au cours de l’année 1969, plusieurs es-
peces de bivalves ont été élevées au
laboratoire de Zoologie de la Faculté des
Sciences de Brest (France). Les tech-
niques utilisées dérivent de celles que
Loosanoff € Davis (1963) ont mis au point
des 1946 au laboratoire de Milford
(U.S.A.). La ponte des géniteurs est
provoquée par stimulation thermique:
variations de la température de l’eau et
quelque fois émersion.

Les larves, obtenues aprés fécondation
artificielle, sont élevées dans des cuves en
plastique contenant 20 a 30 litres d eau de
mer. La stérilisation de Геаи se fait au
moyen d'un appareil Millipore dont les
filtres retiennent а leur surface toutes les
particules excédant 0,22 u. L'eau des cuves
est renouvelée journellement jusqu'à ce
que les larves atteignent une longueur de
300 и environ.

La nourriture des larves est composée de
Phytoflagellées: Monochrysis lutheri et
Isochrysis galbana, et de Diatomées dont
Chaetoceros calcitrans.

L'étude des charnières nécessite une
manipulation délicate qui consiste à ouvrir
les jeunes coquilles. Celles-ci sont mises
dans l'eau de Javel concentrée (hypo-
chlorite de sodium) pendant 2 à 5 minutes,

CHARNIERES CHEZ VENERIDAE LARVAIRES 227

ouvertes sous la binoculaire à l'aide de
deux fines aiguilles puis rincées à l'eau dis-
tillée et mises dans l'alcool glycériné pour
observation au microscope. L'alcool
glycériné (50% alcool-50% glycérine)
permet de garder les valves orientées
perpendiculairement au champ de vision
du microscope et facilite l'étude des char-
niéres. Les valves sont ensuite mesurées au
micrometre oculaire, photographiées et les
dessins des charniéres sont réalisés d’apres
les agrandissements photographiques.

RESULTATS

1. Charniere de Venus striatula

La prodissoconque de 3 jours, 103u x
87u, a une charniére droite, non fonc-
tionnelle, mesurant 64a. Le plateau car-
dinal prend naissance le long du bord dor-
sal de la coquille mais il est interrompu a
l'endroit où se formera le ligament.

La prodissoconque de 7 jours (Fig. 1) a
un plateau cardinal épaissi. Les crénelures
larvaires se forment et sont visibles sur une
coquille de 142u x 118u. Le ligament ap-
paraît dans le prolongement du plateau
cardinal au cours de la deuxième semaine.

Au stade qui précéde la métamorphose,
la coquille de 220u x 205u (Fig. 1) présente
des crénelures larvaires trés visibles, mais
non différenciées entre elles. Le ligament
est en forme de demi-cercle, du cóté du
bord postérieur de la coquille.

La dissoconque donne naissance a la
premiere dent juvénile. Elle nait sous
forme dun bourgeon émergeant du bord
de la coquille. La premiére dent apparait
sur la valve droite et sur la valve gauche de
facon simultanée.

Chez une coquille de 292 u x 261 u (Fig.
1) la valve droite présente une lame
primitive, I, trés allongée occupant une
partie du bord antérodorsal et se con-
tinuant jusqu'au milieu du plateau car-
dinal. Sur la valve gauche la lame
primitive, II, occupe seulement la partie
dorsale du bord antérieur de la coquille.

Au bout de 40 jours la coquille de 348 u
x 316 и (Fig. 2) posséde encore des
crénelures larvaires qui s estompent peu a
peu. Une dépression médiane apparait sur
la lame primitive de la valve droite délimi-

tant 2 dents dans un plan inférieur, 1, et
supérieur, III. La lame primitive, II, de la
valve gauche s est allongée jusqu au liga-
ment qui prend une position oblique par
rapport au plateau cardinal.

A 42 jours la coquille mesure 355 и x 320
и (Fig. 2), la lame primitive de la valve
gauche s est recourbée sur elle-méme et
$ est aplatie а son sommet. Sur la valve
droite la deuxième lame, III, s'allonge. Les

crenelures larvaires sont presque т-
distinctes. Le ligament devient
opisthodete.

Au 50e jour la coquille mesure 442 u x
395 u. La valve droite possede une dent
juvénile, I, et une lame située au-dessus et
qui se divise en 2 dents 3a et 3b.

Le sommet de la lame primitive, II, de
la valve gauche s est élargi et se scinde en
deux parties 2a, 2b, dans за portion
médiane. Une deuxieme dent juvénile, IV,
nait au centre du plateau cardinal et croit
perpendiculairement а ce dernier. Les
crénelures larvaires ne sont plus visibles.
Le ligament est de plus en plus oblique.

2. Charniere de Venus verrucosa

La prodissoconque de 3 jours, 110 их 85
и, a une charniére droite représentée par
un plateau cardinal se formant le long du
bord dorsal de la coquille. Les crénelures
larvaires apparaissent chez la
prodissoconque de 5 jours qui mesure 130
их 96 pu.

Au 13e jour, la coquille mesure 174 u x
150 u (Fig. 4), les crénelures larvaires sont
tres inégales et leur dénombrement est im-
possible. Les crénelures larvaires grandis-
sent au fur et à mesure que $ épaissit le
plateau cardinal qui les porte. Le ligament
devient visible lors de la deuxiéme
semaine. I] apparait dans le prolongement
des crénelures larvaires et a une forme en
demi cercle. La premiére dent apparait
durant le passage de la prodissoconque а la
dissoconque, de facon simultanée pour les
2 valves.

Sur une coquille de 21 jours mesurant
220 их 205 u les crénelures larvaires sont
trés visibles, inégales et méme absentes en
certains endroits; le ligament est bien
formé et la premiére dent apparait comme

228 M. L. M. LE PENNEC

un bombement intéressant le bord de la
coquille. Au 30e jour la coquille mesure
253 их 240 и: la premiere lame s'étale de
plus en plus dans la zone des crénelures
larvaires (Fig. 4). Au 32e jour la valve

droite montre deux lames primitives dis-
posées l’une au-dessus de l'autre; il s’agit
de la lame I et II. Le ligament prend une
position oblique par rapport au plateau
cardinal. Les crénelures larvaires disparais-

и \ 126 X 95 E
/ |
/ \
au =
150 X 126
166 X 134

221 X 205

FIG. 1. Venus striatula—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére

(longueur puis largeur)

CHARNIERES CHEZ VENERIDAE LARVAIRES 229

sent peu а peu, la lame II de la valve
gauche s est recourbée sur elle-méme et
son sommet s épaissit.

La coquille de 35 jours (Fig. 4) mesure
332 их 308 u. Les lames I et III de la valve
droite se sont allongées. La lame II de la
valve gauche présente un sommet trés
élargi qui va se scinder en deux parties
dans sa position médiane pour donner les
dents 2b et 2a.

Le ligament devient opisthodete.

3. Charniere de Venus fasciata

Le plateau cardinal devient visible chez
la prodissoconque de 3 jours, mesurant 110
их 88 y (Fig. 6).

Les crénelures larvaires apparaissent sur
la coquille de 134 u x 102 u.

Le ligament se forme des le 7e jour. Au
17e jour la larve se métamorphose et
mesure 190 их 158 u (Fig. 6). La premiere
lame primitive apparait simultanément sur
la valve droite et sur la valve gauche sous
forme d'un mamelon intéressant le bord
de la coquille auprés de la zone des
crénelures larvaires.

348 X 316

Nous observons chez les dissoconques
de У. fasciata la formation d'une lame sur
le bord de la coquille, auprés du ligament.

La dissoconque montre la premiére dent
juvénile (Fig. 7). Cette dent s'allonge еп
direction de la zone des crénelures lar-
vaires. Sur la valve gauche la lame se
recourbe sur elle-même et s'étire à son
sommet suivant le modéle que nous avons
vu chez Venus striatula et Venus
verrucosa. Sur la valve droite la premiere
dent commence а se différencier du bord
de la coquille quand celle-ci mesure 280 u.
Avant ce stade elle n'apparaît que sous
forme d'un mamelon assez étiré le long du
bord de la coquille.

Le ligament, d'abord interne et dans le
prolongement des crenelures larvaires,
devient de plus en plus oblique 4 mesure
que la dissoconque grandit.

4. Charniere de Venerupis pullastra

Le faible nombre d'échantillons élevés
au laboratoire ne nous a pas permis de
suivre l’évolution de la charnière de façon

a NN
2a
VALVE GAUCHE

FIG. 2.
(longueur puis largeur).

442 X 395

VALVE DROITE

Venus striatula—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére

230 MeL. М. LE PENNEC

Valve ING Valve
gauche и EN LE “à N droite

FIG. 3. Venus striatula—1-Prodissoconque de 10 jours: 1404 x 120u-Naissance des crénelures. 2-25 jours: 240u x
220 и:итБо proéminent: crénelures difficilement dénombrables. 3-40 jours: 355 u x 316 u:valve gauche:la lame
primitive II se forme valve droite:I et Ш présentes. 4-48 jours: 387 u x 340 u:valve gauche:la lame II donne 2a et
2b bourgeonnement de la lame IV sur le plateau cardinal.

aussi nette que dans les cas précédents. d'évolution de la charniére se rapproche
Cependant, les quelques observations que de celui de Venerupis aurea.
nous avons faites au cours de la croissance Le plateau cardinal s épaissit au fur et à

de la larve, montrent que la schéma mesure que grandit la prodissoconque. Les

CHARNIERES CHEZ VENERIDAE LARVAIRES 231

plateau cardinal et sont facilement dénom- crénelures larvaires apparaissent au bout
brables 2 jours aprés leur naissance (Fig. de 4 à 5 jours aprés la formation de la larve

9). Sur les exemplaires étudiés leur nombre D. Elles poussent perpendiculairement au

126 X 103 И

174 X 150

182 X 166

253 X 245

FIG. 4. Venus verrucosa—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiere
(longueur puis largeur).

232 M. ТМ: LE PENNEC

varie entre 8 et 10 et est donc inférieur à semaine, dans le prolongement des créne-
celui de Venerupis aurea où généralement lures larvaires et dans le même plan que
on compte 12. ces derniéres.

Comme chez les espéces précédentes le Га premiére dent apparait lors de la
ligament apparaît lors de la deuxiéme transformation de la prodissoconque en
Valve Valve

auc . 7 eue N droite
gauche 4 I QA

Y / N
\

/

O 1

FIG. 5. Venus verrucosa—1-13 jours: 1604x140u-Premieres crénelures larvaires. 2-21 jours: 2104x1904-Umbo
bien formé. Crénelures non dénombrables. 3-60 jours: 330ux305u-Coexistence dents juvéniles et crénelures.
Ligament conservé sur les 2 valves. 4-61 jours: 335ux310u-Dent juvénile de valve droite grandit et s aplatit;
crénelures larvaires encore présentes.

CHARNIERES CHEZ VENERIDAE LARVAIRES 233

dissoconque, au cours de la troisième sent comme des excroissances se differen-
semaine, et de facon simultanée pour les 2 ciant des parois latérales de la coquille,
valves. dans un plan inférieur а celui des créne-
Les lames primitives, I de la valve lures larvaires (Fig. 9).
droite, et II de la valve gauche, apparais- Au bout d 1 mois environ nous voyons
110 X 88

158 X 126

166 X 143

182 X 150

190 X 158

FIG. 6. Venus fasciata—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére
(longueur puis largeur).

234 M. L. M. LE PENNEC

2

270 X 240

276Х 243

FIG. 7. Venus fasciata—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entière
| 1

(longueur puis largeur).

sur la valve gauche (Fig. 9) que les créne-
lures larvaires sont encore présentes mais
indifférenciées entre elles et tendent а se
confondre dans la masse du plateau car-
dinal. La lame II s est recourbée sur elle-
méme en délimitant avec la paroi de la
coquille un profond sillon oú vient prendre
place la lame primitive I de la valve droite
lors de la fermeture des 2 valves. Le
sommet de la lame II s est allongé et on
voit nettement qu une dépression se forme
dans la partie médiane d'où la formation
de 2 parties qui évolueront en dents car-
dinales 2a et 2b. Au centre des crénelures
larvaires on remarque un petit bourgeon
qui est | ébauche de la dent cardinale IV.

Le ligament est devenu oblique par rap-
port au plan des crénelures larvaires et
tente de gagner le bord extérieur de la co-
quille pour devenir opisthodete.

Sur la valve droite les crénelures lar-
vaires sont indistinctes. La lame I est peu
visible sur la photo 3 (Fig. 10). La lame Ш,
située dans le plan des crénelures est bien
formée, la pointe médiane donnera la dent
cardinale 3b.

Le ligament est oblique et situé sur le
bord de la coquille.

5. Charniére de Venerupis aurea

Les 2 valves de la prodissoconque de 24
heures sont maintenues jointes gráce au
périostracum qui se continue d'une valve á
l'autre. Peu а peu le plateau cardinal
$ épaissit le long du bord dorsal de la co-
quille et des crénelures larvaires apparais-
sent au cours de la premiére semaine.
Mais, alors que chez les 3 espéces du genre
Venus les crénelures étaient indifféren-
ciées, ici elles sont facilement dénom-
brables 2 jours aprés leur formation (Fig.
11). On en compte généralement 12, de
taille variable.

Le ligament se forme lors de la deux-
iéme semaine comme dans le cas des 4 es-
peces précédentes.

La naissance de la premiére dent a lieu
chez la dissoconque de facon simultanée
pour les 2 valves et suivant le schéma que
nous connaissons (Fig. 11). Les crénelures
larvaires sont encore trés visibles chez le
juvénile (Fig. 11 et 12). Sur la valve
gauche la lame II se recourbe et son
sommet s élargit pour donner les 2 dents
juvéniles 2a, 2b. Au centre de la zone des
crénelures larvaires et done dans un plan
supérieur а celui de la lame Il apparrait la

CHARNIERES CHEZ VENERIDAE LARVAIRES 235

Valve Valve
gauche Grouse

o
=

FIG. 8. Venus fasciata—1-14 jours: 18lux150u-Crénelures présentes mais non dénombrables. 2-21 jours:
230ux197u-Ligament visible sur les 2 valves. 3-23 jours: 250ux220u-Naissance de la premiere lame primitive. 4-
41 jours: 276ux225u-Crénelures encore fonctionnelles. 5-45 jours: 290ux275u-Premiére dent bien visible.

236 M. L. M.

lame IV. Sur la valve droite les 2 lames I et
ПГ se sont formées dans 2 plans différents,
la lame Ш, au niveau des crénelures lar-
vaires, la lame I dans un plan inférieur.
Ces 2 lames sont bientót séparées par un
profond sillion.

Le ligament est de plus en plus oblique
par rapport au plateau cardinal et finit par
gagner le bord antéro-supérieur de la co-
quille. Les crénelures larvaires sont encore
visibles sur la coquille de 790 u x 670 u.

La dissoconque de 840 u x 750 и (Fig.
12) montre que sur la valve gauche la lame
primitive IV pousse perpendiculairement
au plateau cardinal en laissant une fossette
entre elle et la dent 2b, ой vient se loger la
dent 3b de la valve droite. Les dents 2a et
2b divergent dune de l'autre à partir
dune partie commune qui tend a gagner
l'umbo (coquille de 1150 их 1020 и). Dans
la fossette ainsi formée par les dents 2a et
2b vient se loger la dent I de la valve
droite. Sur la valve droite les dents 3a et 3b
forment entre elles un angle presque droit
et délimitent, avec la dent I, un profond
sillon ой viennent prendre place les dents
2a et 2b de la valve gauche.

Га coquille de 4,000 и nous montre
l'allure presque définitive de la charniere.

200 X190

LE PENNEC

Les dents semblent diverger a partir de
l'umbo, vers la base du plateau cardinal en
délimitant entre elles de profondes
fossettes.

Le ligament d'abord interne et situé
dans le prolongement des crénelures lar-
vaires a maintenant gagné le bord externe
antéro-supérieur de la coquille; il est
devenu opisthodete.

CONCLUSION

D'après les renseignements ainsi
obtenus nous pouvons dresser une cl& de
determination pour les 5 especes étudiées
(Fig. 15). Il ressort de ce tableau une
difference entre les crénelures de la char-
niere du genre Venerupis et Venus qui
permet de distinguer ces deux genres dés
les premiers stades de vie larvaire.

Chez Venerupis aurea et Venerupis
pullastra les crenelures larvaires sont
dénombrables peu de temps aprés leur for-
mation et persistent longtemps aprés Гар-
parition des premiéres dents juvéniles. On
peut encore les observer sur une coquille
ágée de 40 jours et mesurant 400 u en-
viron.

Il semble que chez Venerupis aurea le
nombre des crenelures larvaires est

FIG. 9. Venerupis pullastra—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille en-

tiere (longueur puis largeur).

CHARNIERES CHEZ VENERIDAE LARVAIRES 237

- Valve
gauche

Valve
droite

FIG. 10. Venerupis pullastra—1-10 jours: 180ux170u:Crénelures larvaires apparaissant nettement. 2-20 jours:
215ux205u:Bourgeonnement lames primitives I (V.d.) et II (V.g.): ébauches dents cardinales. Ligament visible.
3-27 jours: 364ux323u :Crénelures larvaires régressent cependant que dents cardinales se différencient.

supérieur a celui de Venerupis pullastra
(12 dans le premier cas pour 8 4 10 dans le
second cas). Ce serait donc un caractére de
différenciation de ces 2 expéces.

Chez Venus striatula, Venus verrucosa
et Venus fasciata les crénelures larvaires
forment une zone indifférenciée, le long
du plateau cardinal. Elles perdent trés vite
leur identité lors de la formation des dents
juvéniles.

Enfin, chez Venus fasciata les dis-

soconques possèdent des formations
latérales qui les différencient de celles de
Venus verrucosa et Venus striatula.

Un caractère morphologique externe
déja signalé par Rees en 1950 permet de
separer Venus verrucosa et Venus striatula:
cette derniere possede des stries de
croissance très marquèes, des la deuxiéme
semaine.

On peut supposer que l'observation des
charniéres de bivalves au microscope élec-

M: L. М. LE PENNEC

bo
C2
00

118 X 95

141 X 125

237,X 229

323 X 308

379 X 340

426 X 402

L

MN
Els SEN

FIG. 11. Venerupis aurea—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére

(longueur puis largeur)

CHARNIERES CHEZ VENERIDAE LARVAIRES 239

626 X 550 E

840X 750

1140 X1020

FIG. 12. Venerupis aurea—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére
(longueur puis largeur).

240 М. L. М. LE PENNEC

tronique а balayage permettra de se faire
une idée plus exacte sur la genése des
dents (lieu de formation, formes, dimen-
sions, nombre, etc. ). Les quelques résultats

x
x

So

que nous avons déjà obtenus confirment
cette hypothese.

Il sera alors possible, en combinant
l'étude des charniéres au microscope op-

Valve
droite

a.

y

FIG. 13. Venerupis aurea—1-5 jours: 120ux104u: Prodissoconque au stade de la charnière droite; les crénelures
larvaires se forment. 2-14 jours: 197ux181a: Crénelures facilement dénombrables. Ligament bien conservé sur
valve droite. 3-30 jours: 235ux218u: Formation premiere dent juvénile. 4-34 jours: 290ux260u: Crénelures lar-

vaires et premiere dent juvénile.

CHARNIERES CHEZ VENERIDAE LARVAIRES 241

tique et au microscope électronique а critéres les plus sûrs pour établir l'identité
balayage, de conclure que examen des des larves de bivalves récoltées dans le
charniéres des coquilles larvaires est un des plancton.

Valve gauche

FIG. 14. Venerupis aurea—5-40 jours: 370ux340u: Lame primitive 11 (У. gauche) III (У. droite). 6-60 jours:
500ux485u: Bourgeonnement lame IV sur valve gauche. 7-64 jours: 840ux750u: Les dents juvéniles grandissent.
8-70 jours: 11404x10204: Charniére juvénile totalement transformée. Les dents prennent leur allure definitive.

242 М. L. М. LE PENNEC

aprés la fécondation

36-48 heures

70-100 p

Prodissoconque de Bivalves

lére semaine
at QC) ®

Famille des Veneridae
Un trait caractéristique : épaules dissymétriques

Crénelures distinctes: Crénelures indistinctes :

Cas général

genre Venerupis genre Venus

PA

eS

Généralement 12 crénelures De 8 а 10 crénelures

Umbo proéminent : Forme globuleuse de a y

e es :

E | la coquille : Е

Venerupis aurea Venus strtatula
Venerupts pullastra

: 7
Stries de croissance Venus verrucosa

As .
seme semaine

0-400
)-400 р

5
Présence de formations
latérales: FL:

Venus fasciata
-Persistance des crénelures larvaires aprés la formation des lames primitives :
genre Venerupis.
-Disparition des crénelures larvaires lors de la formation des lames primitives :
genre Venus.

FIG.15. Clé de determination pour 5 especes de Veneridae.

CHARNIERES CHEZ VENERIDAE LARVAIRES

REFERENCES BIBLIOGRAPHIQUES

BERNARD, F., 1895-97, Sur le développe-
ment et la morphologie de la coquille chez
les lamellibranches. Bull. Soc. géol. France,
Ser. 3, 23 (1895): 104-154; 24 (1896): 54-82,
412-449; 25 (1897): 559-566.

CHANLEY, Р. E., 1965, Larval development
of the large blood clam, Noetia ponderosa
(Say). Proc. natn. Shellfish. Assoc., 56: 53-58.

CHANLEY, P. E., 1969, Larval development
of the coquina clam, Donax variabilis Say,
with a discussion of the structure of the lar-
val hinge in the Tellinacea. Bull. mar. Sci.,
19: 214-224.

LE PENNEC, M., 1970, Elevages au
laboratoire de Mollusques Bivalves:
Morphogenese de la coquille des Veneridae.
These de Зе cycle: 1-95.

LE PENNEC, M. € A. LUCAS, 1970, Com-
parative growth and morphology of some

243

Venerid larvae (Bivalvia, Veneridae).
Malacol. Rev., 3: 175-183.

LOOSANOEE V. lL.) & He С. DAVIS; 1963,
Rearing of bivalve mollusks. In: Advances in
Marine Biology. F. S. Russell, Ed., Academic
Press, Inc., London, 1: 1-136.

NEUMAYR, 1891, Beitrage zur liner
morphologischen Eintheilung dee Bivalven.
Densk. К. К. Akad. Wiss. Wien, math. nat.
cl., 58: 701-801.

REES, С. B., 1950, The identification and
classification of lamellibranch larvae. Hull
Bull. mar. Ecol., 3: 73-104.

SULLIVAN, C. B., 1948, Bivalve larvae of
Malpeque Bay, Р.Е.1. Bull. Fish. Res. Bd.
Canada, 77: 1-36.

WERNER, B., 1939, Uber die Entwicklung
und Artum terscheidung von Muschellarven
des Nordseeplanktons, unter besonderer
Berücksichtigung der Schalenentwicklung.

Zool.-Jahrb. Abt. Anat., 116(1): 1-54.

ABSTRACT
MORPHOGENESIS OF THE HINGE IN 5 SPECIES OF VENERID BIVALVES
M. L. M. Le Pennec

Laboratory culture of 5 species of Veneridae from the coast of Brittany has provided
data on the development of the hinges. Metamorphosis was accomplished by all species.
Daily observations of larval shells allowed detailed observations of the growth of the
hinge: first the notches of the prodissoconch, then formation of the first thin plates of the
dissoconch, and finally the regression of the notches. We have also noted the formation
and position of the ligament. The results have been used to construct a key for the iden-
tification of the 5 species.

The genus Venerupis is characterized, from the end of the first week, by obvious
notches whereas these remain indistinct in the genus Venus. Within the genus
Venerupis, variation in the number of notches allows one to distinguish the species:
Venerupis pullastra has 8-10, Venerupis aurea generally 12. At the end of the second
week lateral formations appear in Venus fasciata. The marked striations on the Venus
striatula shell aid recognition of this species. No particular morphological character is
applicable for Venus verrucosa.

It seems from this study that larval hinge structure is a good criterion for identification
of larval bivalves taken from the plankton. However, larval identification using this
method is not possible before establishment of the hinge which occurs at the end of the
first week.

ZUSAMMENFASSUNG

MORPHOGENESE DES SCHLOSSES BEI FUNF
MUSCHELARTEN DER FAMILIE VENERIDAE

M. L. M. Le Pennec

Laborzuchten von 5 Veneriden von der Kiiste von Brittany haben Daten zur
Schloßentwicklung erbracht. Die Metamorphose wurde von allen Arten vollständig

244

M. L. M. LE PENNEC

durchlaufen. Tägliche Beobachtung der Larvengehäuse erlaubte, das Schloßwachstum
eingehend zu verfolgen: zuerst die Einkerbung des Prodissokonchs, dann die Bildung
der ersten dünnen Dissokonch-Platten, schließlich das Verschwinden der Kerben. Auch
über Bildungsweise und Anlageort des Ligaments konnte Aufschluß gewonnen werden.
Die Ergebnisse wurden dazu verwendet, einen Schlüssel zur Identifikation der 5 Arten
aufzustellen.

Die Gattung Venerupis ist vom Ende der 1. Woche an durch auffällige Kerben
gekennzeichnet, die dagegen in der Gattung Venus undeutlich bleiben. Innerhalb der
Gattung Venerupis erlaubt die Differenzierung der Kerbenzahl die Artunterscheidung:
Venerupis pullastra hat 8-10, Venerupis aurea im allgemeinen 12. Am Ende der 2.
Woche erscheinen laterale Bildungen bei Venus fasciata. Die kräftige Streifung auf der
Schale von Venus striatula erleichtert das Erkennen dieser Spezies. Für Venus verrucosa
gibt es kein verwendbares besonderes morphologisches Kennzeichen.

Nach den vorliegenden Untersuchungen scheint der larvale Schloßbau ein geeignetes
Merkmal zur Bestimmung von Muschellarven aus Planktonfängen darzustellen. Die
Larvenbestimmung nach dieser Methode ist allerdings erst nach Anlage des Schlosses
möglich, also vom Ende der ersten Lebenswoche an.

C.M.-B.

RESUMEN

MORFOGENESIS DE LA CHARNELA EN CINCO ESPECIES DE
BIVALVOS VENERIDOS

M. L. M. Le Pennec

El cultivo en laboratorio de cinco especies de Veneridae de la costa de Bretaña
suministró datos sobre el desarollo de la charnela. Todas las especies tuvieron metamor-
fosis. Se observó diariamente en detalle, el crecimiento de la charnela de las conchillas
larvales: primero las muescas de la prodisoconcha, formación de las primeras delgadas
placas de la disoconcha, y finalmente la regresión de las muescas. Se notó también la for-
mación y posición del ligamento. Los resultados se utilizaron para construir una clave de
identificación para las cinco especies.

El género Venerupis se caracterizó, al finalizar la primera semana de desarrollo, por las
muescas muy evidentes, mientras que estas permanecieron indistintas en el género
Venus. Dentro de Venerupis, la variación en el número de muescas permite distinguir las
especies: Venerupis pullastra con 8-10, Venerupis aurea generalmente con 12. Al ter-
minar la segunda semana aparecieron, en Venus fasciata, formaciones laterales. Las mar-
cadas estrias en la concha de Venus striatula contribuyen al reconociemto de esta especie.
Ningún caracter morfologico particular es aplicable a Venus verrucosa.

Este estudio parece desmonstrar que las estructuras larvales de las charnelas, otrecen
un buen criterio para la identificación de bivalvos larvales tomados del plankton. Sin em-
bargo, tal método de identificación larval no podria usarse antes del establecimiento de la
charnela, el cual ocurre al final de la primera semana de desarrollo.

J.J.P.

CHARNIERES CHEZ VENERIDAE LARVAIRES

ABCTPAKT

МОРФОГЕНЕЗ ЗАМКА У 5 ВИДОВ МОЛЛЮСКОВ ИЗ CEM.
VENERIDAE (BIVALVIA)

М.Л. ЛЕ-ПЕННЕК

В лабораторной культуре у 5 видов двустворчатых моллюсков Veneridae с
берегов Британии были получены данные по развитию замка. У всех видов
был прослежен метаморфоз. Ежедневные наблюдения развития личиночных
раковин сопровождались детальными наблюдениями роста замка: сначала

выемок продиссоконха, затем образования первой тонкой пластинки
диссоконха и, наконец, - регрессии выемок продиссоконха. Отмечено также
образование и расположение лигамента. Полученные результаты были

использованы для ключа для определения 5 видов моллюсков. Род Venerupis
характеризуется, начиная с конца первой недели жизни, наличием заметных

выемок, которые у видов рода Venus неразвиты. Внутри рода Venerupis
изменение количества выемок имеет видовое значение: y Venus pullastra ux
8-10, у Venerupis aurea обычно 12. В конце первой недели развития у

Venus fasciata появляются слабые боковые выросты, а заметная исчерченность
раковины y Venus striatula помогает определить этот вид. У Venus verrucosa
нет никаких особых морфологических отличий.

Из этих наблюденнй выяснилось, что структура личиночного замка
является хорошим критерием для идентификации личиночных планктонных форм
двустворчатых моллюсков. Однако, определение этим методом видов на
личиночной стадии возможно лишь после образования замка, в конце первой
недели жизни.

Zi AT:

245

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Oly HAVAADEMUAIA MOST PRE ТАУ

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| N а’ ak
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MALACOLOGIA, 1973, 12(2): 247-263

EFFECT OF CARBONIC ANHYDRASE INHIBITION
PENETRATION
BY THE MURICID GASTROPOD UROSALPINX CINEREA

ОМ SHELL

Melbourne В. Carriker! and Howard H. Chauncey?

ABSTRACT

A study was made of the effect of a series of concentrations of DiamoxR(2-acetylamine-
1,3,4-thiadiazole-5-sulfonamide), a specific inhibitor of the enzyme carbonic anhydrase
(CA), on the penetration of shell of the oyster Crassostrea virginica by the boring
muricid gastropod Urosalpinx cinerea follyensis. Forty-five initially boring snails con-
tinued boring and fed on oysters in Diamox solutions ranging in concentration from 5x-
10-4M to 1x10°2M. Forty-five initially nonboring snails identified, mounted, and began
penetration in the same range of concentrations. Snails were able to complete boreholes
and to feed in concentrations up to 5х10-3М.

The total number of complete boreholes decreased by 2/3 while the total number of
incomplete holes almost doubled with increasing concentrations of Diamox during the 6
day experiment. All 90 snails survived the 6 days, as well as an additional month in nor-
mal running seawater where they bored and fed actively.

Blots of secretion collected from active accessory boring organs (ABO) of live snails on
a valve model, as well as secretion released by the ABO in the ABO pore, were positive
for CA when tested by histochemical techniques. Treatment with Diamox inhibited the
CA in both.

Control halves of ABOs, excised from actively boring snails, etched polished shell,
while increasing concentrations of Diamox applied to the experimental half of these
ABOs, increasingly reduced etching. In the 5х10-3М and 1х10-2М solutions the etching
was almost totally inhibited. A suspension of pure bovine erythrocyte CA in seawater
produced no etching of shell.

These experiments indicate that CA plays a vital role in shell dissolution during boring
by this species of snail, but do not confirm its function as a direct demineralizing agent.

INTRODUCTION

The calcareous exoskeleton of bivalves
such as Crassostrea virginica (Gmelin) and
Mytilus edulis Linné can be penetrated by
many marine invertebrate predators
(Carriker & Smith, 1969). The penetrating
behavior of one, Urosalpinx cinerea (Say),
has been described (Carriker, 1969;
Carriker & Van Zandt, 1972).

The shell of the bivalve prey of
Urosalpinx cinerea consists of calcium car-
bonate in the form of calcite and aragonite
crystals embedded in organic matrices
(Travis & Gonsalves, 1969; Mutvei, 1969,
1970; Taylor, Kennedy & Hall, 1969).

As currently understood, boring in-
volves a chemical phase followed by a
mechanical phase. During the chemical
phase the accessory boring organ (ABO) is
extended into the borehole and secretes a
substance that dissolves a thin layer of the
shell. In the mechanical phase the pro-
boscis is extended into the borehole and
the bottom is briefly rasped by the radula.
The weakened shell removed by the
radular cusps is then swallowed by the
snail. By repeated alternation of chemical
activity and mechanical rasping, the snail
penetrates the shell of its prey, inserts its
proboscis and initiates feeding on the soft
tissues within.

ISystematics-Ecology Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, U.S.A.—Pre-
sent address: College of Marine Studies, Field Station, University of Delaware, Lewes, Delaware 19958, U.S.A.
2Veterans Administration Center, Bay Pines, Florida 33504, U.S.A.

(247)

248 CARRIKER AND CHAUNCEY

Various hypotheses have been offered to
explain the chemical phase of shell
penetration. These include solubilization
by acids, proteolytic enzymes, and
chelating substances (Carriker, Scott &
Martin, 1963; Carriker € Smith, 1969).
The histochemical localization of cyto-
chrome oxidase and succinic dehydro-
genase in the secretory epithelium of the
ABO has provided an indication that these
cells can metabolize aerobically (Person et
al., 1967). In addition these cells contain
dense populations of mitochondria (Nylen,
Provenza & Carriker, 1969), and the secre-
tion in actively boring snails has a pH of
approximately 3.8 (Carriker, Charlton &
Van Zandt, 1967). Since carbonic
anhydrase is involved in aerobic respira-
tion and is responsible for the formation of
hydrochloric acid in human gastric
mucosa, we assumed that carbonic
anhydrase should be present.

Subsequently, Smarsh et al. (1969)
demonstrated carbonic anhydrase activity
in the microvillar zone of the ABO in both
actively boring and inactive snails. Histo-
chemical localization of carbonic
anhydrase revealed that the secretory
epithelium of the ABO exhibited very high
activity, in contrast to tissues such as con-
nective tissue of the ABO stalk, the buccal
mucosa, and the esophagus. Only the car-
tilages of the odontophore, the mantle,
and certain muscle groups of the proboscis
showed nearly comparable activity. The
addition of DiamoxR (2-acetylamine-1,3,4-
thiadiazole-5-sulfonamide) in concen-
trations as low as 2x10-5M inhibited the
carbonic anhydrase activity.

In vitro chemical assay of carbonic
anhydrase and total nonspecific esterase
activities in homogenates of the ABO of
Urosalpinx cinerea were carried out
(Carriker et al., 1968). Samples from 60
nonboring, 75 boring, and 60 feeding
snails were evaluated. Alpha naphthol
acetate was used as substrate for non-
specific esterase, and Diamox inhibition
was used to reveal carbonic anhydrase ac-
tivity. Specific enzyme reactivity was

recorded in nanomoles/min/mg of pro-
tein. Carbonic anhydrase activity was es-
sentially identical for each of the 3 groups,
being 0.88+0.11, 1.04+0.10, and 0.95+0.01,
respectively. Preliminary results of
differential centrifugation studies т-
volving isolation of a 30,000 xg pellet, a
105,000 xg pellet, and the 105,000 xg
supernatant fluid indicated that most of
the carbonic anhydrase and nonspecific es-
terase activities were present in the 105,-
000 xg supernatant fluid.

The presence of carbonic anhydrase ac-
tivity in the ABO suggested that this en-
zyme might be a responsible factor in the
production of certain substances used in
the chemical phase of shell penetration by
Urosalpinx cinerea. The purpose of this
paper is to report the effect of Diamox, a
specific inhibitor of carbonic anhydrase,
on the penetration of shell by live boring
U. cinerea; the presence of carbonic
anhydrase in the ABO secretion after its
normal release by the gland; the effect of
Diamox on etching of polished shell by the
excised ABO; and the action of pure car-
bonic anhydrase on polished shell. The
study, begun in the summer of 1967, was
carried out at the Marine Biological
Laboratory, Woods Hole (Carriker, 1967).

MATERIALS AND METHODS

The following experiment was con-
ducted to determine the effect of a graded
series of Diamox? concentrations on the
capacity of living snails (Urosalpinx
cinerea follyensis Baker) to identify,
mount, bore, and feed on _ oysters
(Crassostrea virginica(Gmelin)).The snails
were collected in Wachapreague, Virginia.
They had been maintained in our
laboratory for several weeks in running
seawater, and fed local oysters. Ninety
snails, 28-40 mm in shell height, and 15
clean oysters, 6-8 ст long, were divided
into 5 groups containing 18 snails and 3
oysters each. Each group contained 9 bor-
ing snails, 3 per oyster, and 9 nonboring
snails, in a continuously aerated clean glass
dish 20 ст in diameter (Figs. 1, 2).

3 Diamox supplied by Lederle Laboratories Division, American Cyamid Co., Pearl River, New Jersey.

INHIBITION OF SHELL PENETRATION BY UROSALPINX 249

FIG. 1. Arrangement of 5 aerated covered dishes in running seawater of relatively constant temperature (about
20С) used in study of effect of graded series of concentrations of Diamox on the capacity of live Urosalpinx
cinerea follyensis to identify, mount, bore, and feed on Crassostrea virginica. Each dish 20 cm in diameter.

FIG. 2. Positions of marked Urosalpinx cinerea follyensis and Crassostrea virginica in one of the dishes
photographed in Fig. 1.

250 CARRIKER AND CHAUNCEY

To obtain boring snails, we placed
oysters in the stock tank of snails 36 hours
prior to the experiment. At the time of
transfer all but 3 of the snails which had
mounted and were boring were removed
from each oyster. Nonboring snails were
those which neither had been boring nor
feeding, but were crawling on the sides of
the stock tank. They were identified by a
mark on the shell spire, and placed at ran-
dom on the bottom of each bowl.

The following concentrations of
Diamox, in clear unfiltered seawater, were
employed: 5х10-4М, 1х10- 3M, 5х10-3М,
and 1х10-?М. The final pH of the sea-
water solution was adjusted to 8.10+0.02
with 0.1N HCl. It was calculated that the
resultant NaCl formed by HCl neutraliza-
tion of the sodium hydroxide in the con-
centrated Diamox solution did not
significantly alter the salinity (from 320/00
to 330/00) of the test solutions. The sea-
water control (pH 8.12) contained neither
Diamox nor HCl. One liter of solution was
placed in each of the 5 dishes. Aeration by
bubbling was carefully controlled in each
dish to maintain a uniform level of oxygen
and permit normal oxidation of
metabolites released by the oysters and
snails. The dishes, loosely covered with
glass plates to keep the snails from crawl-
ing out, were immersed in a shallow tray of
running seawater at approximately 20°C
(Fig. 1). Throughout the day, and oc-
casionally in the early evening, fluorescent
light illuminated the experiment.

On day 3 the solutions were replaced us-
ing clean dishes. The experiment was ter-
minated after 6 days. A daily record of the
number of nonboring and boring snails on
each oyster, and whether the oysters were
closed or pumping, was maintained. At the
termination of the experiment the snails
from each dish were placed in separate
perforated plastic cages containing fresh
oysters. Similarly, the nonpenetrated
oysters, as well as the penetrated but still
viable oysters, were placed in perforated
cages. The cages were immersed in run-
ning seawater. This was done to determine
the rate of recovery and ability of the snails
to bore after the Diamox treatment. The

live oysters were continuously observed to
note their recovery, or expiration due to
penetration injury.

The series of Diamox concentrations
used was based on the concentration re-
quired to inhibit reactivity of carbonic
anhydrase in frozen sections of snail tissue
for a minimum of 3 hours (Smarsh et al.,
1969). In preliminary tests in nonaerated
seawater we noted that boring was prac-
tically nonexistent, even in the seawater
control, while a final Diamox concentra-
tion of 5x10 2M, first inactivated and then
proved lethal to both snails and oysters. It
was also observed that if filtered
(Millipore) seawater was used none of the
nonboring snails mounted or bored
oysters. For these reasons unfiltered
aerated seawater was used.

The presence of carbonic anhydrase in
the ABO secretion, after its release from
the gland, was investigated both with
specimens of secretion collected using a
valve model and with frozen sections of
snail pedal tissue.

For the collection of specimens of secre-
tion, we allowed a snail to penetrate ap-
proximately halfway through the shell of
an oyster. Then the opposing oyster valve
and the flesh were removed underwater.
Next the valve and snail were inverted and
supported in running seawater under a
binocular microscope (Carriker € Van
Zandt, 1972). When the snail penetrated
the upturned inner surface of the valve
and the borehole was of sufficient
diameter to allow the ABO to extrude, but
was not wide enough to accommodate the
full proboscis, we elevated the valve model
until its inner face was above the water.
Seawater remaining around the borehole
was thoroughly removed Бу blotting.
Under these conditions the snail main-
tained the ABO in the borehole and con-
tinued to secrete fluid. A small wedge of
cellulose acetate Millipore filter paper (Зи
pore size) was placed on the crown of the
exposed ABO to absorb the thin layer of
secretion. The filter paper was then air
dried at room temperature for 20 min.
Representative specimens were taken from
several snails. The sections of filter paper,

INHIBITION OF SHELL PENETRATION BY UROSALPINX 251

unfixed, but air dried, were then processed
for carbonic anhydrase activity (Smarsh et
al., 1969).

For the demonstration of carbonic
anhydrase in the ABO pore, we removed a
cube of pedal tissue surrounding the with-
drawn ABO after the shell was cracked and
the foot amputated. Unfixed frozen sec-
tions of the cube, cut 9-12u thick in a
cryostat, were placed on filter paper and
tested for carbonic anhydrase by a
modification of Häuslers (1958) tech-
nique (Smarsh et al., 1969). Sections from
several snails were examined. Inhibition
by Diamox, in a concentration of 2x10-5M,
was used as a confirmatory test for the
presence of carbonic anhydrase, both for
the secretion collected and the material
within the ABO pore.

To study the effect of Diamox on the
etching capacity of excised ABOs, we em-
ployed a device (Fig. 5) patterned after an
earlier model (Carriker € Van Zandt,
1964). The ABO was excised from large,
actively boring Urosalpinx cinerea in the
manner described by Carriker et al. (1963).
It was then placed in a drop of seawater on
a teflon block, and cut into 2 equal parts.
One half was placed in seawater while the
other half was put in seawater-Diamox
solution for either 5 or 10 min. The con-
centrations of Diamox used were: 5x-
10-4M, 1х10-3М, 5х10-3М, and 1х10-2М.
ABO halves were then transferred in а
drop of seawater or Diamox solution to a
small piece of plastic plankton cloth (pore
size approximately 854) which was overly-
ing the inner nacreous surface of a square
of polished surf clam (Spisula solidissima)
shell. The ABO sections were then covered
with a disk of thin plastic membrane. A
minute collar of lead weighted the edge of
the membrane. This membrane kept the
gland moist and pressed it gently against
the underlying cloth screen which allowed
the secretion expressed from the gland to
contact the surface of the shell.

The gland-shell preparation was held in
a moist chamber at room temperature for
21 hrs. During this time pressure from the
taut plastic membrane and relaxation of
the half gland caused it to spread to about

twice its original diameter (0.5 to 0.8 mm).
At the end of the incubation period, the
half ABO was flushed from the shell with
seawater, and the shell surface quickly
rinsed with distilled water and rapidly
dried with a stream of air. The etched sur-
face was then coated in vacuum with gold
and subsequently examined as well as
photographed with the light microscope
and with a scanning electron microscope
(JEOLCO JSM-U3).

The action of pure carbonic anhydrase
on polished shell was demonstrated as
follows: one end of a 6 mm section of intra-
medic polyethylene tubing with an inter-
nal diameter of 6 mm was fastened to the
surface of a polished shell with a thin layer
of Dow Corning high vacuum grease. Ten
sections were thus secured to squares of
polished shell. Care was taken to insure
that the shell surface within the diameter
of the tube was free of grease. Three drops
of filtered fresh seawater were pipetted
into 5 tube sections as controls, while 3
drops of a freshly prepared seawater solu-
tion of carbonic anhydrase, from bovine
erythrocytes (Mann Biochemicals) con-
taining 1 mg/ml (pH 8.15), were added to
each of the remaining tube sections. The
outer end of each section was then covered
with a disk of plastic membrane to control
evaporation.

After incubation at room temperature
for 18.5 hrs., the tube sections were remov-
ed and the shell surface was rapidly wash-
ed with distilled water. The surface was
then immediately dried with a stream of
air and examined with direct as well as
polarized incident light at 200 and 400
magnifications.

RESULTS

Effect of Diamox on boring. None of the
snails, or oysters which escaped pene-
tration, died during the 6 day experiment.
Daily checks of the oysters showed that
some were open in all solutions of Diamox.
Two oysters which gaped after being
bored, 1 in the seawater control and 1 in
the 1x10°3M Diamox, were completely de-
fleshed by feeding snails.

The number of initially boring snails

bo

52

which remained on oysters, as well as the
number of initially nonboring snails which
mounted oysters and remained mounted,
decreased with time (Table 1). The 6-day
cumulative number of initially boring
snails on oysters did not vary in accordance
with different Diamox concentrations in
each of the 5 containers. In contrast the
cumulative number of initially nonboring
snails decreased slightly with increasing
concentrations of Diamox.

The total number of boreholes, both in-
complete and complete, on the valves of
the 3 oysters in each dish was 14+2. While
the total number of boreholes per dish was
not significantly different, the ratio of
completed to incompleted boreholes in the
control versus the Diamox solutions was
quite different. Whereas the seawater con-
trol and the 5x10°*M and 1х19-3М
Diamox solutions had an equal or greater
number of complete holes than incomplete
holes, the 5х10-3М and the 1x10-2M
solutions of Diamox had 2x and 4x as many
incomplete holes as complete holes,
respectively.

The data indicate that an average of 78%
of the initially boring snails in the 4

TABLE 1.

CARRIKER AND CHAUNCEY

Diamox solutions continued boring, while
67% of the initially boring snails in the
seawater control dish remained boring. On
the other hand, only 47% of the initially
nonboring snails in the Diamox solutions
mounted and remained mounted, while
67% of the initially nonboring snails in the
seawater control were mounted.

The 90 snails employed in the experi-
ment all survived for the next month, dur-
ing which they bored and fed actively on
small oysters, mussels, and surf clams.

Viability and recovery of oysters in each
of the concentrations of Diamox in sea-
water were as follows:

5x10~4M. Out of 3 oysters, 2 had 3 com-
plete boreholes and 1 had 2 complete
holes. All 3 oysters were alive at the ter-
mination of the study, but died within 7
days after being placed in running sea-
water.

1x10°3M. One of the 3 oysters con-
tained 4 complete boreholes and was con-
sumed during the experimental period.
The 2nd oyster, with 1 complete hole, died
2 days after isolation in running seawater,
while the remaining oyster, which had 2
holes, died after 30 days.

Effect of Diamox solution on shell penetration by live Urosalpinx cinerea. Three oysters

and 18 snails per dish, initially 9 boring snails (on oysters) and 9 nonboring snails.

Cumu-
Ps No. snails on lative No. boreholes in oyster shells
Diamox Initial к É ers LES Cis
; be oysters per day по. snails after 6 days
concentration activity Е E
of snails Sen я
а 1 2 3 4 5 6 ters in Incomplete Complete Total
6 days
Seawater Boring Во. 6 "107225 36 1 9 16
Nonboring Tt MG) ES A Wat) att! 36
0.0005M Boring eh. OS tor le) 46 4 5 12
Nonboring COTTON об 37
0.001 M Boring Ta” a ee Oe a? 37 7 7 14
Nonboring NIDO AI 5 ИЗ 29
0.005 M Boring OIE SS IH 46 10 5 15
Nonboring Bea On Ar 24
0.01M Boring rl 515 40 11 3 14
Nonboring 6 1 1 7 29 13
Total Boring 40’ 40°86 °86 31722
Nonboring 29 25 24 19 18

24

a a - р 3
Indicates number from maximum of 9.

b One of the oysters gaping, snails feeding on it; flesh removed by following day.

INHIBITION OF SHELL PENETRATION BY UROSALPINX 253

wedge

C/7

FIG. 3. Sketch of a blot of secretion from the accessory boring organ of Urosalpinx cinerea follyensis on a wedge
of Millipore paper demonstrating reactivity of carbonic anhydrase (CA), black granules, by Hiusler’s test.

Diameter of blot about 1.5 mm.

ИВО SIRUS
120)

ИВО stalk

ProPOoIIUM

ABO pore

CA

FIG. 4. Diagram of a frozen median sagittal section of the accessory boring organ of a male Urosalpinx cinerea
follyensis, cut from a cube of pedal tissue, demonstrating reactivity of carbonic anhydrase (CA), black granules,
in secretion released by the accessory boring organ into the pore and outside the foot onto the supporting paper.
Háusler's test. Accessory boring organ about 1 mm wide.

5x10 3M. One oyster which contained
only 1 newly completed borehole survived
beyond the 30 day holding period. Of the
2 other oysters, with 2 holes each, 1 sur-
vived for 7 days while the other died 14
days after isolation.

1x10°2M. Only 2 oysters contained com-
plete boreholes, and 1 had 2 newly com-
pleted holes. This latter oyster and the one
which was not penetrated survived
throughout the 30 day recovery period.
The remaining oyster, with 1 complete
hole, died 3 days after termination of the
test period.

Seawater control. The 3 oysters in this
container each had 3 complete boreholes.

Two oysters died during the experimental
period, and the 3rd died 3 days after isola-
tion.

Release of carbonic anhydrase in ABO
secretion. The specimens of ABO secre-
tion collected with Millipore paper and in-
cubated in Háusler's substrate were all
distinctly positive. The dried secretion
which initially was a light watery-cream
color exhibited a vivid black granular
deposit (Fig. 3). Treatment of represen-
tative specimens with 2x10 5M Diamox
completely inhibited activity.

The material present in the ABO
vestibule and pore also showed a positive
carbonic anhydrase reaction. Black

254 CARRIKER AND CHAUNCEY

granules were conspicuously present
within the vestibule, adjacent to the
secretory eqithelium of the ABO, and on
the paper outside the pore (Fig. 4). Activi-
ty was inhibited by 2х10-5М Diamox.

Effect of Diamox on etching by excised
ABOs. The ABO halves excised from ac-
tively boring snails and tested in seawater
etched the polished surface of shell from
Spisula solidissima (Figs. 6, 7). The degree
of etching varied from very deep to a trace
(Table 2). The same variability of etching
by whole excised ABOs, from both boring
and nonboring snails, was observed
previously (Carriker et al., 1963). Thus the
variability observed in the experiment was
not attributed to dissecting the glands. In
5x10°-4M Diamox the half ABOs etched
slightly more conspicuously than in the
seawater controls, while in the 1x10°3M
Diamox etching activity was reduced ap-
proximately by half. In the 5х10-3М and
1x10°2M Diamox solutions only a faint
trace of etching was evident.

Action of pure carbonic anhydrase on
polished shell. No etching of the shell sur-
face was visible either with the seawater or
the carbonic anhydrase solution at
magnifications up to 400X.

DISCUSSION

The current investigation revealed that
initially boring Urosalpinx cinerea were
able to continue boring and feed on oysters
in concentrations of Diamox ranging from
5x10-4M to 1x10°2M, while initially in-
active snails, to a lesser degree, were able
to identify, mount, bore, and feed on

oysters in all but the highest Diamox con-
centration. In addition, the number of
complete boreholes decreased, while the
number of incomplete holes increased,
with increasing concentrations of Diamox.
However, the cumulative number of bore-
holes, complete as well as incomplete, was
quite constant for the seawater control and
4 Diamox solutions.

The observation that initially inactive
snails mounted and bored oysters would
seem to indicate that the oysters were ac-
tive, at least for a time, since snails usually
will not mount and bore closed oysters
(Carriker & Van Zandt, 1972). The aban-
donment of oysters by a few of the initially
boring snails, after transfer to the dishes,
was probably due to the mechanical dis-
turbance. Certain of the initially inactive
snails never mounted oysters. This is often
the case with inactive or nonboring snails,
probably because they are not hungry.
Furthermore, oysters with almost no food,
as was the case in the containers, soon
become less attractive to resting snails.
This may also explain, in part, why few
snails mounted oysters after the experi-
ment was in progress.

The occasional movement of snails on
and off oysters accounted for the apparent
disparity between the total number
(complete plus incomplete) of holes in
oyster valves in each container and the
total number of mounted snails (initially
active plus initially inactive) on oysters in
the same dish on any given day. The fact
that most initially inactive snails which
had mounted oysters crawled off by the

BG

RY OF 2218

collar

membrane

seawaler

FIG. 5. Diagram of the cross section of a square of polished shell of Spisula solidissima and accessories used to
test etching (dissolution) by an excised half accessory boring organ of Urosalpinx cinerea follyensis. Long dimen-
sion of shell, 20 mm. Half accessory boring organ spread to about 2 mm.

255

INHIBITION OF SHELL PENETRATION BY UROSALPINX

т ++++ ZI
F ++++ Il
т ++++ OI
т +++++ 6

a +++++ 8

0 = L

++ ++++ 9

++ ++++ с

+ ++ р

++++ +++ 8

++++ +++ 7

++++ +++ |
W100 19JEMPIS N£00'0 19JEMB9S W000 JOVLMLIS WS000'0 19]PMBOS OAV
‘ON

SUOHNIOS XOUIBI( ит pue [043402 19JBMBIS ur SOGY JPY Aq Buryoja JO ээл8эр pur хоше JO иоцезиэриоо)

‘sIY [5 10} эт]елэ4шэ} WOO! ye [Joys UO poyeqnoul uy)
‘шит ОТ 10} UOTNIOS XOUIBI( ur pod элэм SOGY JPY [в}иэцилэах ‘++ +++ d99p Алэл ‘+ +++ 4ээр ‘+++ эзвлэрош ‘+ + 3431 ‘+ 1481]
Алэл “F 99.1 ‘0 9UOU :SOGY J[ey Aq Buryoja Jo asuey “SOU V Fey pastoxa Aq |Jays paystpod Jo 3uryoja uo чоци[оз хошес( JO 99 YA A'IAVL

256 CARRIKER AND CHAUNCEY

FIG. 6. Pattern of dissolution of polished shell of Spisula solidissima produced by half an excised accessory bor-
ing organ of Urosalpinx cinerea follyensis. Darkest areas represent deepest etching. Maximum dimension of

etching, 3 mm. Light micrograph.

2nd day in the highest concentration of
Diamox suggests that at least the higher
concentrations may have caused snails to
abandon oysters and their boreholes. This
may have been responsible for the inverse
trend in the number of complete to incom-
plete boreholes associated with increasing
concentrations of Diamox.

Nothing, however, is known of the
effect of Diamox on the overall physiology
of snails. If Diamox had inhibited hole bor-
ing by seriously affecting the snails, they
might not have bored at all in concen-
trations of 5x10-3M and above—which
was not the case.

An explanation for the inverse trend in
the number of completed boreholes is
suggested by the results of the experiments
with the pure secretion and the excised
ABOs where it was shown that the secre-
tion from normally functioning ABOs as
well as excised ABOs contained carbonic
anhydrase and etched shell. Diamox in-
hibited carbonic anhydrase activity in the
released secretion, and also inhibited
etching of polished shell by excised half
ABOs even though a purified solution of
bovine erythrocyte carbonic anhydrase
itself did not affect the shell.

It has been reported that shell penetra-
tion by Urosalpinx cinerea consists of rasp-

ing on the chemically weakened shell at
the bottom of the incomplete borehole,
followed by passage of the middle portion
of the propodium across the bottom of the
hole and insertion of the ABO for further
chemical dissolution (Carriker € Van
Zandt, 1972). During rasping, seawater
passes around the proboscis and enters the
borehole. The propodium, however,
presses the seawater out of the hole prior
to insertion of the ABO. The effectiveness
of the propodium appears to vary among
snails and some seawater may remain in
the incomplete borehole. Any residual
Diamox solution in the hole could inhibit
the shell dissolving properties of the
released secretion and/or be absorbed into
the ABO to inhibit reactivity of carbonic
anhydrase in the secretory epithelium. In
either case, the result would be a decelera-
tion of shell penetration, the rate of boring
decreasing with the extent of exclusion of
seawater-Diamox by the propodium, and
with increasing concentrations of Diamox.
Thus behavioral elimination of seawater
from the borehole by the propodium
might be responsible, at least in part, for
the decrease in the number of complete
boreholes and the increase in the number
of incomplete holes, as well as the varia-
tion in the time of completion of holes in a

FIG. 7. Scanning electron micrographs of the pattern of dissolution of the surface of polished shell of Spisula
solidissima etched by the secretion of half an accessory boring organ of Urosalpinx cinerea follyensis. Shell sur-
face was coated with gold in vacuum prior to examination in the scanning electron microscope. 10,000X.

Top. Normal polished surface of the shell. The diagonal scratch line was cut by grit on the wet silicon carbide
paper during polishing of the surface. The minute nodular structures are part of the morphology of the shell.

INHIBITION OF SHELL PENETRATION BY UROSALPINX 257

, ь ® are WERT Las >
> a or y AS
EWR hat na

Middle. Moderately etched surface. The secretion dissolved the outside of most of the nodules bringing them
into strong relief, and more deeply etched clusters of them leaving deep interstices. The slightly darker central
portion of the micrograph represents minimal dissolution.

Bottom. Example of the most deeply etched shell surface. The nodular units are still distinctive, irregular clusters
of them exaggerated by deep dissolution resulting in a complex spongelike appearance.

258 CARRIKER AND CHAUNCEY

given concentration of Diamox seen with
increasing concentrations of Diamox.

The presence of carbonic anhydrase in
bivalve mantles has been demonstrated
previously (Maetz, 1946; Freeman &
Wilbur, 1948; Stolkowski, 1951). Wilbur &
Jodrey (1955) indicated that Diamox in-
terferes with calcium translocation in the
oyster. In studies of the electric potential
in clam mantle, Istin & Kirschner (1968)
presented a model equation which incor-
porates observed potential differences and
calcium movement across membranes.
They indicated that when the СО? tension
is increased and the pH is thus decreased,
the concentration of ionized calcium is in-
creased. These authors noted that the in-
crease in transmantle potential differences
associated with rising concentrations of
СО? was lowered by the addition of
Diamox. Since carbonic anhydrase is
necessary for the hydration of COz, they
believe that this enzyme plays an impor-
tant role in transmembrane calcium flux.
In view of the presence of enzymes in-
volved in aerobic metabolism in the ABO
(Person et al., 1967), it is possible that
metabolic COz production by this gland
may regulate its ability ultimately to
solubilize calcareous substrates.

Some controversy still exists regarding
the use of the inhibitory action of low con-
centrations of Diamox (1x10~>M) in histo-
chemical techniques for confirmation of
the presence of carbonic anhydrase
(Muther. 1972). However, recent studies
dealing with carbonic anhydrase, the sul-
fonamides, and calcium flux have in-
dicated that 1x10-5M acetozolamide and
1x10-$M methazolamide will inhibit para-
thyroid hormone-induced resorption of
bone in organ culture (Minkin & Jennings,
1972). Studies of this nature thus tend to
confirm the validity of the histochemical
localization of carbonic anhydrase and
provide an in vitro mammalian counter-
part to our findings in the marine environ-
ment. The importance of carbonic
anhydrase in controlling the calcium con-
tent of body fluids and tissues continues to
be investigated (Chauncey & Weiss, 1958;
Kenny, 1972; Nielsen & Frieden, 1972).

It has been demonstrated (Dugal, 1939)
that aerobic conditions are requisite for the
deposition of shell calcium by mantle. We
have observed that Urosalpinx cinerea is
capable of active penetration of shell only
under aerobic conditions. If we
hypothesize that the ABO epithelium acts
by producing a secretion which contains
water, carbonic anhydrase, and CO», this
secretion would be acidic and have the
capacity to solubilize calcium carbonate.
That the secretion is acidic has already

been demonstrated (Carriker et al., 1967).
However, Pigman, Feagin & Walker
(1970) have indicated that the

bicarbonate-carbonate system, and
specifically bicarbonate ions, can be re-
sponsible for decalcification even at pH
values above neutrality. This might ex-
plain the ability of excised ABOs to etch
polished shell at alkaline pH values
(Carriker et al., 1963, 1967).

CONCLUSIONS

The present study is part of a continuing
effort to describe the mechanism of shell
penetration by boring gastropods and
other shell penetrating organisms, and the
role of this mechanism in the behavioral
ecology of these species. By histochemical
techniques we found high carbonic
anhydrase reactivity in the ABO of
Urosalpinx cinerea. Differential ultra-
centrifugation of an homogenate of excis-
ed ABOs indicated that the major portion
of the carbonic anhydrase was in soluble
form. We previously observed that an
acetone-insoluble cation-binding granular
material was present in the ABO microvilli
which may function to chelate the calcium
of the shell into a water-soluble complex
for rapid removal. This hypothesis was
strengthened by our observation in the
ABO of microbodies which contain soluble
calcium (Smarsh et al., 1969).

Our observations that hole boring
decreased in increasing concentrations of
Diamox are corroborated by Chétail and
associates in the French muricid snail
Thais lapillus. Chetail & Binot (1967) and
Chetail & Fournié (1969) found carbonic
anhydrase in both active and inactive

INHIBITION OF SHELL PENETRATION BY UROSALPINX 259

ABOs of this snail, and later demonstrated
an increase of calcium ions in the ABO
during active shell penetration (Chétail &
Fournié, 1970). They demonstrated, by a
manometric method, using ABO homo-
genates of T. lapillus, that although car-
bonic anhydrase is always present in both
boring and inactive glands, it is present in
variable amounts. Tests of fluid outside of
whole ABOs by the same method in a sub-
strate made isotonic with mannitol were
negative, which was taken to indicate that
carbonic anhydrase was found only intra-
cellularly. In experiments with live snails
held in closed seawater aquaria, in con-
centrations of Diamox ranging from 1x-
10-3М to 7x10°3M, for 4 weeks, they
found that at low concentrations the num-
ber of complete holes drilled decreased or
disappeared while the number of in-
complete holes increased. At 5x10~3M and
above, full inhibition of boring took place
(Rossenberg, Chétail & Fournié, 1968;
Chétail & Fournié, 1969). In another ex-
periment, where they bubbled a mixture
of 5% СО? and 95% Oz through the sea-
water the rate of boring increased two fold.
This reinforced their conclusion that car-
bonic anhydrase in the ABO of T. lapillus
“is responsible for dissolution of СаСОз”
(Chétail & Fournié, 1969).

We demonstrated greater reactivity in
both active and inactive ABOs of
Urosalpinx cinerea than in adjacent secre-
tory tissues (Smarsh et al., 1969), and in
this paper we report the presence of car-
bonic anhydrase in the released secretion
of the ABO and inhibition by Diamox of
shell dissolution by live snails and excised
ABOs. These results support our earlier
suggestion of a vital role of this enzyme in
shell dissolution during boring by this snail
and provide support for Chétail et al.’s
(1969) statement of a similar role for the
enzyme in shell boring Thais lapillus. It
appears unlikely, however, that the car-
bonic anhydrase functions as a direct
demineralizing agent.

Carbonic anhydrase has been im-
plicated in dissolution of shell by 2
different genera of boring gastropods and
by a species of burrowing barnacle (Tur-

quier, 1968). Whether carbonic anhydrase
is involved in the dissolution of calcareous
substrata by the many other calcibio-
cavites already known (Carriker & Smith,
1969) remains to be determined.

Because of its ravage, especially of
young oysters, Urosalpinx cinerea has been
of concern to oyster farmers in the United
States for at least the last 100 years. These
snails apparently became а serious
problem concurrently with the develop-
ment of widespread transplantation and
cultivation of oysters (Carriker, 1955).
Plantings in other parts of the world are
plagued by other species. U. cinerea has so
far resisted efforts to control it. Recogni-
tion of the importance of carbonic
anhydrase and the oxidative enzymes in
shell boring may lead to methods of con-
trolling this and other predatory muricid
gastropods.

ACKNOWLEDGEMENTS

Anne Smarsh conducted the histo-
chemical phase of the study and tested the
ABO secretion blots for CA. Dirk Van
Zandt assisted in the overall study, and
took the light photomicrographs. The
scanning electron microscopy was done in
collaboration with Dr. Virginia Peters. The
live Urosalpinx cinerea follyensis were
supplied by Michael Castagna. We are
grateful to these persons for their generous
belp, and to Dr. Philip Person for sug-
gestions and review of the manuscript.

The research was supported by Public
Health Service Research Grant DE 01870
from the National Institute of Dental Re-
search and by the Veterans Administra-
tion.

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260 CARRIKER AND CHAUNCEY

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NYLEN, М. U., РВОУЕМАА , DE
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PERSON, Р., SMARSH, A., LIPSON, 5. J. &
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INHIBITION OF SHELL PENETRATION BY UROSALPINX 261

Aerobic and related oxidative systems. Biol.
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ROSENBERG, А, CHETAIE, М... &
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TAYLOR} 0. (KENNEDY, №. Jo& HALL;
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Comparative ultrastructure and organization
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WILBUR, K. M. & JODREY, L. H., 1955, The
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365.

ZUSAMMENFASSUNG

DIE AUSWIRKUNG EINER CARBOANHYDRASE-HEMMUNG AUF DIE
SCHALENBOHRFAHIGKEIT DER MURICIDE UROSALPINX CINEREA

M. R. Carriker und H. H. Chauncey

Uber die Auswirkung einer Reihe von Konzentrationen von Diamox (2-Acetylamin-
1,3,4-thiadiazol-5-sulfonamid), eines spezifischen Hemmers des Enzyms Car-
boanhydrase (CA), auf die Bohrleistung der bohrenden Muricide Urosalpinx cinerea
follyensis an der Schale der Auster Crassostrea virginica wurde eine Untersuchung
ausgeführt. 45 zu Versuchsbeginn bohrende Schnecken bohrten und frassen an Austern
weiter, wenn sie in Diamox-Lósungen von Konzentrationen zwischen 5x107*M und
1х10-2М verbracht wurden. 45 zu Versuchsbeginn nicht bohrende Schnecken erkannten
die Beutetiere in demselben Bereich von Konzentrationen, krochen auf sie hinauf und
bohrten sie an. Die Schnecken waren in der Lage, in Konzentrationen bis hinauf zu
5x10°3M Löcher fertigzubohren und Austern anzufressen.

Während des sechstägigen Experiments nahm die Gesamtzahl fertiger Bohrlöcher mit
steigender Diamox-Konzentration um 2/3 ab, während die Gesamtzahl nicht vol-
lendeter Löcher sich verdoppelte. Alle 90 Schnecken überlebten die 6 Tage sowie auch
einen weiteren Monat in normalem fliessenden Meerwasser unter emsigem Bohren und

Fressen.

Sekret, das von tätigen accessorischen Bohrorganen (ABO) lebender Schnecken auf
einem Schalenmodell abgetupft wurde, wie auch solches, das aus dem ABO-Porus
austrat, reagierte in histochemischen Tests positiv auf CA. Diamox-Behandlung in-

hibierte die CA in beiden Sekreten.

Aus aktiv bohrenden Schnecken excisierte Kontrollhäften von ABOs ätzten polierte
Schalen an, wogegen auf die halbierten Versuchs-ABOs einwirkende steigende Diamox-
Konzentrationen die Atzwirkung zunehmend verringerten. In den Konzentrationen von
5х10-3М und 1x10°2M war die Ätzfähigkeit fast völlig inhibiert. Eine Suspension von
reiner Schafserythrocyten-CA in Meerwasser führte nicht zur Schalenanätzung.

Diese Versuche zeigen an, dass CA eine wesentliche Rolle beim Schalenauflösen
während der Bohrtätigkeit dieser Schneckenart spielt; sie bestätigen auf der anderen
Seite nicht ihre Funktion als direktes demineralisierendes Agens.

C.M.-B.

262

CARRIKER AND CHAUNCEY

RESUME
EFFET DE L INHIBITION DE L'ANHYDRASE
CARBONIQUE SUR LA PERFORATION
DE COQUILLE PAR LE MUREX UROSALPINX CINEREA

M. R. Carriker et H. H. Chauncey

Une étude a été faite sur une série de concentrations de Diamox (2-acétylamine-1,3,4-
thiadiazole-5-sulfonamide), qui est un inhibiteur de Гепхуте anhydrase carbonique
(AC), sur la perforation de la coquille de l'huítre Crassostrea virginica par le bigorneau
perceur Urosalpinx cinerea follyensis. Cinquante cing individus qui étaient initialement
en train de perforer ont continué а perforer et а se nourrir sur des huitres dans des solu-
tions de Diamox se situant а des concentrations comprises entre 5x10~4M et 1x10°?M.
Quarante cing individus qui ne perforaient pas initialement, sont montés sur les huitres
et ont commencé а percer aux concentrations précédentes. Les murex se sont montrés
capables de terminer leur trou de perforation et de se nourrir jusqu à des concentrations
de 5х10-3М.

Le nombre total de perforations completes décroit des 2/3 tandis que le nombre total
de perforations incomplétes double presque а mesure que Гоп augmente les concentra-
tions de Diamox, pendant les 6 jours d’experimentation. Tous les 90 murex ont survécu
les 6 jours, ainsi d'ailleurs que le mois suivant ou ils étaient dans une eau de mer courante
normale ou ils pouvaient perforer et se nourrir activement.

Les extraits de sécrétion récoltés а partir d'organes accessoires de perforation (O.A.P.)
en activité, sur des individus vivants sur un modele de valve, ainsi que les produits de
sécrétion libérés par ГО.А.Р. au niveau du pore de ГО.А.Р., se sont montrés positifs
pour ГАС lorsqu'ils ont été testés par des techniques histochimiques. Le traitement par
Diamox a inhibé ГАС dans les 2 cas.

Des moitiés d'O.A.P. utilisées comme témoins, excisés sur les murex en activité de per-
foration, ont érodé des coquilles polies, tandis que des concentrations croissantes de
Diamox appliquées aux moitiés expérimentales de ces O.A.P., ont progressivement réduit
leur capacité d’eroder. Dans des solutions de 5х10-3М et 1х10-?М, I abrasion était
presqu entiérement inhibée. Une suspension en eau de mer d'AC pure d érythrocyte de
bovin п’а provoqué aucune abrasion de coquille.

Ces expériences indiquent que ГАС joue un róle vital dans la dissolution de la coquille
pendant la perforation chez cette espéce, mais ne confirment pas ses fonctions comme
agent direct de déminéralisation.

А. Lb.

RESUMEN

EFECTO INHIBITORIO SOBRE LA ANHIDRASA CARBONICA
EN LA PERFORACION DE OSTRAS POR EL GASTROPODO
MURICIDO UROSALPINX CINEREA

M. R. Carriker y H. H. Chauncey

Se estudiaron los efectos de una serie de concentraciones de Diamox (2-acetilamina-
1,3.4-thiadiazol-5-sulfonamida), como un inhibidor especifico de la enzima carbónica
anhidrasa (CA), sobre la penetración en la concha de la ostra Crassostrea virginica por el
gastrópodo muricido perforador Urosalpinx cinerea follyensis. 45 caracoles que ya habian
iniciado la perforación, continuaron la acción y se nutrieron en las ostras, en soluciones
de Diamox de 5х10-4М a 1x10-2M. Otros 45 que no habian iniciado la perforación la
comenzaron en las mismas soluciones. Los caracoles fueron capaces de completar la
horadación de las ostras en concentraciones de 5x1072M.

El número total de orificios completos en las ostras decreció dos tercios, mientras que
el número de los incompletos se duplicó en concentraciones mayores de Diamox durante

INHIBITION OF SHELL PENETRATION BY UROSALPINX

los 6 dias de experimentación. Los 90 caracoles sobrevivieron los 6 dias, y aún hasta un
mes más en agua de mar corriente normal, en la cual perforaron y se alimentaron ac-
tivamente.

Residuos de secreción tomados de los órganos perforadores activos accesorios (ABO) en
caracoles vivos sobre una valva modelo, así como secreciones emitidas por el ABO en el
poro ABO, fueron positivas para CA cuando se probaron con técnicas histoquímicas.
Tratamiento con Diamox produjo inhibición de CA en ambos.

Mitades controladas de ABO, sacadas de caracoles perforadores activos, mordieron
conchas pulidas, mientras el aumento de concentraciones de Diamox, aplicadas a la
mitad experimental de estos ABO, redujeron esa acción proporcionalmente. En las
soluciones 5х10-3М y 1x10°2M el mordiente fué, casi totalmente, inhibido. Una suspen-
sión de eritrocitos CA bovinos puros, pero en agua de mar no produjeron efecto mor-
diente en las conchas.

Estos experimentos indican que CA desempena un rol vital en la acción disolvente
durante la perforación de la concha por esta especie de caracol, pero no confirma su fun-
ción como un agente desmineralizador directo.

LIE

263

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MALACOLOGIA, 1973, 12(2): 265-281

SOME ASPECTS OF THE BIOLOGY AND FUNCTIONAL MORPHOLOGY
OF THE ORGANS OF FEEDING AND DIGESTION OF LIMNOPERNA
FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA)

Brian Morton

Department of Zoology, The University of Hong Kong
ABSTRACT

Limnoperna fortunei (Dunker) has recently been introduced into the fresh water supp-
ly system of Hong Kong. The initial occurrence of the mollusc can be related to the com-
mencement of supplies of water to Hong Kong from the East river in China.

It is suggested that Limnoperna could emulate the rapid expansion of range
experienced by Dreissena polymorpha in Europe and Corbicula manillensis in N.
America. For this reason pertinent aspects of the functional morphology and biology of
Limnoperna have been investigated. Comparisons have been made with other mytilids,
and with Dreissena which Limnoperna superficially resembles. The possibility of a
phylogenetic affinity between these 2 animals is discounted; the similarities being due to
convergent evolution and the adoption of similar habits. The evolution of the
heteromyarian condition in the Mytilacea and Dreissenacea, followed by the subsequent
evolution of osmoregulating powers, has enabled Limnoperna and Dreissena to
successfully invade the hard surfaces of fresh-water systems. In this habitat there is no
competition from the specialised infaunal bivalves characteristically found in fresh
waters. The colonisation of this habitat has conflicted in Dreissena, and may possibly
conflict in the case of Limnoperna, with the interests of man in the supply of fresh water.

INTRODUCTION

In recent years the attention of water
supply engineers and biologists in Europe
and North America has been drawn to the
problems of fouling caused by fresh-water
bivalve molluscs.

In the 19th century and in this century
Dreissena polymorpha has expanded its
range from an initial restricted area
focused on the Caspian Sea to one encom-
passing much of the European continent.
It has been suggested that much of the ap-
parent success of this animal is attributable
to the construction of waterways, thereby
facilitating the artificial expansion of
range. This is certainly the reason for the
expansion of range that Dreissena under-
took in Great Britain in the 19th century
(Kerney & Morton, 1970). Dreissena also
possesses a byssus and is thus adapted to
the colonisation of solid surfaces (such as
are found in the pipes and conduits of
water supply systems) hitherto inaccessible
to the typically infaunal bivalve con-

stituents of fresh-water faunas (Morton,
1969а), e.g., the Unionacea and Cor-
biculacea. This has led to a situation in
which many European countries, in-
cluding Great Britain, spend time, money
and effort in controlling Dreissena (Mor-
ton, 1969c).

Corbicula manillensis has recently been
introduced into North American
waterways and has caused similar
problems of fouling (Sinclair, 1964). First
observed in 1938 in Washington this
species has since expanded its range to en-
compass all of the major North American
river basins (Sinclair, 197la, b). The
fouling problems caused by Corbicula are
somewhat different from those caused by
Dreissena in that Corbicula is essentially
an infaunal species and thus, although it
does clog pipes and condensers, also causes
additional problems when occurring in
sands dredged for ultimate use in the
manufacture of concrete. Like Dreissena
the rapid expansion of range experienced
by Corbicula may be attributable to man’s

(265)

266 В. MORTON

development of artificial waterways for
water supply purposes.

In Asia, the original home of Corbicula
manillensis, there are few instances of
molluscs causing problems with regard to
water supply, largely one would suspect
because in many cases water supply
systems themselves are not as extensive or
as refined as they are in Europe and North
America.

The mytilid Limnoperna fortunei
(Dunker) occurs in the rivers of Asia but
has aroused little interest. There is a
dearth of information on this animal, most
records being found in obscure and an-
cient journals. Limnoperna is of interest,
however, from a number of viewpoints. In
the first instance it is, for a mytilid, living
in a unique habitat. Secondly, Limnoperna
possesses a striking superficial similarity to
Dreissena and, in view of the recent sub-
mission by Purchon & Brown (1969) of a
common ancestry between the Mytilacea
and Dreissenacea, it is considered that
Limnoperna may test the validity of this
concept. Finally, and most importantly,
Limnoperna was, prior to 1968 unknown
in Hong Kong. Its appearance in part of
the water supply complex of Hong Kong
may be a re-enactment of the pattern of
colonisation typical of Corbicula and
Dreissena (i.e., via man-made systems).
Thus Limnoperna might Бе potentially
detrimental to water supply in Hong Kong
in particular and Asia in general.

There is thus a need to set any further
studies on Limnoperna upon а firm
footing. This study was undertaken to
fulfill, in part, this need.

MATERIALS AND METHODS

A large number of specimens of Lim-
noperna fortunei were obtained from a
channel used for conveying water to Tai
Lam Chung reservoir, Hong Kong.
Further samples were subsequently ob-
tained from Plover Cove reservoir.

Material to be sectioned was fixed in
alcoholic Bouin Duboscq and ultimately
stained in either Heidenhain s

haematoxylin, Masson s trichrome ог
Mallory 's triple stain. Where necessary,
decalcification of the shell was achieved by
immersion, subsequent to fixation and
prior to sectioning, in R.D.O.! rapid bone
decalcifier for a period of 4 hours. The
ciliary currents elucidated in this work
were demonstrated by the application of
either suspended carmine or milk.

NOMENCLATURE

Volsella fortunei (Dunker 1857) is in all
probability synonymous with Modiola
lacustris (von Martens 1875) and Modiola
fortunei (Reeve 1858). It is probably also
synonymous. with Dreissena siamensis
(Morelet 1866). The generic name Lim-
noperna Rochebrune 1888 was erected to
distinguish this apparently monotypic
genus from the other mytilids. The
elucidation of these differences is one of
the aims of this paper.

DISTRIBUTION AND HABITS

Prior to 1968 Limnoperna was not found
in Hong Kong. Its subsequent discovery in
1968 in certain major tunnels, culverts and
pipelines of Hong Kong's water supply
system would seem to suggest accidental
and artificial introduction. The ap-
proximate timing of its appearance coin-
cides with the supply to Hong Kong in
1967 of water derived from the East river
in China. Limnoperna has been reported
from the Pearl river estuary (Miller €
McClure, 1931), of which the Shum Chun
river of Hong Kong is a component, and it
is thus possible, though unlikely, that in-
troduction was via this path. The sudden
occurrence, however, in pipelines of the
water supply system strongly suggests that
the former possibility was the primary
(and maintained) source of infection. No
information is available to indicate if this
animal is a nuisance in China, although
Limnoperna has been reported as ос-
curring in Tung-Ting lake, which connects
up with the Yangtsekiang river, in Hunan
Province (Tchang, Li € Liu, 1965).

Whatever its origin, however, Lim-

‘Supplier; Du Page Kinetic Laboratories, Inc., Р.О. Box 416, Downers Grove, Illinois 60515, U.S.A.

BIOLOGY AND FEEDING OF LIMNOPERNA

noperna is now firmly established in the
rapidly expanding and _ increasingly
sophisticated water supply system of Hong
Kong. The pattern of colonisation reflects
that of Corbicula and Dreissena, but of
course on a much smaller scale. It is now a
significant and established member of the
epifauna of the Plover Cove reservoir and
its associated pipelines.

Limnoperna is very like Dreissena
(Morton, 1969c) in that when living in
relatively slow flowing waters it
characteristically occurs in clumps or
“nodules” of individuals living bound
upon the dead shells of their predecessors
by a very stout byssus. In very fast flowing
waters, such as are found in pipelines or
culverts, Limnoperna inhabits crevices
and pits, although from these foci
succeeding generations can spread out to
cover more and more of the exposed sur-
face of the pipe. Its byssus makes it
extremely difficult to dislodge in such
situations.

ADEE TATIONS USED IN, THE

FIGURES
is Auricle
AA Anterior adductor muscle or scar
ABR Anterior byssal retractor muscle
or scar
B B type sorting area
BG Byssus gland
BS Branchial septum
BY Byssus
CS Crystalline style
DD Digestive diverticula
DDD(1)-(5) Ducts of the digestive diverticula
DH Dorsal hood
DHT Dorsal hood tract
DS Dorsal septum
ES Exhalant siphon
Е Foot
ЕС Food sorting caecum
GS Gastric shield
ID Inner demibranch
IG Intestinal groove
IP Inflected periostracum
IS Inhalant siphon
E Ligament
BP Left pouch
LT Left duct tract
M Mouth

267
MG Mid gut
MM Mantle margin
MT Minor typhlosole
O Oesophagus
OD Outer demibranch
OS Opening of food sorting
caecum into stomach
OV Ovary
В Pericardium
PA Posterior adductor muscle or scar
PBR(1),(2) Posterior byssal retractors muscle
or scar
PL Pallial line
POG Proximal oral groove
PPR Posterior pedal retractor muscle
or scar
R Rectum £
RP Right labial palp
RT Right duct tract (SA3)
SA2 Sorting area
SS Style sac
E Major typhlosole
RE Tongue of major typhlosole
U Umbo
V Ventricle
VM Visceral mass
ANATOMY

The shell and ligament

The equivalve, heteromyarian shell of
Limnoperna fortunei is superficially very
similar to that of Xenostrobus securis
(Wilson, 1967) (Fig. 1, A & B). In par-
ticular, in both species the shell is dark
brown above the umbonal keel and a paler
yellow-brown below. This is caused by the
nacre of the interior of the shell being pur-
ple above and white below the keel. The
presence of a nacreous layer in Limnoper-
na displaces this genus from all contact
with the Dreissenacea (Taylor, Kennedy &
Hall, 1972).

The outer periostracal layer of the shell
is smooth and shiny and where it curls in-
wards at the shell margin is thick. The um-
bones are very nearly terminal and the
dorsal ligamental margin is straight or, at
most, only slightly curved. The ventral
margin of the shell is the most variable
feature and in different specimens varied
between the 2 extremes of being either
straight or distinctly arcuate. There are no
hinge teeth and no byssal notch.

268 B. MORTON

FIG. 1. Limnoperna fortunei. Views of the
exterior (A) of the left shell valve and
interior (B) of the right shell valve. (For
abbreviations see p 267).

The overall dimensions of the shell are
regular for the population sampled in this
study as can be seen from Fig. 2 and by the
ratio of width: height: length which is: 1:
1.18 + 0.18: 2.60 + 0.50. The ratios of
shell width : length and shell height
length have been calculated as being 0.38
+ 0.06 and 0.45 + 0.06 respectively.

The opisthodetic ligament of Limnoper-
na consists of 2 layers with staining reac-
tions similar to those of Mytilus edulis
(Trueman, 1950; Beedham, 1958). The
outer layer stains red and the inner layer
bright blue with both Mallory's triple stain
and Masson's trichrome. Other mytilids
e.g., Modiolus, Lithophaga (Yonge, 1955),
Septifer (Yonge & Campbell, 1968) and
Fungiacava (Goreau, Goreau, Soot-Ryen
& Yonge, 1969) possess a ligament with a
similar structure. In all these forms, and in
Limnoperna, the periostracum extends
over the ligament, thereby adding another
layer. Yonge & Campbell (1968) regard
this ligamental structure as being typical
of the Mytilacea. The results of this work
on Limnoperna agree with this premise.
The ligament of Dreissena polymorpha has
a totally different structure (Yonge &
Campbell, 1968); it is an uniquely complex
opisthodetic ligament.

SHELL LENGTH (mm)

2 6 10 14
SHELL WIDTH (mm)

FIG. 2. Limnoperna fortunei. Width : length
ratios of a large sample from Hong
Kong.

The mantle

Mantle fusion occurs dorsally above the
exhalant siphon and between the exhalant
siphon and inhalant aperture. Mantle fu-
sion is of the inner mantle folds only and
thus of type A (Yonge, 1957).

The periostracum that is secreted by the
epithelia delimiting the periostracal
groove is composed of 3 layers. The outer
layer is thin (54), and stains very slightly

BIOLOGY AND FEEDING OF LIMNOPERNA 269

grey with Heidenhain's haematoxylin but
not at all with Mallory s or Masson s stains.
The middle layer is 20-254 thick at its
greatest depth and is composed of a yellow
substance that is unaffected by the routine
stains used in this study. This layer does
not, as does its counterpart in Mytilus
(Beedham, 1958), possess vacuoles. An in-
ner laminated layer ultimately achieves a
thickness of between 25 and 35 и and
when first secreted stains red with both
Mallory's and Masson’s stains. Toward the
margin of the valve the outer laminations
of this layer stain blue. Ultimately all the
laminae stain blue. The structure of the
periostracum and the epithelia that secrete
the component zones bear a close similari-
ty to those possessed by Mytilus
(Beedham, 1958) but are very different
from the Eulamellibranchia in general and
Dreissena polymorpha in particular (Mor-
ton, 1969a). The mantle distal to the man-
tle margin contains, as in other mytilids,
much of the gonadial tissue of the animal.
This is not so in Dreissena.

The siphons

The exhalant siphon (Fig. 3, ES) of Lim-
noperna is formed by fusion between the
inner mantle folds only, this being type A
(ii) (Yonge, 1957). The inhalant aperture is
not separated from the pedal/byssal aper-
ture by fusion of the opposite mantle lobes
but is separated functionally by their ap-
position. It can thus be referred to as a
siphon, even though this is not strictly cor-
rect. Such a situation is typical of the
Mytilacea, e.g., Mytilus (White, 1937),
Lithophaga (Yonge, 1955), Adula
(=Botula) (Yonge, 1955; Fankboner, 1971)

and Xenostrobus (Wilson, 1967). Neither

the inhalant siphon nor the exhalant
siphon bear tentacles or papillae (Fig. 3,
A). Externally each mantle lobe is
patterned with a brown stripe; these fuse
dorsally to the exhalant siphon to form a
single stripe. А similar brown stripe
patterns the internal surfaces of the mantle
lobes forming the inhalant siphon, and
there is a dorsal median stripe on the in-
halant siphon at the point of fusion of the
mantle lobes forming the exhalant siphon
(Pig. oo Ay):

A branchial septum (Fig. 4, BS) con-
nects the ctenidia (ID, OD) to the mantle
at the point of fusion of the mantle lobes
separating the exhalant from the inhalant
siphon. This septum effectively separates
posteriorly the infra-branchial from the
supra-branchial chamber. When the
animal is actively filtering and the siphons
are extended, the branchial septum is
horizontal, but folds up when the siphons
are withdrawn. In Adula (Fankboner,
1971) this septum apparently acts as a
valve.

The musculature

The anterior adductor muscle (Fig. 4,
AA) is small and is located on the antero-
ventral floor of the shell valves. In this
respect Limnoperna is very similar to
Xenostrobus (Wilson, 1967) and Mytilus
(White, 1937). The anterior byssal retrac-
tor muscle (ABR) has its origin on the
antero-dorsal roof of the shell like X.
securis and X. pulex (Wilson, 1967). The
posterior adductor muscle (PA) is large
and the posterior byssal retractor muscle
(PBR) is divided into 2 component units as
in X. inconstans (Wilson, 1967) and M.
edulis (White, 1937). There is a small
posterior pedal retractor muscle (PPR) that
has its origin anterior to the posterior
byssal retractors and not posterior as in
Dreissena (Yonge € Campbell, 1968).

The ciliary currents of the mantle, visceral
mass and foot

The ciliary currents of the mantle
(including the siphons), visceral mass and
foot are all rejectory in nature and serve to
keep the mantle cavity free of too large or
unwanted particles.

The ciliary currents of the visceral mass
(Fig. 4, VM) and foot (F) pass particles
posteriorly to be concentrated at the
postero-ventral tip of the visceral mass.
From this point they are presumably
removed by (a) the ventrallv, or (b) the
dorsally, directed ciliary tracts of the
ascending lamella of the inner demibranch
(ID) to be rejected respectively by the sor-
ting mechanism of the ventral ctenidial
marginal food groove or the dorsal food
groove in the junction of the inner

HIG.3:

FIG. 4.

В. MORTON

B C

Limnoperna fortunei. A posterior view of the animal showing (A) the patterning on the
mantle and siphons and the shape of the shell. The inhalant a am (broken arrows), ех-
halant stream (open arrows) and ciliary rejection currents (solid arrows) of an actively filter-
ing animal (B) and a disturbed animal (C) are also shown. (For abbreviations see p 267).

PBR (1)

Limnoperna fortunei. The anatomy and the ciliary cleansing currents of the mantle, foot and
visceral mass. The ciliary currents of the ascending lamella of the inner demibranch are also
shown. The shell valve, mantle and ctenidium of the right side have been removed. (For ab-
breviations see p 267).

BIOLOGY AND FEEDING OF LIMNOPERNA 271

demibranch and visceral mass. In both
cases (if they are too large) the particles ul-
timately pass onto the mantle.

Particles falling on to the mantle are
passed posteriorly from the region of the
mouth and labial palps (RP) to the in-
halant siphon (IS). Pseudofaeces are not
concentrated at the base of the inhalant
siphon to be expelled by the rapid adduc-
tion of the shell valves, as in the typical
eulamellibranchs possessing a distinct

siphon. Instead in Limnoperna the lobes of
the inhalant siphon are highly mobile and

bear on their inner surfaces strong ciliary
tracts which pass the pseudofaeces dorsally
towards the exhalant siphon (Fig. 3, В).
When actively filtering, with the inhalant
lobes fully expanded, water can pass into
the mantle cavity. The ciliary currents can
take the pseudofaeces towards the
exhalant siphon against this stream. Rapid
closure of the shell valves forces water out
of both siphons, but particularly the
exhalant siphon, thereby ejecting the
pseudofaeces (and faeces). When the
animal is disturbed, the shell valves only

FIG. 5. Limnoperna fortunei. The labial palps and ctenidium of the right side showing the various
ciliary currents. (For abbreviations see p 267).

bo
I
bo

partially open (Fig. 3, С), but open suf-
ficiently to allow pseudofaeces to be
similarly removed from the mantle cavity
via a reduced inhalant aperture.

The ctenidia and labial palps

The ctenidia comprise 2 sub-equal
demibranchs of which the outer
demibranch is the longer. The ventral
margin of the outer demibranch (Fig. 4,
OD) was found to always lie tucked behind
the incurving mantle margin (MM) with
the associated periostracum (IP). The up-
per margins of the ascending lamellae of
the outer and inner demibranchs are at-
tached to the mantle and the visceral mass
respectively by ciliary fusions. The
ctenidia are flat, homorhabdic and
filibranchiate (eleutherorhabdie).
Ctenidial cohesion is maintained by ciliary
discs as in other mytilids. Like many other
mytilids listed by Fankboner (1971), the
outer demibranchs of Limnoperna for-
tunei are some 5 or 6 filaments shorter at
their anterior ends than the inner
demibranchs. A similar arrangement exists
in Dreissena (Morton, 1969a) and Petricola
(Purchon, 1955). Fankboner (1971) states
that “a functional advantage for this
anatomical reduction is unclear.” For
Limnoperna the advantage of this arrange-
ment is clear in that it enables the ventral
marginal food grooves of both
demibranchs to be in contact with both
labial palps thereby greatly increasing the
efficiency of particle selection by the
palps. In other genera this is apparently
not so well developed. The ctenidial-labial
palp junction of Limnoperna thus falls into
Category I elucidated by Stasek (1963) and
is thus typical of the Mytilacea in general.
D. polymorpha, on the other hand, has a
ctenidial-labial junction that is of Category
Ш (Morton, 1969a).

The ciliation of the ctenidial surfaces is
of type В (1) (Atkins, 1937) (Fig. 5). Accep-
tance tracts are situated on the ventral
margins of both demibranchs, in the
ctenidial axis and in the junctions of the
ascending lamella of the inner and outer
demibranchs with the visceral mass and
mantle respectively. Only those particles
arriving on the labial palps inside the ven-

В. MORTON

tral marginal food groove of the inner
demibranchs pass into the proximal oral
groove and directly to the mouth. Particles
arriving at the anterior end of the
ctenidium via (1) the crests of the ventral
marginal food grooves of both inner and
outer demibranchs, (2) inside the ventral
food groove of the outer demibranch and
(3) in all 3 dorsal food grooves are sub-
jected, before ingestion, to the ciliary
selection currents of the labial palps. The
abrupt termination of the outer
demibranch (Fig. 5), facilitating this un-
usually complicated sorting process has
not been observed in other bivalves, and is
markedly different from that possessed by
Dreissena (Morton, 1969a). Particles are
probably removed from the ctenidial ter-
mini by the unridged portion of the labial
palps, the ciliary currents of which subse-
quently pass the particles onto the sorting
portion of the palps. This function is the
attribute of the system of parallel ridges
and grooves which pass selected particles
of a suitable nature and size over the crests
of the ridges toward the proximal oral
groove for ultimate ingestion. Too large or
unwanted particles are passed laterally
toward the opposite free edge of the palp
for rejection. Recirculatory currents also
exist. Details of the palp ciliation need not
be gone into here since they are essentially
the same as those described by Fankboner
(1971) for Adula and are typical of mytilids
in general.

The ciliary currents of the lips of the
mouth (M) are rejectory in nature passing
unwanted material back to the palps for
rejection along the prescribed course.

The alimentary system

The oesophagus passes upwards from
the mouth, which lies between the anterior
byssal retractor muscles and is closely
applied to the anterior adductor muscle.
The ciliated oesophagus opens into the
stomach which is located under the antero-
dorsal margin of the shell and is sur-
rounded by the dark digestive diverticula
(Fig. 4, DD).

From the posterior end of the stomach
arises the combined style sac and mid-gut
(MG) which passes backwards between the

BIOLOGY AND FEEDING OF LIMNOPERNA 273

posterior byssal retractors (PBR (1), (2) ).
Just dorsal to the posterior adductor (PA)
the style sac terminates but the mid-gut
loops forwards to pass back between the
posterior byssal retractors. The mid-gut
loops again on the right side of and just
before the stomach and passes posteriorly
to penetrate the ventricle of the heart (V)
and terminate in the anus near to the
exhalant siphon. The detailed structure of
the style sac and mid-gut of Limnoperna is
essentially the same as that described for
Mytilus edulis by Giusti (1971).

The stomach of Limnoperna (Fig. 6) is
elongate and bears a close similarity to the
stomachs of other mytilids,e.g., Lithophaga
(Purchon, 1957), Mytilus edulis (Graham,
1949: Reid, 1965), Adula (Fankboner,
1971), Botula, Lithophaga and Perna
(Dinamani, 1967) and thus belongs to type
Ш and Section I of the stomach types
elucidated by Purchon (1957) and
Dinamani (1967) respectively. An attempt
has been made in this description of the
stomach of Limnoperna to combine the
nomenclatural systems of Purchon (1957)
and Reid (1965).

In Limnoperna, as in all bivalves, the
floor of the stomach is dominated by the
major typhlosole (T) and associated in-
testinal groove (IG) which arise in the style
sac (SS) and pass forwards to penetrate the
food sorting caecum (FC). The major
typhlosole does not divide as reported for
Adula by Fankboner (1971). The minor
typhlosole (MT) also arises in the style sac
and passes, for a short distance, along the
right side of the stomach. The crystalline
style (CS) is secreted in the style sac (SS)
and, protruding into the stomach, rotates
against the typically saddle-shaped gastric
shield covering the left dorso-lateral wall
of the stomach. The gastric shield sends a
flare into the left pouch (LP). The left
pouch (Fig. 7) sees the origin of what Reid
(1965) has termed the left duct tract
(LDT), which passes into the food sorting
caecum (Fig. 8, FC). On the right side of
the stomach the right duct tract (RT) also
passes into the food sorting caecum.
Associated with the right duct tract are 2
groups of ducts to the digestive diverticula

[DDD(1) & DDD(2)]. Similarly in the left
pouch (Fig. 7) there are 2 further
groupings of ducts leading to the digestive
diverticula [DDD(3) € DDD(4)]. Purchon
(1957) considered the right duct tract to be
a sorting area and termed it sorting area 3
(SA3). The equivalent sorting area of the
left duct tract would appear to be the floor
and walls of the left pouch (Fig. 7). A
further sorting area (SA2) can be recogniz-
ed dorsal to the entrance of the food sor-
ting caecum and separating this opening
from the entrance to the left pouch. Each
of these sorting areas is a system of ridges
and grooves which Reid (1965) has called
type A and which is found in all bivalves.

The food sorting caecum is a com-
paratively long finger-shaped pocket
penetrated to its apex by the tongue of the
major typhlosole (Fig. 8, TT). At the apex
there is a sorting area which is of type B
(Reid, 1965) and which is found only in
those bivalves which Purchon (1960; 1963)
has grouped together as the Gastrotriteia,
and which is characteristic of the
Mytilacea (Reid, 1965).

In the stomach, cilia on the crests of the
major typhlosole (Fig. 6) and inner folds of
the left and right duct tracts pass food
material entering the stomach into the
food sorting caecum (Fig. 8). Ciliary
currents in the grooves of the inner folds of
the left and right duct tracts and the in-
current fold of the intestinal groove also
pass particles into the food sorting caecum.
At the apex of the caecum the B type sor-
ting area (Reid, 1965) sends acceptable
particles of a suitable size into the outer
folds of the left and right duct tracts which
pass this material to the ducts of the
digestive diverticula of the left pouch and
right duct tract. Rejected particles pass out
of the food sorting caecum in the excurrent
intestinal groove of the major typhlosole
and pass to the mid-gut for ultimate
defecation. Particles of intermediate size
are probably recirculated by the dorsal
hood tract passing them back to the dorsal
hood and gastric shield. Limnoperna
possesses ducts leading to the digestive
diverticula in the food sorting caecum

(Fig. 8, DDD(5)). It is not known if these

ducts occur in other mytilids although
Fankboner (1971) illustrated similar ducts
in the food sorting caecum of Adula. The
minor the major
typhlosole in clearing the stomach of un-
wanted food into the mid-gut. No appen-
dix could be observed in the stomach of
Limnoperna as reported for Mytilus (Reid,
1965) and Adula (Fankboner, 1971).

The basic structure of the ducts and the
digestive tubules comprising the digestive
diverticula bear a close similarity to those
described by Owen (1955) for Mytilus
edulis.

typhlosole assists

DISCUSSION

Limnoperna fortunei has recently
colonised the pipes, conduits and channels
of part of the water supply system of Hong
Kong. Details of the world-wide distribu-
tion of this animal are unknown but it is

DDD (2)

GS

B. MORTON

believed to be restricted to S.E. Asia and to
be widely distributed in the rivers of
China. It seems likely that Limnoperna
has been introduced into Hong Kong
either indirectly via the Pearl river or
directly as a result of the intake of raw
water into Hong Kong from China sub-
sequent to 1967. The first widespread
reports of this animal in 1968 would sup-
port the latter view and indicate that Lim-
noperna is capable of undertaking an ar-
tificial expansion of range given a suitable
habitat. In this case, as apparently
happened with Dreissena in Europe and
Corbicula in North America, this process is
facilitated by the construction of inter-
connecting water supply systems.
Whatever the source, Limnoperna has
now firmly established itself in the water
supply system of Hong Kong. Like
Dreissena polymorpha in Europe, it would

DDD (1)

Ao
1mm

RT

FIG. 6. Limnoperna fortunei. The structure and ciliary currents of the interior of the stomach after
opening by a horizontal incision in the right side (For abbreviations see p 267).

BIOLOGY AND FEEDING OF LIMNOPERNA 275

DDD (5)

FIG. 7. Limnoperna fortunei. The structure
and ciliary currents of the food sorting
caecum of the stomach. (For ab-
breviations see p 267).

seem that Limnoperna is ideally adapted
in the possession of a stout byssus and
heteromyarian form to a life in fast flowing
waters. Dreissena, however, can also thrive
in the relatively static waters of reservoirs
(Morton, 1969b) and in this habit can
cause problems of sedimentation
(Milheev, 1967; Stanczykowska, 1968). It
may be significant that very recently Lim-
noperna has been dredged up from the
bottom of Hong Kong's newest and largest
reservoir, Plover Cove. It would seem that
both of these animals, despite their ap-
parently specialized form, are liberal in
their choice of habitat and are potentially
detrimental at all stages of the water supp-
ly process.

The close similarity in choice of habitat
and form existing between Limnoperna
and Dreissena could suggest some degree
of phylogenetic affinity between the
Dreissenacea and МуШасеа, as recently
postulated by Purchon & Brown (1969).
Yonge & Campbell (1968) showed that the
similarities that existed between Dreissena
and the mytilid Septifer were due to con-

vergence. Morton (1970) and Taylor,
Kennedy & Hall (1972) agree with this
view and further suggest that from both a
palaeontological and a morphological view
the affinities of Dreissena lie with the Cor-
biculacea. Dreissena would thus be more
closely related to Corbicula manillensis, a
pest of North American water supply
systems.

From Table 1 it can be seen that in near-
ly all major anatomical respects Dreissena
and Limnoperna are very different, and it
is hard to account for the high degree of
similarity obtained for Dreissena and the
mytilids studied by Purchon € Brown
(1969).

Most of the few similarities that do exist
between the 2 groups, e.g., the
heteromyarian condition which occurs in a
variety of unrelated Bivalvia, are at-
tributable to convergent evolution and the
colonisation of similar habitats. It is en-
visaged both for Dreissena and Limnoper-
na that the neotenous retention of the
byssus (Yonge, 1962) in their respective
ancestors resulted in the evolution in both
groups of the heteromyarian form (Yonge
& Campbell, 1968). Both have sub-
sequently exploited this condition, with
the development of osmoregulatory
powers, in the colonisation of fresh waters.

The close phylogenetic affinities of Lim-
noperna are at present unknown. Soot-

DDD (4)

DDD (3)

FIG. 8. Limnoperna fortunei. The structure
and ciliary currents of the left pouch of
the stomach. (For abbreviations see р

267).

276 В. MORTON

Ryen (1955) did not mention this genus in
his report on the family Mytilidae.
However, Limnoperna shows a close
similarity to the Australian species of
Xenostrobus securis and X. inconstans
(Wilson, 1967) in the possession of com-
parable anatomical characters, e.g., the
posterior byssal retractor muscle is divided
into 2 and the mid-gut loops on the right
side of the stomach. Furthermore both X.
securis and X. inconstans live at the head
of estuaries whilst other species, e.g., X.
pulex are marine (Wilson, 1967). It would
seem possible that Limnoperna evolved
from forms essentially similar to these.
Significantly Dreissena is closely related to
the estuarine dreissenid species of
Mytilopsis (Keen, 1969; Morton, 1970).
It would thus seem that Dreissena and
Limnoperna represent the apices of 2
phyletic streams both adapted for life in

fresh waters. Significantly the hard sur-
faces found in fresh water systems in many
parts of the world are not normally
colonised by bivalves, most species being
infaunal, e.g., Unionacea, Corbiculacea.
The hard surfaces niche was therefore a
suitably vacant target for both Dreissena
and Limnoperna. Significantly, within
their own spheres of influence, both
species would appear to be colonising this
habitat as fast as it is artificially made for
them.

The ways in which Dreissena is adapted
morphologicallv to a life in fresh waters
has earlier been reported upon (Morton,
1969a). Limnoperna possesses ciliary tracts
on the internal surfaces of the inhalant
siphon which carry pseudofaeces towards
the exhalant siphon. The intermittent
rapid expulsion of water from the exhalant
siphon blows these away together with the

TABLE 1

Limnoperna fortunei

Mantle 1. Periostracum 3 layered

bo

. Mantle fusion type A

3. Mantle fusion forms

exhalant siphon only
Shell 4. Heteromyarian
5. No byssal notch

6. Internal nacreous layer

Ligament 7. Simple opisthodetic

Musculature 8. Anterior adductor located

on shell

9. Posterior pedal retractor

located anteriorly

Ctenidia 10. Homorhabdic, filibranchiate

11. Ciliation of type B(1)

by ciliary fusion

13. Outer demibranch terminates

abruptly
14. Ctenidial-labial palp
junction |
Alimentary 15. Style sac and mid-gut
canal conjoined
16. Style sac and mid-gut
loop between the
byssal retractors
17. Stomach Type 3
Stomach Туре 1

2. Ctenidia attached dorsally

Dreissena polymorpha

Periostracum 2 layered
Mantle fusion type A
(Yonge, 1957)
Mantle fusion forms both
inhalant and exhalant siphons
Heteromyarian
Byssal notch
No internal nacreous layer
Complex opisthodetic
Anterior adductor located on
shell shelf
Posterior pedal retractor located
posteriorly
Homorhabdic, eulamellibranchiate
Ciliation of type C(1)
(Atkins, 1937)
Ctenidia attached dorsally by
cuticular fusion
Outer demibranch terminates
gradually
Ctenidial-labial palp
junction Ш (Stasek, 1963)
Style sac and mid-gut
separate
Style sac and mid-gut loop
around the byssal
retractors
Stomach type 5 (Purchon, 1957)
Stomach type ШО (Dinamani, 1967)

BIOLOGY AND FEEDING OF LIMNOPERNA 277

faeces. Living as it can do in fast flowing
waters, its siphons invariably facing the
current, this process is a significant aspect
of the morphology of Limnoperna since it
enables the animals to feed and remove
pseudofaeces at the same time but more
importantly blows the waste material over
the top of the animal and not straight out
in front of it. This prevents the
pseudofaeces from being taken back into
the mantle cavity. The outer demibranchs
of the ctenidia of Limnoperna are unusual-
ly long. This adaptation gives a greater
surface area for filtration and also places
rejected particles travelling anteriorly on
the crests of the ventral marginal food
groove in much closer proximity to the
rejection tracts of the mantle. The outer
demibranch being longer dorso-ventrally
but abruptly shorter antero-posteriorly to
the inner demibranch also enables the
labial palps to exert their selective т-
fluence upon all 4 of the gill lamellae. For
an animal living as Limnoperna can do in
relatively silt-free, fast flowing waters this
ctenidial-labial palp relationship ensures
that all particles reaching the anterior end
of the ctenidia are potentially usable as
food.

The alimentary system of Limnoperna is
typical of the Mytilidae in general
although the relatively large food sorting
caecum in this species, when compared
with the short caeca of species described
by Dinamani (1967), may indicate a
greater selective need in Limnoperna and
thus ensure that all the potential food
material is utilized. This would be perti-
nent for such an animal living in silt-free,
fast flowing waters. Significantly those
mytilids (except Adula (Fankboner, 1971))
living in silt laden burrows possess small
caeca (Dinamani, 1967). The food sorting
caecum of Limnoperna and Adula
(Fankboner, 1971) possess ducts to the
digestive diverticula. These ducts in Lim-
noperna, by increasing the total number of
apertures to the digestive diverticula, may
increase the capabilities of the animal for
collecting a greater number of particles
from a sparse food supply. Significantly
perhaps, Dreissena polymorpha (Morton,

1969a) possesses an enlarged right caecum
with a greater number of ducts to the
digestive diverticula.

Limnoperna is thus a relatively un-
specialised mytilid, but those
specialisations that do exist are concerned
with greater efficiency in food collection
and utilization. There are quite obviously
physiological specialisations, especially
with regard to the osmoregulatory
processes. In essence, however, Limnoper-
na is a typical mytilid and consequently
possesses many primitive characters.
Similarly Dreissena polymorpha is,
anatomically, unspecialised and it has
been suggested before (Morton, 1969b)
that it is the retention of primitive
characters in a habitat where there has
been а trend in other lamellibranchs
toward greater and greater specialisation
that makes the possession of such primitive
characters, e.g., the byssus and free swim-
ming larvae, so successful. Limnoperna
substantiates this view anatomically, but it
yet remains to be seen whether or not Lim-
noperna can be as successful as Dreissena
in utilising these potentialities in the
colonisation of new waterways. The oc-
currence of Limnoperna in Hong Kong
suggests that this may be so.

SUMMARY

The Asian fresh water bivalve Lim-
noperna fortunei has recently been in-
troduced into Hong Kong. In 4 years it has
successfully colonised a large part of the
water supply system. It thus reflects the
pattern of colonisation of fresh water supp-
ly systems in Europe and North America
by Dreissena polymorpha and Corbicula
manillensis respectively.

Limnoperna possesses a highly efficient
filtration and digestive system adapted for
the collection and utilisation of food
materials in fast flowing waters which
may, characteristically, be devoid of much
suspended material.

Investigations into the anatomy of Lim-
noperna show that it is a typical mytilid
and is thus not related to Dreissena. Both
animals show а superficial similarity to
each other occasioned by convergent

278 В. MORTON

evolution and the adoption of similar
habits.

Limnoperna further demonstrates the
success of the anisomyarian condition in
fresh waters typically possessing an in-
faunal bivalve population.

ACKNOWLEDGEMENTS

| am grateful to Dr. Tadashige Habe of
the National Science Museum, Tokyo,
Japan and Dr. Barry Wilson of the
Western Australian Museum, Perth,
Australia for confirming the identity of
Limnoperna fortunei. I am also grateful to
Dr. Wilson for sending me specimens of
Xenostrobus securis and for his comments
on the synonyms of Limnoperna. Гат т-
debted to the Director of the Waterworks
Department of the Hong Kong Goverment
for facilities provided during the course of
this investigation and to Mrs. D. W. Kwan
and Mr. D. Chi for technical assistance.

REFERENCES

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BEEDHAM, G. E., 1958, Observations on the
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DINAMANI, P., 1967,
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Malacologia, 5: 225-268.

FANKBONER, P. V., 1971, The ciliary
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GIUSTI, F., 1971, The fine structure of the
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MILLER, В. С. € McCLURE, Е. A 1937
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MORTON, B. S., 1969b, Studies on the biology
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MORTON, B. S., 1969c, Studies on the biology
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MORTON, B. S., 1970, The evolution of the
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PURCHON, R. D., 1955, The structure and
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PURCHON, R. D., 1957, The stomach in the
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РОВСНОМ, В. D. € BROWN, D., 1969,
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REID, В. С. B., 1965, The structure and func-
tion of the stomach in bivalved molluses. J.
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SINCLAIR, В. M., 1964, Clam pests in
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BIOLOGY AND FEEDING OF LIMNOPERNA

SINCLAIR, В. M., 1971а, Corbicula variation
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153-159.

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SOOT-RYEN, T., 1955, A report on the family
Mytilidae (Pelecypoda). Allan Hancock
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STANCZYKOWSKA, A., 1968, The filtration
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affecting circulation of matter in the lake.
Ekol. Pol., B14: 265-270. (In Polish)

STASEK, C. R., 1963, Synopsis and discussion
of the association of ctenidia and labial palps
in the bivalved Mollusca. Veliger, 6: 91-97.

TAYLOR; J., KENNEDY, W. J: & HALL; A,
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279

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WILSON, В. R. 1967, A new generic name for
three recent and one fossil species of
Mytilidae (Mollusca-Bivalvia) in Southern
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279-295.

YONGE, C. M., 1955, Adaptation of rock-
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YONGE, C. M., 1957, Mantle fusion in the
Lamellibranchia. Publ. Staz. zool. Napoli,
29: 151-171.

YONGE, С. M., 1962, Оп the primitive
significance of the byssus in the Bivalvia and
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YONGE, C. M. & CAMPBELL, J. I., 1968, On
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Roy. Soc. Edinb., 68: 21-43.

ZUSAMMENFASSUNG

EINIGE ASPEKTE DER BIOLOGIE UND FUNKTIONELLEN
MORPHOLOGIE DER NAHRUNGSAUFNAHME-
UND VERDAUUNGSORGANE VON LIMNOPERNA
FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA)

B. Morton

Limnoperna fortunei (Dunker) wurde in letzter Zeit in das Wasserversorgungssystem
von Hongkong eingeschleppt. Das erste Auftreten dieses Weichtiers kann mit dem
Beginn der Wasserzufuhr vom East River in China nach Hongkong in Verbindung
gebracht werden.

Vermutlich wird Limnoperna die rasche Arealerweiterung erreichen kónnen, die wir
bei Dreissena polymorpha in Europa und bei Corbicula manillensis in Nordamerika
erlebt haben. Daher wurden die diesbeziiglichen Aspekte der funktionellen Morphologie
und Biologie von Limnoperna untersucht. Vergleiche wurden angestellt mit anderen
Mytiliden und mit Dreissena, die Limnoperna auf den ersten Blick ähnelt. Die
Möglichkeit einer phylogenetischen Verwandtschaft zwischen diesen 2 Tieren wird als
gering angesehen; die Ahnlichkeiten sind vielmehr auf konvergente Evolution und die
Einnahme ähnlicher Lebensräume zurückzuführen. Die Entstehung der Heteromyarier-
Verhältnisse bei Mytilacea und Dreissenacea, zusammen mit der nachfolgenden
Ausbildung osmoregulatorischer Fähigkeiten, hat Limnoperna und Dreissena befähigt,
Hartsubstrat in Süßwassersystemen zu erobern. In diesem Lebensraum begegnet ihnen
keine Konkurrenz von Seiten der spezialisierten bodenbewohnenden Muscheln, wie sie

280

B. MORTON

für Süßwasser kennzeichnend sind. Die Besiedelung dieses Lebensraums überschneidet
sich bei Dreissena mit den Interessen des Menschen, soweit sie seine Wasserversorgung
betreffen; bei Limnoperna muß man damit vielleicht ebenso rechnen.

C.M.-B.

RESUME

ASPECTS DE LA BIOLOGIE ET DE LA MORPHOLOGIE
FONCTIONNELLE DES ORGANES DE NUTRITION ET DE DIGESTION
DE LIMNOPERNA FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA)

B. Morton

Limnoperna fortunei (Dunker) a été recemment introduit dans les canalisations du ser-
vice d eau de Hong Kong. La premiere apparition du mollusque peut étre rapportée au
commencement de la mise en service de canalisations entre Hong Kong et la Riviere de
l'Est en Chine.

On pense que Limnoperna pourrait imiter la rapide expansion spatiale réalisée par
Dreissena polymorpha en Europe et Corbicula manillensis en Amérique du Nord. Pour
cette raison, on a étudié les aspects significatifs de la morphologie fonctionnelle et de la
biologie de Limnoperna. Des comparaisons ont été faites avec d autres mytilidés et avec
Dreissena qui ressemble superficiellement а Limnoperna. Га possibilité d'une affinité
phylogénétique entre ces 2 animaux est écartée; les similitudes étant dues a une
évolution convergente et à l'adoption d'un mode de vie similiare. L'évolution de
l'hétéromairie, chez les Mytilacea et les Dreissenacea suivie de l’évolution du pouvoir os-
morégulateur, a rendu capable Limnoperna et Dreissena d'envahir avec succés les sur-
faces dures des canalisations d'eau douce. Dans cet habitat il п’у a plus la compétition
des bivalves endogés caractéristiques des eaux douces. La colonisation de cet habitat a
provoqué un conflit entre Dreissena et peut-ére aussi Limnoperna, et les intéréts
humains en matiére de distribution d eau douce.

ALE:

RESUMEN

ALGUNOS ASPECTOS DE LA BIOLOGIA Y MORFOLOGIA FUNCIONAL
DE LOS ORGANOS DIGESTIVOS DE LIMNOPERNA FORTUNEI
(DUNKER) (BIVALVIA- MYTILACEA)

B. Morton

Limnoperna fortunei (Dunker) fué introducida recientemente en el sistema de
abastecimiento de agua potable en Hong Kong. Esta introducción se relacionó con la in-
iciación de la toma de agua en Hong Kong del río del Este, en China.

La rápida expansión de Limnoperna sugiere que puede repetirse la experiencia de
Dreissena polymorpha en Europa y Corbicula manillensis en Norte América. Por tal
razón se investigaron los aspectos pertinentes a la morfología funcional de Limnoperna, y
se hicieron comparaciones con otros mitilidos, y con Dresissena a la cual Limnoperna se
asemeja superficialmente. Se descarta la posibilidad de afinidad genética entre esos dos
animales, y las similaridades que presentan se deben a evolución convergente y a la adop-
ción de hábitos semejantes. La evolución de la condición heteromiaria en los Mytilacea y
Dreissenacea, seguida de una evolución subsequente de poder osmoregulatorio, ha

BIOLOGY AND FEEDING OF LIMNOPERNA

capacitado a Limnoperna y Dreissena para la invasion favorable de las superficies duras
en los sistemas fluviales: en tal habitat estan libres de la competencia de los bivalvos que
son caracteristicos de las aguas dulces. La colonización de Dreissena, que ha entrado en
conflicto con los intereses humanos para la provisión de agua dulce, puede repetirse con
el mismo conflicto en el caso de Limnoperna.

J.J.P.

АБСТРАКТ

НЕКОТОРЫЕ АСПЕКТЫ БИОЛОГИИ И ФУНКЦИОНАЛЬНОЙ МОРФОЛОГИИ
ОРГАНОВ ПИТАНИЯ И ПИЩЕВАРЕНИЯ ЛВУСТВОРЧАТОГО МОЛЛЮСКА
LIMNOPERNA FORTUNEI (DUNKER), MYTILACEA

Б. МОРТОН

Limnopevna fortunei (Dunker) недавно была интродуцирована в пресноводнук
систему водоснабжения Гонконга. Изначальная встречаемость этого моллюска
здесь может быть связана с началом водоснабжения Гонконга из рек
восточного Китая.

Предполагается, что Limnoperna могла бы конкурировать C быстрым

расселением Dreissena polymorpha в Европе и Corbicula manillensis в Северной

Америке. Поэтому были исследованы соответствующие аспекты функциональной
морфологии и биологии Limnoperna. Было проведено сравнение с другим!

митилидами и с Dreissena, на которую Limnoperna внешне похожа. Возможность
филогенетической близости между этими двумя животными не принимается в
расчет. Сходство происходит благодаря конвергентной эволюции и адаптации
к сходным условиям обитания. Эволюция гетеромиарных признаков у Mytilacea
и Dreissenacea, сопровождалась последующей эволюцией осморе гулятерных
способностей и дала возможность Limnoperna и Dreissena успешно освоить
твердый субстрат в пресноводных системах. В таких местообитаниях у них
нет конкуренции с не специализированными двустворчатыми моллюсками
инфауны, характерными для пресных вод. Заселение этого меестосоитания

ДЛрейссеной и, возможно, Limnoperna, может вступать в противоречения ©
интересами людей, имея ввиду снабжение пресной водой.

Z.A.F.

281

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MALACOLOGIA, 1978, 12(2): 283-293

THE RECTUM OF “MODIOLUS” DEMISSUS
(DILLWYN) (BIVALVIA: MYTILIDAE): A CLUE TO
SOLVING A TROUBLED TAXONOMY!

Sidney K. Pierce, Jr.

Department of Zoology
University of Maryland
College Park, Maryland 20742, U.S.A.

ABSTRACT

The ribbed mytilid mussel Modiolus demissus (Dillwyn) has been placed in several
genera during the past 150 years. Although Arcuatula (Jousseaume) Lamy, 1919,
Geukensia, Van de Poel 1959, and Ischadium Jukes-Brown, 1905, have all been recently
proposed as the correct generic taxonomic position for this species, M. demissus has per-
sisted in the general literature.

Data are reported which demonstrate a profound morphological difference between
the relationship of the organs in the pericardial cavity of both Modiolus demissus and
Ischadium recurvum, and that of other mytilids. The rectum of these 2 mussels, rather
than passing through the pericardial cavity inside the ventricle as in other mytilids,
leaves the heart through the dorsal surface of the ventricle about mid-way through the
pericardial cavity. The rectum then passes in an are to the posterio-dorsal region of the
pericardial cavity. Thus, the posterior end of the ventricle is not anchored in place as oc-
curs in other mytilids.

Internally, the typical mytilid rectum shows a reduced, flattened typhlosole. The
Modiolus demissus rectum, in contrast, has a well-developed typhlosole which protrudes
markedly into the rectal lumen.

These morphological features, in company with shell morphology and some previously
reported physiological data, are used to support the isolation of the ribbed mussel both

from Modiolus and from other mytilid genera, and its relocation in Arcuatula.

INTRODUCTION

The systematics of the family Mytilidae
has long been in turmoil. Thus, although a
burgeoning literature deals with the
various aspects of the biology of the
mytilids, the continuing taxonomic
juggling and the resulting incorrect iden-
tifications have made interpretation of this
literature most difficult. B. R. Wilson, in
Australia, is presently attempting the
monumental task of sorting out the
taxonomy and systematics of this family on
the basis of soft-part morphology (pers.
comm. ).

The specific taxon Mytilus demissus
Dillwyn 1817 has been shuffled amongst

several generic groups during the past 150
years. It has been perhaps most commonly
recognized as a member of Modiolus
Lamarck, 1799. Soot-Ryen (1955),
however, placed this species in Arcuatula
(Jousseaume) Lamy 1919, pointing out
that Jousseaume chose Modiola plicatula
Lamarck (=demissa Dillwyn) as the type
of the genus although *Arcuatula certainly
was intended to be used for Modiola ar-
cuatula Hanley.” Soot-Ryen (1955), essen-
tially redescribing Arcuatula, lists the
following shell characteristics in support of
the change: “the radial sculpture,
crenulated anterior margin resulting from
radial folds on the lunule, weak nymphae
and light ligament.” Subsequently, Van de

! Contribution No. 4 from the Tallahassee, Sopchoppy and Gulf Coast Marine Biological Association

(283)

284 5. К. PIERCE

Poel (1959) proposed Geukensia Van de
Poel (1959) as the appropriate generic
designation for “Modiolus” demissus
simply stating that Soot-Ryen (1955) had
badly interpreted Lamy's (1919) descrip-
tion. Most recently, Kenk (1966) has
placed “Modiolus” demissus in Ischadium
Jukes-Brown 1905, thereby allying it with
another problematical mussel I. recurvum
Rafinesque, 1820. Kenk (1966) used both
shell and soft-part morphologies to support
this generic change, but she ignored
several important differences in the shell
morphologies which seem to make her
change inappropriate. These differences
are discussed subsequently. Apparently
none of these suggestions has been widely
accepted, for the designation Modiolus
demissus persists.

Mention should also be made of some
taxonomic confusion presented by another
mytilid mussel used in this study.
Modiolus americanus Leach, 1815, a taxon
applied to subtidal mussels from the west
coast of Florida, is apparently a mixture of
2 species (Beauperthuy, 1967). On the
basis of shell characteristics, a new species
M. squamosus Beauperthuy, 1967, has
been described as distinct from M.
americanus. Modiolus squamosus is the
predominant subtidal mussel found in
Apalachee Bay and St. George Sound off
the coast of north Florida. Although the
identity of the species used in this study
has been confirmed for me by Wilson
(pers. comm.) as being M. squamosus, R.
T. Abbott (Delaware Museum of Natural
History, pers. comm.) considers this
mussel to be a subspecies of M. modiolus
(Linnaeus) since, according to him, half-
grown specimens of M. modiolus and M.
squamosus are absolutely inseparable.
However, the morphology of the
periostracum of the 2 species is quite
different (see Soot-Ryen, 1955, and
Beauperthuy, 1967), and regardless of size,
members of the 2 forms can readily be dis-
tinguished on the basis of this structure.
Since the morphology of the periostracum
is used as a taxonomic character,
Beauperthuy's species should probably
stand.

Consideration of characteristics, other
than shell structure, might facilitate the
construction of a more reliable and
durable mytilid classification, free of the
present taxonomic conflicts. To this end, a
study of the comparative morphology of
the pericardial region of several mytilids
was carried out, after preliminary ex-
amination of this region in several species
of “Modiolus” had already indicated some
morphological variation. A considerable
literature on the comparative morphology
(both gross and histological) of the bivalve
pericardial cavity and associated struc-
tures indicates familial constancy of the
arrangement of organs contained therein
(e.g. White, 1942; Jegla & Greenberg,
1968a,b). The pericardial complex in 5 dif-
ferent species was examined here for both
organological and histological organiza-
tion and its variation. The differences pre-
sented here elucidate the taxonomy of the
genus Modiolus.

MATERIALS AND METHODS

The mytilids used in this study were
Mytilus edulis (Linnaeus), Modiolus de-
missus granosissimus (Sowerby), Modiolus
demissus demissus (Dillwyn), Modiolus
squamosus (Beauperthuy), and Ischadium
recurvum (Rafinesque). Specimens of М.
edulis were obtained from the Supply
Department of the Marine Biological
Laboratory, Woods Hole, Massachusetts.
Modiolus demissus granosissimus were
collected in a salt marsh on the tip of Alli-
gator Point, Franklin County, Florida; the
northern subspecies, M. d. demissus, were
collected from the shore of the Patuxtent
River near Solomons Island, Maryland.
Modiolus squamosus specimens were
found just below the low tide mark on the
seaward edge of a sand bar in Alligator
Harbor, Franklin County, Florida.
Ischadium recurvum were collected from
oyster trays suspended from the pier of the
Chesapeake Biological Laboratory,
Solomons Island, Maryland.

The morphological relationships of the
pericardial regions of these mussels were
studied by both gross dissection and light
microscopy. The following histological

RECTUM OF MODIOLUS 285

procedure was used. The ventricle,
auricles, and rectum were removed intact
from large mussels and fixed in aequeous
Bouin s fixative. Small whole animals were
placed in formic Bouin s fixative in order
to simultaneously decalcify the valves and
fix the tissues. Fixed tissues were de-
hydrated in an alcohol series, cleared in
methyl salicilate, and imbedded in paraf-
fin for sectioning. Sections were cut at a
thickness of 7-10u and stained with either
Masson's trichrome stain or Azure A and
eosin (cf. Humason, 1967).

The valve measurements reported were
taken from single valves using vernier
calipers or dividers and a mm scale.

OBSERVATIONS AND DISCUSSION

Kenk (1966) placed “Modiolus”
demissus in Ischadium listing the fol-
lowing distinctive features of the shell
morphology: “sculpture consisting of
bifurcating radial striations covering most
or all of the shell, dorsal angle obtuse and
broadly rounded, umbonal keel low, an-
terior hinge teeth consisting of crenula-
tions corresponding to the anterior ex-
ternal ribbing, post ligamental teeth
absent. This is a misleading description,
both of “Modiolus” demissus and of the
type of genus, I. recurvum. The anterior
hinge teeth of I. recurvum are dysodont
teeth corresponding to the radial ridges of
the lunule and appearing quite like those
of Mytilus edulis. “Modiolus” demissus, of
course, totally lacks anterior hinge teeth.
In addition, the valves of the 2 species
differ in several other respects which Kenk
(1966) either attributed to allometric
growth or failed to mention. Ischadium
recuroum is characterized by a broad
mytiliform shape, anterior slightly sub-
terminal umbones, ligament which
extends anteriorly past the anterior byssus
retractor muscle scar, and the lack of an
anterior adductor scar. In contrast, the
shell of “Modiolus demissus is basically
an elongated modioliform shape, with dor-
sal angle much less obtuse, no hinge teeth,
umbones more inflated and posterior than
I. recurvum, ligament beginning well
posterior to the anterior byssus retractor

scar, and an obvious, ovoid anterior adduc-
tor scar. Thus, on the basis of shell
morphology alone, “ Modiolus’ demissus
does not seem to belong in Ischadium.
In spite of the differences in shell
morphology between these 2 species, the
soft parts of “Modiolus” demissus and I.
recuroum have in common а striking
morphological feature which distinguish
them not only from other species of
Modiolus but also from those of Mytilus as
well. This feature occurs within the peri-
cardial complex and concerns the rela-
tionship of the rectum with the ven-
tricle. Most mytilid ventricles are
suspended from 4 points: anteriorly from
the aorta and rectum, posteriorly from the
rectum and laterally from the auricles. The
rectum passes longitudinally through the
entire lumen of the ventricle, and therein
throughout the length of the pericardial
cavity. Such an arrangement of rectum
and ventricle has been described in several
mytilids (Field, 1922; White, 1942; Jegla
& Greenberg, 1968a), and is illustrated in
Modiolus squamosus, in Fig. 1.

The suspension of the ventricles of
“Modiolus” demissus (Fig. 2) and
Ischadium recurvum is quite different
from the standard mytilid plan and results
from the modified path of the rectum
through the pericardial cavity. The rectum
passes only through the anterior portion of
the ventricle. Then, emerging from the
dorsal surface of the ventricle, it arches
dorsally, in its own sheath, along the roof
of the pericardial cavity, proceeding to its
exit at the posterior end of the cavity. The
posterior half of the ventricle, unsup-
ported by the rectum, hangs freely in the
pericardial cavity. The anterior end of the
ventricle is suspended and anchored by
the auricles and the rectum. One obvious
physiological consequence of this arrange-
ment is that the direction of ventricular
beat in these 2 species is from posterior to
anterior, rather than from lateral to medial
as in most mytilids.

It is difficult to ascribe any functional
advantage to either plan of rectum
traverse through the pericardial cavity of
these mussels. There is, however, another

286 5. К. PIERCE

ДА ee =< u ad «re = > SERLE ler Ro Tr Sa
xs > > => y E ers

FIG. 1. The pericardial complex of Modiolus squamosus. The pericardial membrane has been
removed to reveal the ventricle with the rectum (1) passing internally between the anterior
(2) and posterior (3) attachments of the ventricle. Note that throughout the length of the
pericardial cavity, the rectum is inside the ventricle. The ventricle is suspended laterally, at
the atrio-ventricular junction (4), by the glandular auricles (5).

FIG. 2. The pericardial complex of Modiolus demissus granosissimus. The pericardial membrane
has been removed. The rectum enters the ventricle at the anterior end of the pericardial
chamber (1). The rectum then passes through the anterior portion of the heart and emerges
through the dorsal surface of the ventricle (2), leaving the posterior portion of the ventricle
(3) free in the pericardial chamber. Laterally, the ventricle is suspended by the atria (4) at
the atrio-ventricular junction (5). Note that the rectum has been separated from the mantle
(6) posterior to its exit from the ventricle.

RECTUM OF MODIOLUS 287

TABLE 1
Distances from the most dorsal point of the posterior muscle scar to the dorsal valve edge of Mytilus
edulis and Modiolus demissus. (n=25/species)

Distance from
Species Valve length Valve width posterior muscle
at longest point at widest point scar to dorsal
valve edge

Mytilus edulis 58.9° 28.4 4.6
(+5.8) (43.3) (ESO)

Modiolus demissus 61.1 24.0 3.8
(Gallo) (E12) (+0.6)

° Distance in mm
(+ S.D.)

FIG. 3. Cross-section of the ventricle and rectum of Mytilus edulis in the region of the atrio-
ventricular junction showing the reduced typhlosole (T) and the mid-ventral furrow (М).
Trichrome stain, 40Х. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum;
C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V-ventricular
muscle.

288 5. ©. PIERCE

morphological difference between Mytilus
edulis, Modiolus squamosus and Modiolus
demissus which may account for the plan
shown by M. demissus. The rectum in
these mytilids, after leaving the ventricle
and pericardial cavity, passes dorsally over
a complex of muscles comprised of the pos-
terior adductor, posterior byssus retractor,
and posterior pedal retractor. If this mus-
cle complex were located farther dorsad
with respect to the heart in М. demissus
than in М. edulis, the rectum of М.
demissus would also have to follow a more
dorsal route. In order to test this possibili-
ty, measurements were made of the dis-
tance between the highest point of the
posterior muscle scar complex and the dor-

sal edge of the valve in specimens of M.
demissus and M. edulis of approximately
equal length. These measurements, sum-
marized in Table 1, indicate that, indeed,
the posterior muscle complex of М.
demissus is located some 20% closer
(P<0.1) to the dorsal valve margin than
that of M. edulis.

I hasten to acknowledge the difficulties
of drawing comparative conclusions based
on valve measurements from different
species of bivalves. The necessary assump-
tions of identical growth patterns, iden-
tical size and shape and identical organ
placement are at best tenuous and most
likely unwarranted (for a detailed dis-
cussion see Stasek, 1963; Stanley, 1970). In

FIG. 4. Cross-section of the ventricle and rectum of Modiolus squamosus in the region of the atrio-
ventricular junction showing the reduced typhlosole (T) and the mid-ventral furrow (М).
Trichrome stain, 40X. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum;
C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V-ventricular
muscle.

RECTUM OF MODIOLUS 289

FIG. 5. Cross-section of the ventricle and rectum of Ischadium recurvum in the region of the atrio-
ventricular junction showing the reduced typhlosole (T) and mid-ventral furrow (M). The
rectum has already passed out of the dorsal surface of the ventricle. Azure A and eosin stain,
40X. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum; C-connective
tissue layer; W-outer wall of rectum; V-ventricular muscle.

fact, there may be a sound embryological
or physiological explanation for the heart-
rectum plan exhibited by Modiolus
demissus and Ischadium recurvum, but to
date an alternative explanation is not evi-
dent.

While it is tempting to stress the
taxonomic implications of the similarities
of organ arrangement in the pericardial
cavities of Modiolus demissus and
Ischadium recurvum rather than the
difference in shell morphology, the rectum
itself offers further evidence in favor of the
generic separation of these 2 species.

The internal morphology of the rectum
of “Modiolus” demissus is also different
from that of other mytilids including
Ischadium recurvum. Fig. 3 shows a cross-

section of the rectum of Mytilus edulis, as
it passes through the ventricle in the
region of the atrio-ventricular junction.
Fig. 4 shows a similar section for Modiolus
squamosus and Fig. 5 a similar section for
I. recuroum. The rectums of these 3
mussels correspond quite closely to that of
the generalized rectum of the Anisomyaria
described by Jegla & Greenberg (1968a,b).
In particular they are thin-walled, with
few muscle fibers and the intestinal
typhlosole is reduced to 2 wide ridges with
a mid-ventral furrow. The rectum of М.
demissus (Fig. 6), on the other hand, de-
viates from this plan. While it is also thin-
walled and shows few muscle fibers, the
typhlosole protrudes markedly into the
rectal lumen, resembling more closely the

290 5. Ke/ PIERCE

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FIG. 6. Cross-section of the ventricle and rectum of Modiolus demissus granosissimus in the region
of the atrio-ventricular junction showing well developed typhlosole (T) and median ventral
furrow (M). Note that the rectum has already passed out of the dorsal surface of the ventri-
cle. Trichrome stain, 40X. LR-lumen of rectum; E-ciliated columnar ephithelial lining of
rectum: C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V-
ventricular muscle; P-pericardial space.

RECTUM OF MODIOLUS 291

rectum of Atrina rigida Solander, 1786
[Pinnidae], than that of other mytilids (see
Jegla & Greenberg, 19684).

Interestingly, observed pharmacological
differences between Modiolus’ demissus
and other mytilids may substantiate the
suggested taxonomic validity of the
morphological findings reported here.
Greenberg (1968) has observed that the
tone and amplitude of beat of the isolated
heart of M. demissus is depressed by 5-
Hydroxytryptamine (5-HT). The hearts of
M. americanus (actually M. squamosus)
and M. modiolus, as well as Mytilus spp.
are excited by 5-HT (Greenberg, 1968).
Greenberg (1968) suggested that this dif-
ference is a taxonomic feature. Unfor-
tunately comparable pharmacological data
are not available for Ischadium recurvum.
Physiological data of this kind may prove
to be a useful taxonomic tool, for although
many physiological differences exist
between M. demissus and other mytilids,
most appear to be a function of the ex-
tremely high intertidal position occupied
by M. demissus (Lent, 1969; Pierce, 1970,
1971). Pharmacology, on the other hand,
would appear to be a physiological
parameter which is not intimately depen-
dent on environmental influences.

Finally, “Modiolus” demissus occupies
a habitat which is rare or unique among
the bivalves. One of the mussels used in
this study, Modiolus squamosus occurs
subtidially in marine environments only.
Both Mytilus edulis and Ischadium recur-
vum are found in the intertidal zone and
occur well up into brackish water. М.
demissus, also occurring in the intertidal
zone and in brackish water, occupies a
habitat that is virtually semi-terrestrial. In
fact, in most areas of its occurrence along
the eastern and Gulf coasts of the United
States, М. demissus spends more time ex-
posed to the atmosphere than submerged.
Unlike other bivalves which close the
valves tightly while exposed to air, М.
demissus keeps its valves ajar and respires
aerially (Lent, 1969).

Thus, “Modiolus” demissus exhibits
several morphological and physiological
features, along with an unusual еп-

vironmental position, which serve to dis-
tinguish it from other members of the
genus Modiolus and from other genera in
the Mytilidae. These data, together with
the shell morphology described by Soot-
Ryen (1955), strongly support the shifting
of this species into the mytilid genus Ar-
cuatula (Jousseaume) Lamy 1919.

ACKNOWLEDGEMENTS

The author thanks Dr. Michael J.
Greenberg for providing the facilities with
which much of this research was done.
Thanks also to Dr. Barry W. Wilson for
verification of the identification of
Modiolus squamosus and for helpful com-
ments on the preliminary manuscript.
Finally, the author is grateful to Mr. Larry
Wolter for his excellent assistance with the
valve measurements.

LITERATURE CITED

BEAUPERTHUY, I., 1967, Los Mitilidos de
Venezuela (Mollusca: Bivalva). Bol. Inst.

Oceanog. Univ. Oriente, 6: 7-115.

FIELD, I. A., 1922, Biology and economic
value of the sea mussel Mytilus edulis. Bull.
Bur. Fish., 38: 127-259.

GREENBERG, M. J., 1968, Comparative
physiology of the heart: Current trends.
Experientia, Suppl., 15: 250-265.

HUMASON, G. L., 1967, Animal tissue
techniques, W. H. Freeman and Co., San
Francisco, 569 p.

ТЕСТА, T. С. € GREENBERG, M. J", 1968a,
Structure of the bivalve rectum, I.
Morphology. Veliger, 10: 253-263.

JEGLA, T. C. & GREENBERG, M. J., 1968b,
Structure of the bivalve rectum, II. Notes on
cell types and innervation. Veliger, 10: 314-
319.

КЕМК VIDA © 1966;
Brachidontes (Mollusca-Bivalvia).
thesis, Harvard University.

‚AMY, E., 1919, Les Moules et les Modioles de
la Mer Rouge (D’apres les materiaux
recueillis par M. le Dr. Jousseaume). Bull.
Mus. Hist. Nat. Paris, 25: 173-178.

LENT, C. M., 1969, Adaptations of the ribbed
mussel, Modiolus demissus (Dillwyn), to the
intertidal habitat. Amer. Zool., 9: 283-292.

PIERCE, 5. K., JR., 1970, The water balance of
Modiolus (Mollusca: Bivalvia: Mvtilidae):

А revision of
PhD;

—

292

Osmotic concentrations in changing
salinities. Comp. Biochem. Physiol., 36: 521-
533.

PIERCE, S. К., JR., 1971, Volume regulation
and valve movements by marine mussels.
Comp. Biochem. Physiol., 39A: 103-117.

SOOT-RYEN, Т., 1955, A report on the family
Mytilidae, Allen Hancock Pacific
Expeditions, 20: 1-174.

STANLEY, S. M., 1970, Relation of shell form

эк. -PIERGE

STASEK, C. R., 1963, Orientation and form in
the bivalved Mollusca. J. Morphol., 112: 195-
214.

VAN DE POBLE, Ш. 1959. Faune
malacologique du Hervien, Troisieme note
(premiere partie). Bull. Inst. Roy. Sci. Nat.
Belgium, 35: 1-26.

WHITE, K. M., 1942, The pericardial cavity
and the pericardial glands of the
Lamellibranchia. Proc. malacol. Soc. Lon-

to life habits in the Bivalvia (Mollusca). Geol.

don, 25: 37-88.

Soc. Amer., Memoir 125, 296 p.

ZUSAMMENFASSUNG

DAS REKTUM VON “MODIOLUS” DEMISSUS
(DILLWYN) (BIVALVIA: MYTILIDAE):
EIN SCHLUSSEL ZUR LOSUNG EINES
VERWORRENEN TAXONOMISCHEN PROBLEMS

5. К. Pierce, Jr.

Die gerippte Mytilide Modiolus demissus (Dillwyn) wurde in den vergangenen 150
Jahren in wechselnden Gattungen untergebracht. Zwar wurden Arcuatula (Jousseaume)
Lamy, 1919, Geukensia, Van de Poel, 1959, und Ischadium Jukes-Brown, 1905, in letzter
Zeit als korrekte Gattungszugehórigkeit ftir diese Art vorgeschlagen, doch hat sich
Modiolus demissus allgemein in der Literatur gehalten.

Es werden Daten geliefert, mit denen ein tiefgreifender morphologischer Unterschied
in den Verhältnissen der Organe der Pericardialhöhle zwischen М. demissus und I.
recurvum einerseits und anderen Mytiliden andererseits gezeigt werden kann. Anstatt im
Innern des Ventrikels durch die Pericardialhöhle zu verlaufen, wie bei anderen
Mytiliden, verlässt das Rektum dieser 2 Muscheln das Herz vielmehr durch die dorsale
Oberfläche des Ventrikels, ungefähr durch die Mitte der Pericardialhöhle. Dann verläuft
das Rektum bogenförmig in den posteriodorsalen Teil des Pericards. Das hintere Ven-
trikelende ist also nicht hier verankert, wie das bei anderen Mytiliden der Fall ist.

Innerlich zeigt das typische Mytiliden-Rektum eine zurückgebildete abgeflachte
Typhlosolis. Das M. demissus-Rektum hat dagegen eine voll ausgebildete Typhlosolis,
die deutlich ins Darmlumen ragt.

Diese morphologischen Merkmale werden, zusammen mit der Schalenmorphologie
und einigen früher berichteten physiologischen Angaben, dazu verwendet, die
Aussonderung der gerippten Muschel sowohl aus der Gattung Modiolus als auch aus
anderen Mytilidengattungen und die Wiedereingliederung in die Gattung Arcuatula zu
unterstützen.

C.M.-B.

RESUME

LE RECTUM DE “MODIOLUS” DEMISSUS
(DILLWYN) (BIVALVIA, MYTILIDAE):
UN INDICE POUR RESOUDRE UNE TAXONOMIE INSTABLE

5. К, Pierce, Jr.
La moule striée Modiolus demissus (Dillwyn) a été placée dans plusieurs genres,

durant les 150 derniéres années. Bien que Arcuatula (Jousseaume) Lamy, 1919, Geuken-
sia, Van de Poel, 1959 et Ischadium, Juke-Brown, 1905, aient été récemment proposés

RECTUM OF MODIOLUS

comme position correcte en taxonomie générique pour cette espéce, Modiolus demissus a
persisté dans la littérature scientifique.

Certaines données démontrent une profonde différence morphologique entre les
organes de la cavité péricardique d'une part de М. demissus et 1. recurvum et, d autre
part, ceux des autres mytilidés. Le rectum de ces 2 moules, bien que traversant la cavité
péricardique à l'intérieur du ventricule, comme chez les autres mytilidés, quitte le coeur
par la surface dorsale du ventricule à peu pres à mi-chemin а travers la cavité péricar-
dique. Le rectum passe alors dans un arc vers la région postérodorsale de la cavité
péricardique. Ainsi, la partie postérieure du ventricule n'est pas tenue en place comme
cela arrive chez les autres mytilidés.

Intérieurement, le rectum typique de mytilidé montre un typhosole réduit, aplati. Le
rectum de M. demissus, par contre, posséde un typhosole bien développé qui fait nette-
ment saillie dans la lumiére du rectum.

Ces faits morphologiques, en relation avec la morphologie de la coquille et de
quelques données physiologiques précédemment décrites, sont utilisés pour établir la
distinction de la ‘moule striée” vis-a-vis de Modiolus et des autres genres de mytilidés et
pour l'intégrer dans le genre Arcuatula.

ACL:

RESUMEN

EL RECTO DE “MODIOLUS” DEMISSUS (DILLWYN)
(BIVALVIA: MYTILIDAE): INDICADOR PARA LA
SOLUCION DE UNA INTRINCADA TAXONOMIA

S2 К Pierce ir:

El mytilido -mejillón rayado- Modiolus demissus (Dillwyn) ha sido, durante los últimos

150 años, colocado en varios géneros diferentes. Aunque Arcuatula (Jousseaume) Lamy

1919, Geukensia Van de Poel, 1959, e Ischadium Jukes-Browne, 1905 fueron todos, en
época más reciente, propuestos como las posiciones taxomicas correctas para esta especie,
Modiolus demissus persistió generalmente en la literatura.

Los datos que se han registrado evidencian una profunda diferencia morfológica entre
la relación de los órganos de la cavidad pericardial de M. demissus e I. recurvum, y
aquellos de otros mytilidos. El recto, en las dos especies mencionadas, en lugar de pasar
adentro del ventrículo a través de la cavidad pericardial -como en otros mytilidos-, sale
del corazón cruzando la superficie dorsal del ventrículo, en la parte relativamente media,
a través de la cavidad pericardial. Pasa, entonces, formando un arco, a la región postero-
dorsal de la cavidad. Así, la extremidad posterior del ventrículo no esta fijada al lugar en
que ocurre en otros mytilidos.

Internamente, el recto de un mytilido típico, muestra un ciego reducido y aplanado.
En M. demissus el recto contrasta por tener un ciego bien desarrollado como una
protuberancia que se interna marcadamente dentro del lumen rectal.

A estos caracteres morfológicos internos, acompañan aquellos de la concha y, junto
con otros datos registrados previamente acerca de su fisiologia, todos se utilizan para cor-
roborar la separación del mejillón rayado, tanto de Modiolus, como de los otros géneros
de mytilidos, y su re-colocación en Arcuatula.

LLP.

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MALACOLOGIA, 1973, 12(2): 295-338

THE ORIGIN AND EVOLUTION OF THE NEOGASTROPODA

W. F. Ponder

The Australian Museum
Sydney, Australia

ABSTRACT

The order Neogastropoda probably evolved from the Archaeogastropoda or from a
very primitive mesogastropod type, and not from the higher mesogastropods as is
generally believed. It is suggested that the unique features of the neogastropod alimen-
tary canal could be derived from existing structures in the archaeogastropods. The
Neogastropoda appear to have evolved into 3 groups, which are regarded here as super-
families, the Muricacea, Conacea and Cancellariacea.

The evolution of the various organ systems within the Neogastropoda is outlined and
the tendency to modify structures in a parallel fashion is noted. The relationships of each
family in the Muricacea is discussed. With 2 exceptions, it appears that within this group,
there are no natural higher groupings, probably because all of the families evolved from
a common ancestral form more or less simultaneously. Thus various structures are dis-
tributed in an almost random fashion throughout the superfamily according to the way in
which each family has evolved. The Marginellidae and Volutomitridae may have arisen
independently, whereas the Buccinidae, Melongenidae, Nassariidae and Fasciolariidae

are so closely related that they could possibly be regarded as subfamilies.

INTRODUCTION

The order Neogastropoda or Steno-
glossa is generally regarded as containing
the most highly advanced prosobranch
gastropods. They are characterized by the
elongate siphonal canal of the shell and
rachiglossate or toxoglossate radula. The
order is a large one, having at least 1119
Recent and fossil genera and subgenera
(Taylor & Sohl, 1962). This number is
similar to that of the Archaeogastropoda,
but is exceeded by the Mesogastropoda (as
defined by Thiele, 1929 and Wenz, 1938-
1943).

The large number of species and genera
speaks for the success of the
Neogastropoda. Although they are not
known to have invaded the land, and few
have penetrated into freshwater, they have
adapted to almost every marine environ-
ment, commencing with an explosive
radiation during the Cretaceous Period.

The order Neogastropoda is usually
divided into 2 suborders, the Toxoglossa
and the Rachiglossa. Thiele (1929) and
Wenz (1938) divided the Rachiglossa into

3 superfamilies (Stirps), the Muricacea,
Buccinacea and Volutacea. These
divisions have been accepted by the ma-
jority of later authors. The use of these
groupings is here considered open to ques-
tion and they have been abandoned for the
purpose of the following discussions.
Instead the name Rachiglossa will be used
to cover all 3 of them.

The object of this paper is to attempt to:
(1) clarify the origin of the Neogastropoda
and therefore its relationship to the
Mesogastropoda, (2) briefly examine the
various organ systems within the group,
and the evolution of the group and (3) re-
view the distinctive features of the families
of the rachiglossate neogastropods and to

arrange them in meaningful higher
categories.
Recommendation 29A of the Inter-

national Commission on Zoological
Nomenclature (ICZN) in 1961 recom-
mends the superfamily ending—oidea, but
this is not used in this paper because the
ending—acea has been used consistently
by most molluscan workers and this en-

(295)

296 W. F. PONDER

ding is used in the Treatise on Inverte-
brate Paleontology, a work which will be a
major reference source for students of the
Mollusca for a long time.

Some of the facts presented here are
based on the writer s unpublished observa-
tions. They are noted by the inclusion of
the writers initials in parenthesis
following such information.

The following account is divided into 3
parts; a discussion of the origins of the
neogastropods, the evolution of the main
organ systems and the higher clas-
sification of the order.

PART 1.
THE ORIGIN OF
THE NEOGASTROPODA
Most authors have indicated that the
neogastropods evolved’ from
proboscidiferous mesogastropods, such as
the Tonnacea. This belief has been
expressed by workers who have looked at
several different organ systems, including
Amaudrut (1898), Bouvier (1887),

Troschel (1865-1875), Perrier (1889),
Graham (1941), and Wilsmann (1942).

Morton (1963) expressed the belief that
there is little difference between the
higher Mesogastropoda and the Neo-
gastropoda and this view was also held by
Risbec (1955). Cox (1960) combined the
Mesogastropoda and the Neogastropoda,
calling them the Caenogastropoda. He
suggested that the Caenogastropoda were
polyphyletic, being derived from various
archaeogastropod taxa, which may have
even been distinct suborders, and that
they have no more in common than that
they have advanced to a certain stage
along more-or-less parallel lines of gas-
tropod evolution. One group, the Hetero-
gastropoda, was later separated from the
Mesogastropoda (Kosuge, 1966).

Knight, et al. (1954) have given the
most detailed scheme to be advanced re-
cently on the evolution of the Gastropoda.
They indicated that the Neogastropoda
were probably derived from the extinct
Subulitacea in the Mesozoic, that this
superfamily divided into the Muricacea,
Buccinacea and the extinct Nerineacea,

and that the latter gave rise to the
Volutacea and Conacea.

The 4 Recent superfamilies existed in
the early Cretaceous, all arising more-or-
less simultaneously, and all were clearly
recognizable and surprisingly modern in
appearance by the middle Cretaceous
(Sohl, 1964).

Patterson (1969) has shown that the
chromosome numbers of the
Mesogastropoda and Neogastropoda are
very different. The haploid number varies
from 28-36 in the Neogastropoda, 7-20 in
the Mesogastropoda and 9-21 in the
Archaeogastropoda. There is therefore lit-
tle relationship in the chromosome num-
bers of the neogastropods to those of the
other 2 orders; althowgh* the
Neogastropoda could have arisen by
polyploidy from either.

The evidence given below suggests that
the Neogastropoda are a group derived in-
dependently from an archaeogastropod or
a very primitive mesogastropod ancestral
form. They have followed certain general
gastropod evolutionary trends which have
resulted in their superficial similarity to
other groups, such as the carnivorous
mesogastropod superfamily Tonnacea.
These lines of evolution include the forma-
tion of a proboscis, the reduction of the
ctenidia to a single, monopectinate gill,
and the enlargement of the left os-
phradium and marked increase in its sen-
sory surface by the formation of lateral
leaflets. The enlargement of the os-
phradium was probably coupled with the
formation of an anterior siphon. A siphon
was probably present in the Subulitacea as
members of this group had а well-
developed anterior notch in the aperture.
The osphradium functions as an efficient
chemoreceptive organ in the
neogastropods (Kohn, 1961b), the anterior
siphon giving it directional significance.

Fig. 1 indicates how the foregut of the
Neogastropoda may have evolved. The
salivary glands (sg) in the early
archaeogastropods (Fig. 1, A) are simple
glandular sacs attached to the buccal cavi-
ty. They lie just behind the nerve ring (nr)
in many archaeogastropods, and probably

EVOLUTION OF NEOGASTROPODA 297

the salivary ducts of the ancestral
neogastropod were pulled, by the elonga-
tion of the snout, through the nerve ring at
this primitive stage of development (Fig.
1, B-D) as Graham (1941) suggested.

Two pairs of histologically different
salivary glands are found in the Acmaeidae
(Thiem, 1917) and also in some Neritidae.
In the latter family, in Theodoxus
(Whitaker, 1951) and Septaria (Bourne,
1908), the 2nd pair of salivary glands are
blind, glandular tubules which open into a
short, ventral extension of the buccal cavi-
ty below the odontophore. In structure
and position these glands resemble the
accessory salivary glands (asg) in the
Neogastropoda. The 2nd pair of salivary
glands found in some Archaeogastropoda
were probably present in the group that
give rise to the Neogastropoda, although it
is highly unlikely that the Neritacea or the
Patellacea were this group.

The structure of the mid-oesophagus is
of particular interest in the neogastropods
because it is this part of the alimentary
canal, together with the radula, which
provides the most distinctive and reliable
means of separating the group from the
remainder of the Prosobranchia.

Amaudrut's (1898) and Graham s (1941)
hypothesis for the derivation of the gland
of Leiblein (or “unpaired foregut gland”)
from an oesophageal gland is in keeping
with the hypothesis advanced here for an
archaeogastropod origin for the
Neogastropoda, although these authors
believed the group to have originated from
the highly evolved mesogastropod group,
the Tonnacea.

The valve (or pharynx) of Leiblein (vl)
(=esophageal bulb of Hyman, 1967) is
always composed of a glandular pad lying
around a ciliated cone or fold (v) which
acts as an oesophageal valve (Graham,
1941). Apparently the only function of the
glandular pad is to bind together food par-
ticles. There is not complete agreement
over the derivation of the valve of
Leiblein. Graham (1941) suggested that it
represents an enlargement of the
oesophageal dorsal folds. Amaudrut (1898)
supposed that this structure, together with

the glandular mid-oesophageal folds, 15
homologous with the oesophageal pouches
of the mesogastropods. Graham (1941)
rejected the idea because the oesophageal
pouches in mesogastropods, unlike the
dorsal folds, are ventral structures.

It does, however, seem possible that the
valve of Leiblein is homologous with the
buccal (or oesophageal) pouches (bp) of
primitive archaeogastropods (Fig. 1, A)
such as Haliotis and, other Zeugobranchia,
the Trochidae, and the Patellacea. These
pouches, at least in Haliotis, are lined with
tall, glandular cells which stain with acid
dyes (Crofts, 1929). Just behind the buccal
pouches in Haliotis are dorsal and ventral
ciliated valves and immediately behind
lies the glandular mid-oesophagus. The
oesophageal gland is confluent with the
mid-oesophagus over all of its length and
gradually revolves from a ventral to a dor-
sal position (Fig. 1, A; og). The homology
of the oesophageal pouches and the
stenoglossan valve of Leiblein is implied
by Hyman (1967) who refers to this struc-
ture in the oesophagus of all prosobranchs
as the “esophageal bulb.”

The anterior oesophagus of the
rachiglossan neogastropods probably
represents an elongation, coupled with a
ventral closure, of the roof of the buccal
cavity in front of the buccal pouches. This
idea is supported by the presence of dorsal
folds and the absence of ventral folds in
the rachiglossan anterior oesophagus. In
addition, the dorsal folds generally lie
laterally or ventro-laterally. In the more
advanced archaeogastropods and in the
mesogastropods, the anterior oesophagus
appears to have been derived by elonga-
tion behind the buccal pouches and valve
(Fig. 1, H, I) and, consequently,
sometimes has a pair of ventral folds. Thus
the anterior oesophagus in the Rachiglossa
and Mesogastropoda have different
origins. The buccal pouches and valves in
the Rachiglossa would thus be separated
from the buccal mass (Fig. 1, D) and, after
being pulled through the nerve ring by the
general elongation of the anterior gut,
would lie in the correct morphological
position for the valve of Leiblein (Fig. 1,

298 W. Е. PONDER

FIG. 1. Hypothetical evolution of the anterior and mid-gut of the ancestral types of the main groups of the
Neogastropoda. The oesophageal gland and salivary glands are stippled and the nerve ring is shown in solid
black. The dotted line in В, Е, and С indicate the scar left by the removal of the oesophageal gland; in E it
represents the dorsal food channel. The double-headed arrows indicate the area of elongation of the oesophagus.
A, Hypothetical archaeogastropod forerunner; В, conacean; С, cancellariacean; and D, muricacean ancestral
types. E, Hypothetical fore-runner of marginellid-volutomitrid group. F, Families showing torsion within or
behind nerve ring; С, Families showing torsion within valve of Leiblein. H, I, Mesogastropoda.

asg, accessory salivary glands; be, buccal cavity; bp, buccal pouch; df, dorsal folds; nr, nerve ring; og,
oesophageal gland; pr, proboscis; sg, salivary gland; у, oesophageal valve; vf, ventral folds; vl, valve of Leiblein.

EVOLUTION OF NEOGASTROPODA 299

E, Е, С). The glandular parts of the buccal
pouches must have spread around the
oesophageal wall and thus form the glan-
dular part of the valve of Leiblein. The
oesophageal valves would be homologous
with the ciliated cone overlying this pad.

The salivary ducts, which in other
prosobranchs enter the buccal wall, are
often embedded in the anterior
oesophageal wall (usually lying beneath
the dorsal folds) in rachiglossans, this
providing further evidence of the buccal
derivation of the anterior oesophagus in
the Rachiglossa.

The buccal pouches are variable in posi-
tion in the archaeogastropods, lying along-
side the buccal cavity in Haliotis, but be-
hind (as in Fig. 1, A) in Nacella (Haller,
1894) and in some lower mesogastropods
(Fig. 1, I) such as Littorina (Fretter €
Graham, 1962). The ancestral
neogastropod possibly had the glandular
buccal pouches lying on either side of the
anterior end of the mid-oesophageal gland
because the valve of Leiblein sometimes
lies at the site of torsion.

The buccal ganglia lie beneath the valve
of Leiblein, perhaps indicating the valve's
buccal origin. In the Cancellariidae
(Graham, 1966) and in proboscidiferous
mesogastropods, the buccal ganglia are
situated just behind the buccal mass and
have very long connectives, which pass
through the proboscis. Graham (1966)
showed that the mid-oesophagus lies in
front of the nerve ring in Cancellaria (Fig.
1, C) and that the valve of Leiblein is just
behind the buccal cavity. The mid-
oesophageal gland is probably represented
by a zone of glandular tissue lying below
the dorsal folds of the oesophagus. Thus,
in Cancellaria, the mid-oesophagus has
been pulled through the nerve ring and
the ventral valve of Leiblein (buccal
pouches) has not departed from its
primitive position.

In the toxoglossans the valve of Leiblein
has been lost (Smith, 1967) and may never
have evolved past the oesophageal pouch
stage. The mid-oesophagus presumably
commences immediately behind the buc-

cal cavity. This is suggested by the salivary
ducts entering the buccal cavity without
being attached to the oesophageal walls
and by the relative position of the nerve
ring. The development of a poison gland
by the stripping off of the glandular, mid-
oesophageal dorsal folds (Ponder, 1970a),
probably took place before the separation
of the Terebridae and Conidae from the
Turridae.

Graham (1941) stated that Nucella and
Buccinum must have evolved from
different groups because they exhibit dif-
ferent positions of torsion in the mid-
oesophagus. If this were the case then the
Vexillidae (Ponder, 1972b), Marginellidae
(Ponder, 1970a) and the Olividae (W.F.P.)
must have evolved from a 3rd group,
because in all of these families torsion oc-
curs just behind the nerve ring (Fig. 1, Е).
In the Muricidae, Turbinellidae (Ponder,
1973b), Volutidae (Ponder, 1970b) and
possibly the Mitridae (Ponder, 1972b) tor-
sion of the gut occurs within the valve of
Leiblein (Fig. 1, G), but in Buccinum
there is a gradual rotation throughout the
mid-oesophagus. There is a similar vari-
ability in the position of torsion in the
Archaeogastropoda (Fretter & Graham,
1962). The variations in the neogastropods
might have resulted from similar varia-
tions in the archaeogastropod ancestor that
were in evidence before the valve of
Leiblein was pulled through the nerve
ring. In the Volutomitridae (Fig. 1, E) the
oesophageal gland appears to have
retreated from the anterior part of the
mid-oesophagus and has become stripped
off from behind forwards (Ponder, 1972b).

Thus it would appear that the
divergence of the various rachiglossan
families commenced before the main

elongation of the proboscis and the
associated changes in the foregut and,
therefore, before the site of torsion of the
gut in each group became a stabilized
feature. If these suppositions are correct,
similarity in the position of torsion in 2 or
more groups would not necessarily in-
dicate a close relationship, as it would
probably have been evolved independent-
ly,

300

There are thus 3 basic
organization of the foregut in the
Neogastropoda. It is maintained here that
each has evolved quite separately and that
all were probably derived from an early
neogastropod forerunner before the
elongation of the snout to form a
proboscis. These groupings are: (1) The
rachiglossan group in which the dorsal
wall of the buccal cavity provided elonga-
tion of the oesophagus during the forma-
tion of the proboscis; (2) The cancellariids

in which the mid-oesophagus is the site of

elongation after being pulled through the
nerve ring; and (3) The toxoglossan
families in which the buccal mass has
remained in its primitive position im-
mediately in front of the nerve ring, the
formation of a proboscis being brought
about by the elongation of a tube connec-
ting the buccal cavity with the mouth (Fig.
В):

The 3 types of organization referred to
above form 3 natural groups within the
living Neogastropoda and will be referred
to in the following discussion in parts 1
and 2 as the Conacea, Cancellariacea and
Rachiglossa respectively. In part 3 it is sug-
gested that the name Muricacea be used
for the whole of the Rachiglossa but this
usage is avoided at this stage because of
the confusion that is likely to arise be-
tween the restricted and extended inter-
pretations of the Muricacea.

The origin of the rachiglossan and toxo-
glossan radulae has generally been
regarded as a natural progression from the
taenioglossan type. However, both the
taenioglossan and the stenoglossan radula
could have been produced from a reduced
rhipidoglossan type. A convenient
ancestral stenoglossan radula would have a
multicuspid central tooth, a pair of large
lateral teeth and a pair or more of marginal
teeth in each row (Fig. 2, No. 8). Such a
radula could have given rise to the steno-
glossan and taenioglossan types. A similar
radula with only one pair of marginal teeth
is seen in some members of the Clavinae
(Turridae). From this type of radula, the
rachiglossan and toxoglossan types may
have been derived. With the loss of the

patterns of

W. F. PONDER

lateral teeth and the central tooth the nor-
mal toxoglossan radula would result. Maes
(1971) believes that many turrid radulae
have 4 marginal teeth in each transverse
row. If this is the case the primitive toxo-
glossan radula would have had 2 marginal
teeth and may have closely resembled the
taenioglossan type. The cancellariid type
consists of a single row of peculiar,
elongated teeth (see Olsson, 1970), which
are probably pes with the central
teeth of the remainder of the
Neogastropoda.

Graham (1941) advanced the hypo-
thesis that the oesophageal gland in the
Rachiglossa was stripped from the mid-
oesophagus, during the elongation of the
proboscis, when the valve of Leiblein was
dragged forward through the nerve ring
(Fig. 1, F, G). The removal of this bulky
oesophageal gland left a scar, which shows
its original line of attachment. The gland
then opens by a narrow duct into the
posterior end of the mid-oesophagus. This
is a much more satisfactory arrangement in
a carnivorous gastropod than the widely
open connection seen in most meso-
gastropods and archaeogastropods. A
narrow duct to the oesophageal gland has
evolved independently in the Triphoridae
(Fretter, 1951). Possibly the advantages of
the possession of a narrow duct
precipitated its evolution in the
Rachiglossa, rather than the mechanical
explanation offered by Graham.

The stomach of some neogastropods re-
tains a gastric shield and recognizable style
sac (Smith, 1967a), and thus resembles
those of generalized archaeogastropods,
such as Monodonta (Graham, 1949). A
pronounced posterior caecum is found in
many neogastropod species, which may, in
some cases, be a secondary structure,
although in others it is probably the rem-
nant of a sorting caecum. Graham (1949)
summarized the advances of the
neogastropod stomach as including (1) the
loss of the caecum and therefore the ab-
breviation of the major typhlosole and in-
testinal groove, (2) the anterior migration
of the opening of the oesophagus coupled
with its opening into the main gastric cavi-

EVOLUTION OF NEOGASTROPODA 301

ty, (3) the loss of the sorting areas, and the
disappearance of the gastric shield. These
simplifications, Graham concluded, are
due to the carnivorous diet of the
neogastropods. These features were
observed by Graham (1949) in the
Muricidae, but Nassarius reticulatus (Lin-
naeus) was shown to have a gastric shield,
a long posterior caecum and a remnant of a
posterior sorting area. Morton (1960) and
Brown (1969) recorded a crystalline style
in 2 species of the Nassariidae, and Ponder
(1972b) noted a prominent gastric shield in
the Microvolutidae. Thus some of the
features of the archaeogastropod stomach
are. present in some groups of
neogastropods, whereas in others it has
become simplified, or, as in Alcithoe
arabica (Gmelin) (Ponder, 1970b), secon-
darily complex.

An anal (rectal) gland, such as that oc-
curring in many Neogastropoda has not
been definitely encountered in any
Mesogastropoda (Fretter & Graham, 1962,
р 233). Simple types do occur in the
Archaeogastropoda, in some members of
the Trochidae and Scissurellidae (Fretter
& Graham, 1962, p 233), where they are
actually an enlargement of the intestinal
groove or a pouch on the side of the end of
the rectum. They apparently have a
lubricating function, but it is conceivable
that a gland derived in this way could take
over an excretory function like that shown
for the neogastropod anal gland (Fretter,
1946).

The possession of а gonopericardial
canal in the male genital system of a few
neogastropods is a very primitive feature
and this is not shared by any
mesogastropod, although some show
traces of such a duct (Fretter & Graham,
1962). The development of an ingesting
gland from a median sperm pouch must
also have been an early development for at
least 2 of the superfamilies (Muricacea,
Conacea; as here recognized) have this
structure.

Other evolutionary trends in the
neogastropods run largely parallel to those
in the mesogastropods. The coiled shell
causes a loss of the right auricle, right renal

organ and right pallial complex. The right
renal organ remains only as an element in
the organization of the genital ducts,
whereas the pallial glandular parts of the
genital ducts may have been derived from
the right hypobranchial gland. The reduc-
tion and loss of the organs on the right side
has allowed the expansion of the left
ctenidium, osphradium and hypobranchial
gland, and also the migration of the rec-
tum to the right side of the pallial cavity.
Associated with these changes, the rectum
no longer penetrates the ventricle as it
does in many archaeogastropods and both
structures come to lie on opposite sides of
the body. The shell has lost its nacreous
layer and the operculum its spiral form.

Many of the above changes also took
place in the early mesogastropods, so that
it is probable that the 2 orders may have
been derived from the same
archaeogastropod group which was begin-
ning to show these tendencies. Separation
must, however, have been at a very early
stage if this were the case.

In summary it is suggested that the
neogastropods arose from an archaeo-
gastropod, or very primitive mesogastro-
pod, for the following reasons: 1.
Neogastropods have some organs not
found in mesogastropods but known in
some archaeogastropods. These include 2
types of salivary glands, a rectal pouch
(anal gland of neogastropods) and a gono-
pericardial duct in the male reproductive
system. 2. The anterior alimentary canal in
the mesogastropods and neogastropods
differs in the following ways. (a) The
salivary ducts pass through the circum-
oesophageal nerve ring in mesogastropods
and do not in the neogastropods. (b) The
valve of Leiblein seems to be derived from
the oesophageal pouches of an archaeo-
gastropod because in mesogastropods
these lie ventrally and the oesophageal
valve is lost. (c) The site of elongation of
the oesophagus is different in the
mesogastropods and in the 3 groups of
neogastropods.

The Subulitacea have all of the shell
features required in an ancestral
neogastropod. As well as the loss of the

302 W. Е. PONDER

nacreous layer and development of an
anterior notch, they have lost the primitive
median sinus and many have a columellar
fold. Knight, et al. (1960) suggested that
this group originated in the
Loxonematacea.

The adoption of a carnivorous mode of
life set the ancestral neogastropods apart
from their microphagous forebears. They
probably commenced feeding on en-
crusting and other colonial animals, a
habit seen in some modern archaeo-
gastropods, and still found in some
neogastropods. The Magilidae, for exam-
ple, may have been at first predatory
grazers on corals and have now become
suctorial, whereas the primitive vexillid
genus, Austromitra, is still found to feed
on ascidians (Ponder, 1972b).

The adoption of a carnivorous habit re-
sulted in a complex radiation, in which
nearly every marine environment was
penetrated. Rapid specialization followed
in feeding habits, habitat preferences and
morphology, so that the various family
groups appear more-or-less simultaneously
in the fossil record.

The rapid rise in the importance of the
neogastropods is paralleled by a similar,
but even more diversified, radiation in the
mesogastropods (Sohl, 1964).

PART 2.
EVOLUTIONARY TRENDS IN
THE NEOGASTROPODA

One of the most significant factors of
neogastropod evolution is the well-marked
tendency towards parallel evolution of the
various organ systems. Each family,
equipped as it was with a fundamental
neogastropod structure, has shown, de-
spite some degree of adaptive radiation, an
independent evolutionary tendency
towards a similar modification of the inter-
nal organs. Their internal structure is, on
the whole, rather uniform, but it is sug-
gested that the head-foot, shell and radula
underwent early adaptive modifications
which, from the outset, stamped a distinc-
tive pattern on each major group and on
the separate families within them.

The Shell, Head-foot and Pallial Cavity

These 3 parts of the animal will be
treated together, as they deal with the ex-
ternal environment and are often the first
structures to be modified by it. The basic
structure of the pallial cavity and head-
foot is shown in Fig. 5.

The shell in most neogastropods is large,
usually fusiform, rather heavy, has a long
or short anterior siphonal canal, and usual-
ly the animal can withdraw into it com-
pletely.

The great variability in shell form is
found within the Buccinidae and the
families allied to it that are included in
Thiele's Buccinacea (Fasciolariidae, Nas-
sariidae, Galeodidae, Turbinellidae,
Colubrariidae and Pyrenidae). The mem-
bers of these families are capable of
living on hard and soft substrata and their
foot is usually of moderate proportions,
but in those species found on hard sub-
strata the foot is often small (e.g., Buccinu-
lum (Bu:cinidae) and many
Fasciolariida ) and they generally have a
short anterio: siphon. The Nassariidae live
mainly on soft substrata and have a larger
foot, which reaches a considerable size in
Bullia (H. & A. Adams, 1853; Quoy &
Gaimard, 1833), and a long siphon. The
shell and foot are sometimes well adapted
for burrowing (e.g., Cyclope; Morton,
1960). Versatility in ecology is the keynote
to the success of these families.

The Turbinellidae and some
Fasciolariidae have developed columellar
plaits as a means of providing additional
surface for the attachment of the colu-
mellar muscle.

The pallial cavity in all of the above
families opens in front and on the right
side of the animal, but it is not placed as
far back on the right as in some of the
other families that are modified for
burrowing. An exception is seen in the
Pyrenidae in which the aperture is often
elongate.

Although the hypobranchial gland pro-
duces copious quantities of mucus and
other pale-coloured secretions, no purple
fluid is produced in any of the families
listed above.

EVOLUTION OF NEOGASTROPODA 303

The foot usually bears an operculum, al-
though this is lost in some Pyrenidae,
possibly because of their elongate con-
stricted apertures. The Nassariidae have 2
short tentacles on the posterior end of the
foot and the operculum is usually small.
The opercular nucleus in all of the above
families is usually terminal in position.

In contrast with the above families, the
Muricidae have solid, strongly or-
namented shells which often bear varices,
although parallel examples are occasional-
ly encountered in the Buccinidae (e.g.,
Phos, Hindsia). The muricids generally
live on hard surfaces so that the foot is
usually small. Concholepas peruviana
(Lamarck) is limpet-shaped, being the end
product of a trend in the “thaid” group to
enlarge the aperture and foot as an adap-
tation to life on wave-swept shores.

The pallial cavity in the Muricidae is
unspecialized and is probably the closest to
the primitive neogastropod type that exists
in the modern neogastropods. A purple
hypobranchial secretion is produced by
most muricids and has been shown by
several workers to contain a poisonous
component (reviewed by Halstead, 1965).

The siphon rarely projects much be-
yond the end of the siphonal canal of the
shell, although the canal itself, as in some
species of Murex, is occasionally very long.
The operculum is usually large and has a
terminal, subterminal or lateral nucleus.
On the sole of the foot there is an accessory
boring organ that secretes an acid and pos-
sibly a calcase enzyme which aids in the
boring of shells, a feature for which this
family is well known (Fretter, 1946;
Carriker, 1961, 1967; Smarsh, et al., 1969).

The Columbariidae have a small foot
and a very long anterior canal projects
from the small, round aperture of the shell.
The shell often bears 1 or 2 rows of spines;
the operculum is large and has a terminal
nucleus. Little is known of their habits ex-
cept that they mostly occur in deep water.

One of the most bizarre neogastropod
groups is the Magilidae. This family con-
tains genera whose shells resemble those of
the Muricidae (e.g., Coralliophila,
Tolema), and others in which the shells

have become limpet-shaped (e.g.,
Quoyula) or are embedded in coral and be-
come vermiform (e.g., Magilus). The
pallial cavity of the Magilidae is similar to
that of the muricids, but the osphradium is
small (Gohar € Soliman, 1963). The foot
in sedentary forms functions as a sucker,
aiding in boring the holes in which the
animals live (Gohar € Soliman, 1963). In
Tolema, which is presumably a free
moving member of the family, the foot is
similar in size to that of members of the
Muricidae (W.F.P.). An operculum with a
lateral nucleus is present in members of
this family.

Thiele's Stirps Volutacea contains an
assemblage of unrelated families, most of
which are modified, to some degree, for
burrowing in soft substrata. These families
are the Mitridae, Vexillidae,
Volutomitridae, Harpidae, Volutidae,
Marginellidae and Olividae. The first 4
families are the least modified, although
their shells have long, often narrow aper-
tures, an adaptation which culminates in
displacing the right angle (exhalant aper-
ture) of the pallial cavity far towards the
posterior end of the shell. This allows the
pallial cavity to function efficiently while
the animal is burrowing. The shells of the
first 3 families are sometimes elaborately
ornamented and are never covered by the
mantle or parts of the foot, and the foot is
of moderate size only. Some of the genera
in the Mitridae and Marginellidae have
become adapted to hard substrata but it
seems likely that they have been derived
from a burrowing ancestral form. In the
other families the shell is sometimes sculp-
tured, but rarely elaborately, and is usually
smooth.

By contrast with the earlier families,
most Marginellidae and a few Volutidae
have the mantle edges overlapping the
shell. In these 2 families the pallial cavity
has swung completely to the right, the
siphon lying immediately above the head
and the exhalant aperture opening on the
posterior edge of the long body whorl. In
most Volutidae the shield-shaped head is
formed from the fusion of the tentacle
bases, over the rhynchostome. There is

304 W. F. PONDER

usually a pair of siphonal lappets, which
aid in blocking off the anterior end of the
pallial opening.

In the Olividae the foot has reached its
greatest development. Lateral and anterior
flaps from the foot are developed which
sometimes enclose the shell completely
(e.g., Ancilla, Amalda). Pallial tentacles
are sometimes developed, but it appears
that the mantle never covers the shell in
the Olividae. The eyes are reduced or ab-
sent in the Olividae and small in most
Volutidae. The foot in the Olividae is
usually divided into an anterior segment
(propodium) and a large posterior portion
(metapodium). Wilson (1969) has shown
how the propodium is used as a swimming
organ in Ancillista cingulata (Sowerby).
D Orbigny (1841) recorded swimming ac-
tivity effected by movement of the
metapodial flaps in Oliva tehuelchana
(d’Orbigny), and Olsson (1956) and Mar-
cus & Marcus (1959) reported the same
type of swimming in Olivella species.

The Harpidae have a very large foot
which has a distinct propodium, as in the
Olividae, but the shell is not covered by
the animal (Quoy & Gaimard, 1833).

The columellae of all of the families in
this burrowing group of families, except
the Harpidae and Olividae, usually have
strong plicae, whereas the latter 2 have
weak plaits. Usually the foot is large in the
Volutidae, Olividae, Harpidae and
Marginellidae and the operculum lost,
although this is retained in some Olividae
and a few Volutidae. A purple hypo-
branchial secretion occurs in at least some
mitrids and volutes.

The enlargement of the foot, and par-
ticularly its encroachment on the shell in
the Olividae, has resulted in loss of the ver-
satility of movement seen in the Buc-
cinidae and its allies.

The Cancellariidae have neither the foot
nor the mantle cavity particularly
modified. They have all lost the oper-
culum and the shell is sculptured, ovate,
and usually has columellar folds. Little is
known about the habits of this family.

The conacean families have only 1 over-
all distinctive feature of the shell, and that

is the presence of a posterior sinus in the
aperture. The shell of the Turridae is often
spindle-shaped, with a long or short
anterior canal. The turrids appear to
match the Buccinidae in versatility of
habitat but, although there are a great
number of species, they are rarely in-
dividually abundant, and in particular are
lacking in the intertidal zone. The
Conidae, on the other hand, are often
abundant as individuals and also live on
both hard and soft substrata. Their shells
are cone-shaped, usually smooth, and the
spire is usually very short. In the sand
burrowing Terebridae the shell has a long,
slender spire, and it is smooth or weakly
sculptured. The foot in the majority of
conacean species is small, and the head in
the Conidae and Turridae bears prominent
eyes, which are often situated near the tips
of the tentacles. The eyes and tentacles are
usually reduced or lost in the Terebridae
and at least some species in this family pro-
duce a purple hypobranchial secretion.

The parallel evolution of shell features
has often resulted in a confused taxonomy.
Several families have developed members
that have a superficial resemblance to
genera in other families. Some examples
are the overall resemblance of the
Mitridae, Vexillidae and Volutomitridae,
the similarity of some Muricidae (e.g.,
Uttleya) to the Buccinidae and the
resemblance of genera such as Phyllo-
coma (Muricidae) and Colubraria
(Colubrariidae) to the Cymatiidae (Ton-
nacea).

The Alimentary Canal

The basic lay-out of the rachiglossan
alimentary canal is shown in Fig. 5. The
feeding habits of the majority of groups
are not discussed here, but a detailed sum-
mary is given by Purchon (1968).

The Proboscis: The proboscis in the
Rachiglossa is always of the pleurembolic
type and this form is also found in the
Cancellariacea (Graham, 1966). The
proboscis is usually relatively short and
broad in the small species of every family,
but in the larger species noticeable dif-
ferences occur. Those families which

EVOLUTION OF NEOGASTROPODA 305

specialize in grasping the prey with the
foot (Olividae, Volutidae) and the
Muricidae (which must use the pedal
accessory boring organ in conjunction with
the buccal mass in order to drill the shell of
their prey) have a short proboscis. The
Buccinidae, Nassariidae, Galeodidae and
Fasciolariidae usually have а long
proboscis and the walls of the proboscis
sac are normally capable of almost
complete introversion. This also applies to
Vasum in the Turbinellidae, but in Tur-
binella the very long, slender proboscis is
coiled in a wide, thin walled sac which is
not capable” of introversion (Ponder,
1973b). A similar sac with an even longer
proboscis is found in Columbarium spp.
and Coluzea spp. in the Columbariidae
(W.F.P.), whereas an intermediate type is
seen in Ratifusus reticulatus (A. Adams)
(=mestayerae Iredale), in the
Colubrariidae (Ponder, 1968) and in some
Mitridae (Ponder, 1972b). The species
with a long proboscis can “feed at a dis-
tance’ and are thus capable of preying on
animals that live in crevices, narrow holes
and tunnels. If additional length is
required in a proboscis that is already
packed into the cephalic cavity, the sheath
must become a wide sac to accommodate
the longer, and of necessity, narrower
proboscis.

The 2 specialized types of proboscis in
the Turridae that were described by Smith
(1967) can be derived from a more basic
type which also occurs within the family.
In the primitive subfamilies that extend
back into the Paleocene, the Turrinae,
Borsoniinae and the Clavinae, and the
even earlier Turriculinae (Powell, 1966)
(the Conorbiinae has not been examined
by the writer) there is a simple intraem-
bolic proboscis within a wide
rhynchodeum (proboscis sac). The long
tube, characteristic of the Conacea,
traverses the proboscis from the buccal
cavity at its base. In Splendrillia debilis
Finlay (Clavinae), Comitas onokeana
vivens Dell (Turriculinae) and Epidirona
gabensis (Hedley) (Turrinae) the proboscis
is of moderate size compared with the
rhynchodeum, but in Borsonia sp. and

Scrinium neozelanicum (Suter) (Bor-
soniinae) it is more elongate (W.F.P.).
This type also occurs in the Conidae
(Alpers, 1931; Shaw, 1915) and in Terebra
cancellata (О. € С.) (Risbec, 1953) and it
presumably gave rise to the advanced type
of intraembolic proboscis (Smith, 1967) by
the invagination of the distal end seen in
Parabathytoma luhdorffi (Lischke) in the
Borsoniinae (W.F.P.). Many species of
Mangeliinae have the advanced, intra-
embolic type of proboscis (Robinson, 1960;
Smith, 1967; W.F.P.) and some Conidae
have also developed it (Amaudrut, 1898).
It is characterized by a method of
proboscis retraction not found in the other
2 neogastropod superfamilies.

Another development from the primi-
tive toxoglossan proboscis resulted in the
reduction of the proboscis and an in-
creased emphasis on the development of
the mobile lips of the rhynchostome.
Intermediate stages in the development of
the polyembolic (Smith, 1967) type of
proboscis can be seen in some turrids, in
which the relatively small original
proboscis fills only half of the
rhynchodeum in the contracted state. A
very powerful sphincter surrounds the
long, narrow rhynchostomal opening
which is often produced into a snout. This
condition is seen in some advanced
Clavatulinae (Phenatoma rosea (Quoy €
Gaimard) and Maoritomella albula (Hut-
ton) (W.F.P.)) and in Pontiothauma spp.,
in the Daphnellinae (Pace, 1903). The
final stage of this development, in which
the rhynchostome forms a pseudoproboscis
(Rudman, 1969) which can be inverted, is
generally associated with the shortening of
the original proboscis. In some species
however, the 2 structures, both of
moderate length, coexist (Philbertia pur-
purea (Montagu) (=boothi Wood); Smith,
1967; and Hastula cinerea (Born); Marcus
& Marcus, 1960). Species in which the
original proboscis has become atrophied
include Philbertia leufroyi (Michaud)
(Mangeliinae); Cenodagreutes spp.
(Smith, 1967), Daphnella cancellata (Hut-
ton) (W.F.P.) (Daphnellinae), Terebra
maculata (Linnaeus) and certain other

306 W. F. PONDER

species of the Terebridae (Rudman, 1969).
Terebra maculata has the pseudoproboscis
greatly developed, so that it is folded into
the rhynchodeum.

The pseudoproboscis or polyembolic
proboscis is thus a new structure
developed from the rhynchostome and
is not homologous with the original
neogastropod proboscis. Whereas the
original proboscis was developed by the
elongation of the archaeogastropod snout,
in the Conacea a new elongation of the
“pseudosnout has resulted in a “pseudo-
proboscis. |

Since the above was written Miller
(1971) has produced a preliminary report
on his work on the feeding mechanisms of
the Terebridae. He shows that there are 3
main types of feeding mechanism in this
family. Туре 1 has a pseudoproboscis,
salivary glands and а short proboscis.
There is no poison gland or radula. Type 2
are typically toxoglossan having a long
proboscis, a poison gland and a radula.
Туре 3 has а peculiar accessory feeding
organ consisting of a “long posterior glan-
dular and muscular stalk, terminating
anteriorly in a series of muscular papillae. ”
This type does not have a radula or poison
glands and many have lost the salivary
glands and buccal tube as well.

Rudman (1969) has described a 4th type
in Pervicacia tristis (Deshayes) which is
similar to Miller s Ist type but differs in
the possession of a radula with an odon-
tophore.

The loss of salivary glands, poison gland
and radula is sometimes associated with
the development of the polyembolic type
of proboscis or pseudoproboscis ( Terebra
maculata (Rudman, 1969), Cenodagreutes
spp. (Smith, 1967)).

The Buccal Cavity and Salivary Glands:
The buccal cavity, although showing a
general uniformity throughout the
Neogastropoda, has been modified т
some families. The mouth opens directly
into the buccal cavity in most families, but
is surrounded by a peristomial rim in the
Muricidae (Carriker, 1943) and Mitridae
(Ponder, 1972b). There is a long oral tube
in the Vexillidae (Ponder, 1972b), and the

Cancellariidae (Graham, 1966). No true
jaws are found in the Neogastropoda, but
members of the Muricidae have a median,
dorsal, jaw-like sclerite (Carriker, 1943;
Wu, 1965).

In the Magilidae the buccal cavity
appears to extend to the base of the
proboscis and the odontophore and radula
have disappeared. In this family the buccal
cavity is used as a pump in feeding on the
coelenterate prey (Ward, 1965). A minute
buccal apparatus is found in some
Colubrariidae (Ponder, 1968), the Har-
pidae (Bergh, 1901), and Vitularia in the
Muricidae (W.F.P.), and Coluzea in the
Columbariidae (W.F.P.). The conacean
families have a long tube leading from the
buccal cavity which lies at the base of the
proboscis but not at its distal end as in the
Rachiglossa. In this group many species
lose the muscular odontophore and,
although this is retained in several
primitive genera (W.F.P.), it seems unlike-
ly that it is ever protruded from the mouth,
as in rachiglossans.

The duct of the unpaired foregut gland
in the Rachiglossa and its toxoglossan
homologue, the poison gland, opens into
the buccal cavity in the Conacea and in
some Marginellidae (Graham, 1966;
Ponder, 1970a). A few terebrids (Troschel,
1856-1893; Bouvier, 1887; Risbec, 1953)
and turrids (Smith, 1967), have lost the
radula, salivary glands and poison gland.

Many neogastropods possess 2 types of
salivary gland (see Fig. 1) or buccal glands
(Hyman, 1967).

One type is homologous with the “nor-
mal’ salivary glands (sg) of most other
gastropods. These are white, usually
paired, often irregular, bodies composed of
masses of minute tubules made up of
cuboidal secreting cells. Their ducts usual-
ly open laterally into the buccal cavity.
These glands will be referred to in the
following discussion as “salivary glands.’

The 2nd type of salivary gland, often
termed accessory salivary gland (asg),
usually consists of a pair of elongate
vesicles containing the secretion рго-
duced by glandular tissue adhering to their
outsides. They open by way of a very

EVOLUTION OF NEOGASTROPODA 307

narrow duct at the anterior end of the buc-
cal cavity.

Nearly all neogastropods have salivary
glands. These glands are usually massive
in the Muricidae and Mitridae, as well as
in the Buccinidae and its allied families. In
these groups there are usually 2 types of
cells making up the glandular epithelium
(Dakin, 1912 (Buccinum); Fretter &
Graham, 1962 (Nassarius); Ponder, 1972b
(Strigatella); W.F.P. (Taron, Cominella)
and Wu, 1965 (Drupa, Morula)). They are
also large in the Turbinellidae (Ponder,
1973b) but their histology has not been
examined. The salivary glands of the
VolmtidaecesPonder. 1970b)0.the
Marginellidae (Ponder, 1970a), the Micro-
volutidae, the Vexillidae (Ponder, 1972b)
and the Olividae (Marcus & Marcus, 1959)
are composed of more-or-less discrete
tubules, in which there is only 1 type of
secretory cell, and the entire gland is often
small.

The salivary glands of the Conacea are
frequently rather small, and sometimes are
reduced to a single gland with only 1 duct
(which may be 2 fused ducts), as in Conus
lividus (Briig.)(Alpers, 1931). There is only
1 type of gland cell present and in Conus it
is tall and vacuolate (Alpers, 1931), but in
the Turridae it is like the normal
neogastropod salivary cell (W.F.P.).

The cancellariids have long, narrow
salivary glands that lie within the
proboscis (Bouvier, 1887; Amaudrut, 1898;
Graham, 1966).

The salivary ducts often lie beneath
the dorsal folds in the oesophageal wall,
but are free in some Buccinidae,
Nassariidae, Mitridae and Olividae and in
the Conacea and Cancellariacea. They
usually open into the posterior end of the
buccal cavity above the opening to the
radular sac, but in the Pyrenidae (Marcus
& Marcus, 1962a) and Conacea (Smith,
1967) they open into this sac. In the
Pyrenidae the salivary ducts sometimes
form a small vesicle just before they open.
In the Volutomitridae and Vexillidae
(Ponder, 1972b) the ducts migrate ven-
trally to open on the buccal floor and in
the Mitridae (Ponder, 1972b) they are pro-

jected in front of the mouth by an
epiproboscis. In Olivella (Marcus & Mar-
cus, 1959) the salivary ducts open at the
anterior end of the buccal cavity and in
Coralliophila abbreviata (Lamarck) they
unite dorsally before entering the buccal
cavity (Ward, 1965).

The accessory salivary glands consist of
a vesicle lined with columnar epithelium
in the Muricidae (Bouvier, 1888: Fretter &
Graham, 1962; Wu, 1965) and squamous
epithelium in the Olividae (Kiittler, 1913)
and the Volutidae (Ponder, 1970b). This
epithelium is surrounded by a layer of cir-
cular and some longitudinal muscles, and
these are penetrated by the ducts of gland
cells lying outside the muscles. The glan-
dular layer consists of 1 or more layers of
irregular, subepithelial cells and the secre-
tion fills the vesicle of the gland.

Paired accessory salivary glands have
been recorded in the above families and in
Фе Vexillidae (Risbec, 1928; Ponder,
1972b) and the Cancellariidae (Amaudrut,
1898; Graham, 1966), but are not found in
the Mitridae (Risbec, 1928; Ponder,
1972b), Harpidae (Bergh, 1901),
Terebridae (Risbec, 1953; Marcus & Mar-
cus, 1960) and most Turridae (Smith,
1967; W. Е. P.), although the writer has
located them in 2 species of the Bor-
soniinae. None of the families that are
generally regarded as related to the Buc-
cinidae possess them (Dakin, 1912; Thiele,
1929), including the Pyrenidae (Risbec,

19542 Marcus). do.) Miareus..1 19623)
Galeodidae (Pierce, 1950; W.F.P.),

Nassariidae (Bouvier, 1888; Risbec, 1952;
Graham, 1941), Fasciolariidae (Marcus &
Marcus, 1962) and the Colubrariidae
(Ponder, 1968). The Columbariidae
(W.F.P.), Turbinellidae (Moses, 1923;
Ponder, 1973b) and the Magilidae
(Bouvier, 1888; Ward, 1965; W.F.P.) also
lack them, whereas in the Volutomitridae
(Ponder, 1972b) and the Marginellidae
(Ponder, 1970a) a single gland is present,
though it is sometimes absent in the latter
family.

The function of the accessory salivary
glands 15 still obscure. Bouvier (1888)
found it in all of the Muricidae that he

308 W. F. PONDER

examined, it being very minute in Murex
trunculus( Linnaeus), larger but embedded
in the normal salivary glands in Trophon
philippianus Dunker and very large in
Ocenebra erinaceus (Linnaeus) and
Nucella lapillus (Linnaeus). The ability to
bore into shells is best developed in
Nucella and Ocenebra and so, in this fami-
ly, its size may be correlated with the
animals feeding habits. Wu (1973) has
shown that at least 2 muricids lack these
glands. However none of the other
families that possess it have so far been
shown to have the ability bore into
shells, but the structure of the gland
nearly identical in all, except for the
difference in the internal epithelium in the
Muricidae mentioned above.

Several workers have tested the secre-
tion of the accessory salivary gland and
have failed to find anything significant.
The salivary glands of some Muricidae
contain proteolytic enzymes (Mansour-
Bek, 1934) and a toxic secretion has been
recorded in some Buccinidae (Welsh,
1956; Fange, 1960).

The Radula: There is an overall tenden-
cy toward reduction of the number of
radular teeth and their cusps in most of the
families of the Neogastropoda, as also oc-
curs in the Opisthobranchia. Examples in-
dicating this trend are shown in Fig. 2.
The inner circle shows а hypothetical
ancestral type of radula. The next zone (A)
includes examples of multicuspate
radulae, showing the maximum number of
teeth present in each family. The
maximum number found in all the
Rachiglossa is 3 teeth in each row, but
some of the Clavinae (Turridae) in the
Conacea have 5 teeth in each row (No. 20).
Some families are not represented in this
zone (A), but this does not necessarily in-
dicate that the radular teeth in families
such as the Muricidae are any more
specialized than those included in the in-
ner zone. The diagram indicates trends
and is not necessarily of phylogenetic
significance.

Zone B includes those radular teeth that
show some simplification or modification
from a more basic pattern. Some are

assumed to be secondarily multicuspid
such as Olivella (No. 16), and Vexilla (No.
32). The Olivellinae (Olividae) (No. 16)
and the Nassariidae (Nos. 43, 45) often
develop accessory plates between the cen-
tral and lateral teeth. These are probably
independently evolved, new structures be-
cause they occur in all stages of develop-
ment in both groups.

The variation in radular pattern in the
Buccinidae, and the general similarity in
the teeth of all of the families included in
Thiele’s Buccinacea, should be noted.

The radular teeth shown in zone C are
those in which the number of teeth has
become reduced. In the Mitridae,
Volutidae, Marginellidae, Volutomitridae
and Cancellariidae the lateral teeth have
been lost, but in the Buccinidae, Pyrenidae
and the toxoglossan families the central
tooth has disappeared. The lateral teeth in
some Harpidae (Peile, 1939) and Volutidae
(Pace, 1902) are vestigial, whereas in the
Pyrenidae the large lateral teeth may func-
tion as tweezers (Marcus & Marcus,
1962а).

The marginal teeth of advanced
toxoglossan genera (Nos. 25-27) are hollow
and capable of being charged with poison.
They are used as harpoons in the capture
of active prey (Kohn, 1959; Pearce, 1966)
which is then swallowed whole. Some
Conacea have more primitive radulae that
probably function in tearing the prey (Nos.
21, 28), while the “prototypic” type in the
Clavinae (No. 20) is probably capable of
combining a food tearing and a spearing
function. There are undoubtedly other
methods of employing the varied types of
radula (Nos. 22, 23) within the Turridae.
The Cancellariidae have a single row of
elongated, blade-like teeth (Barnard,
1958; Graham, 1966), each an aggregate of
“rectangular tubes which form a canal
system which transverse the whole length
of the radular filaments’ (Olsson, 1970).

Several families have lost the radula
altogether, these being indicated in the
outermost zone (D). Only the Magilidae
have no known members with a radula.
Some of these “aglossate” forms are
probably suctorial feeders (Magilidae,

EVOLUTION OF NEOGASTROPODA 309

Marginellidae), whereas others
(Terebridae, Turridae) probably engulf
their prey whole. It is not known how the
Cancellariidae feed, although Olsson
(1970) suggests that they may feed on
micro-organisms, these being transported
down the minute tubes that make up each
tooth.

The Mid-oesophagus and Сапа of
Leiblein: The evolution of the mid-
oesophagus (mo) in the Rachiglossa
follows 2 main trends, which run parallel
in several families. These are (1) the strip-
ping off of the gland of Leiblein and
oesophageal dorsal folds from the
oesophagus to form a “poison gland” and
(2) the loss of the original, glandular
oesophageal dorsal folds. Both of these
trends have ultimately resulted in genera
that have lost all of the glandular struc-
tures associated with the mid-oesophagus.

The oesophageal gland attached by a
narrow duct is usually referred to as the
“gland of Ге ет.” Hyman (1967) uses
the name “unpaired foregut gland.” In
order that the following discussion be
clarified the use of these terms will be
strictly defined. The unpaired foregut
gland can be used for the unpaired gland
which enters the oesophagus by way of a
narrow duct. This can include the poison
gland of the conaceans, as I have recently
shown (Ponder, 1970a) that it is probably
homologous to the unpaired foregut gland
of the rachiglossans. The gland of Leiblein
can be used for that part of the unpaired
foregut gland that was derived from the
oesophageal gland. In some species the
unpaired foregut gland consists solely of
the gland of Leiblein but in others it in-
volves other parts of the oesophagus, as is
shown below.

Fig. 3 shows the evolution of the
rachiglossan mid-oesophagus. A and В
show a generalized type of mid-
oesophagus (although not necessarily the
most primitive) which is encountered in
several families as the least specialized
type. The unpaired foregut gland consists
only of the small gland of Leiblein (gl).
The mid-oesophagus (mo) is moderately

long (A), or short (B) and has glandular
dorsal folds and a prominent valve of
Leiblein (vl).

The type shown in diagram A occurs in
the Volutidae (Volutocorbis abyssicola
(Adams & Reeve); Woodward, 1900) and
the Vexillidae (Austromitra rubiginosa
(Hutton); Ponder, 1972b), but in some
Olividae (Oliva sayana Ravenel and
Olivancillaria (Lintricula) auricularia
(Lamarck); Marcus & Marcus, 1959) the
mid-oesophagus is shorter, as in diagram
B.

The unpaired foregut gland increases in
bulk in the Muricidae (diagram C) but still
usually only consists of the gland of
Leiblein. The mid-oesophagus is some-
times short but still contains the glan-
dular dorsal folds (Graham, 1941; Wu,
1965). The “Trophoninae,” probably the
most primitive of the muricid groupings,
has the smallest gland of Leiblein. In the
Columbariidae (W.F.P.) and the
Magilidae (Ward, 1965; W.F.P.) the dorsal
folds are not glandular, but the valve of
Leiblein is large (diagram D).

In the families Buccinidae (Dakin, 1912;
Graham, 1941), Nassariidae (Graham,
1941; Risbec, 1952), Fasciolariidae (Mar-
cus & Marcus, 1962), Pyrenidae (Risbec,
1954; Marcus & Marcus, 1962a) and Tur-
binellidae (Ponder, 1973b), the dorsal
folds are lost or have become т-
conspicuous, the valve of Leiblein 15
sometimes reduced in size, and the un-
paired foregut gland (entirely gland of
Leiblein) remains small and sometimes
becomes very thin walled and saccular
(diagram E). Busycon canaliculatum (Lin-
naeus) (Pierce, 1950) and B. contrarium
Conrad (W.F.P.) in the Galeodidae are
organized like the Buccinidae, but some
members of the Galeodidae (Melongena
melongena (Linnaeus) Vanstone, 1894; M.
corona (Gmelin; W.F.P.) have lost the
gland of Leiblein (diagram F). In
Melongena the valve of Leiblein is much
reduced and a caecum-like expansion lies
just behind the nerve ring which may be
homologous with a similar, short caecum
found in the anterior part of the posterior
oesophagus in Buccinum undatum and

310 W. F. PONDER

FIG. 2. The evolutionary trends in the neogastropod radula. Levels A to D are explained in the text.

Mitridae (1) Cancilla (Domiporta) sp. (Cooke, 1920); (2) Scabricola desetangsii (Kiener) (=variegata Reeve)
(Cooke, 1920); (3) Pterygia crenulata (Gmelin) (Thiele, 1929).

Volutidae (4) Volutocorbis abyssicola (Ad. & Rve.) (Thiele, 1929); (5) Voluta musica Linnaeus; (6) Scaphella
junonia Shaw (Clench & Turner, 1964); (7) Alcithoe arabica (Gmelin) (original).

(8) Hypothetical ancestral radula.

Marginellidae (9) Diluculum inopinatum Barnard (Barnard, 1962); (10) Persicula persicula (Linnaeus) (Thiele,
1929); (11) Volvarina (Haloginella) philippinarum (Redfield) (Troschel, 1868).

Volutomitridae (12) Paradmete typica Strebel (Thiele, 1929); (13) Microvoluta australis Angas (Peile, 1922).

Olividae (14) Pseudoliva crassa (Gmelin) (Thiele, 1929); (15) Oliva sayana Ravenel; (16) Olivella verreauxii
(Duclos) (Marcus € Marcus, 1959).

Harpidae (17) Harpa amouretta (Róding) (Peile, 1939).

Vexillidae (18) Vexillum sp.; (19) Pusia sp. (original).

Turridae (20) Drillia umbilicata (Gray) (Thiele, 1929); (21) Hormospira maculosa (Sowerby) (Powell, 1942); (22)
Aforia goodei persimilis (Dall); (23) Polystira picta (Reeve); (24) Inquisitor cf crennularis (Lamarck)
(Powell, 1966); (25) Phenatoma rosea (Quoy & Gaimard) (Thiele, 1929).

Conidae (26) Conus (Asprella) mucronatus Reeve (Thiele, 1929 (after Bergh)).

Terebridae (27) Hastula (Impages) coerulescens (Lamarck) (Troschel, 1866); (28) Diplomeriza duplicata (Lin-
naeus) (Troschel, 1866).

Cancellariidae (29) Cancellaria sp. (original).

Columbariidae (30) Columbarium pagodum (Lesson) (Habe, 1943).

Muricidae (31) Bedeva hanleyi (Angas); (32) Vexilla taeniata (Powis) (Thiele, 1929).

Turbinellidae (33) Turbinella ovoideus (Kiener); (34) Vasum ceramicum (Linnaeus) (Thiele, 1929).

Columbellidae (35) Pseudanachis duclosiana (Sowerby) (Thiele, 1929); (36) Pyrene (Strombina) gibberula
(Sowerby) (Troschel, 1869, after Moerch); (37) Paxula paxillus (Murdoch) (original).

Buccinidae (38) Proneptunea duplicarinata Powell (Powell, 1951); (39) Liomesus dalei (Sowerby) (Thiele, 1929);
(40) Mohnia mohni Friele (Thiele, 1929 after Kobelt); (41) Buccinum undatum Linnaeus (Troschel, 1868);
(42) Meteuthria martensi (Strebel) (Thiele, 1929).

Nassariidae (43) Cyclope neritea (Linnaeus) (Troschel, 1868); (44) Ilyanassa obsoleta (Stimpson) (Troschel,
1869); (45) Cyllene lyrata (Lamarck) (Thiele, 1929).

Fasciolariidae (46) Peristernia australiensis (Reeve) (Thiele, 1929); (47) Granulifusus niponicus (Smith) (Habe,
1945).

Melongenidae (48) Semifusus (Pugilina) тото (Linnaeus) (Thiele, 1929).

Colubrariidae (49) Iredalula striata (Hutton) (Ponder, 1968).

Neptunea antiqua (Linnaeus) (Fretter & been partially stripped from the mid-

Graham, 1962).

The Mitridae (Risbec, 1928; Ponder,
1972b) have no unpaired foregut gland
and the valve of Leiblein and dorsal folds
are inconspicuous.

In Harpa (Bergh, 1901; W.F.P.) the
mid-oesophagus has lost all trace of the
valve and unpaired foregut gland and of
the dorsal folds (diagram P). The mid-
oesophagus of the Colubrariidae (Ponder,
1968) has become secondarily elongate
and glandular after the loss of the un-
paired foregut gland (diagram С).

The mid-oesophagus is very long in
the muricid Poirieria zelandica (Quoy &
Gaimard) (W.F.P.) and the glandular dor-
sal folds are conspicuous (diagram H). In
Murex tenuispina Lamarck (=M. pecten
Lightfoot) (Haller, 1888) and in Vexillum
spp. (Ponder, 1972b) the dorsal folds have

oesophagus (diagram I) by the fusion of
their apices. This process has proceeded
still further (diagram J) in Xymene am-
biguus (Philippi), Paratrophon quoyi
quoyi (Gray) (Muricidae), Amalda
(Baryspira) australis (Sowerby) (Olividae)
(W.F.P.) and in most Volutidae (Clench &
Turner, 1964; Ponder, 1970b). In these
species the dorsal folds have been stripped
from the mid-oesophagus up to the edge of
the nerve ring. The resultant glandular
tube lies, as a more-or-less convolute mass,
anterior to the gland of Leiblein (sensu
stricto). The whole structure (the unpaired
foregut gland) is usually referred to as the
gland of Leiblein, but in fact, the part
derived from the dorsal folds (the tubular
part) is the main secretory area. The gland
of Leiblein itself (the terminal bulbous
part) is merely a muscular appendage with

EVOLUTION OF NEOGASTROPODA 311

Melongenidae

Colubrariidae

1 4 NM
Buccinidae 41 / VAS eS
И Nie 43
1
1

y Se Я

Pyrenidae м 34
NZ in
и

“Ay

Muricidae

Turbinellidae

Magilidae

a rather thin epithelium which appears to
have hardly any functional significance.
The Volutomitridae (diagram K) appear
to have derived the gland of Leiblein from
the oesophageal gland in a different
fashion from other Rachiglossa (Ponder,
1972b). It appears to have been stripped
from the oesophagus forwards, rather than
backwards. This family has several
features in common with the
Marginellidae, and if it is possible that
they both had a common origin, the gland
of Leiblein in the Marginellidae may have
arisen in the same way as
Volutomitridae. There is, however, no
direct evidence to support this assumption

eo

Columbariidae

in the

Mitridae

Volutidae

Ÿ I “ Marginellidae
BIN <
> NA er ee
Ro 9 ©
yf, 5 Volutomitridae
1]
Sera
À
\
\

DI
Olividae
E \
<
15 \

\
\
‘
‘

17
Ws ca 26 pike ae
Sy) DM нае
18 er Y )
ON
о Vexillidae

№ ‘

A
A /
de 74
. 4
. 4
ee | /
= / я К uf
À zi \
22 Ay
in 7 97 Terebridae
21 ER \ ys

Cancellariidae

(Ponder, 1970a). In the most primitive
marginellid examined (Diluculum sp. ), the
small gland of Leiblein has been stripped
from the mid-oesophagus (diagram L), to
which it is attached by only a narrow duct
(Ponder, 1970a). The following stages in
the evolution of the marginellid unpaired
foregut gland have been described in
detail elsewhere (Ponder, 1970a). Briefly it
includes the formation of a pre-torsional
tube that bypasses the valve of Leiblein
(diagram L) and, following this, the com-
plete stripping off of the dorsal folds along
the remainder of the mid (diagrams M, N)
and anterior oesophagus (diagram О).
Thus a separate tube is formed which

312 W. F. PONDER

opens directly into the buccal cavity

(diagram О).

The formation of a poison gland in the
Conacea probably occurred in a similar
fashion to that in the marginellids. In the
Conacea, however, there is either a very
short anterior oesophagus or this is absent
altogether, so that the process would be
simplified. Evidence in support of the
poison gland having formed in this way is
provided by the lack of any reports of
oesophageal dorsal folds in the Conacea. A

detailed account of the structure of the
poison gland of Conus mediterraneus
(Briig.) was given by Martoja (1960). The
nature of the mid-oesophagus in the
cancellariids is described above.

Graham (1941) suggested that because
of the different position of the scar in-
dicating the path of torsion in Buccinum
and Nucella, the Muricacea and Buc-
cinacea must have had different origins.
The scar in Buccinum shows torsion oc-
curring in that part of the oesophagus

FIG. 3. The evolutionary trends in the mid-oesophagus of the Muricacea. The gland of Leiblein is shown stippl-
ed and the mid-oesophagus and the valve of Leiblein are hatched. The valve of Leiblein and the glandular parts
of the mid-oesophagus are indicated as broader portions of the mid-oesophagus. For explanation, see text.

EVOLUTION OF NEOGASTROPODA 313

which passes through the nerve ring, and
Marcus & Marcus (1962) have shown a
similar type in the Fasciolariidae. Most
Buccinidae, Pyrenidae (Marcus & Marcus,
1962a), Olividae (Marcus & Marcus, 1959)
and Nassariidae (Graham, 1941) do not
show the path of torsion. The same is true
for the Mitridae (Ponder, 1972b), although
there is some indirect evidence that it oc-
curs at the site of the valve of Leiblein, as
it does in the Muricidae (Graham, 1941),
Volutidae (Ponder, 1970b) and Tur-
binellidae (Ponder, 1973b). А 3rd type
which probably represents a modification
of that seen in the Buccinidae, shows tor-
sion occurring just behind the nerve ring.
This is seen in the Marginellidae (Ponder,
1970a), Vexillidae (Ponder, 1972b) and in
the Olividae (Amalda (Baryspira) australis,
W.F.P.). The Volutomitridae have had the
anterior part of the mid-oesophagus pulled
through the nerve ring so that the position
of torsion now lies a little behind the valve
of Leiblein, whereas, originally it probably
lay just behind the nerve ring (Ponder,
1972b).

The secretion of proteases by the un-
paired foregut gland has been investigated
in Murex (Mansour-Bek, 1934; Hirsch,
1915), Buccinum (Brock, 1936) and
Babylonia (Yamaguchi, et al., 1961).
Studies by Kohn, et al. (1960) and Whyte
€ Endean (1962) have been made on the
chemical and pharmacological properties
of the venom of Conus and a summary of
this work, together with some new infor-
mation, is provided by Halstead (1965).

The pyriform valve of Leiblein is a
characteristic feature of the Rachiglossa. A
reduction in its size is often associated with
a small unpaired foregut gland (as in Buc-
cinum) and when this gland is absent the
valve is either very small or completely
missing (Melongena, W.F.P.; Harpa,
Bergh, 1901; Mitridae, Ponder, 1972b).
Alternatively if the oesophagus 1$ Бу-
passed by the unpaired foregut gland, as in
the Conacea and in some Marginellidae,
the valve of Leiblein is lost (Smith, 1967;
Graham, 1966; Ponder, 1970a). Thus the
main function of the valve is probably to
retain the enzymatic secretion from the

unpaired foregut gland and from the glan-
dular dorsal folds within the mid and
posterior oesophagus.

The Stomach: Graham (1949) outlined
the features of the neogastropod stomach,
which he based on a study of Nassarius
reticulatus (Linnaeus), Nucella lapillus
(Linnaeus) and Ocenebra erinacea (Lin-
naeus). Smith (1967a) suggested that 2
evolutionary trends were represented in
the stomachs of the neogastropods that he
investigated. He found that in the buc-
cinids and the turrids the stomach in-
dependently takes on a U-shape. The
neogastropod stomach has, in fact, evolved
in several different ways. The anterior
migration of the oesophagus has occurred
in all groups, resulting in a basically U-
shaped stomach.

Many neogastropod stomachs (see Fig.
5) have primitive features not found in
higher mesogastropods. This is especially
noticeable in the Nassariidae (Graham,
1949; Smith, 1967a) and the Pyrenidae
(Marcus & Marcus, 1962a), both of these
families having species which still retain
the gastric shield, style sac and vestiges of
a sorting area.

The tendency to form а spacious
posterior caecum (с) occurs in several
groups, all of which have a distinct style
sac area (ss) with recognizable typhlosoles.
These include Neptunea antiqua (Smith,
1967a) and Buccinum undatum (Brock,
1936) in the Buccinidae, and the
Nassariidae (Graham, 1949; Morton, 1960;
Smith, 1967a), it being especially
pronounced in Nassarius (Alectrion)
aoteanus Finlay (W.F.P.). Morton (1960)
has shown that a crystalline style occurs in
Cyclope neritea (Linnaeus), whereas
Jenner (1956) and Brown (1969) have
reported one in Nassarius (Ilyanassa) ob-
soletus (Say). Oliva sayana Ravenel has a
caecum, but in Olivella verreauxii (Duclos)
this has been transformed into a cuticle
lined gizzard (Marcus & Marcus, 1959). A
gizzard is also found in the Mitridae
(Ponder, 1972b) but in this family it is
formed in the oesophageal region of the

stomach, there being no caecum. The
Vexillidae (Ponder, 1972b) have a broad

314 W. Е. PONDER

caecum, and so does Peculator hedleyi
(Murdoch) in the Volutomitridae (Ponder,
1972b).

In the above examples having a caecum,
the digestive gland apertures open near
the entrance of the oesophagus. Cominella
spp., Buccinulum spp., Austrofusus glans
(Röding) (W.F.P.), and Penion adustus
(Philippi) (Ponder, 1973a) in the Buc-
cinidae and Microvoluta biconica (Mur-
doch & Suter) in the Volutomitridae
(Ponder, 1972b) do not have a caecum. A
prominent gastric shield is present in some
Nassariidae, some Pyrenidae, and in the
Volutomitridae, but certain other families
have examples which show remnants of
this structure.

А general

tendency for the gastric

Nassariidae

Fasciolariidae

Pyrenidae

Columbariidae pr, os)
| -
||

|

/

lumen (1.е., the stomach cavity excluding
the style sac) to elongate is seen in
Cominella (W.F.P.) and Colus gracilis (da
Costa) (Smith, 1967a) in the Buccinidae
and «Taron ‘dubius (М. EAP?)
and Leucozonia nassa (Gmelin) (Marcus &
Marcus, 1962) in the Fasciolariidae. In
these examples the 2 digestive gland aper-
tures have become widely separated and
lie at each end of the gastric lumen. This
tendency is increased in Penion (Ponder,
1973a) and Buccinulum (Buccinidae)
(W.F.P.) in which the gastric lumen ос-
cupies most of the stomach and is, itself,
U-shaped.

In the Buccinidae the oesophagus opens
into the stomach behind the intestine, but
in the Colubrariidae (Ponder, 1968) it

Buccinidae

Melongenidae

Colubrariidae

\ Turbinellidae

“

N
N
N

Mitridae

y „

-

О
\
| N Vexillidae
is
Muricidae Г DS
1 <
1 PEN
\ 1 IS
N Г
\ - 7 Volutomitridae
Magilidae
a x
iS E Mar ginellidae
Ca
Volutidae i aa ae is
= Er Olividae
Harpidae

FIG. 4. The evolution of the families of the Muricacea. The inner, solid circle represents the lower Mesozoic,
ancestral neogastropod group. The middle circle indicates the boundary of the Mesozoic and Tertiary Periods.
The relative size of each family at the edge of the outer circle is approximately proportional to the total number
of Recent and fossil genera within each group. No attempt has been made to show the proportions of the genera
throughout the Tertiary Period.

EVOLUTION OF NEOGASTROPODA 315

opens at the anterior end of the very
elongate stomach, which has the intestine
opening posteriorly and the style sac is lost
altogether.

Narrow, superticially U-shaped
stomachs have been evolved in the
Turridae (Smith, 1967a) and the
Terebridae (Marcus & Marcus, 1960), but
in these families the wide oesophagus oc-
cupies most of the left side of the U,
whereas the right side is derived from the
style sac. In the Turbinellidae (Ponder,
1973b) the style sac area occupies nearly
all of the U.

The muricid stomach has evolved a bag-
like, posterior swelling which is, in reality,
a wide, short caecum (Graham, 1949;
Righi, 1964; Wu, 1965; Smith, 1967a).
The marginellid stomach (Ponder, 1970a)
has incorporated the digestive gland duct
as part of the fundus of the stomach in
some species at least, and, as in Alcithoe
arabica (Gmelin) in the Volutidae (Ponder,
19706) the style "sac; although
recognizable, has lost its typhlosoles. The
posterior part of the stomach of Alcithoe,
which is homologous with the gastric
lumen in other neogastropods, contains
complexly ciliated, leaf-like structures.

The overall trend in the neogastropod
stomach is toward a large, relatively simple
sac with the walls closely opposed. This
allows the available ciliary currents to act
to the best advantage in moving waste
material, or in keeping food particles in
suspension so that they mix with the en-
zymatic secretion from the digestive
gland. Achievement of these conditions is
obtained by the elongation of either the
style sac or mixing area, or by the forma-
tion of a caecum.

The formation of a crop in the posterior
oesophagus of many neogastropods serves
to store food and, in many cases, it is a site
of preliminary digestion. Thus the food
can often be broken down before reaching
the stomach.

The Anal Gland: An anal (or rectal)
gland is found in many neogastropod
families. It is possessed by species in all 3
superfamilies and has a similar structure in
at least 2 of them (its histology has not

been described in the Cancellariidae). It
usually consists of 1 or more branching
tubules, that, in the Muricidae (Fretter,
1946), some Magilidae (W.F.P.) and
Volutidae (Ponder, 1970b) form a large
black mass. Fretter (1946) stated that the
gland in Nucella lapillus (Linnaeus) has an
excretory function, but this has not been
demonstrated in any other neogastropod.
Smith (1967a) commented on the structure
of the gland in the Turridae and the
Muricidae.

Other families in which the gland occurs
are the Columbariidae (W.F.P.), Olividae
(Marcus € Marcus, 1959), Vexillidae,
Mitridae, Volutomitridae (Ponder, 1972b),
Marginellidae (Ponder, 1970a), Tur-
binellidae (Ponder; ВО,
Cancellariidae (Graham, 1966), and the
Terebridae (Marcus & Marcus, 1960).

In some families normally possessing the
anal gland, certain genera appear to have
lost it, these including Уазит in the Tur-
binellidae (Ponder, 1973b) and Diluculum
in the Marginellidae (Ponder, 1970a). In
some species it is very small and possibly of
little functional importance. Ward (1965)
has shown that Coralliophila abbreviata
(Magilidae) does not possess an anal gland.

None of the families in Thiele's Buc-
cinacea appear to have the gland, nor has
the Colubrariidae.

Smith (1967a) pointed out the similarity
of the granules in the anal gland of some
neogastropods to those in the amoebocytes
surrounding the digestive gland. In some
instances, however, they do not resemble
these latter granules. The refringent
granules encountered in renal tissue and
often seen in the gland of Leiblein are also
similar.

The Male Genital Ducts

In all neogastropods the male genital
duct (see Fig. 5) consists of a coiled, upper
vas deferens modified to form a sperm
storing seminal vesicle (sv) and, in some
species, the walls ingest spermatozoa
(Fretter, 1941; Smith 1967b). The lower or
renal part of the vas deferens is usually
straight and it is connected to the pericar-
dium by a renopericardial duct or a strand

316 W. Е. PONDER

of tissue representing it. The
Volutomitridae (Ponder, 1972b), the turrid
Oenopota (=Lora) travelliana (Turton)
(Smith, 1967b) and possibly the turbinellid
Vasum turbinellum (Linnaeus) (Ponder,
1973b) have a gonopericardial duct. The
remnants of this duct have been recorded
in some Muricidae, Buccinidae (Fretter,
1941), Fasciolariidae (Marcus & Marcus,
1962) and Turridae (Smith, 1967b). Some
others have the renal vas deferens located
so close to the pericardial wall that the
existence of a vestigial duct cannot be es-
tablished. A diverticulum of the renal
organ approaches the renal vas deferens in
the Marginellidae (Ponder, 1970a) and in
Leucozonia in the Fasciolariidae (Marcus
& Marcus, 1962).

In the most primitive condition, the
renal vas deferens opens into an open
pallial groove lined with prostatic tissue,
such as occurs in the Volutomitridae
(Ponder, 1972b), Harpidae (Bergh, 1901),
and in some volutes (Woodward, 1900;
Pace, 1902). In Alcithoe arabica in the
Volutidae, the sides of this groove become
massive, glandular lobes (Ponder, 1970b).
A line of fusion showing where the lobes
were sealed is found in some muricids
(Fretter, 1941) and some turrids (Smith,
1967b), whereas in the Turbinellidae all
gradations between open and closed pallial
grooves are found (Abbott, 1959; Ponder,
1973b) and Wu (1973) has noted the
existence of 3 types of prostate gland in the
Muricidae.

It thus appears as though the closed
prostate gland (p) developed independent-
ly in at least several families. In most
families in which a closed prostate gland is
found, there is no trace of a line of fusion
but they usually have a narrow, posterior,
pallial connection, either in the form of a
short, ciliated tube or a slit. Such a situa-
tion is found in all of the remaining
families except the Fasciolariidae which
(in Leucozonia at least) has lost the
posterior opening of the prostate (Marcus
& Marcus, 1962).

The penis (pen) is usually of moderately
large size, and the duct mostly sealed and
embedded in the central part of the penis.

There is, however, an open penial groove
in some Turbinellidae (Tudicula; Abbott,
1959), Volutidae (Volutocorbis;
Woodward, 1900) and in the
Volutomitridae (Ponder, 1972b). Several
forms show a line of fusion representing
the edges of an originally open groove
such as Olivancillaria (Olividae) (Marcus
& Marcus, 1959), Alcithoe (Volutidae)
(Ponder, 1970b) and several genera in the
Turbinellidae (Abbott, 1959; Ponder,
1973b).

Prostatic cells occur in the penial ducts
of Buccinum, Nassarius (Fretter, 1941),
some Marginellidae (Ponder, 1970a),
Mangelia (Turridae) (Robinson, 1960),
and in the Olividae (Marcus & Marcus,
1959). The Volutomitridae have prostatic
tissue lying within the penis and dis-
sociated from the penial groove (Ponder,
1972b).

The Pyrenidae have some unusual
modifications in the male genital system
(Marcus & Marcus, 1962a). In some, the
penis lies within a pouch between the
hypobranchial gland and the pallial roof,
and some have a seminal vesicle lying
either just behind, or in front of, the upper
pallial opening of the pallial sperm duct.
In 1 species the prostate is divided into 2
separate bodies, but it usually forms a con-
volute part of the duct. In other species the
prostate gland is absent, and in some the
penial duct contains prostatic tissue.

Bouvier (1888) and Gohar € Soliman
(1963) have shown that the burrowing
Magilidae have a penis, however it is
sometimes rudimentary. Although copula-
tion cannot take place, spermatozoa are
apparently taken in by the inhalant
current of the female and fertilization is in-
ternal (Gohar € Soliman, 1963).

The Female Genital Ducts

The basic organization of the
neogastropod female genital tract is shown
in Fig. 6. Nucella lapillus and Ocenebra
erinacea (Fretter, 1941) have a typical
structure and have been thoroughly de-
scribed. The duct in these 2 species con-
sists of a short, upper and renal oviduct
(od) leading from the ovary with a gono-

EVOLUTION OF NEOGASTROPODA 317

st

FIG. 5. Generalized muricacean neogastropod removed from its shell and viewed dorsally with the pallial cavity
and anterior body cavity opened mid-dorsally and the proboscis extended.

adg, anterior lobe of digestive gland; ag, anal gland; ao, anterior oesophagus; asg, accessory salivary gland;
bm, buccal mass; с, caecum; cog, circum-oesophageal ganglia; ct, ctenidium; ed, ejaculatory duct; f, foot; hg,
hypobranchial gland; gdf, glandular dorsal folds; gl, unpaired foregut gland; m, mouth; mo, mid-oesophagus; о,
operculum; os, osphradium; р, prostate gland; pc, pericardium; pdg, posterior lobe of digestive gland; pen,
penis; po, posterior oesophagus; r, rectum; ro, renal organ; sd, salivary duct; sg, salivary gland; ss, style sac; st,
stomach: sv, seminal vesicle; t, cephalic tentacle; tes, testis; v, ventricle; vl, valve of Leiblein.

318 W. F. PONDER

pericardial duct (gpd) at the junction of
the latter duct with the albumen gland.
The albumen gland (ag) is a thickened
part of the oviduct itself in Nucella, and is
humped, with the ventral surface of both
halves in contact. A much lobulated in-
gesting gland (rs) opens by way of a sperm
storing duct into the area between the
albumen and capsule glands. The capsule
gland (cg) forms most of the pallial section
of the duct and at its anterior end there is a
thin-walled ventral channel (vc) that is
a short, muscular vagina (vag). A short,
muscular bursa copulatrix (be) opens into
the vestibule, running from which is a
thin-walled ventral channel (vs) that is
overlain by 2 ciliated folds and a heavy,
glandular lobe on the right.

A gonopericardial duct is present in at
least some Muricidae, Buccinidae,
Nassariidae (Fretter, 1941), Olividae (Mar-
cus & Marcus, 1959), Pyrenidae (Marcus &
Marcus, 1962a) and Cancellariidae
(Graham, 1966). The renal oviduct of the
Volutomitridae sometimes has a connec-
tion with the renal organ instead of the
pericardium (Ponder, 1972b), and a blind,
renal diverticulum lies alongside the renal
oviduct in the Marginellidae (Graham,
1966; Ponder, 1970a).

The albumen gland in most Conacea
and Rachiglossa is similar to that in
Nucella, but has often been separated
from the oviduct completely, so that it
communicates by a separate duct into the
region between the capsule and albumen
gland into which the ingesting gland and
renal oviduct open. This is the case in the
Vexillidae and Volutomitridae (Ponder,
1972b), Vasum in the Turbinellidae
(Ponder, 1973b) and at least some
Marginellidae (Ponder, 1970a). There is
apparently no albumen gland in Tur-
binella (Ponder, 1973b).

The ingesting gland has tall, brown-
coloured cells which ingest spermatozoa
and sometimes yolk (Fretter, 1941;
Ponder, 1972b). Although Fretter record-
ed sperm ingestion in Nassarius reticulatus
(Linnaeus), Johansson (1957) did not
observe it in N. pygmaeus (Lamarck) or in
N. incrassatus (Stróm.). In at least some

Fasciolariidae (Leucozonia, Marcus &
Marcus, 1962; Taron dubius, W.F.P.) the
epithelium of the “ingesting gland” con-
sists of simple, short, columnar cells that
do not ingest spermatozoa, but instead the
“gland” acts as a seminal receptacle.

Seminal receptacles have been recorded
in Olivella and Oliva sayana Ravenel
(Marcus & Marcus, 1959) and in both of
these species there is no functional in-
gesting gland, although there is one in
another member of the Olividae, Olivan-
cillaria (Lintricula) auricularia (Marcus &
Marcus, 1959). Narrow accessory ducts to
the ingesting gland in Alcithoe (Volutidae)
(Ponder, 1970b) store sperm and may be
related to the seminal receptacles of the
olivids.

The duct of the ingesting gland usually
acts as a seminal receptacle, storing orien-
tated spermatozoa. In the species in-
vestigated by Fretter (1941) (members of
the Buccinidae, Muricidae and
Nassariidae), and in the Volutidae
(Ponder, 1970b) the ingesting gland duct
opens into the ventral part of the gland
and is not ciliated. In the Mitridae and
Vexillidae (Ponder, 1972b) it is ciliated and
opens into the dorsal part of the gland
which is, in addition, not as lobed as in the
preceding families. Ciliated ducts that do
not store sperm are found in the
Volutomitridae (Ponder, 1972b) and the
Marginellidae (Ponder, 1970a), and the
gland in these families is lined with large
cuboidal cells that do not ingest sper-
matozoa. The ingesting gland of some
turrids is capable of sperm absorption
(Smith, 1967b), but Martoja-Pierson
(1958) did not find any evidence for this in
Conus mediterraneus (Brüg.). There is, ap-
parently, no albumen gland or ingesting
gland in Turbinella pyrum (Linnaeus)

(Ponder, 1973b).

The capsule gland is usually the largest
gland in the female oviduct, although in
Alcithoe (Ponder, 1970b) it is shorter than
the albumen gland. Typically it has several
zones showing different staining proper-
ties and has a ventral channel. This
channel is overhung by ciliated folds,
usually 2 or 3 in most rachiglossans,

EVOLUTION OF NEOGASTROPODA 319

FIG. 6. Generalized neogastropod oviduct viewed laterally from the right side.
ag, albumen gland; be, bursa copulatrix; cg, capsule gland; 0, ovary; od, upper oviduct; rs, seminal receptacle
or ingesting gland; v, vestibule; vag, vagina; ve, ventral channel.

but the smaller species are rather
anomalous, the Pyrenidae having 0 to
2 (Marcus & Marcus, 1962a) and the
Marginellidae being similarly variable
(Ponder, 1970a). Alcithoe arabica
(Volutidae) has 1 ciliated fold on the right
(Ponder, 1970b) and Strigatella pauper-
cula (Linnaeus) in the Mitridae has only
the left fold present, but Imbricaria con-
ularis (Lamarck) has an additional, small,
right fold (Ponder, 1972b).

A glandular lobe on the left side of the
capsule gland also overlies the ventral
channel in some Muricidae (Fretter, 1941)
and in Alcithoe (Ponder, 1970b). Wu
(1973), however, has shown that there are
at least 4 types of organization in the
Muricidae. One ciliated fold is present on
the right side in Conus mediterraneus
(Martoja-Pierson, 1958) but Haedropleura
septangularis (Montagu), a member of the
primitive turrid subfamily Clavinae, has a
capsule gland like that of Nucella (Smith,
1967b). Thus, probably, the loss of the
ciliated folds and even of the ventral
channel in some other turrids (Smith,
1967b) is a secondary feature.

The bursa copulatrix is a terminal sac for
sperm reception, but in some species it has
become modified for other purposes. In
the majority of the Rachiglossa there is lit-

tle variation in the bursa copulatrix,
although it is very large in Vexillum spp.
(Ponder, 1972b) and in Oliva sayana (Mar-
cus & Marcus, 1959). It is often modified
for storing orientated sperm as well as
catering for temporary sperm storage im-
mediately after copulation. A separate bur-
sa copulatrix is missing in some
marginellids (Graham, 1966), Turbinella
pyrum (Ponder, 1973b) and some turrids
(Smith, 1967b).

Some Turridae (Smith, 1967b) have 2
regions in the anterior part of the oviduct,
1 modified for sperm receiving, therefore
strictly speaking a bursa copulatrix, and
the other for sperm storage. This latter
organ is referred to by Smith as a sperm
sac, but is almost certainly homologous
with the separate bursa copulatrix of other
neogastropods and turrids. The “bursa
copulatrix in those species with a sperm
sac (and in some without) opens directly
into the capsule gland and is thus
homologous with the vagina of other
Neogastropoda. There is little advantage
in changing the names of these structures
which have acquired slight alterations (or
presumed alterations) in function.

The vestibule and vagina sometimes
form a long outgrowth from the capsule
gland. In the turrid genus, Mangelia

320 W. F. PONDER

(Robinson, 1960; Smith, 1967) there is an
elongated part of the oviduct in front of
the short capsule gland and по bursa
copulatrix. In the terebrid Hastula a
similar, but open, structure occurs, as well
as a small bursa copulatrix (Marcus & Mar-
cus, 1960). A narrow, tubular vagina runs
alongside the massive bursa copulatrix in
Vexillum spp. (Ponder, 1972b).

Olivella (Marcus & Marcus, 1959) has a
bulb lying between the capsule and
albumen glands and this is connected by a
long, separate duct to the very short
vagina. This bulb is lined with tall
epithelial cells and contains faecal material
with which the egg capsules are covered. It
is possible that the long, ciliated duct of
this bulb is the pinched-off ventral
channel of the capsule gland and that the
sperm groove now found in the capsule
gland is a new structure. Alternatively it
may be a bursa copulatrix as Marcus &
Marcus suggest, but there is a small pouch
near the genital aperture that could also be
homologous with the bursa copulatrix. In
Olivancillaria (Lintricula) (Marcus & Mar-
cus, 1959) the gonopore lies near the junc-
tion of the capsule gland and albumen
gland where the bursa copulatrix and in-
gesting gland also open.

The Pyrenidae have several unusual
features in the female reproductive system
(Marcus & Marcus, 1962a). They fall into
2 groups; 1 having no albumen gland, a
gonopericardial duct which, together with
the pericardium stores sperm, and a pallial
opening from the pericardium. In 1 species
sperm is ingested in the gonopericardial
duct. The 2nd group has an albumen
gland but no gonopericardial duct and
does have an anteriorly placed, sperm
storage organ (bursa copulatrix) the
epithelium of which ingests spermatozoa
in some species. The vestibule is, in addi-
tion, usually very muscular, with folded
walls, and in 1 species there are 2 separate
gonopores, | to receive the penis and the
other for the passage of eggs.

Smith (1967b) has shown that Propebela
(=Lora) turricula (Montagu) is an her-
maphrodite.

Many neogastropods have а ventral

pedal gland in the female, which aids in
moulding the egg capsule. This appears to
be absent in at least some members of the
Vexillidae, Volutomitridae (Ponder,
1972b) and the Turridae (Smith, 1967b).

Egg Capsules

The resistant, chitinous, neogastropod
egg capsule is a useful taxonomic feature,
particularly at the generic and specific
level, because the egg capsules have
become diagnostic in shape, yet extremely
varied in overall pattern. Many
neogastropod egg capsules have been
described in the literature, but the majori-
ty remain unknown. Ankel (1929) and
Fretter (1941) have shown how the capsule
is moulded by the ventral pedal gland in
the female.

Within each major family group there is
an evolutionary trend in the shape of the
egg capsules. This involves a progressive
raising of the primitive, lens-shaped cap-
sule from the substratum and its eventual
attachment by a narrow stalk. In many
cases the examples and references given
below are only a few of those actually
available in the literature.

The most primitive type of capsule is the
lens-shaped form, which is encountered in
the lower mesogastropods (Littorinacea
and Rissoacea) and in the ar-
chaeogastropod Neritacea. This type is
found in most Turridae (Thorson, 1935,
1946; Knudsen, 1950; Lebour, 1934,
1937), some Marginellidae (Knudsen,
1950: Ponder, 1970a) and Olividae (Mar-
cus € Marcus, 1960a), in the
“Trophoninae in the Muricidae (Hedley,
1917; Habe, 1960; Amio, 1957; Dell, 1964;
Thorson, 1940b, 1946), and Sipho spp. in
the Buccinidae (Thorson, 1935, 1949;
Lebour, 1937). The lens-shaped type pre-
sumably gave rise to the hemispherical
type, there being every gradation between
these 2 forms. Hemispherical
capsules are found in the Volutomitridae
(Ponder, 1972b), in some Marginellidae
(Knudsen, 1950) and Volutidae (Cooke, et
al., 1895; Allan, 1934; Cotton, 1937;
Graham, 194la), in Austromitra in the
Vexillidae (Ponder, 1972b), and in

EVOLUTION OF NEOGASTROPODA 321

Volutopsis norwegicus (Gmelin) in the
Buccinidae (Thorson, 1935). A progressive
elongation of the capsule, with the even-
tual formation of a basal stalk, follows in
several families. These include the Buc-
cinidae, Pyrenidae, Nassariidae,
Muricidae, Marginellidae and Turridae.
The latter 2 families and the Pyrenidae
have only a few examples with stalked cap-
sules (Knudsen, 1950; Risbec, 1929) but
these occur in the majority of the genera
in the other 3 families. Thais (Muricidae)
and allied genera often have parallel-sided
capsules (Lebour, 1945; Hedley, 1906).
Long chains of capsules on a common stalk
occur in the Turbinellidae (Turbinella,
Hornell, 1922), the Galeodidae (Busycon,
Abbott, 1954) and the Buccinidae (Austro-
fusus glans (Riding) (W.F.P.). Ball-like
clusters of capsules are found in some buc-
cinids (Buccinum spp. Thorson, 1935;
Neptunea spp. Golikov, 1961; and Penion
adustus (Philippi), Ponder, 1973a).

The Mitridae (Ostergaard, 1950) have
vase-shaped capsules, whereas the
Conidae (Ostergaard, 1950; Kohn, 1961a)
and the Harpidae (Risbec, 1932) have
flattened pouches. The Magilidae have
thin-walled egg sacs which are retained in-
side the pallial cavity of the female (Gohar
€ Soliman, 1963). The capsule of
Cancellaria sp. described by Knudsen
(1950) is scalpel-shaped and attached by a
long stalk. Some volutid egg capsules have
a calcareous covering, secreted by the
pedal gland (Graham, 1941a).

The types of larval development in the
neogastropods are reviewed by Anderson
(1960).' Planktonic development of the
veliger larva is retained in many
Nassariidae, Pyrenidae, Muricidae,
Mitridae, Conidae, some Turridae,
Magilidae and Terebridae. Complete
development within the egg capsule is
found in at least some Buccinidae,
Galeodidae, Fasciolariidae, Turbinellidae,
Marginellidae, Volutomitridae, Olividae,
Volutidae and Vexillidae.

Several families such as the Turridae,
Muricidae and Pyrenidae combine both
types of development and closely allied
genera, or even subgenera, often have
different types of life history. Clearly the
length of larval life has adaptive
significance and the suppression of the
free-swimming stage is probably brought
about initially by environmental pressures.
There is no definite example of the secon-
dary acquisition of a free-swimming larval
stage.

In those families exhibiting direct
development, usually a large number of
“nurse eggs” do not develop, but provide
nutriment for those that do (Portmann,
1925; Thorson, 1940a, b). Some, ш-
cluding the Marginellidae (Ponder, 1970a)
and Vexillidae (Ponder, 1972b), appear to
rely only on yolk contained within the
large egg(s), while others use albumenous
material secreted by the pallial oviduct
(e.g., Alcithoe arabica, Ponder, 1970b).

The Renal Organ

The renal organ (Fig. 5; ro) lies at the
base of the pallial cavity. Perrier (1889)
divided the neogastropods into 2 groups,
the Méronéphridiens and the Pye-
nonéphridiens, on the basis of the struc-
ture of their renal organs. These, he con-
cluded, were 2 natural divisions, the
former group having the primary and
secondary renal lamellae separated and
the latter having them interdigitated. This
classification was not used by later authors
because of the obvious working dis-
advantages and, like many classifications
that rely on the structure of a single organ,
it has little phylogenetic significance. Both
of these types of renal organs occur in the
Turbinellidae (Ponder, 1973b) and the re-
mainder of the families fall into 1 or the
other groups, so far as is known. However,
relatively few species have been examined,
and with further work the variation within
each family group may be found to be
greater than our present knowledge in-

'A detailed summary of patterns of development in neogastropods has recently been given by Radwin, С. E. and
Chamberlin, J. L., 1973 (Patterns of larval development in stenoglossan gastropods. Trans. San Diego Soc. Nat.

Hist., 17(9): 107-117).

322 W. Е. PONDER

dicates. It is by no means certain which
arrangement is the more primitive.

Most Méronéphridiens have the
primary and secondary lamellae (or fila-
ments) interdigitating to a slight extent.
The families with this type of renal organ
are the Conidae (Perrier, 1889), the
Terebridae (Marcus & Marcus, 1960), the
Volutidae (Perrier, 1889; Ponder, 1970b),
the Pyrenidae (only partially separated)
(Marcus & Marcus, 1962a), the Olividae
(Marcus & Marcus, 1959), the Mitridae
(Ponder, 1972b) and the Marginellidae
(Ponder, 1970a).

The Pycnonéphridien group includes
the Muricidae, Buccinidae (Perrier, 1889),
Vexillidae, Volutomitridae (Ponder,
1972b), Fasciolariidae (Marcus & Marcus,
1962) and the Harpidae (Perrier, 1889).

The Nervous System

The nervous system of the
Neogastropoda has received relatively lit-
tle attention. The studies of Haller (1882,
1888), Bouvier (1887) and Marcus & Mar-
cus (1959, 1960, 1962, 1962a) have pro-
vided much of the detailed information
available.

The nervous system of the Rachiglossa
usually shows considerable concentration
of all of the circum-oesophageal ganglia
and the buccal ganglia are attached by
very short connectives to the cerebral
ganglia. This type of situation is seen in
the Muricidae (Haller, 1882, 1888;
Bouvier, 1887), the Buccinidae (Bouvier,
1887; Dakin, 1912), the Pyrenidae (Marcus
€ Marcus, 1962a), the Fasciolariidae
(Haller, 1888; Bouvier, 1887; Marcus &
Marcus, 1962), the Marginellidae
(Bouvier, 1887), the Mitridae (Bouvier,
1887; Ponder, 1972b), the Vexillidae and
the Volutomitridae (Ponder, 1972b), the
Harpidae (Bouvier, 1887; Bergh, 1901)
and in some Volutidae. A few species in
the last family have the supra-oesophageal
ganglion separated by a long connective
from the right pleural ganglion (details
given by Ponder, 1970b).

The cancellariids (Bouvier, 1887;
Graham, 1966) have concentrated ganglia,
but their buccal ganglia lie just behind the

buccal mass at the distal end of the
proboscis, thus having very long connec-
tives. In the Conacea the ganglia are, in all
3 families, much more separated than they
are in any rachiglossans, with the excep-
tion of the cerebral and pleural ganglia
(Bouvier, 1887; Shaw, 1915; Marcus &
Marcus, 1960).

There are 2 or 3 visceral ganglia near the
base of the pallial cavity, these being well
separated from the circum-oesophageal
ganglia to which they are connected by the
visceral loop.

PART. 3
THE CLASSIFICATION OF
THE NEOGASTROPODA

The classification of the neogastropods
has attracted the attention of many
authors, not only because of the many con-
spicuous groups it contains, but also
because the order contains some of the
more economically and biologically impor-
tant gastropods.

It is not intended to give a detailed ac-
count of the history of the classification of
this order, but a brief examination of some
of the more important contributions is
necessary in order to understand the
derivation of the modern classification.

Contributions to the classification of this
group can be divided into 2 groups. Firstly
there are those that are reviews of the
whole of the gastropods. In these accounts
the classification is mainly concerned, out
of necessity, with the shell. The other
group includes studies on various organ
systems, the results of which have been
used to modify existing classification.

The work of Adams € Adams (1853) is
the earliest comprehensive account of the
Mollusca that we need to consider. Their
treatment of the families now included in
the Neogastropoda differed in a number of
cases from the modern interpretation, but
nevertheless, the majority of the family
groups were much as we know them at
present. The names Stenoglossa, Toxo-
glossa and Rachiglossa were used in
Troschel's (1856-1893) classification, bas-
ed on the radula, which is essentially like
that in use today. The classifications of

EVOLUTION OF NEOGASTROPODA 323

Perrier (1889) based on the renal organ
and Bouvier (1887) on the nervous system
mostly supported the familiar classification
based on dentition.

Certainly any classification based on a
single structure must have its short-
comings, but the radula has the advan-
tages of being readily accessible, as well as
easily interpreted and preserved. The
radula has indeed proved to be a fairly
reliable indicator of the familial position of
species in the Neogastropoda, but parallel
development of similar types has occurred
in distinct families as shown above.

Tryon (1880-1884) and Fischer (1887)
produced comprehensive reviews of the
families of neogastropods, but their classi-
fication differs little from that of Troschel.
Thiele (1929) and Wenz (1938-1943) have
both provided similar, detailed accounts of
gastropod classification and it is these
which are generally in use today. The only
modern attempts at a critical assessment of
gastropod classification are those of Risbec
(1955) and Fretter & Graham (1962).

The curious classification of Iredale &
McMichael (1962) of the Rachiglossa calls
¿for comment. They use, apparently for the

y first time in several cases, a number of
“family” names and include some hetero- 7

At gastropods in this group. Their new
y amilies are, without exception, erected

without indication or any explanations,
and in some cases represent the up-
grading of already existing subfamilies.
Since Troschel's (1856-1893) momen-
tous work on the gastropod radula, the
Neogastropoda (Stenoglossa) have usually
been divided into the Rachiglossa and the
Toxoglossa. Apart from the inclusion of the
Mitridae (e.g., Risbec, 1955) and the
Cancellariidae (e.g., Troschel, 1856-1893;
Keen, 1958), the Toxoglossa is equivalent
to the Conacea discussed above. The main
distinguishing characters of the 3 super-
families given briefly earlier in this paper
ane, outlined in Table 1. The
Neogastropoda, can be defined as follows:

Order Neogastropoda

Shell without inner nacreous layer, and
with anterior siphonal canal. Operculum,

if present, chitinous, with terminal or
lateral nucleus. Radula, if present, with
each row consisting of combinations of a
central tooth, and a pair of lateral and
marginal teeth. Animal with mono-
pectinate ctenidium, bipectinate os-
phradium and anterior siphon. Proboscis
usually pleurembolic, but may be intra-
embolic or polyembolic. Mid-oesophagus
usually with oesophageal gland connected
by a narrow duct (unpaired foregut gland).
Buccal pouches, if present, forming a pad
of glandular tissue at anterior end of the
mid-oesophagus and surrounding the
oesophageal valve to form the valve of
Leiblein. Salivary glands with ducts not
passing through nerve ring, and accessory
salivary glands often present, their ducts
opening at the anterior edge of the buccal
cavity. Anal gland often present; intestine
short and relatively straight. Usually car-
nivorous. Circum-oesophageal ganglia at
least moderately concentrated but visceral
connectives rather long. Sexes usually
separate, female typically with an in-
gesting gland (sometimes a seminal recep-
tacle) lying between a pallial albumen and
capsule gland, and with a ventral pedal

‚ gland which aids in forming the usually

horny egg capsules. Male duct with an
open or closed pallial portion, and with a
penis. Only left auricle and renal organ
present, the latter containing 2 types of
lamellae and a nephridial gland.

Superfamily Cancellariacea
(Synonym Nematoglossa Olsson, 1970)

There are 2 families assigned to this
superfamily, the Cancellariidae and
Paladmetidae. The latter family is an
extinct group lacking columellar folds, and
is discussed in some detail by Sohl (1964).

Olsson (1970) has provided the order
Nematoglossa for the cancellariids, stating
that the radula “is unique and differs so
fundamentally from those of other named
taxa that a new term based upon radular
structure is necessary. In most other
respects the Cancellariidae falls within the
neogastropod group and it is unnecessary,
in my opinion, to separate this family at
the level of order or suborder.

324 W. F. PONDER

Table 1. Comparison of the main features of the neogastropod superfamilies
Muricacea Сопасеа Cancellariacea
о >
no
na
not distinct usually distinct not distinct à ©
=o"
9
=
=:
с
n
pleurembolic with buccal intraembolic or polyembolic pleurembolic; >
cavity at its distal end with buccal cavity at its with buccal e
proximal end cavity at its 2
distal end a
usually present sometimes present very elongate Corral
teeth 8
Ну present rarely present absent al =
usua resen
УР УР teeth a
Marginal
bsent resent absent
MT P teeth
3.9
behind nerve ring behind nerve ring in front of nerve ring i =
85
as
a
©
[=
n
о
ES
usually long absent absent 98
во
(о en |
с
n
5
at posterior end of immediately behind os
anterior oesophagus, absent buccal mass, ventral o я
pyriform Zico
o
e]
short short long 3 @ 9
E
<
2
usually concentrated; usually loosel y usually closely connected; Q SO
lie just behind valve of Leiblein connected; lie just lie near base of proboscis 2 8 8
behind buccal cavity ag 3
8
. . ос
Separated from mid- separated from mid- not separated from Е E 5
oesophagus oesophagus from mid-oesophagus (or 2 ас Е
absent ?) 27370
OS
o
3

EVOLUTION OF NEOGASTROPODA 325

Superfamily Conacea
(Synonym Toxoglossa Troschel, 1848)

The families of the Conacea (Conidae,
Turridae, Terebridae and Speightiidae)
will not be discussed in detail. Powell's
(1942) placing of the extinct Speightiidae
in the Conacea is based on the presence of
a posterior sinus in the aperture, but other-
wise the shells look like fasciolariids.
Powell (1966) has reviewed the genera and
subfamilies of the Turridae and McLean
(1971) has proposed 3 additional sub-
families in a review of the higher clas-
sification of the Turridae. Rudman (1969)
has created a new family, Pervicaciidae,
but his basis for its separation from the
Terebridae is very slight, particularly in
view of Miller's (1971) findings on the
variation in the morphology of the
terebrids, and its recognition does not
appear to be necessary.

Superfamily Muricacea

(Synonym Rachiglossa Troschel, 1848,
and a combination of Thiele's (1929)
Muricacea, Buccinacea and Volutacea,
together with Risbec’s (1955) Mitracea and
Olsson’s (1956) Olivacea.)

Every attempt on the part of the writer
to determine detailed patterns of relation-
ship in the families of the Muricacea has
met with little success. It appears, from the
morphological and palaeontological
evidence, that most of the muricacean
families arose independently in the
Mesozoic (Fig. 4) and are all more-or-less
equally distinct, with the exception of the
Buccinidae, Galeodidae, Fasciolariidae
and Nassariidae. The muricacean families
are discussed below in an attempt to
clarify their relationships to one another.
Table 2 summarizes some of the more im-
portant features of each family.

The family group names Muricacea,
Buccinacea and Volutacea all date from
Rafinesque, 1815 and were erected in the
above order, and Thiele (1929) and Wenz
(1938) both use the superfamily names in
the same order. For this reason the name

Muricacea has been chosen. The name
Rachiglossa does not suit the require-
ments for formal use as a superfamily
name, as it is not based on a contained

genus name (Article 11(e), ICZN, 1961).

Buccinidae, Nassariidae, Fasciolariidae,
and Galeodidae

Differentiation between these groups is
usually possible on shell features and/or
radular features. The magnitude of the
differences, however, is not great and
there are practically no anatomical
features which can be used consistently to
separate them. The writer has followed the
generally accepted practice of retaining
these groups as families but, in fact, they
show levels of differentiation from one
another that could be treated as sub-
familial.

The Buccinidae is an extremely large
and varied family (as listed by Wenz,
1938) and about 20 family and subfamily
names have been based on the genera con-
tained within it. Tryon (1881) included 6
subfamilies, and Fischer (1887) and Coss-
mann (1901) used 7 within the 1 family.?

Powell (1929) recognized 3 family
groups, the Buccinidae, Cominellidae and
Neptuniidae, but in 1951 he made the
cominellids a subfamily of the Buc-
cinulidae. These groups are based on
radular and opercular characters that seem
very minor when the total variation within
the group is considered, and should not be
recognized even as subfamilies. The
majority of the other groups erected have
been based solely on shell features and,
even on this basis, they are hardly
separable.

Many Buccinidae pass through their lar-
val stages within the egg capsules, this
resulting in a paucispiral protoconch, but
the nassariids often have a free swimming
larval stage. This difference may, in part,
be due to the Buccinidae mainly being in
temperate latitudes whereas the majority
of nassariids are tropical or subtropical in
distribution. This view is reinforced by

*Habe, T. and Sato, J., 1972, (A classification of the family Buccinidae from the north Pacific, Proc. Jap. Soc.
Syst. Zool., 8: 1-8) have recognised 6 subfamilies among the larger buccinids of the north Pacific.

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EVOLUTION OF NEOGASTROPODA 327

Phos and some other tropical/subtropical
buccinid genera having multispiral proto-
conchs. The group including Phos and its
allies are sometimes separated as a family,
Photidae. Risbec (1952) and Bouvier
(1888) both show that the Nassariidae and
Buccinidae lack any distinctive morpho-
logical features that could separate them
into 2 groups. The presence of 2 posterior
tentacles on the foot does, however, give
the nassariids a certain distinctiveness.
The radula of the Nassariidae is very
similar to that of many Buccinidae,
although it often bears an accessory plate,
a structure not known in the Buccinidae.
The group is a very homogeneous one,
although Cossmann (1901) recognizes 3
subfamilies within it. Some Nassariidae
have become, secondarily, deposit feeders
and have a crystalline style in the stomach
(Morton, 1960; Brown, 1969).

The Fasciolariidae differs from the
above families and from the Galeodidae in
usually having a red-pigmented head-foot.
The radula, too, is distinctive, with mul-
ticuspid lateral teeth and small central
teeth. In the 2 species investigated, the
structure in the female pallial genital tract
that functions as an ingesting gland in the
above 2 families acts as a seminal recep-
tacle only. Typical members of the
Fusinus group appear to differ from the
remainder of the family only in having a
long siphonal canal, although they are
sometimes separated as a family, the
Fusinidae. However, there are many
genera difficult to place in 1 group or the
other so that the recognition of this group
is not recommended.

No members of the Galeodidae
(=Melongenidae, Volemidae) have been
described in detail, but their anatomy
appears to be like that of the Buccinidae
(Vanstone, 1894; Kesteven, 1904; Pierce,
1950; W.F.P.) except that species in the
genus Melongena have lost the unpaired
foregut gland.

The morphological similarity of these 3

families, together with the allied families
Pyrenidae and Colubrariidae, might sug-
gest that Thiele's Buccinacea should be
used to cover this homogeneous group. If

this were done then the difficulty of
placing families such as the Turbinellidae
and Mitridae, which also show many “buc-
cinacean” features, would show that the
distinctiveness of such a group was, in
fact, well below the normal level that one
would expect in a superfamily. If one were
to retain a division Buccinacea, then most
of the other neogastropod families would
require different superfamilies.

The similarity of the Pyrenidae to the
Buccinidae may be due to parallel evolu-
tion, although there are по records of
species assigned to this family before the
Paleocene, whereas the galeodids, buc-
cinids, and fasciolariids were all present in
the Upper Cretaceous (Wenz, 1938; Sohl,
1964).

Colubrariidae (= Fusidae )

The features of this family, based on
Ratifusus reticulatus (A. Adams) (=
mestayerae (Iredale)) and Iredalula striata
(Hutton), are outlined by Ponder (1968).
This group was probably derived from an
early buccinid stock. The protoconch is
small and multispiral, so that it is probable
that they have a pelagic larval life. The
stomach and mid-oesophagus are different
from those encountered in the Buccinidae.
The shell of Colubraria is superficially like
that of some members of the Cymatiidae
(Tonnacea, Mesogastropoda), but some
other genera in the family have a
resemblance to certain buccinids.

Cernohorsky (1971) indicated that the
anatomical information presented by
Ponder (1968) for Ratifusus and Iredalula
suggested their placement in the Buc-
cinidae, and not that the Colubrariidae is
“buccinacean”. This view he attempted to
substantiate by showing that the type
species of Colubraria, C. maculosa
(Gmelin, 1791) (= muricata Lightfoot,
1786) does not have a radula whereas

' Ratifusus and Iredalula do have a minute

radula, which is, however, virtually
vestigial. A study of the anatomy of
Colubraria cf. sowerbyi (Reeve) (W.F.P.)
has shown that it possesses the same
peculiar glandular mid-oesophagus that
differentiates Ratifusus and Iredalula from

328 W. F. PONDER

the Buccinidae and the other features of
the anterior alimentary canal are also
similar except that there is no odontophore
or radula. It thus appears that some
Colubrariidae have lost the radula and that
it is relatively small or vestigial in the
remainder. It is possible that the whole
Metula-Ratifusus series discussed by Cer-
nohorsky (1971) belong in the
Colubrariidae as they all have similar shell
features.

The Upper Cretaceous genus Fulgerca
Stephenson is possibly a colubrariid,
although Sohl (1964) includes it doubt-
fully in the Buccinidae. Another possible
Upper Cretaceous colubrariid is
Plesiotriton cretaceus Sohl (Dr. A. G. Beu,
pers. comm.). Colubraria extends back to
the Paleocene (Wenz, 1938).

Turbinellidae (=Vasidae, =Xancidae)

The features of this family will be dis-
cussed elsewhere (Ponder, 1973b). It
shows similarity, on the one hand, with the
Buccinidae and its allied families, in not
having accessory salivary glands and in the
possession of a thick, heavy, spindle-
shaped shell, large operculum and long
proboscis. Discordant features are the
radula and anal gland of Turbinella, the
open or partially fused pallial sperm
grooves and the columellar folds. Vasum
has a radula like that of Melongena, and it
apparently does not possess an anal gland.
The first appearance of this family, like
many of the Muricacea, is during the
Cretaceous (Fig. 4) and it seems likely that
most of its features were derived quite in-
dependently from, but in a parallel fashion
to, the buccinid-nassariid-galeodid-
fasciolariid complex. The Pyrenidae, too,
probably acquired the “buccinacean”
features of the alimentary canal т-
dependently.

The subfamilies Turbinellinae and
Vasinae appear to be quite distinct
anatomically (Ponder, 1973b).

Pyrenidae (=Columbellidae)

The pyrenids exhibit both specialized
and primitive features. Risbec (1954) and
Marcus € Marcus (1962a) have provided

most of the available information on the
anatomy of the family. The alimentary
canal is rather uniform and is similar to
that of the Buccinidae. The radula shows a
tendency towards suppression of the cen-
tral teeth and the lateral teeth are usually
attached by narrow bases. The reproduc-
tive system shows considerable diversity
and Marcus & Marcus (1962a) suggest that
the family could eventually be divided
into 2 groups on the basis of the structure
of the genital organs. Some pyrenids have
become herbivorous (Marcus € Marcus,
1962a). Many species have lost the oper-
culum and their shells usually have long,
narrow apertures.

Muricidae (=Thaididae, etc.)

Distinctive morphological features of
the Muricidae (in the broad sense) include
accessory salivary glands, a purple hypo-
branchial secretion, a massive gland of
Leiblein, a broad caecum in the stomach,
an anal gland and a large, closed, prostate
gland. The path of torsion is indicated in
the conspicuous valve of Leiblein by a
narrow groove, and the primary and secon-
dary lamellae of the renal organ are not
separated. The small foot has an accessory
boring organ on its anterior, ventral sur-
face and the radula has 3 teeth in each
transverse row, the central tooth usually
having 3 primary cusps. The muricids
form a rather homogeneous group in
which Cossmann (1903) recognized 5 sub-
families (Ocenebrinae, Muricinae,
Trophoninae, Typhinae, and Rapaninae),
with the Purpuridae (=Thaididae) as a
separate family. The differentiation be-
tween the subfamilies is small, although
they do appear to form fairly natural
groups. The Thaididae is no more distinct
than any of the subfamilies contained
within the Muricidae and could be
regarded as one also. Morphological
differentiation between the “subfamilies”
is slight, but, judging from the few species
that have been examined, the accessory
salivary glands show a progressive en-
largement and separation from the normal
salivary glands through the Muricinae and
Trophoninae to the Thaidinae,

EVOLUTION OF NEOGASTROPODA 329

Ocenebrinae and Вараптае. The small
radular and shell differences that have
been cited between the various groups
(e.g., Vokes, 1964) do not appear to be
consistent (Ponder, 1972a), although the
case for use of several subfamilies has
been put strongly by Radwin & D Attilio
(1971) and Vokes (1971). The operculum
has often been cited as evidence for the
separation of Thaidinae and Ocenebrinae
from the remainder of the family because
in these groups it has a lateral nucleus.
However opercula with both terminal and
lateral nuclei occur within the genus
Murex and other exceptions are known.
There appears to be little advantage in
retaining these subfamilial groupings until
stronger evidence for their distinctiveness
is forthcoming.

Wu (1973) has outlined some of the
variation of anatomical structures in the
Muricidae.

Radwin & D'Attilio (1971) recognize the
Rapanidae, Thaididae, and the Muricidae
as separate families on the basis of shell,
radular and opercular details.

Magilidae (=Coralliophilidae, Rapidae)

The shells of some members of the fami-
ly closely resemble those of some
Muricidae, but the 2 groups can be
separated on the absence of a radula in the
Magilidae. The unpaired foregut gland is
massive and its interior is divided trans-
versely by conspicuous partitions (Bouvier,
1888; Ward, 1965). This structure was mis-
identified as the stomach by Gohar €
Soliman (1963). The sedentary species that
live in burrows within coral appear to
possess an anal gland (W.F.P.) whereas the
actively mobile Coralliophila abbreviata
(Lamarck) (Ward, 1965) does not. It is pos-
sible that some magilids may be found to
possess a vestigial radula and it might be
found that, in such species, the Magilidae
and Muricidae closely approach one
another. The few species of the Magilidae
investigated however, have only 1 pair of
salivary glands, the ducts of which join to
form a common dorsal duct in
Coralliophila abbreviata (Ward, 1965).

In the sedentary and freely moving

species so far examined the female stores
the egg capsules inside the mantle cavity,
a habit not seen in any other
neogastropod.

These gastropods feed suctorially on
coelenterates (Robertson, 1970), although
it is not certain how species such as
Magilus (which are permanently em-
bedded in their coral host with only a tiny
external aperture through which the
proboscis can emerge) feed.

Columbariidae

The possession of a very long proboscis
makes this group distinct from the
Muricidae. The radula, too, is rather
different from the normal muricid type.
The family resembles the Muricidae in
having a large unpaired foregut gland and
an anal gland, but is similar to the Buc-
cinidae in the lack of any glandular dorsal
folds in the mid-oesophagus and in the
absence of accessory salivary glands.

Thiele (1929) included Columbarium in
the Muricidae but Tomlin (1928)
separated it, as a family, on shell and oper-
cular features. It was reduced to a sub-
family of the Muricidae by Wenz (1938),
but Iredale (1936) gave it full family
status, which is followed here, based on
the anatomy of Coluzea spiralis (A.
Adams) and С. mariae (Powell) (W.F.P.).
Iredale placed the family near the
“Fusinidae (Fasciolariidae). This family
has recently been reviewed by Darragh
(1969).

Volutidae

Distinctive features of the majority of
the Volutidae include the broad hood over
the rhynchostome, formed by the tentacle
bases, the large foot, and the siphonal
appendages. Both types of salivary gland
are present and there is sometimes a pur-
ple hypobranchial secretion. The dorsal
folds of the mid-oesophagus are usually in-
corporated as a duct-like structure in the
unpaired foregut gland and the path of
torsion is indicated in the valve of
Leiblein. The primary and secondary renal
lamellae are separated and the pallial,
male, genital tract is often an open groove

330 W. Е. PONDER

or prostate gland. Typically the shell has
columellar plaits, and there is usually no
operculum. The radula nearly always con-
sists of only the central teeth. Develop-
ment is nearly always complete in the cap-
sule, although some species have small
multispiral protoconchs suggesting pelagic
larval development.

Cossmann (1899) used 6 subfamilies in
the Volutidae, but Wenz (1938) used only
4 (excluding the Volutomitrinae). Pilsbry
& Olsson (1954) introduced 8 new sub-
families and a number of tribes. Altogether
they divided the family into 12 sub-
families and 8 tribes. While this is almost
certainly excessive considering the
evidence available, there should be no
doubt as to the pure composition of each of
their groups. It is probable that an assess-
ment of the characters of the male genital
system, together with the radula and shell,
would derive a more conservative clas-
sification that would, at the same time, be
natural. Clench & Turner (1964) divided
the subfamilies on the basis of the
appearance of the salivary glands, the un-
paired foregut gland and the shape of the
radula. Weaver & duPont (1970), in their
monograph of the family, recognize 9 sub-
families among the Recent species.

Olividae

Olsson (1956) created a superfamily for
the Olividae in which Marcus & Marcus
(1959) included the Harpidae. The
morphology of the Olividae has so much in
common with that of the rest of the
Muricacea that, in the writer s opinion, a
separate superfamily is unwarranted.

Olsson (1956) included 4 subfamilies
and, doubtfully, a 5th, the Pseudolivinae,
which he suggested possibly does not
belong in the family in which it is placed
by Thiele (1929) and Wenz (1938). Coss-
mann (1899) included the Pseudolivinae in
the Buccinidae.

Marcus & Marcus (1959, 1968) gave a
detailed account of the morphology of 5
species of Olividae. Olivella stands out
sharply in its morphological differentia-
tion.

Marcus & Marcus (1959) suggest that

the Olividae has some features in common
with Thiele's Buccinacea and Volutacea
and may have been derived from a com-
mon ancestor. Perhaps this is so, but the
common features they mention such as the
large foot and concentrated nervous
system were probably derived by parallel
evolution, and do not indicate a direct
relationship.

The olivids superficially resemble the
harpids and volutids, but differ from them
in having the sides of the foot extending
over the shell. The harpids have no
accessory salivary glands, but these are
found in most olivids and the region of tor-
sion in the gut of the olives is different
from that in the volutes. The radula of
Harpa is more like that of the Volutidae
than the type that is found in most olivids.
Both Harpa and the olivids have a distinct
propodium, a feature not found in any
other neogastropods, but this by itself does
not necessarily indicate their close rela-
tionship. The Olividae and the Harpidae
may have both independently developed
the muscular propodium of the foot, which
is such a useful digging tool. There are
several other differences between the 2
families, for example the harpids have a
pallial sperm groove (Bergh, 1901), but
this is a closed duct in the olivids.

Harpidae

An account of the morphology of this
family is given by Bergh (1901) and Quoy
& Gaimard (1833). These authors describe
how the posterior end of the foot can be
automatized. The valve and gland of
Leiblein have been lost and there is ap-
parently no anal gland or purple
hypobranchial secretion. There is no oper-
culum.

The lack of an anal gland and accessory
salivary glands, together with the pyc-
nonéphridien condition of the renal organ,
suggest affinity with the Buccinidae. This,
however, is rather unlikely considering the
other morphological features.

Volutomitridae and Marginellidae

A list of morphological features of these
2 families is given by Ponder (1970a,

EVOLUTION OF NEOGASTROPODA

1972b). They have several unusual
features in common and thus they may
have arisen from a common stem. These
characters include а single accessory
salivary gland; the seminal receptacle
lined with large, cuboidal cells; the
absence of an ingesting gland; and a
narrow diverticulum of the renal organ
which approaches or enters the renal
genital duct. From the situation in the
Volutomitridae, it would appear also that
the unpaired foregut gland may have been
stripped off the mid-oesophagus forwards
instead of backwards.

Both families consist of species with

small shells which have columellar plaits.\
All marginellids and many microvolutids D

have lost the operculum but some micro-
volutids have retained it or have it as a
rudiment. The lateral radular teeth are ab-
sent in the Marginellidae and weak or ab-
sent in the Microvolutidae. Differences be-
tween the 2 families include the structure
of the mid-oesophagus, the male repro-
ductive system, the stomach and the renal
organ. Cernohorsky (1970) has reviewed
the Volutomitridae.

Wenz (1938) gives an Eocene origin for
the Marginellidae, but the Upper
Cretaceous genus Myobarbum Sohl is
possibly an early marginellid.

Mitridae and Vexillidae

The structural differences between
these 2 families have been outlined by
Ponder (1972b). The 2 groups appear to
have evolved quite independently, but
show a remarkable parallelism in their
shell morphology. Differences in the ali-
mentary canal, including the radula, and
in the renal organ, set the 2 families apart.
There is a similarity in the reproductive
organs, but this is probably part of the
general uniformity in these organs
throughout the Neogastropoda. Cer-
nohorsky (1970) has reviewed these 2
families (as the Mitridae) in some detail.

ACKNOWLEDGEMENTS

I would like to thank Dr. M. Winter-
bourne, Dr. D. Hoese, Dr. V. Fretter, Prof.

3Now the National Museum.

331

A. Graham and Dr. R. D. Turner for their
comments on the manuscript and my wife
for help in checking the manuscript. Mr.
E. K. Yoo prepared Fig. 1. This work was
largely completed while I was employed at
the Dominion Museum, Wellington, and
forms part of a Ph.D. thesis completed un-
der the supervision of Prof. J. E. Morton,
Auckland University.

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ZUSAMMENFASSUNG
ABSTAMMUNG UND ENTWICKLUNG DER NEOGASTROPODEN
W. F. Ponder

Die Ordnung Neogastropoda entwickelte sich wahrscheinlich aus den
Archaeogastropoden und nicht von den höheren Mesogastropoden, wie allgemein
angenommen wird. Es wird angenommen, daß die Eigenarten des Verdauungssystems
der Neogstropoden von Bildungen abgeleitet werden können, die bei den Arch-
aeogastropoden existieren. Die Neogastropoden haben sich augenscheinlich in 3
Gruppen entwickelt, die hier als Oberfamilien betrachtet werden, die Muricaceae,
Conaceae und Cancellariaceae.

Die Entwicklung der verschiedenen Organsysteme bei den Neogastropoda wird skiz-
ziert und dabei die Tendenz bemerkt, Struktureren in paralleler Richtung zu
modifizieren. Die Beziehungen der einzelnen Familien innerhalb der Muricaceae un-
tereinander werden diskutiert. Es scheint, daß innerhalb dieser Gruppe keine
natürlichen höheren Gruppierungen existieren, zwei Fälle ausgenommen, Wahrschein-
lich, weil alle diese Familien von der gleichen Stammform mehr oder weniger
gleichzeitig abgezweigt sind. So sind verschiedene Strukturen ziemlich zufällig durch die
Oberfamilie verteilt, je nach der Weise, wie sich jede Familie weiterentwickelt hat. Die

EVOLUTION OF NEOGASTROPODA

Marginellidae und Volutomitridae können unabhängig entstanden sein, während die
Buccinidae, Melongenidae, Nassariidae und Fasciolariidae so nahe verwandt sind, daß
sie möglicherweise als Unterfamilien angesehen werden können.

HZ:

RESUME
L'ORIGINE ET L EVOLUTION DES NEOGASTROPODES

W. F. Ponder

L’ordre des Néogastropodes а probablement évolué а partir des Archéogastropodes et
non des Mésogastropodes supérieurs, comme on le сгой généralement. П est probable
que les caractéres uniques du canal alimentaire des néogastropodes aient pu dériver de
structures existant chez les archéogastropodes. Les néogastropodes semblent avoir évolué
en 3 groupes qui sont ici considérés comme des superfamilles: les Muricacea, Conacea et
Cancellariacea.

Dans la présente étude on a tracé à grands traits l’évolution des divers appareils а
l’intérieur des néogastropodes et Гоп y a noté la tendance à modifier les structures dans
des voies paralleles. Les liens de parenté entre chaque famille chez les Muricacea, ont été
discutés. A deux exceptions pres, il apparait que dans ce groupe, il n y a pas de groupe-
ments naturels de plus haut niveau, sans doute parce que toutes les familles évoluent а
partir Чип ancétre commun а peu prés simultanément. Ainsi les divers types de struc-
tures sont distribuées presqu au hasard à travers la superfamille, selon la voie dans
laquelle chaque famille a évolué. Les Marginellidae et Volutomitridae peuvent étre ap-
parues indépendamment, tandis que les Buccinidae, Melongenidae, Nassariidae et
Fasciolariidae sont de parenté si proche, qu elles peuvent étre considérées comme des
sous-familles.

A.L.

RESUMEN
ORIGEN Y EVOLUCION DE LOS NEOGASTROPODA
W. F. Ponder

El orden Neogastropoda probablemente tuvo descendencia de los Archaeogastropoda
y no, como generalmente se cree, de los mäs evolucionados Mesogastropoda. Se sugiere
que las caracteristicas, únicas, del canal alimenticio en neogastrópodas, pueden haber
derivado de estructuras ya existentes en arqueogastrópodos. Parece que, en su evolución
los Neogastropoda han producido tres grupos, a los cuales se asigna aqui el rango de
superfamilias: Muricacea, Conacea y Cancellariacea.

Se han delineado en forma general los varios sistemas de órganos en Neogastropoda, y
se hace notar la tendencia hacia la modificación de estructura en modo paralelo. Se dis-
cute tambien las relaciones entre las familias de los Muricacea. Con un par de excep-
ciones, no parece haber dentro del conjunto grupos naturales de más alta jerarquia,
probablemente porque todas las familias se derivan de un antecesor común más o menos
simultaneamente. Asi, varias estructuras se distribuyen casi al azar en toda la super-
familia, de acuerdo al modo en que cada familia ha evolucionado. Los Marginellidae y
los Volutomitridae pueden haber tenido independiente origen, mientras que los Buc-
cinidae, Melongenidae, Nassaridae y Fasciolariidae estan tan estrechamente
relacionados, que posiblemente podrían considerarse como subfamilias.

PIE:

337

338

W. F. PONDER
ABCTPAKT

ПРОИСХОЖДЕНИЕ И ЭВОЛЮЦИЯ NEOGASTROPODA
В.Ф. ПОНДЕР

Отряд возможно развился из Archaeogastropoda, a не от высших Mesogastropoda,
как это обычно считают. Предполагается, что характерные черты строения
пищеварительного канала y Neogastropoda можно произвести OT yxe
существующих их структур У Archaeogastropoda. Neogastropoda видимо должны
быть разделены на 3 группы, которые автором рассматриваются как
надсемейства - Muricacea, Сопасеа И Cancellariacea.

Рассматривается эволюция систем различных органов внутри отряда
Neogastropoda и подчеркивается тенденция к параллелизму в модификации их
структур. Обсуждаются родственные связи каждого семейства в отряде
Muricacea. За двумя исключениями внутри этого отряда видимо нет более
высоких естественных группировок, может быть потому, что все семейства
произошли более или менее одновременно от общего предка. Таким образом,
различные структуры встречаются довольно случайно BO всем
надсемействе, соответственно происхождению каждого входящего в него
семейства.

Marginellidae и Volutomitridae могли возникнуть независимо друг от друга, в
то время, как Buccinidae, Melongenidae, Nassariidae и Fasciolariidae имеют такое
близкое родство, что их возможно рассматривать как надсемейство.

Z.A.F.

MALACOLOGIA, 1973, 12(2): 339-378

SUR LES MOLLUSQUES FLUVIATILES DE MADAGASCAR

E. Fischer-Piette et D. Vukadinovic

Muséum National d’ Histoire Naturelle
55, rue de Buffon, Paris Ve, France

RESUME

Ce travail est ип complément а celui de Starmühlner paru dans MALACOLOGIA en
1969. Il le compléte surtout en mentionnant les Lamellibranches en plus des
Gastéropodes et en donnant pour beaucoup de Gastéropodes des provenances plus nom-
breuses.

Pendant trés longtemps la faune malacologique fluviatile de Madagascar ne fit l'objet
d aucun travail important! Enfin, en 1969, Starmühlner (Malacologia, 8(1-2)) a publié un
gros mémoire ou les Gastéropodes sont étudiés, et souvent de facon trés approfondie, en
particulier au point du vue de l'anatomie, histologie comprise.

Le present travail est en somme ип complément а celui de Starmühlner, pour celles des
especes dont cet auteur пе s était pas occupé (Lamellibranches, etc.), et aussi, pour les
autres, pour faire connaître des localités supplémentaires, grâce à l’abondance des
matériaux qui depuis longtemps se sont accumulés au Muséum de Paris.

Clithon brevispina Lamarck

1822 Neritina brevi-spina, LAMARCK, 6(2): 185.

1838 Neritina brevispina, POTIEZ & MICHAUD, p 301, pl. 29, fig. 3, 4.

1841 Neritina brevispina, DELESSERT, pl. 32, fig. 5.

1843 Neritina auriculata, SGANZIN, p 20.

1850 Neritina brevispina, PETIT de la SAUSSAYE, 1: 76.

1849 Neritina brevispina, SOWERBY, 2: 524, pl. 110, fig. 45, 51, 52.

1860 Neritina brevispina, MORELET, 2: 126.

1888 Neritina brevispina, TRYON, 10: 65, pl. 23, fig. 16-18; pl. 24, fig. 19-28, 31-34.
1956 Clithon brevispina, FRANC, 13: 17, fig. 8.

Espece а trés large répartition. Le premier auteur qui Гай citée de Madagascar est
Sganzin, qui la dit “tres commune dans toutes les rivieres de Madagascar. Les autres
auteurs qui l'ont citée de l'île, Petit de la Saussaye et Morelet, n'ont pas donné de
provenance précise.

Nous doutons que cette espéce soit aussi bien représentée que Га dit Sganzin, car nous
nen avons pas trouvé dans les nombreuses récoltes de Madagascar qui nous sont
parvenues, si ce n'est un échantillon que nous avons extrait d'un lot de №. madecassina qui
était accompagné de l'étiquette suivante:

“Mr. Férussac l'avait dans sa collection pour le nom de Мег. Barbabac nom pour lequel
on la lui avait envoyée de Madagascar.

“donné par Mr. Sganzin.”

(339)

340 FISCHER-PIETTE ET VUKADINOVIC

Clithon (Clithon) longispina Recluz

1841 Neritina longispina, RECLUZ, p 312.

1849 Neritina longispina, SOWERBY, 2: 522, pl. 110, fig. 62, 63.

1860 Neritina longispina, MORELET, 2: 120, 126.

1879 Neritina longispina, MARTENS, ed. 2, 2(10): 147, pl. 15, fig. 16, 17, 20, 21.
1888 Neritina longispina, TRYON, 10: 63, pl. 23, fig. 3-5.

1908 Paranerita (Neritina) longispina, BOURNE, р 847.

1969 Clithon (Clithon) longispina, STARMUHLNER, 8: 56.

Espéce a large répartition. Pour Madagascar, nous ne croyons pas qu aucune
provenance précise ait jamais été donnée. Les collections du Muséum renferment, avec la
seule indication Madagascar” neuf lots; ceux pour lesquels le donateur ou récolteur est
indiqué sont de Eydoux, Texor de Ravisi, 1853, et Lamare Piquot, 1865.

Clithon madecassina Morelet

1795 Nerita corona Bengalensis, CHEMNITZ, 11: 176, pl. 197, fig. 1911.

1838 ?Neritina Bengalensis, POTIEZ € MICHAUD, p 300, pl. 29, fig. 1, 2.

1849 Neritina Bengalensis, SOWERBY, 2: 525, pl. 109, fig. 30, 31.

1850 Neritina Bengalensis, RECLUZ, 1: 148.

1860 Neritina madecassina, MORELET, 2: 122, pl. 6, fig. 2.

1879 Neritina (Clithon) madecassina, MARTENS, ed. 2, 2(10): 149, pl. 16, fig. 1-3.

Il est possible que la dénomination Neritina Bengalensis Pot. et Mich. doive l'emporter
sur Neritina madecassina Morelet. Mais Potiez & Michaud disent que leur espéce est
“d'un beau vert-pomme tacheté de jaune fauve.” Or vonMartens (1879, р 149) dit n avoir
pas rencontré de teinte vert-pomme, et il en est de méme pour nous. Nous ne connaissons
que du vert olive ou du brun parfois trés foncé.

Espece répartie assez largement. La seule localité précise qui avait été donnée pour
Madagascar est l’île Sainte-Marie (Morelet). Les collections du Muséum permettent d’a-
jouter les provenances suivantes: Rivière des Caimans (Decary); Maroansetra, ruisseau
(Brygoo, 1957); embouchure de la riviére Mananara (Decary, 1920); Ivontaka (Decary,
1920); Anjahambe, riviére Manantsatrana (Brygoo, 1957); Ampasina, riviére Maningory
(Brygoo, 1957); riviére Ivoloina (G. Petit, 1926); Foulpointe, riviére Onibe (Decary, 1920).

Toutes ces localités sont portées sur notre Fig. 1. On remarquera que toutes sont sur la
cóte, et uniquement dans le Nord et le Nord-Est.

Clithon (Clithon) spiniperda Morelet

1860 Neritina spiniperda, MORELET, 2: 121, pl. 6, fig. 3.

1879 Neritina spiniperda, MARTENS, ed. 2, 2(10): 266.

1881 Neritina spiniperda, CROSSE, 29: 208.

1883 Neritina spiniperda, MORELET, 31: 203.

1888 Neritina spiniperda, TRYON, 10: 70, pl. 26, fig. 78.

1890 Neritina (Clithon) spiniperda, BOETTGER, 22: 101.

1892 Neritina (Clithon) rhyssodes, BOETTGER, 24: 57.

1969 Clithon (Clithon) spiniperda, STARMUHLNER, 8: 28, fig. 4-7.

Cette езрёсе était connue de Nossi-Bé et Nossi-Comba. Les collections du Muséum
permettent d'ajouter une autre provenance: Ambanja-Anorotoangana (Waterlot). Voir
carte Fig. 1.

Neritina rhyssodes avait été décrite par Boettger sans figure, mais le type a été figuré
par Hass (1929), sous le nom Neritina (Clypeolum) pulligera knorri.

MOLLUSQUES DE MADAGASCAR 341

eClithon madecassina norel.
AClithon spiniperda xorel

Nossi-Bé

Nossi- Comba

A

Amlboanja _{ Wa

Maroansetra

Mananara

Ile St’ Marie
Ampasina

Ivontaka hiba

Anjahambe____,

-
MOI Foulpointe

FIG. 1. Distribution de Clithon madecassina Mor. et de Clithon spiniperda Mor.

Neritina (Neritina) pulligera Linné

1767 Neritina pulligera, LINNE, 12: 1253.

1786 Nerita Rubella, Pulligera, CHEMNITZ, 9: 64, pl. 124, fig. 1078, 1079.

1841 Nerita Knorri, RECLUZ, p 274.

1849 Neritina pulligera, SOWERBY, 2: 510, pl. 111, fig. 65, 66.

1849 Neritina Knotrii, SOWERBY. р 511, pl. 111, fig. 78; pl. 113, fig. 150.

1860 Neritina Knorri, MORELET, 2: 120.

1879 Neritina pulligera, MARTENS, ed. 2, 2(10): 49, pl. 1, fig. 4, 5.

1879 Neritina Knorri, MARTENS, ed. 2, 2(10): 55, pl. 8, fig. 4-6.

1881 Neritina Knorri, CROSSE, 29: 207.

1888 Neritina pulligera, TRYON, 10: 56, pl. 18, fig. 6-13; pl. 19, fig. 14-19, 22, 24.
1890 Neritina (Neritaea) knorri, BOETTGER, 22: 98.

1890 Neritina (Neritaea) stumpffi, BOETTGER, 22: 99.

1914 Neritina (Clypeolum) pulligera var. knorri, ROBSON, 32: 377.

1919 Neritina pulligera var. knorri, ODHNER, 12: 43.

1929 Neritina pulligera, DAUTZENBERG, 3: 526.

1929 Neritina (Clypeolum) pulligera knorri, HAAS, 57: 428, fig. 27 (fig. 25-26 excl.).
1969 Neritina (Neritina) pulligera, STARMUHLNER, 8: 69, fig. 73-76.

Neritina stumpffi Boettger, décrite sans figure a été placée par Haas (qui en a figuré le
type, fig. 27) dans la synonymie de pulligera; Starmühlner $ est conformé а cette opinion;
nous faisons de méme, la description donnée étant détaillée. Une autre espéce, créée sans
figure, Neritina truncata Sganzin (1843) de Madagascar, a été placée par Starmühlner

342 FISCHER-PIETTE ET VUKADINOVIC

dans la synonymie de pulligera, mais il est impossible de savoir de quoi il s agit, ce nom
truncata n étant accompagné que de quelques mots si insuffisants que c'est à peu pres un
nomen nudum.

Cette езрёсе, а trés large répartition, était connue pour Madagascar, des provenances
suivantes: Nossi-Bé, Morelet, Crosse, Boettger; Nossi-Comba, Boettger; riviere An-
drohibe, Odhner; Majunga, Haas; entre Tamatave et la baie d'Antongil, Robson.

Les collections a Muséum permettent d'ajouter les provenances suivantes: riviére des
Caímans (Decary); Ambanja (Waterlot); riviere Andranomalaza а Maromandia (Decary,
1922); и (Н. Soula, 1968); Ankavanana (H. Soula, 1968); Ambatofotsy sur
riviere Ankavia (Н. Soula, 1969); Virembina (H. Soula, 1969); Antsiafapiana (H. Soula,
1969); Maroansetra (D. Brygoo, 1957); Andratambe, riviere Mananara (Decary); An-
dranomavo (С. Petit, 1926); riviere Kapiloza (С. Petit, 1926); Fenerive (Brygoo, 1957);
Tamatave (G. Petit).

Toutes ces localités sont portées sur notre carte Fig. 2. On remarquera, d'une part

qu'elles sont toutes sur la côte ou non-loin, et d'autre part qu elles sont toutes dans le tiers
Nord de Tile.

Neritina (Neripteron) auriculata Lamarck

1822 Neritina auriculata, LAMARCK, 6: 186, pl. 455, fig. 6 de ГЕпсусюр. méth.
1838 Neritina auriculata, DESHAYES, ed. 2, 8: 572.

1843 Neritina auriculata, SGANZIN, р 20.

1860 Neritina auriculata, MORELET, 1: 126.

1879 Neritina auriculata, MARTENS, ed. 2, 2(10): 30, pl. 6, fig. 13-15, 24-27.
1888 Neritina (Neripteron) auriculata, TRYON, 10: 73, pl. 21, fig. 58-63.

1969 Neritina (Neripteron) auriculata, STARMUHLNER, 8: 56, fig. 58.

Espece à trés large répartition, citée à plusieurs reprises de Madagascar, mais une seule
fois (Starmühlner) avec une localité précise, St. Augustin. Les collections du Muséum
permettent d'ajouter les provenances suivantes: Maroansetra (Brygoo, 1957 ); enbouchure
de la riviere Mananara (Decary, 1920); Maintinandry, riviere Sakamila (Brygoo, 1957) et
Sandranoro (H. Bertrand, 1970). Voir notre carte Fig. 3.

Neritina (Vittina) turrita Chemnitz

1786 Nerita turrita, CHEMNITZ, 10(2): 71, pl. 124, fig. 1085.

1849 Neritina turrita, SOWERBY, 2: 539, pl. 112, fig. 91, 113, 114.

1850 Nerita turrita, RECLUZ, 1: 152, pl. 3, fig. 8.

1879 Nerita turrita, MARTENS, ed. о, 210): 105. 21.72. fig 5; ple Al fig. 18-21
1888 Nerita turrita, TRYON, 10: 37, pl. 11, fig. 1, 2.

Espece à trés large répartition.

Aucune localisation précise à l’intérieur de l'île de Madagascar n'est donnée dans la
littérature. De même, c'est avec la seule indication Madagascar” que se trouvent, dans la
collection du Muséum, des lots au nombre de sept, venant de Liautaut, 1843; Amiral de
Hell, 1847: Cloue, 1850; Texor de Ravisi, 1853; Ballot, 1887; Largentiere, 1887; Denis,
1945.

Neritina (Vittina) gagates Lamarck

1822 Neritina gagates, LAMARCK, 6(2): 185.

1828 Neritina caffra, GRAY, In: WOOD, pl. 8, fig. 10.

1877 Nerita caffra, ANGAS, p 527.

1879 Neritina gagates, MARTENS, ed. 2, 2(10): 94, pl. 16, fig. 11, 12; pl. 10, fig. 18, 19; pl. 13,
fig. 8.

1882 Neritina gagates, SMITH, p 387.

1882 Neritina fulgetrum, SMITH (non REEVE), p 387, pl. 22, fig. 23, 24.

MOLLUSQUES DE MADAGASCAR 343

1888 Neritina gagates, TRYON, 10: 35, pl. 10, fig. 77-79, 97, 98; pl. 11, fig. 6.
1890 Neritina (Neritaea) gagates, BOETTGER, 22: 99.

1914 Neritina gagates, ROBSON, 32: 377.

1929 Neritina gagates, DAUTZENBERG, 3: 526.

1929 Neritina (Neritina) gagates, HAAS, 57: 427.

1969 Neritina (Vittina) gagates, STARMUHLNER, 8: 61, fig. 63-66.

Cette espéce était connue des provenances suivantes: Tsararano, Dautzenberg; Nossi-
Bé, Dautzenberg, Starmühlner; Nossi-Comba, Boettger; Marodasatia (baie d'Antongil),
Robson; Antanambe, Haas; Tamatave, Robson, Haas, Smith; Ekongo, Angas; St.
Augustin, Starmühlner.

Les collections du Muséum permettent d ajouter les provenances suivantes: rivière des
Caïmans (Decary); Пе Nosy-Lava, pres Ananalava (Waterlot); Virembina (H. Soula, 1969);
Antsiafapiana, 8 km S.S.O. de Maromandia dans la vallée de la Sahefihitra (H. Soula,
1969), Androhofary, 2 km environ au N.-O. d’Ambohibe (H. Soula, 1969); Ат-
bohivoangibe, 3 km au N.-E. d Ampohibe pres Antsirabato pres Mohatsara (H. Soula,
1969); riviere Manambolosy (H. Bertrand, 1970); embarcadére de Marovoay, eau
saumátre (С. Petit, 1926); riviere Soanierana, pres Tamatave (С. Petit, 1927); riviere entre
Soanierana et Maningory Manansatrana (G. Petit, 1927); Tamatave (G. Petit);
Foulpointe, riviere Onibe (Decary, 1920); Andevoranto, estuaire du Zaroka (С. Petit,
1926); riviére Sandramanongy (Brygoo, 1957); village Manakambahiny, canton Vatoman-

Nossi-Be Riviere des Caimans

Nossi- Comba |
ns
Ambanja

Maromandıa

Androhibe wa ans

Virembina Antsiafapiana
Ambatofotsy

Maroansetra

Andranomavo—®

Entre Tamatave et Andratambe

la Baie d'Antoneil no

Fenerive

-Tamatave

FIG. 2. Distribution de Neritina pulligera Linné.

344 FISCHER-PIETTE ET VUKADINOVIC

dry (Brygoo, 1957); eau saumátre d'un petit lac pres d’ Andrahomana (Mission Grandidier,
1901) et Marovary.

On voit que les provenances connues а ce jour sont toutes sur la cóte ou а faible dis-
tance, et sur toute la longueur de l'île. L'intérieur de l’île n'en a pas donnée. Voir notre
carte Fig. 4.

Maroantsetra

Mananara

Maintinand ry
Sandrano — 4

SE Augustin

FIG. 3. Distribution de Neritina auriculata Lk.

MOLLUSQUES DE MADAGASCAR 345

Septaria (Septaria) borbonica Bory

1803 Patella borbonica, BORY DE St. VINCENT, 1: 287, pl. 37, fig. 2.

1816 Navicella elliptica, LAMARCK, (Vers), Expl. pl. 456, fig. 1.

1832 Navicella depressa, LESSON, p 386.

1843 Navicella Cookii, RECLUZ, р 197.

1850 Navicella suborbicularis, SOWERBY, 2: 551, pl. 117, fig. 3; pl. 118, fig. 30, 31.
1856 Navicella Cookii, REEVE, 9: pl. 4, fig. 14.

Riviere des Caimans
Tsararano

Nossi-Bé

Nossi-Comba

NOoSSi-Lava —
Virembina

Marovoay

Ansiafapiana— Androhofary

Ambohivoangibe

Entre Tamatave et

Manambolosy
la Baie A'Antongil

Antanambe

Soanierana
Manansatrana

_ Tamatave
Foulpointe

aes ae -Andevoranto

Vatomandry

| Sandramanoney
lac Andrahomana

E kongo
Marovary

st AUQUStin

.—

FIG. 4. Distribution de Neritina gagates Lk.

346

1860
1860
1860
1876
1576
1876
1877
1878
1881

1581

1581

1882
1587
1588
1589
1590
1892
1921

1929
1938
1956
1969

FISCHER-PIETTE ET VUKADINOVIC

Navicella Cookii, MORELET, 2: 126.

Navicella porcellana L., MORELET, 2: 119, 126.

Navicella suborbicularis, MORELET, 2: 126.

Navicella elliptica, MARTENS, 3: 252.

Navicella suborbicularis, MARTENS, 3: 253.

Navicella Cookii, MARTENS, 3: 253.

Navicella suborbicularis, MORELET, 25: 344.

Navicella porcellana, KOBELT, 5: 180.

Navicella bimaculata, CROSSE, 29: 207.

Navicella borbonica, MARTENS, ed. 2, 2(10a): 10, pl. 1, fig. 4-18.
Navicella junghuhni Herkl., MARTENS, p 23, pl. 1, fig. 13-15.
Septaria borbonica, MORELET, 30: 200.

Septaria borbonica, MORELET, 35: 291, pl. 9, fig. 5.

Navicella (Cimber) borbonica, TRYON, 10: 78, pl. 27, fig. 2-12.
Navicella bimaculata, BOETTGER, 21: 41.

Navicella borbonica var. depressa, BOETTGER, 22: 98.
Septaria (Elara) suborbicularis, BAKER, 2: 33, No. 208.
Septaria borboniciensis, GERMAIN, p 398.

Septaria borbonica, HAAS, 57: 428.

Septaria (Septaria) borbonica, WENZ, p 429, fig. 1055.

Septaria borbonica, FRANC, 13: 26, pl, 3, fig. 26.

Septaria (Septaria) borbonica, STARMUHLNER, 8: 76; fig. 85, p 78.

Espece а tres large répartition. En ce qui concerne Madagascar, les auteurs l'ont citée
de Nossi-Bé (Crosse; Martens; Boettger; Starmühlner), de Nossi-Comba (Crosse;
Boettger) et d Antanambe (Haas). Nous y ajoutons Analalava (Waterlot) et Ivontaka
(Decary, 1920). Ces provenances sont portées sur notre carte Fig. 5.

1822
1822
1856
1877
1877
1881
1883
1888
1888
1938
1938

Septaria (Navicella) lineata Lamarck -

Navicella lineata, LAMARCK, 6(2): 182 (Encycl. méth., pl. 456, fig. 2).
Navicella tessellata, LAMARCK, 6(2): 182 (Encycl. méth., pl. 456, fig. 3, 4).
Navicella eximia, REEVE, 10: pl. 6, fig. 26.

Navicella lineata, ANGAS, p 527.

Navicella eximia, ANGAS, p 527.

Navicella tessellata, MARTENS, ed. 2, 2(10a): 37, pl. 7, fig. 8-17; pl. 8, fig. 1-9.
Septaria tessellata, MORELET, 31: 204.

Navicella tessellata, TRYON, 10: 81, pl. 29, fig. 57.

Navicella lineata, TRYON, 10: 82, pl. 29, fig. 58.

Septaria tessellaria, CONNOLLY, p 601, pl. 17, fig. 20, 21.

Septaria (Navicella) tessellata, WENZ, p 430, fig. 1057.

Espèce а tres large répartition. Elle n'avait été citée de Madagascar, à notre con-
naissance, que par Angas, а Ekongo.

Nos collections nous permettent d’ajouter d'autres provenances, toutes sur la cóte Est
(carte No. 5): Maroansetra (Brygoo, 1957); embouchure de la riviere Mananara (Decary,

1920);

Foulpointe, riviere Onibe (Decary, 1920); canal des Pangalanes (Gaud, 1951);

Maintinandry, riviere Sakamila (Brygoo, 1957); riviere Sandramanongy (Brygoo, 1957).

1758
1827
1829
1841
1879
1879
1919

Smaragdia viridis Linné

Nerita viridis, LINNE, 10: 778.

Nerita viridis, var., RANG, In: FERUSSAC, 10: 412.

Neritina viridis, RANG, p 193.

Nerita Rangiana, RECLUZ, p 339.

Nerita viridis, MARTENS, ed. 2, 2(10): 246, pl. 4, fig. 14-19.
Nerita Rangiana, MARTENS, ed. 2, 2(10); 249, pl. 23, fig. 27, 28.
Nerita rangiana, ODHNER, 12(6): 33.

MOLLUSQUES DE MADAGASCAR 347

Lokoube —O
Nossi- Comba:

Analalava
Maroansetra

e—Ankasakasa POSES

e_ Maintirano

Demoka
Foulpointe
Miandriva3o Canal des Palangalanes
b
Menale Maintinandry
16 att, Sandramanongy

Morondava " АПК 5 ао

e—Marja

vf
Andranomanintsy

Lac Thotry
Ekongo—A
e—Finerena

Tulear

e Lanistes OVUM Pos
var. orasseti Morel.

A Septaria(Navicella)

lineata Lam.
HO Septaria borbonica sory

FIG. 5. Distribution de Septaria borbonica Bory, Septaria lineata Lk. et Lanistes ovum Peters var. grasseti Mor.

348 FISCHER-PIETTE ET VUKADINOVIC

1921 Smaragdia viridis, GERMAIN, p 395.
1929 Smaragdia (Smaragdia) Rangiana, DAUTZENBERG, 3: 527.
1930 Smaragdia viridis, GERMAIN, 21: 683.

Espece а répartition extrêmement large. Elle est citée aussi bien par des auteurs s occu-
pant de faune terrestre que par des auteurs s occupant de faune marine.

A Madagascar elle est connue depuis fort longtemps (Rang). Les provenances données
sont: Tamatave (Odhner); Hellville, Ankatsepe et Majunga (Dautzenberg). Les divers lots
de Madagascar de nos collections sont dépourvus de provenances précises.

Smaragdia souverbiana Montrouzier

1863 Мегита Souverbiana, MONTROUZIER, 11: 75; 175, pl. 5, fig. 5.
1881 Neritina (Smaragdia) Souverbiana, CROSSE, 29: 208.

1883 Neritina Souverbiana, MORELET, 31: 204.

1888 Neritina (Smaragdia) Souverbiana, TRYON, 10: 55, pl. 18, fig. 93.
1929 Neritina (Smaragdia) Souverbiana, DAUTZENBERG, 3: 527.

Ce n'est que parce qu'elle a été citée de Madagascar (Nossi-Bé) par Crosse et des
Comores par Morelet dans des listes de Mollusques terrestres, que nous mentionnons ici
cette espece marine à trés large répartition.

Nous en avons des échantillons de Nossi-Bé (Jousseaume) et de Tuléar (Geay).

Neritilia consimilis Martens
1879 Neritina consimilis, MARTENS, ed. 2, 2(10): 243, pl. 23, fig. 25, 26.
1883 Neritina consimilis, MORELET, 31: 202.

1888 Neritina consimilis, TRYON, 10: 54, pl. 18, fig. 86.
1921 Neritina (Neritilia) consimilis, GERMAIN, p 394.

Espéce décrite de Maurice, connue aussi des Comores et qui n avait pas encore été citée
de Madagascar. M. Waterlot en a récolté plusieurs dizaines d'échantillons 4 Ananalava,
dans le Nord-Ouest de l'île.

Genre Lanistes

Y a-t-il d Madagascar 2 espéces de Lanistes, ou une seule? Les 11 lots que nous
possedons, faisant au total 70 échantillons, appartiennent tous à une seule forme qui a été
décrite par Morelet sous le nom Ampullaria Grasseti, de Madagascar, puis 4 nouveau, de
l'Afrique orientale par von Martens, sous le nom plicosus, variété de L. ovum (Peters)
Troschel. Nous sommes tout-ä-fait d'avis que cette forme se rattache effectivement а L.
ovum. Mais il faut remarquer que Germain (1909) et Haas (1929) rattachent grasseti, non
pas а ovum, mais а L. olivaceus Sow.

Starmühlner cite de Madagascar deux espéces, ovum Trosch., et une autre qu il appelle
“Lanistes (Meladomus) olivaceus (Sowerby, 1825) grasseti (Morelet, 1863),” il se con-
forme donc a Haas pour cette deuxiéme espéce.

Starmühlner dit, а la page 15 (note infrapaginale relative а la р 14), n avoir pas eu
d'exemplaires de ces espéces. De sorte qu'il ne fait (р 118) qu'en donner des listes de
références et dire quelques notes de répartition basées sur cette littérature: pour ovum,
région de Tuléar (Andranohinaly); pour olivaceus, région de Majunga (Menabe). Dans ces
conditions il п’а pas dü consacrer de temps a ces Lanistes!.

Nous pensons donc que la présence de deux espéces n'est pas prouvée; et nous nous
contentons de donner des références, et la distribution, de la forme costulée de L. ovum.

Puisque nous avons cité Germain, qui considérait striatus comme une forme représen-
tative de olivaceus, notons que nous avons divers lots d'Afrique orientale déterminés par

'Autrement, dans la liste synonymique de olivacea, il n'aurait pas cité Reeve, Conch. Icon., fig. 3, qui représente
une Ampullaria et non un Lanistes.

MOLLUSQUES DE MADAGASCAR 349

Germain, que toutes ses étiquettes portent: Lanistes striatus Martens, et que les nom-
breux échantillons de ces lots sont tous des L. ovum var. Grasseti (=striata).

Deux de nos exemplaires de Madagascar sont des échantillons d'auteur de L. Grasseti
(coll. des types du Journal de Conchyliologie).

Tous nos exemplaires (comme d’ailleurs ceux d'Afrique orientale dont nous venons de
parler) sont de taille médiocre: le moins petit a 35 x 30 mm. Ils sont tous peu étirés, et peu
variables de forme. Les chiffres 35 x 30 et 32 x 32 donnent les limites des proportions de la
hauteur et de la largeur. Les cótes, le plus souvent, sont aussi écartées que sur la figure de
Grasseti, mais elles peuvent étre aussi serrées que sur celle de plicosus de Kobelt (voir plus
loin), et il y a des intermédiaires.

Lanistes ovum var. grasseti Morelet

1851 Ampullaria ovum Peters, PHILIPPI, ed. 2, 1(20): 22, pl. 6, fig. 2.
1863 Ampullaria (Lanistes) Grasseti, MORELET, 11: 267, pl. 10, fig. 2.
1896 Lanistes ovum var. plicosus, MARTENS, p 167.

1896 Lanistes grasseti, MARTENS, p 167.

1909 Lanistes grasseti, GERMAIN, (5) 1: 125, 162.

1911 Meladomus grasseti, KOBELT, ed. 2, 1(20): 13, pl. 23, fig. 8, 9.
1911 Meladomus ovum plicosus, KOBELT, p 12, pl. 29, fig. 1-3.

1929 Meladomus olivaceus grasseti, HAAS, 57: 422.

1950 Ampullaria (Lanistes) Grasseti, FISCHER-PIETTE, 90: 22.

1969 Lanistes (Meladomus) ovum Troschel, STARMUHLNER, 8: 118.
1969 Lanistes (Meladomus) olivaceus grasseti, STARMUHLNER, p 118.

Distribution. Nous portons sur une carte (Fig. 5) celles des localités que nous pu
situer. On voit que L. ovum п’а été trouvé jusqu ici que dans la région Ouest de part et
d'autre de Morondava, et en un point de la côte Est à la latitude de Morondava.

Pila cecillii Philippi

1848 Ampullaria Cecillii, PHILIPPI, 5: 191.

1848 Ampullaria Largillierti, PHILIPPI, p 192.

1851 Ampullaria Largillierti, PHILIPPI, ed. 2, 1(20): 46, pl. 13, fig. 5.
1851 Ampullaria Cecillei, PHILIPPI, p 47, pl. 13, fig. 6.

1856 Ampullaria simplex, REEVE, 10, pl. 21, fig. 98a, b.

1856 Ampullaria Largillierti, REEVE, 10, pl. 23, fig. 109.

1856 Ampullaria Hanleyi, REEVE, 10, pl. 23, fig. 113.

1860 Ampullaria Cecillei, MORELET, 2: 108, 125.

1863 Ampullaria adusta Rve, TRISTRAM, p 60.

1881 Ampullaria Cecillei, CROSSE, 29: 206.

1882 Ampullaria madagascariensis, SMITH, p 384, pl. 22, fig. 8, 9.
1882 Ampullaria subscutata, MOUSSON, 30: 46, pl. 3, fig. 6.

1884 Ampullaria hanleyi, NEVILL, 2: 8.

1889 Ampullaria Cecillei, BOETTGER, 21: 51.

1889 Ampullaria Largillierti, BOETTGER, р 51.

1890 Ampullaria cecillei, BOETTGER, 22: 95.

1890 Ampullaria largillierti, BOETTGER, p 96.

1911 Pachylabra subscutata, KOBELT, ed. 2, 1(20): 57, pl. 33, fig. 8.
1911 Pachylabra largillierti, KOBELT, 1(20): 59, pl. 33, fig. 9.

1911 Pachylabra hanleyi, KOBELT, 59, pl. 33, fig. 10.

1911 Pachylabra simplex, KOBELT, 67, pl. 36, fig. 3.

1911 Pachylabra madagascariensis, KOBELT, 68, pl. 36, fig. 4-6.
1914 Ampullaria madagascariensis, ROBSON, 32: 380.

1919 Ampullaria madagascariensis, ODHNER, 12(6): 43.

1925 Ampullaria madagascariensis, ALDERSON, p 83, pl. 17, fig. 1-3.
1925 Ampullaria Largillierti, ALDERSON, p 84, pl. 17, fig. 4.

1925 Ampullaria subscutata, ALDERSON, p 91, pl. 18, fig. 7.

09

50 FISCHER-PIETTE ЕТ VUKADINOVIC

1925 Ampullaria Cecillei, ALDERSON, p 92, pl. 18, fig. 8, 9.
1929 Pachylabra cecillei, HAAS, 57: 419.
1929 Pachylabra madagascariensis, HAAS, 57: 421.

1969 Pila (Pila) cecillei, STARMUHLNER, 8: 119, fig. 153-156; carte 205, р 157.

Mananjeba Diego-Suarez

Nossi-BÉ

т 0
Nossi- Comba Montagne des Francais

Ambilobe E Ampampamena.
Ambanje Ankarana ~
Analamaho
Andrakata D Farahalana
Andapa: SEIN RS
Marojala —, Ampohafana
| Ambodiangezoka Ampahana
Majunga Andranolava Ambohiovanoy-s Antsahanoro
Lac kinkony ne ¢ _ Marolambo]\ Antsadrarana
kapiloza US 14, Fort- Beros \_Ambchitralalana
Marovoay
tans Satie ' een
Besalam
PY laboha30 er
Maevatananaf — Lac Alaotra
Tsarasaotra — Imerimandrosa
Maintirano Mangabe
Ambatof otsy —»
Lil e Tananarive
in *—Imerina/
Lac Itasy% .— Moramanoa
Miandrivazo
Ambatolampy Sandramanoney

-Antsirabe

Saka fotsy. Mananjary

Marovare—e

FIG. 6. Distribution de Pila cecillei Philippi.

MOLLUSQUES DE MADAGASCAR 351

Espece décrite de Madagascar. Starmühlner en a mis d'autres régions dans sa syn-
onymie. Nous nous limitons ici а la forme de Madagascar. Cette derniére a elle-méme
recu plusieurs noms, que Starmúhlner a mis en synonymie.

Les exemplaires de Madagascar sont assez peu variables pour ce qui est de la forme
générale. La plupart sont conformes a la figure de Largillierti donnée par Philippi (1851);
certes il y en a qui sont plus étroits, comme sur la figure de Cecillei (sur la méme planche
de Philippi), mais nous ne connaissons, de cette derniére forme, que des individus de taille
faible, tandis que la forme plus gonflée se rencontre chez des exemplaires de toute taille.
La forme de l'ouverture est un peu variable. L'ombilic l’est davantage: certains
exemplaires sont imperforés; la plupart ont un ombilic ouvert mais de diametre assez fai-
ble; mais nous avons un lot, récolté par Perrier de la Bathie 4 Majunga, dont un des in-
dividus, de 38 mm de haut sur 36 de large, a un ombilic de 3,5 mm (tandis que chez
d'autres exemplaires du méme lot, il peut étre peu ouvert). Au point de vue de la sculp-
ture, ce lot, fait de 4 échantillons, est trés particulier: les lignes de croissance sont franche-
ment saillantes, comme autant de côtes, tres visibles à l'oeil nu: elles sont aussi saillantes
que celles des Lanistes ovum var. plicosa, tout en étant bien plus serrées. Ce trait peu faire
penser а la description, par Reeve, de Ampullaria filosa. Mais cette espéce est imperforée,
tandis qu ici l'ombilic est ouvert ou trés ouvert.

Ces individus ne montrent pas de sculpture spirale. D'autres en ont une, qui peut étre
bien moins saillante que la sculpture de croissance (elle-même trés peu marquée en
général), ou aussi saillante, ou plus saillante sur les premiers tours rarement conservés in-
tacts). Nous avons un exemplaire, de 51 mm de haut sur 48 de large, récolté par J. Millot a
Moramanga (centre-Est de Madagascar), qui sur le dernier tour a une trés visible sculp-
ture croisée, faite de nombreuses costules de croissance peu saillantes, et de cótes spirales,
bien moins nombreuses mais bien plus saillantes, au nombre de 13, dont l’&cartement est
assez variable.

Le plus grand de nos échantillons de Madagascar récolté lui aussi par J. Millot а
Moramanga, a 69 mm de haut sur 61 de large.

Distribution. Nous portons sur une carte (Fig. 6) les localités que nous avons pu situer,
tant celles que fournissait la littérature, que celles, bien plus nombreuses, qu y ajoutent
nos collections (comparer avec la carte donnée par Starmühlner, 1969, р 157). On voit que
les points de récolte connus à ce jour, sont assez nombreux sauf dans la partie Sud.

Cleopatra amaena Morelet

1851 Melania amaena, MORELET, 2: 192, pl. 5, fig. 9.
1909 Cleopatra amoena, KOBELT, ed. 2, 1(21A): 396, pl. 76, fig. 15.

La description de Morelet est suivie de ce renseignement sur l'habitat: “Palustria ad
orientem insulae Madagascar.”

En 1860, dans la Série Conchyliologique No. 2, Morelet, dans un article sur les Iles
Orientales de l'Afrique, écrit (р 117): “La Melania amaena provient de Zanzibar et des
Séchelles,” sans faire mention de Madagascar.

Haas, 1929, p 425, aprés avoir rappelé que Morelet a décrit son espéce de
Madagascar, écrit: “doch später (1860, р 117u.125) ändert er seine Angabe in Seychellen
und Sansibar um, was nach v. Martens (Besch. Weicht. Dtsch. O.-Afr., 1898, p 187)
für Sansibar richtig ist; weder auf den Seychellen noch auf Madagascar ist Cl. amoena
wiedergefunden worden, wohl aber öfters auf Sansibar. Sie kann also endgültig als nicht
zur madagassischen Tierwelt gehörig betrachtet werden.”

Cette opinion de Haas pouvait passer a priori pour trop catégorique, pour les deux
raisons suivantes. La premiére est que Morelet, en donnant en 1860 des provenances
de Zanzibar et des Seychelles, n'a pas dit que cela annule la premiére provenance qu ‘il

(we)
|
bo

FISCHER-PIETTE ET VUKADINOVIC

avait donnée, Madagascar. La seconde est que cette provenance de Madagascar était
assortie de détails d'habitat du genre de ceux qui généralement impliquent l'authenticité.

En tous cas, nous croyons pouvoir rapporter а cette espéce deux échantillons marqués
de Madagascar, l'un sans autre précision, de Decorse (1900) dont nous avons beaucoup
d'autres récoltes effectuées sans conteste à Madagascar, l’autre envoyé en 1901 par Petit,
médecin а Morondava, dont les autres récoltes que nous avons viennent de la région
méme de Morondava.

On pourrait hésiter sur cette détermination, car les 2 specimens sont plus ou moins
carénés, or nous n avons pas trouvé mention de caréne dans la littérature. Mais la forme
générale correspond tres bien et les tours sont si peu bombés que nous ne voyons guere de
quelle autre espéce il pourrait s'agir, et la ceinture colorée du dernier tour (visible en
mouillant) est semblable. La caréne, sur l'échantillon du Dr. Petit, est une simple rup-
ture de courbe de la surface, qui se voit sur le dernier tour et sur la fin de l'avant-dernier
tour. Sur l'échantillon de Decorse elle se discerne sur tout l'avant-dernier tour, mais sur le
dernier elle disparait rapidement.

Etant donnée la grande variabilité de la sculpture chez certaines espéces de Cleopatra,
nous ne pensons pas que ces faibles carénes constituent un obstacle а notre détermination.
Nous donnons des figures de ces échantillons (Fig. 7, 8).

Ainsi, l’espece est connue des marécages de l'Est, et de la côte Ouest, mais on peut
penser qu elle est beaucoup plus rare à Madagascar que la plupart des autres formes
fluviatiles.

Cleopatra (Cleopatra) colbeaui Craven

1880 Paludina colbeaui, CRAVEN, p 216, pl. 22, fig. 5.

1880 Paludomus madagascariensis, BROT, (non Crosse & Fischer), ed. 2, 1(25): 48, pl. 8, fig. 7.
1881 Paludina Colbeaui, CROSSE, 29: 206.

1888 Paludina moniliata, PAETEL, p 424.

1889 Cleopatra colbeaui, BOETTGER, p 51.

1890 Cleopatra mangoroensis, ANCEY, 7: 344.

1929 Cleopatra colbeaui, HAAS, 57: 424, pl. 2, fig. 24.

1969 Cleopatra (Cleopatra) colbeaui, STARMÜHLNER, 8: 184, 185, 200, fig. 244.

FIG. 7,8. Deux échantillons de Cleopatra amaena
Mor. X 2. /

FIG. 9. Distribution de Cleopatra colbeaui Craven. -

MOLLUSQUES DE MADAGASCAR 353

Distribution. Cette espéce semble n'exister qu'à Madagascar. La littérature donne 4
provenances, Nossi-Bé (Craven, 1880); Périnet (Starmiihlner, 1969); Beforona (Star-
mühlner, 1969); fleuve Mangoro (Апсеу, 1890).

Les localités que nous permettent d'ajouter les collections du Muséum sont, du Nord au
Sud: Diego-Suarez (Waterlot); Montagne des Francais (Waterlot); Nossi-Comba (G.
Petit, 1920); Mizdioko (J. Millot, 1948); Mont Tsaratanana (Paulian, 1951); Antsiraka
(Brygoo, 1957); Ankasakasa (Decary, 1930); Doany (H. Soula, 1969); riviére Kapiloza (G.
Petit, 1926); Namoroko (Perrier de la Bathie); Iabohazo (Waterlot); Andonaka (Dr.
Brygoo, 1957); ilot Anosy, lac Alaotra (Decary, 1921); Fenerive (Brygoo, 1957); Sahamany
(Brygoo, 1957); Ifontsy (Brygoo, 1957); Bemaraha (Decary, 1921); Périnet (Brygoo, 1957);
Manambolo (Brygoo, 1957); Beforona (Brygoo, 1957); Fananzanana (Brygoo, 1957);
Anosibé (J. Millot, 1948); Ambodinonoka (Brygoo, 1957); Mangoro (Gaud, 1951); entre
Anosibé et Moramanga (J. Millot, 1953); Volove (Brygoo, 1957); Mahanoro (Gaud, 1951);
Onive (Brygoo, 1957); Andonabe (Brygoo, 1957); Mahabo (Brygoo, 1957); Ankilizato
(Brygoo, 1957); Цотатру (Brygoo, 1957); Andasibe (Brygoo, 1957).

Ces localités, avec celles de la littérature, sont portées sur notre carte Fig. 9. En plus,
une provenance de la collection du Muséum п’а pu étre située par nous, c est: sommet
Ihovika, 100 m altitude Est (Perrier de la Bathie).

Cleopatra grandidieri Crosse & Fischer

1872 Paludomus Grandidieri, CROSSE & FISCHER, 20: 209.

1878 Paludomus Grandidieri, CROSSE & FISCHER, 26: 73, pl. 1, fig. 3, fig. 4 (var. submitica).
1880 Paludomus Grandidieri, BROT, ed. 2, 1(25): 45, pl. 8, fig. 3, 3a.

1914 Paludomus Grandidieri, ROBSON, p 378.

1929 Cleopatra grandidieri, HAAS, 57: 423.

1950 Paludomus Grandidieri, FISCHER-PIETTE, 90: 78, 150.

1969 Cleopatra (Cleopatra) grandidieri, STARMUHLNER, 8: 205, fig. 267.

Distribution. Il semble que cette espéce ne se trouve qu à Madagascar. Les provenances
connues, ou du moins celles que nous avons situées, se trouvent portées sur notre carte
Fig. 10, qu il s'agisse des données de la littérature, ou de celles, plus nombreuses, que nos
collections y ajoutent. Elles sont presque toutes dans la région moyenne des cótes Est,
toutefois les provenances de Majunga et de Tuléar permettent de penser que nous n avons
encore qu une documentation incomplete.

Cleopatra (Cleopatra) madagascariensis Crosse & Fischer

1872 Paludina madagascariensis, CROSSE & FISCHER, 20: 210.

1882 Cleopatra trabonjiensis, SMITH, p 384, pl. 22, fig. 10, 11.

1894 Cleopatra carinulata, DAUTZENBERG, 42: 105, pl. 4, fig. 4.

1906 Cleopatra multilirata, ANCEY, 20: 45.

1914 Cleopatra trabonjiensis, ROBSON, 32: 377.

1929 Cleopatra madagascariensis, HAAS, 57: 423, pl. 2, fig. 21-23.

1950 Paludina madagascariensis, FISCHER-PIETTE, 90: 78; 180, pl. 5, fig. 75-77.

1969 Cleopatra (Cleopatra) madagascariensis, STARMUHLNER, 8: 201; fig. 263, 264, p 202;
fig. 261, р 200.

Il semble que cette espéce ne vive qu'à Madagascar. Les provenances données par la
littérature étaient, du Nord au Sud: Ambohimarina (Dautzenberg, 1894); Nossi-Bé (Star-
mühlner, 1969); Majunga (Haas, 1929); Trabonjy (Smith, 1882); Lac Alaotra (Robson,
1914); Vinaninony (Ancey, 1906). Les matériaux du Muséum nous permettent d'ajouter
beaucoup d autres localités. Les unes et les autres sont portées sur notre carte de la Fig.
11. On voit que cette espéce, existe du Nord au Sud et de l'Est à l'Ouest, avec des
provenances un peu plus nombreuses dans l'Ouest que dans | Est.

354 FISCHER-PIETTE ЕТ VUKADINOVIC

FIG. 10. Distribution de Cleopatra grandidieri Crosse et Fischer.

Majunga

Manjakandriana Ansage
Bie geal lig Vatomandr
—89
Ambinanindrano—e ~ , Ambodiara
Ivolo
Ambohimanga—e Sakleony
Ranomafana-e °— Masora
Namorona
Fort Carnot,
ite.) == ananjar
Y a

Tulear lantara

MOLLUSQUES DE MADAGASCAR 355

Ambilobe

Anivorano

Ambohimarina
Tsararano

Nossi- Be
Nossi- Comba

Ambanja | e < МЕ Tsaratanana
Antohihy Beanoona

: Sambirano Belambo
Mariarano ma
. + Ankijanibe | Pealan

Maroala Marofinaritra

Marovo cil as | Ankara! tantsika
va
= Trabony —

Io

4
Ankarana

Kapiloza a Tampolo
Namoroka Boina ¢ Ankirihitra Lazafo
Bekodoka Taboha30 ere
Ambatondrazaka Mananoro
AE Bemaraha Lac Alaotra
RenEirans }. Miandriva3o Andreba

e— lily Entre Anosibe

Bekily -— et Moramanpa
N р
Marofandilia Vinaninony Vatomanary
Morondava lac Andranomena
Mahaloo e *—Fitampito
Ankelizato' Ankotrofotsy Man akana
*— Bemarivo Ifanadiana
onto ve
А Fianarantsoa
MIN e-Ihosy Amloalavao
Manombo

7 Fiherena _ betroka
Tulear

tiok
Se ee

e Tongobory
Esira
Tsivory
Marontsiraka

FIG. 11. Distribution de Cleopatra madagascariensis Crosse et Fischer (les points de récolte sans nom sont situés
loin d'un village).

356 FISCHER-PIETTE ЕТ VUKADINOVIC

Viviparus unicolor Olivier
1804 Cyclostoma unicolor, OLIVIER, 2: 39, pl. 31, fig. 9.

1852 Paludina biangulata, KUSTER, ed. 2, 1(21): 25, pl. 5, fig. 11, 12.
1909 Vivipara unicolor, KOBELT, ed. 2, 1(21A): 162, pl. 4, fig. 12, 13; pl. 5, fig, 11, 12.

Nous avons trouvé dans les matériaux indéterminés du Muséum un exemplaire (Fig. 12)
de Viviparus récolté еп 1900 par Decorse а Majunga. Nous le rapportons а У. unicolor
Oliv. On sait que cette espéce est trés variable, dans sa forme générale et dans le fait
qu'elle peut être pourvue d'une ou plusieurs carénes ou nen présenter aucune. Notre
specimen est trés analogue а la figure de Paludina biangulata de Kiister (1852), que
Kobelt (1909) a mis dans la synonymie de У. unicolor; cet auteur nous dit que biangulata,
décrite d habitat inconnu, a été trouvée par Martens en Afrique orientale allemande.

Madagascar est assez loin de cette région. Aussi pourrait-il y avoir doute sur la valeur de
notre determination. Pour qu'on puisse en juger, nous décrirons notre échantillon en
détail et nous le figurerons. Mais, а nos yeux, en ce qui nous concerne, cet habitat n'a rien
d'anormal: nous sommes en effet persuadés que У. unicolor, décrit d'Egypte, se trouve
jusqu'en Afrique du Sud, quels que soient les noms variés que cette espéce ait reçus en
Afrique orientale.

Hauteur 17 mm; largeur maxima 13 mm; ouverture ayant 8,5 sur 6,5 mm; couleur un-
iformément verdatre; 5 tours, étagés par un aplatissement du haut de chacun. La bordure
de cet aplatissement est une caréne bien individualisée en un cordon saillant. Une
deuxième caréne apparaît à partir du sommet de | ouverture, de sorte que le dernier tour a
un aspect bi-anguleux. Cette deuxiéme caréne est bien moins individualisée que I autre, et
s atténue beaucoup en arrivant à | ouverture. A mi-distance entre ces deux carénes se voit
une faible côte spirale. Avec une forte loupe, on constate l'existence d'une fine striation
spirale de toute la surface, un peu plus forte sur la base, qui croise les irréguliéres cótes de
croissance. I] n'y а pas d ombilic.

Melanatria fluminea Gmelin

1767 Buccinum flumineum, GMELIN, 13: 3503.

1822 Pirena spinosa, LAMARCK, 6: 172.

1838 Melanopsis spinosa, POTIEZ & MICHAUD, p 351.
1838 Melanopsis Lamarckii, POTIEZ & MICHAUD, p 351.
1840 Melania madagascariensis, GRATELOUP, 11: 167, pl. 4, fig. 7.
1840 Melania duisabonis, GRATELOUP, 11: pl. 4, fig. 8.
1840 Melania bicarinata, GRATELOUP, 11: pl. 4, fig. 9.
1842 Pirena spinosa, SGANZIN, 3: 19.

1851 Pirena sinuosa, PHILIPPI, p 91.

1859 Pirena (Melanatria) spinosa, CHENU, 1: 298, fig. 2082.
1859 Pirena (Melanatria) granulosa Lk., CHENU, 1: 298, fig. 2081.
1859 Pirena spinosa, REEVE, 12: pl. 2, fig. 9.

1859 Pirena fluminea, REEVE, 12: pl. 2, fig. 10.

1859 Pirena maura, REEVE, 12: pl. 2, fig. 6.

1859 Pirena plicata, REEVE, 12: pl. 2, fig. 11.

1859 Pirena lingulata, REEVE, 12: pl. 2, fig. 7.

1860 Pirena fluminea, MORELET, 2: 118, 126.

1860 Melania bicarinata, MORELET, 2: 125.

1860 Melania Duisabonis, MORELET, 2: 126.

1860 Pirena Lamarckii, MORELET, 2: 126.

1860 Pirena madagascariensis, MORELET, 2: 126.

1860 Pirena sinuosa, MORELET, 2: 126.

1862 Pirena Debeauxiana, CROSSE, p 402, pl. 13, fig. 6.
1863 Pirena (Melanatria) spinosa, TRISTRAM, р 60.

1867 Melanatria fluminea, GRAY, 3: 330.

MOLLUSQUES DE MADAGASCAR 357

ЕТС. 12. Viviparus unicolor Oliv. X 2.

1868 Pirena aspera, BROT, p 49, pl. 1, fig. 6.

1874 Melanatria spinosa, BROT, ed. 2, 1(24): 401, pl. 42, fig. 1, la-c.
1874 Melanatria fluminea, BROT, 1(24): 402, pl. 42, fig. 2, 2a, 2b, 3; pl. 43, fig. 1, la, 2, 2a-c, 3.
1874 Melanatria Debauxiana, BROT, 1(24): 404, pl. 43, fig. 4.

1874 Melanatria Goudotiana, BROT, 1(24): 405, pl. 44, fig. 1, la.

1874 Melanatria Madagascariensis, BROT, 1(24): 406, pl. 43, fig. 5, 5a-c.
1882 Doryssa (Melania) Audeberti, MOUSSON, 30: 47, pl. 3, fig. 7.

1882 Melanatria fluminea, MOUSSON, 30: 183.

1882 Melanatria johnsoni, SMITH, p 383, pl. 22, fig. 6, 7.

1890 Melanatria madagascariensis, BOETTGER, 22: 97.

1894 Melanatria madagascariensis, DAUTZENBERG, 42: 104.

1902 Pirena spinosa, DAUTZENBERG, 27: 199.

1908 Melania madagascariensis, FULTON, 8: 43, 44.

1914 Melanatria fluminea, ROBSON, 32: 378.

1914 Melanatria Johnsoni, ROBSON, 32: 378.

1919 Melanatria spinosa, ODHNER, 12: 43.

1928 Melanatria fluminea, THIELE, 55: 385.

1929 Pirena fluminea, HAAS, 57: 425.

1929 Pirena spinosa, HAAS, 57: 425.

1929 Pirena madagascariensis, HAAS, 57: 425.

1950 Pirena debeauxiana, FISCHER-PIETTE, 90: 20.

1969 Melanatria fluminea, STARMUHLNER, 8: 159, fig. 206-208; fig. 241, p 182.
1969 Melanatria madagascariensis, STARMUHLNER, 8: 182, fig. 241-243.

Le grand nombre d'échantillons dont nous disposons, nous a permis de nous rendre
compte qu'il n'existe à Madagascar qu'une seule Melanatria, tres variable, en particulier
pour les côtes, longitudinales ou spirales et qui souvent sont d'un systeme а un âge et d'un

358 FISCHER-PIETTE ЕТ VUKADINOVIC

autre à un autre âge, pour la convexité des tours, le degré d'épaulement des tours, les
pointes que cet épaulement peut porter, et aussi pour la forme de | ouverture, dont le bord
externe peut étre peu sinueux ou trés sinueux. Sur un méme individu, а ouverture tres
sinueuse, on peut constater а peu de distance en arriére le tracé peu sinueux qui a précédé.

Les noms dús а Reeve laissaient un doute du fait des provenances données par lui, en

Сар dAmbre
Diego- Suarez
Nossi-Be
| Montagne des Francais
Virembina
Andranomaiaza(Maromandia) N Ambohianoibe
h Doan Ampampamena
Andapa* re
Ambato \ Analantsoa
, A \ ohafana Antalaha
Tsitampiky Amp lias «\ Andranonakcho
> Ankarafantsika Ambohivoangy
Hort & Beronono Ranolalina
laboha3o Marovoay Mananara
Ankirihitra Ivontaka
Somoromahitra ste Marie
Antsinjy Lac Alaorra? Sahatavy
$ Fostimano—®* Ivoloina
vondahy ——e
Andravondahy » betampona Vohibary
Antsalova а Ambila
Manjakandriana * Andratambe
vatomandry
.—®
belo u Moramanga
Ambinanindrano-* Manampotsy
—Mahnanoro

Fort-Carnot

Inosy Mananjary
$

Manambia
Marovary

Ankotofotsy

Ranomafana
Тъака

Fort- Dau phin
Manambaro

FIG. 13. Distribution de Melanatria fluminea Gmelin (les points de récolte sans nom sont situés loin d'un
village).

MOLLUSQUES DE MADAGASCAR 359

Afrique occidentale. Mais il s agissait d'exemplaires de Cuming, ог cet excellent récolteur,
tres peu lettré, n'indiquait souvent les provenances qu aprés-coup, et les erreurs d'origine
sont ainsi fort courantes en ce qui le concerne. C'est aussi de Cuming que Crosse tenait
l’exemplaire (que nous avons en mains, coll. des types de Journal de Conchyliologie) qu il
a décrit comme Pirena Debeauxiana: il était, lui aussi, censé venir d’ Afrique occidentale.

Distribution. La littérature donne les provenances suivantes: Nossi-Bé (Philippi, 1851);
Ranomafana (Tristram, 1863); Tamanarivo (Brot, 1874); riviere Kamony (Smith, 1882);
Montagne des Francais (Dautzenberg, 1894); riviére Fanjahira (Dautzenberg, 1902); en-
tre Matilasy et Mangoro; source de la riviére Ihovika; Belolondyi et Tandrahu (Robson,
1914); Tamatave (Odhner, 1919); Ivohibé, Karimbela; Anharimbelo; Marinabo; Sakana
(Haas, 1929); ruisseau Sakanofa et ruisseau Isaka (Starmühlner, 1969).

Ces diverses provenances ont été réunies par Starmiihlner sur une carte (fig. 241, p
182), pour l'ensemble de М. fluminea et М. madagascariensis qu'il considérait comme
deux espéces distinctes. Elles sont situées dans le Sud-Est; dans la région de Tamatave; a
Tananarive; et ä la pointe Nord y compris Nossi-Bé.

Les collections du Muséum nous ont procuré beaucoup d autres provenances dont nous
donnons les emplacements (ceux, du moins, que nous avons pu situer) sur notre Fig. 13.
On constate que Гезрёсе est présente aussi bien à l'Ouest qu'à | Est; qu à l'Est elle se
trouve jusque dans le Nord-Est compris; et qu il n y a que la région axiale de Vile qui
jusqu ici est presque en blanc, ne contenant que quelques provenances.

Thiara (Thiara) amarula L.

1758 Helix amarula, LINNE, ed. 10: 774.

1822 Melania thiarella, LAMARCK, 6: 166.

1850 Melania cornuta, LEA, p 194.

1860 Melania amarula, MORELET, 2: 111.

1874 Melania amarula Brug., BROT, ed. 2, 1(24): 289, pl. 29, fig. 1, la-g.
1874 Melania thiarella, BROT, 1(24): 291, pl. 29, fig. 3, 3a, b.
1877 Melania amarula, ANGAS, p 527-530.

1877 Melania amarula Brug., MORELET, 25: 343.

1879 Melania thiarella, MORELET, 27: 312.

1881 Melania thiarella, CROSSE, 29: 207.

1882 Melania amarula Brug., MORELET, 30: 199.

1889 Melania (Tiara) tiarella, BOETTGER, 21: 53.

1890 Melania (Thiara) tiarella, BOETTGER, 22: 98.

1910 Melania amarula, KOBELT, 32: 92

1910 Melania cornula, KOBELT, 32: 92.

1914 Melania amarula Brug., ROBSON, 32: 379.

1919 Melania cybele Gould, ODHNER, 12: 43.

1921 Melania amarula, GERMAIN, p 358.

1928 Melania amarula, THIELE, 55: 397.

1929 Melania amarula, HAAS, 57: 426.

1929 Melania coacta Meusch., HAAS, 57: 427.

1938 Thiara vouamica Bgt., CONNOLLY, p 564.

1956 Melania amarula Brug., FRANC, 13: 57, fig. 74.

1969 Thiara (Thiara) amarula, STARMUHLNER, 8: 208: fig. 272-275, p 209; carte p 182.

Espece répandue de | Afrique du S.-O. à l'Australie. Pour ce qui concerne Madagascar,
la bibliographie donne les provenances suivantes: Ekongo (Angas, 1877); Nossi-Bé
(Crosse, 1881; Starmühlner, 1969); Nossi-Comba (Boettger, 1890); entre Tamatave et la
baie d'Antongil (Robson, 1914); Androhibe (Odhner, 1919); Tamatave (Haas, 1929);
Karimbela (Haas, 1929).

Les lots de la collection du Muséum permettent Фу ajouter les provenances suivantes:
Diego-Suarez (Ballot, 1887); riviere des Caimans (Decary); Bas-Sambirano (J. Millot,
1945); Maromandia (Decary, 1922); Andaribé (Mme. Bouchard, 1969); Maroansetra

360 FISCHER-PIETTE ET VUKADINOVIC

Die go- Suarez

Nossi-Be ?
Riviere desCaimans
Nossi-Comba & |
ine

e————Bas-Ssambirano
Maromandia

Andaribe

Maroansetra

Bndronibe == S

een Tamatave et
Lvontaka Baie d’Antongil

Y

Mahambo
Andreba —e
Tamatave
Canal des Palangalanes
Sand ramanongy
ЕКОМОО

Karimbela

FIG. 14. Distribution de Thiara amarula L.

MOLLUSQUES DE MADAGASCAR 361

(Brygoo, 1957); Ivontaka (Decary, 1920); Mahambo (С. Petit, 1920); Andreba (Brygoo,
1957); canal des Pangalanes (Gaud, 1951); Sandromangy riviére (Brygoo, 1957).

Ces diverses localités, celles qui étaient connues et celles que nous ajoutons, sont
portées sur une carte (Fig. 14). Ces lieux de récoltes sont bien moins nombreux que ceux
de l’espéce indigéne Melanatria fluminea: ils sont répartis sur le pourtour de [Ге dans ses
parties Nord et Est.

Melanoides tuberculatus Miller

1774 Nerita tuberculata, Müller, р 191.

1786 Nerita tuberculata, CHEMNITZ, 9: 189, pl. 136, fig. 1261, 1262.

1860 Nerita commersoni, MORELET, 2: 116, pl. 6, fig. 4.

1860 Nerita tuberculata, MORELET, 2: 126.

1864 Nerita psorica, MORELET, 12: 287.

1889 Nerita (Striatella) tuberculata, BOETTGER, 21: 52.

1914 Nerita tuberculata, ROBSON, 32: 379.

1929 Melanoides tuberculatus, HAAS, 57: 427.

1935 Melania (Melanoides) tuberculata, GERMAIN, (10), 18: 445.

1958 Melanoides tuberculata, BRYGOO, 26: 86. à

1969 Melanoides (Melanoides) tuberculatus, STARMUHLNER, 8: 224; fig. 293-294, p 209:
carte 319, p 242.

Cette espéce est une de celles qui sont les plus répandues dans le monde. Pour
Madagascar la carte publiée par Brygoo et reproduite par Starmühlner ne donne de nom-
breuses localités que dans le Sud. Nous avons des récoltes qui nous montrent que cette es-
péce est trés abondante dans toute l’île. Nous jugeons inutile de traduire ce renseignement
sur une carte, et méme de donner la liste de ces localités.

Cerithidea decollata Brug.

1842 Cerithium decollatum Brug., KIENER, p 96, pl. 28, fig. 2
1855 Cerithium decollatum L., SOWERBY, 2: 886, pl. 186, fig. 274.
1860 Melania decollata Lk., MORELET, 2: 116, 125.

1866 Cerithidea decollata, L., REEVE, 15: pl. 2, fig. 14.

1881 Melania decollata Lk., CROSSE, 29: 207.

1887 Potamides (Cerithidea) decollatus L., TRYON, 9: 161, pl. 32, fig. 54.
1890 Cerithidea (Pirenella) decollata Lk., BOETTGER, 22: 97.

1894 Cerithidea decollata L., DAUTZENBERG, 42: 91.

1929 Potamides (Cerithidea) decollatus L., DAUTZENBERG, 3: 489
1929 Cerithidea decollata Brug., HAAS, 57: 427.

1969 Cerithidea decollata, Brug., STARMUHLNER, 8: 243.

Nous ne nous sommes pas chargés d'essayer de résoudre la question, fort difficile, de
savoir quel est l’auteur de Гезрёсе de Cerithidea qui habite les côtes de Madagascar (et se
trouverait jusqu en Australie). Nous nous sommes contentés de donner les références aux
figures auxquelles ressemblent les exemplaires que nous avons en collection et d'en
représenter un Fig. 15. Pour cette raison, nous n avons pas indiqué, bien que Starmühlner
la cite, la figure de Brot (Conch. Cab., pl. 7, fig. 10), qui ne représente certainement pas
Гезрёсе digurée par Kiener (ce serait plutöt Melanatria fluminea).

Les provenances malgaches trouvées dans la littérature sont les suivantes: Nossi-Bé
(Morelet, 1860); Diego-Suarez (Dautzenberg, 1894); Amboaniva (Dautzenberg, 1929);
riviere des Catmans (Id.); Tuléar (Id. ).

Les collections du Muséum permettent d'ajouter: Ambanja (Paulian, 1951); Bas-
Sambirano (J. Millot, 1945); Ananalava (Waterlot, 1925); Ambongo (J. Millot, 1948);
Besalampy (Decary, 1938); Morondava et Morombé (Brygoo, 1957).

On voit sur notre carte (Fig. 16) que cette espéce des eaux saumátres a surtout été
récoltée sur la cóte Nord-Ouest et Ouest.

362 FISCHER-PIETTE ET VUKADINOVIC

FIG. 15. Cerithidea decollata, X 1, 5.

_Diego-Suares

s Gé
|- Бе Е =
NOSSI-B Riviere des Caımans

Ambanja Amboaniva

Bas-Sambirano — 7

Besalampy

Morondava

Tulear-

FIG. 16. Distribution de Cerithidea decollata.

MOLLUSQUES DE MADAGASCAR 363

Radix (Radix) hovarum Tristram

1863 Limnaea hovarum, TRISTRAM, p 61.

1882 Limnaea hovarum, SMITH, p 385.

1882 Limnaea electa, SMITH, 385, pl. 22, fig. 12, 13.

1894 Limnaea suarensis, DAUTZENBERG, 42: 100, pl. 4, fig. 3.
1914 Limnaea hovarum, ROBSON, 32: 280.

1920 Limnaea hovarum, GERMAIN, p 160.

Ambilobe

Ampotsihy /_Diego-Suarez

Ambanje (27 & baie cles Amis
Bas E Ankatafa
Nossi-Be
Analalava à |///-Ankarana
Ambondrona MW epi Mahabo
Tsinjomitondraka $* Mont. Tsaratanana
Manaratsandra

e
à Ambalavelona
Amparangidro Mohakibokely R

Ankaboka Ankazombrona| A DN
мым]. I jure || Antsohiny N

Bemarivo
Soalala a. er ge Jang
Ankasakasa NS $ Mandritsara
Manakana Marovoay Antsirabe

Ambato-Boeni*\ \Tsararano
Maevatanana-, befotoana

р à с Alaotr:
anna ES otra

: Marovato
Ikopa eo Tamatave
5 Ambatondrasaka
Miandrivazo N
e- Miarinarivo Ambila
Ankavandra- Manak ambahiny
er Bekily Anosibe Vatomandry
Maintinandr
Morondava e-Mananjaka Mahanoro
Analafaly У bande ana
e— Andrianombo
Ambila
\anonhony-
Betroka
Betioky
Tsivory
Manaravolo-——e

Marohotro

Amboasary
Ambovombe

FIG. 17. Distribution de Bulinus mariei Crosse.

364 FISCHER-PIETTE ET VUKADINOVIC

1957 Lymnaea hovarum, RANSON, (34): 25
1958 Lymnaea hovarum, BRYGOO, 26: 75
1969 Radix (Radix) hovarum, STARMUHLNER, 8: 244-268; fig. 321, 322, р 246; carte, р 267.

Aux trés nombreuses provenances qui étaient connues, les collections de Paris et
Bruxelles en ajoutent un si grand nombre, qu il devient inutile de donner une nouvelle
carte de localités. Il suffit de savoir maintenant que Гезрёсе existe dans toute l'île.

Bulinus (Bulinus) liratus Tristram

1863 Physa (Ameria) lirata, TRISTRAM, p 60, text-fig.

1877 Physa madagascariensis, ANGAS, p 528, pl. 54, fig. 2.

1882 Physa madagascariensis. SMITH, p 386, pl. 22, fig. 18, 19.

1882 Physa lamellata, SMITH, p 386, pl. 22, fig. 14, 15.

1882 Physa obtusispira, SMITH, p 386, pl. 22, fig. 16, 17.

1886 Physa madagascariensis, CLESSIN, ed. 2, 1(17): 282, pl. 40, fig. 6.
1886 Physa Hildebrandti, CLESSIN, 1(17): 351, pl. 49, fig. 9.

1920 Bullinus (Isidora) liratus, GERMAIN, p 161, fig. 8-11.

1920 Bullinus (Isidora) madagascariensis, GERMAIN, p 163.

1953 Bulinus liratus, GRJEBINE € MENACHE, 8: 87.

1957 Bulinus liratus, RANSON, (34): 16.

1958 Bulinus liratus, BRYGOO, 26: 60.

1969 Bulinus (Bulinus) liratus, STARMUHLNER, 8: 268-288; He 353, p 270; fig. 386, p 288.

Distribution. Les cartes publiées par Brygoo, Ranson et Starmühlner sont déjà assez
fournies. Nous aurions encore beaucoup d autres localités а faire connaitre, qu il nous
semble inutile de les énumérer. Qu il nous suffise de dire que cette espéce se trouve en
abondance dans toute l'île.

Bulinus (Pyrgophysa) mariei Crosse

1879 Pyrgophysa Mariei, CROSSE, 27: 209.

1880 Pyrgophysa Mariei, CROSSE, 28: 141, pl. 4, fig. 5.

1881 Pyrgophysa Mariei, CROSSE, 29: 202.

1889 Pyrgophysa Mariei, CROSSE & FISCHER, In: GRANDIDIER, 14: pl. 24, fig. 5.
1889 Pyrgophysa Mariei, BOETTGER, 21: 41.

1894 Pyrgophysa Bavayi, DAUTZENBERG, 42: 103, pl. 3, fig. 7.

1950 Pyrgophysa Bavayi, FISCHER-PIETTE, 90: 161.

1957 Bulinus mariei, RANSON, 34: 21, fig. 5a.

1958 Bulinus mariei, BRYGOO, 26: 56.

1964 Pyrgophysa Mariei, CHEVALLIER, 104: 33.

1969 Bulinus (Pyrgophysa) mariei, STARMUHLNER, 8: 288-306; fig. 387, p 290; carte, p 306.

Les types de P. Mariei et P. Bavayi sont tous deux au Muséum, le premier dans la
collection de l'Atlas de Madagascar et le second dans la collection des types du Journal de
Conchyliologie.

Ranson a montré que В. mariei est une espéce uniquement malgache, distincte de В.
forskalii Ehr.

Les provenances connues, ou du moins celles que nous avons situées, se trouvent
portées sur notre carte Fig. 17, qu'il s'agisse des données de la littérature, ou de celles que
nos collections y ajoutent.

Anisus (Anisus) crassilabrum Morelet

1860 Planorbis crassilabrum, MORELET, 2: 96, pl. 6, fig. 8.
1860 Planorbis trivialis, MORELET, p 97, pl. 6, fig. 7.

1863 Planorbis (Nautilina) caldwelli, TRISTRAM, р 61.
1876 Planorbis crassilabrum, MARTENS, 3: 253.

1878 Planorbis crassilabrum, KOBELT, 5: 180.

MOLLUSQUES DE MADAGASCAR 365

1878 Planorbis trivialis, KOBELT, 5: 180.

1879 Planorbis trivialis, MORELET, 27: 311.

1879 Planorbis crassilabrum, MORELET, 27: 312.

1881 Planorbis crassilabrum, CROSSE, 29: 202.

1883 Planorbis hildebrandti, MARTENS, 10: 83.

1886 Planorbis crassilabrum, CLESSIN, ed. 2, 1(17): 150, pl. 22, fig. 6.
1886 Planorbis crassilabrum, CLESSIN, 1(17): 196, pl. 29, fig. 7.

1894 Planorbis alluaudi, DAUTZENBERG, 42: 101, pl. 4, fig. 2.

1894 Planorbis simpliculus, DAUTZENBERG, 42: 101, pl. 4, fig. 1.
1918 Planorbis (Planorbis) Hildebrandti, GERMAIN, p 46.

1918 Planorbis (Tropidiscus) trivialis, GERMAIN, p 48.

1918 Planorbis (Tropidiscus) simpliculus, GERMAIN, p 49.

1918 Planorbis (Tropidiscus) alluaudi, GERMAIN, p 50.

1918 Planorbis (Gyraulus?) crassilabrum, GERMAIN, p 50.

1921 Planorbis (Propidiscus) trivialis, GERMAIN, 10: 39, pl. 5, fig. 9-14.
1929 Planorbis (Planorbis) trivialis, HAAS, p 413, pl. 2, fig. 14, 15.

1935 Planorbis (Planorbis) trivialis, GERMAIN, (10), 18: 442.

1935 Planorbis (Gyraulus) crassilabrum, GERMAIN, (10) 18: 442, fig. 5-7.
1953 Planorbis trivialis, GRJEBINE & MENACHE, (A), 8: 87.

1953 Planorbis crassilabrum, GRJEBINE € MENACHE, 8: 87.

1957 Anisus crassilabrum, RANSON, 34: 6.

1958 Anisus crassilabrum, BRYGOO, 26: 66.

1969 Anisus (Anisus) crassilabrum, STARMUHLNER, 8: 307-328; fig. 420, 421, p 309.

Distribution. Les cartes publiées par Brygoo et par Ranson sont déja trés fournies.
Nous aurions encore tant d'autres localités à faire connaître, qu'il nous semble inutile
de les énumérer. Qu'il nous suffise de dire que cette espéce se trouve en abondance
dans toute l’île.

Gyraulus (Caillaudia) apertus Martens

1897 Planorbis apertus, MARTENS, p 149, pl. 6, fig. 17.
1969 Gyraulus (Caillaudia) apertus, STARMUHLNER, 8: 328, fig. 452, 453; p 344, fig. 481.

Espéce décrite du Lac Albert-Edouard qui était sa seule provenance connue, et que
Starmühlner a citée récemment de Madagascar, en deux provenances du centre Sud, le
ruisseau Andranomaria, et le ruisseau Amborompotsy (et un de ses affluents). Nous y
ajoutons 14 autres provenances. L'une d elles est due à Waterlot Diego-Suarez (Baie
des Amis). Toutes les autres sont dues au Dr. Brygoo. Ce sont, du Nord au Sud:
Vohemar, Ambilobe, Bemapaza, Bandabe, Ambodiamontana, Mandritsara, Am-
balabongo, Ambalatany, Bekodoka, Antsirasitra, Bevato, Miarina rivo et Ambano (voir
notre carte Fig. 18).

Nous avons comparé nos échantillons avec un lot du Lac Albert Edouard étudié par
Germain (1912, Bull. Muséum, p 80).

Segmentorbis (Segmentorbis) angustus Jickeli

1874 Segmentina angusta, JICKELI, р 220, pl. 7, fig. 24.
1904 Segmentina chevalieri, GERMAIN, p 468.

1918 Segmentina chevalieri, GERMAIN, p 51.

1935 Segmentina angusta, GERMAIN, (10), 18: 444.
1969 Segmentorbis angustus, STARMUHLNER, 8: 345.

Distribution. Les cartes publiées par Brygoo et par Ranson sont déjà tres fournies. Nous
aurions encore tant d'autres localités а faire connaítre, qu'il nous semble inutile de les
énumérer. Qu il nous suffise de dire que cette espéce se trouve en abondance dans toute
Vile.

366 FISCHER-PIETTE ET VUKADINOVIC

Diego- Suarez

Ambilobe —
Ветараза Vohemar

| FIG. 18. Distribution de Gyraulus apertus Martens.

Ambalabongo
| Ambodiamontana
Ambalatany Bandabe —
\ 4
Mandritsara |

Bekodoka —Antsirasitra

Miarinarivo

Antsampandrano
et Amborompotsy

E /
e—Andranomaria

Espece décrite du Lac Albert-Edouard qui était sa seule provenance connue, et que
Starmiihlner a citée récemment de Madagascar, en deux provenances du centre Sud, le
ruisseau Andranomaria, et le ruisseau Amborompotsy (et un de ses affluents). Nous y
ajoutons 14 autres provenances. L'une d'elles est due à Waterlot Diego-Suarez (Baie des
Amis). Toutes les autres sont dues au Dr. Brygoo. Ce sont, du Nord au Sud: Vohemar,
Ambilobe, Bemapaza, Bandabe, Ambodiamontana, Mandritsara, Ambalabongo, Am-
balatany, Bekodoka, Antsirasitra, Bevato, Miarina rivo et Ambano (voir notre carte Fig.
18).

Nous avons comparé nos échantillons avec un lot du Lac Albert Edouard étudié par
Germain (1912, Bull. Muséum, p 80).

Espece africaine а trés large répartition, dont on trouvera davantage de références dans
Germain (1935) et dans Starmiihlner (1969).

Pour Madagascar, les provenances connues sont Majunga (Germain, 1918) et lac
Manampetsa (Germain, 1935). Nous y ajoutons 12 autres provenances. Du Nord au Sud:
Ambanja (Waterlot); Antsohihy (Brygoo, 1957); Ambodiamontana (Brygoo, 1957); An-
dohajango (Brygoo, 1957); Marovoay (Waterlot); Tampolo (J. Millot, 1949); Fenerive (J.
Millot, 1949); Manambolo (Brygoo, 1957); Morondava (Perrier de la Bathie); Vondrove
(Brygoo, 1957); Fiherana (Grandidier); Tuléar (G. Petit, 1925). Les diverses provenances
sont portées sur notre carte Fig. 19.

Ferrissia (Ferrissia) modesta Crosse

1880 Ancylus modestus, CROSSE, 28: 150.

1881 Ancylus modestus, CROSSE, 29: 203, pl. 8, fig. 6.

1882 Ancylus modestus, CLESSIN, ed. 2, 1(6): 73, pl. 9, fig. 10.

1889 Ancylus modestus, CROSSE & FISCHER, In: GRANDIDIER, pl. 24, fig. 6.
1964 Ancylus modestus, CHEVALLIER, 104: 33.

1969 Ferrissia (Ferrissia) modesta, STARMUHLNER, 8: 362, fig. 506.

Nous avons le type dans la collection de |’Atlas de Madagascar.

Cette espéce a été décrite de Nossi-Bé. Starmühlner Га citée en plus de Tananarive, de
la riviére Lily а 100 km de Tananarive, des environs du lac Froid et pres de la voie ferrée
d Antsirabe.

—

MOLLUSQUES DE MADAGASCAR 367

Nos collections y ajoutent: (J. Millot, 1946 et 1947): Marais du lac Alaotra, lac Tsim-

bazaza, Ambositra.
Les diverses provenances sont portées sur notre carte Fig. 19.

Biomphalaria madagascariensis Smith

1882 Planorbis madagascariensis, SMITH, p 387, pl. 22, fig. 20-22.
1905 Planorbis madagascariensis, ANCEY, 53: 320.
1918 Planorbis madagascariensis, GERMAIN, p 45.

Ambanja

Antsohihy

| Majunga Ambodiamontana
Marovoay \
Ambohajango
Г Tampolo
Fenerive
Manamloolo
Lil = Tananarive
Tone x Lac Tsimloazaza
E Lac Froid
Ligne d'Antsirabe |
Morondava
A Ambositra
Vondrove_e
Tulear

e—Fiherena

Lac а :
p- Man mpetsa e Segmentorbis angustus Jick.

NTercissia, Mmoeleska cross=

FIG. 19. Distribution de Segmentorbis angustus Jickeli et de Ferrissia modesta Crosse.

368 FISCHER-PIETTE ET VUKADINOVIC

1953 Biomphalaria pfeifferi, GRJEBINE & MENACHE, 8: 87.

1957 Biomphalaria madagascariensis, RANSON, (34): 1, fig. 2, 3A.

1958 Biomphalaria madagascariensis, BRYGOO, 26: 49, carte, p 51.

1969 Biomphalaria madagascariensis, STARMUHLNER, 8: 345; fig. 482, p 349; fig. 505, p 361.

Distribution. Les cartes publiées par Brygoo et par Ranson sont déja trés fournies. Nous
aurions encore tant d'autres localités а faire connaitre qu il nous semble inutile de les
énumérer. Qu'il nous suffise de dire que cette espéce se trouve en abondance dans toute
Vile.

Caelatura (Zairia) geayi Germain

1911 Unio (Nodularia) Geayi, GERMAIN, p 137, pl. 1, fig. 1, 2, 6, 7.
1918 Nodularia Geayi, GERMAIN, p 36.
1969 Caelatura geayi, HAAS, 88: 187.

La localisation de cette espéce dans l’île est inconnue.

Nous sommes tombés par hasard, dans des matériaux non-classés du Muséum, sur un
lot de 4 Unionidae dépourvus de nom et dont l'étiquette portait seulement * Mission Geay
1911.”

Cette indication prouvant que la provenance était Madagascar nous avons constaté,
avec la plus grande facilité, que 3 des 4 specimens étaient ceux que Germain (1911) avait
figurés sous les noms Unio (Nodularia) Geayi et Unio (?) malgachensis.? Tous les détails
des taches etc. . . se reconnaissent.

HAAS a affirmé que | Unio geayi n'était pas une Caelatura, sans proposer d’ailleurs une
autre affectation. Il п’а pas expliqué les raisons de son affirmation.

Nous ne comprenons pas ce qui Гу a conduit, et nous confirmons pleinement la position
de Germain.

Faisons connaître que l'échantillon non-figuré est une valve gauche de 42 mm sur 23.

Caelatura (?) malgachensis Germain
1911 Unio (?) malgachensis, GERMAIN, р 139, pl. 1, fig. 3-5.

La localisation de cette espéce dans l’île est inconnue.

Comme nous venons de le dire (voir Caelatura (Zairia) geayi), | exemplaire sur lequel
est basée la description de Germain est entre nos mains. De méme que Germain, nous ne
voulons pas l'ouvrir pour ne pas le casser plus que ne le montre la figure 3, de sorte qu il
n'est toujours pas possible de lui assigner une place dans la classification. Certes, Haas af-
firme que c’est un jeune d’ Unio geayi. Nous devons faire remarquer que son sommet n'est
séparé de l'extrémité antérieure que par un septième de la longueur totale de
l’exemplaire, alors que chez Caelatura geayi il est au quart ou entre le quart et le tiers.
Nous savons que le sommet peut s'éloigner de l'avant au cours de la vie, mais nous pen-
sons qu'avant de prendre une décision il faudrait attendre d’avoir а sa disposition des in-
dividus de tous âges.

Unio madagascariensis Sganzin

1841 Unio madagascariensis, SGANZIN, 3: 8.
1918 Unio (?) madagascariensis, GERMAIN, p 37.
1969 Caelatura madagascariensis, HAAS, 88: 187.

2Germain ne prenait vraiment aucun soin des matériaux qu'il avait étudiés. ne leur mettant bein souvent pas
d'étiquettes, ou encore les mélangeant ainsi que leurs étiquettes ou les dispersant dans bien des cas, non seule-
ment n'importe où au Muséum, mais aussi bien dans son appartement de Paris, sa villa d'Angers ou le Musée
d'Angers. Il en résulte que beaucoup de ses types passent maintenant inaperçus, et il se pourrait qu un certain
nombre soit définitivement perdu. Le professeur Fischer-Piette tient à faire connaître clairement cette situation
pour ne pas en être tenu responsable.

MOLLUSQUES DE MADAGASCAR 369

Espece non-figurée et qu on пе peut guere dire avoir été décrite, le texte étant: Cette
coquille, que je crois inédite, est de la grandeur de la mulette littorale; elle est vert et
d'une contexture trés fragile; elle se trouve abondamment dans le Mahoupa, riviere pres
de Tamatave, ile de Madagascar.” Il conviendrait de rechercher cette espéce dans la
région d'où elle était signalée.

Etheria elliptica Lamarck

1807 Etheria elliptica, LAMARCK, 10: 401, pl. 29; pl. 31, fig. 1.
1907 Aetheria elliptica, GERMAIN, p 225.
1945 Aetheria elliptica, FISCHER-PIETTE, p 41.

La provenance indiquée en 1907 et les 2 provenances qui ont été ajoutées en 1945 sont
portées sur notre carte Fig. 20. Jusqu ici il ne s agit donc que du Nord-Est et du Nord-
Ouest.

Betsieka

e-Beandrarezona

sahondra
A-Mahavavy

Fah arantSana-e, ropa

Tananarive—e :
e- Ambohitraimanitra

if

Onive—e Tsinjoarivo

Antsirabe

. —
Manshiatra
e— Fianarantsoa

Mananara—e E
4 vanganidrano

Itomam
Befotaka=e PY
Amboasary —e eCorbicula madagascariensis smith

A Etheria elliptica Lr

FIG. 20. Distribution de Etheria elliptica Lk. et de Corbicula madagascariensis Smith.

370 FISCHER-PIETTE ET VUKADINOVIC

Corbicula madagascariensis Smith

1882 Corbicula madagascariensis, SMITH, p 388, pl. 22, fig. 25-27.
1918 Corbicula madagascariensis, GERMAIN, p 37.

Cette espece n était connue jusqu ici que par le travail de Smith, qui a donné comme
provenance “Twenty miles from Antananarivo.”

Nous en avons un grand nombre d'échantillons de diverses provenances, qui vont nous
permettre de faire connaître le degré de variabilité de l'espece. Voir la charniére de l'un
d'eux, Fig. 21.

Smith a donné les dimensions suivantes: longueur 14 mm; hauteur 11 mm; épaisseur 7
mm. Le plus grand de nos échantillons a: 19 mm; hauteur 16 mm; épaisseur 12 mm
(récolté par Decary dans la riviere Itomampy). Les rapports des dimensions montrent
quelque variabilité. Nous les donnons pour un certain nombre d'individus de tailles
diverses dans le Tableau No. 1.

TABLEAU 1. Dimensions de 20 individus de Corbicula madagascariensis

Rapport Rapport
Longueur Hauteur Epaisseur longueur épaisseur
en mm en mm en mm sur hauteur sur largeur

19 16 12 152 0,60
18 14 8 1,3 0,45
17 15 Ih! 1,1 0,65
17 14 8 12 0,45
16 15 8,5 1,03 0,53
16 14 10 I 0,62
16 13 7,9 1.2 0,47
16 13 8 1,1 0,44
15 13 9,5 11 0,63
15 13 8 1,13 0,44
14 12 7,9 1413 0,53
14 11 6 1:25 0,43
14 10,5 5,5 1,4 0,40
13 10 6 1,3 0,46
12 10 6 1,3 0,46
11 9 5 1,2 0,45
10 8 5,5 1,25 0,55
10 8 5 1,3 0,50

9 7 4 1,3 0,44

8 6,5 4 1,2 0,50

FIG. 21. Corbicula madagascariensis Smith.

MOLLUSQUES DE MADAGASCAR 371

On voit par ce tableau que le rapport de la longueur а la hauteur, varie de 1,1 а 1,4, et
que le rapport de l'épaisseur а la longueur varie davantage de 0,49 à 0,65. Ce tableau ne
montre pas d’evolution nette des rapports des dimensions avec l’äge des individus.

Distribution. A la provenance qui était connue, Tananarive, nous ajoutons (voir carte
Fig. 20): Beaudrarezona (Brygoo, 1957); rivière Кора à Faharantsana; riviere Кора pres
de Tananarive; Ambohitraimanitra canal (Brygoo, 1957); Tsinjoarivo (J. Millot, 1949);
Onive (J. Millot, 1949); Antsirabe (Waterlot); Manshiatra (Perrier de la Bathie);
Fianarantsoa; Mananara (Decary, 1926 et Perrier de la Bathie); Vanganidrano (Decary);
Itomampy (Decary, 1926); Befotaca (Brygoo, 1957); Amboasary (G. Petit, 1932).

Corbicula sikorae Ancey

1890 Corbicula sikorae, ANCEY, 7: 347.
1918 Corbicula sikorae, GERMAIN, p 38.

Cette espece n'est connue que par la description d’Ancey (du fleuve Mongoro) et n’a
jamais été figurée. Germain a seulement dit qu'elle semble bien voisine de С.
madagascariensis. C'est tout-d-fait notre opinion, et nous voulons faire ressortir la
similitude des caracteres. Voici la description donnée par Ancey: “Concha pro genere
tenuis, deplanata, subaequilatera, ovalis, nitida, lutea, epidermide ad nates praecipue
decidua. Nates submediani, obtusati, vix prominentes. Pagina interna livide alba. Area an-
tica ovalis, postica haud angulata nec truncata, subovalis. Basis regulariter lateque ar-
cuata. Superficies sulcis concentricis ad marginem vix tenuiorbus sculpta. Diam. antero-
post., 11%; alt. (e natibus ad basin), 8/2; crass., 5 п.” Ancey dit que son espece differe
“tres notablement” de С. madagascariensis, mais il n'exprime pas des différences.

Nous supposons qu elles consistent dans la taille, petite; dans le fait que les stries de
croissance, dans la région ventrale, s atténuent à peine alors que Smith avait écrit: “The
concentric striae are deep and regular upon the umbones; but towards the ventral margin
they become less regular and finer.”

Mais il se pourrait bien que la petitesse de la coquille d'Ancey soit due ä un Аве moin-
dre, et il serait alors normal que l’affaiblissement des côtes, qui, faisons le remarquer, est
exprimé dans les deux cas, ne fasse que commencer.

Nous supposons aussi ач’еп disant ач’а l’arriere la coquille n était ni anguleuse ni
tronquée, Ancey a voulu apposer ces caractères à “squarish and subtruncate posteriorly
qu exprime et figure Smith. Mais, au sein d'un même lot, nous trouvons avec la plus
grande facilité. aussi bien des contours réguliérement arrondis а | arriére que des aspects
tronqués, et avec tous les intermédiaires.

Nous sommes donc persuadés que C. sikorae est synonyme de C. madagascariensis.
Mais n ayant pas vu d échantillons d'Ancey, nous n opérons pas la suppression de son es-
ресе.

Pisidium casertanum Poli

1791 Cardium casertanum, POLI, p 65, pl. 15, fig. 1.

1906 Pisidium planatum, ANCEY, 20(4): 46, No. 3.

1918 Pisidium planatum, GERMAIN, p 40.

1953 Райт edouardi, KUIPER, р 26, pl. 1; fig. 1, 2, p 27.

1966 Pisidium casertanum, KUIPER, pl. 10, fig. 1-3; pl. 11, fig. 1-5; pl. 12, fig. 1, 2; pl. 15, fig.
13.

Kuiper (1966), a placé dans la synonymie de |’ espéce cosmopolite P. casertanum le P.
edouardi qu'il avait décrit en 1953, et aussi le P. planatum.

Ce dernier n est connu que par la description d'Ancey qui ne Га jamais figuré. Ancey le
dit plus plat que P. madagascariensis Smith. Germain a fait remarquer qu il n'y a jamais
eu de P. madagascariensis Smith. Nous supposons qu Ancey voulait parler, en fait, de P.
johnsoni, qui d’apres les dimensions données est en effet plus gonflé.

372 FISCHER-PIETTE ET VUKADINOVIC

Nous avons au Muséum le type de P. edouardi, ses paratypes, les échantillons sub-
fossiles d’Antsirabe cités par Kuiper (1966, р 50), ainsi qu une vingtaine d'exemplaires
récoltés par Waterlot äTananarive. Voir la carte Fig. 22.

Pisidium johnsoni Smith

1882 Pisidium johnsoni, SMITH, p 389, pl. 22, fig. 28-29.

1918 Pisidium johnsoni, GERMAIN, p 40.

1953 Pisidium pauliani, KUIPER, 93: 28, pl. 2, fig. 1-5.

1960 Pisidium pauliani, KUIPER, 89: 74; fig. 24-29.

1966 Pisidium johnsoni, KUIPER, p 54, pl. 14, fig. 1-6; pl. 15, fig. 16.

Espece décrite des environs de Tananarive. Connue aussi de Betafo (centre de l’île, voir
notre carte Fig. 22) par la description que Kuiper a faite de P. pauliani qu il a ensuite
placée dans la synonymie de P. johnsoni.

Le Muséum ne possede pas d'échantillons de cette espece.

ePisidium casertanum poli
APisidium reticulatum ruipr

Nossi-Be_A

Ankirihitra k

Andriba_ ,

Ambatolaona
Tananarive_, Perinet
Betafo

Antsirabe % Namokely

1
Antsampandrano
/l

FIG. 22. Distribution de Pisidium casertanum Poli et de Pisidium reticulatum Kuiper.

Pisidium betafoense Kuiper
1953 Pisidium betafoense, KUIPER, 93: 30; pl. 3, fig. 1-5, p 31.
1966 Pisidium betafoense, KUIPER, р 55, pl. 15, fig. 17.

Espece décrite sur un seul échantillon, de Betafo (Paulian, 1949). Betafo est au centre
de l'île (voir carte Fig. 22).

Pisidium (Parapisidium) reticulatum Kuiper
1966 Pisidium (Parapisidium) reticulatum, KUIPER, 95: 16, text-fig. 1-4.
Espece décrite de Nossi-Bé et de Rhodésie. Nous en avons deux échantillons dont un

jeune, récolté par Waterlot 4 Ankarihitra pres Maevatanana (Madagascar Nord-Ouest).
Voir notre carte Fig. 22.

MOLLUSQUES DE MADAGASCAR 373

Namoroka

e——Tananarive

Morondava

Antsirabe

FIG. 23. Distribution de Eupera ferruginea Krauss.

Sphaerium madagascariense Tristram

1863 Cyclas (Sphaerium, Scop.) madagascariensis, TRISTRAM, p 61.

1878 Sphaerium Madagascariense, SOWERBY, In: REEVE, 20: pl. 3, fig. 22.
1882 Sphaerium madagascariense, SMITH, p 388.

1918 Sphaerium madagascariense, GERMAIN, p 39.

Cette forme dont nous n'avons pas d'exemplaires sous les yeux, a été décrite de la
région de Tananarive, et trouvée aussi а Betsileo (Smith). Germain en commentant ces
données, émet la supposition qu ‘il n'y a avec Sphaerium capense Krauss, 1848, largement
répandue en Afrique, qu une difference de provenance et qu une mise en synonymie
devra se faire.

Eupera ferruginea Krauss

1848 Cyclas ferruginea, KRAUSS, p 7, pl. 1, fig. 7.

1879 Limosina ferruginea, CLESSIN, ed. 2, 9(3): 247, pl. 46, fig. 1-4.
1882 Limosina ferruginea, SMITH, p 388.

1918 Sphaerium ferrugineum, GERMAIN, p 38.

1929 Eupera ferruginea, HAAS, 57: 429.

1954 Byssanodonta ferruginea, KUIPER, 94: 47; fig. 6-10, p 46.

Cette espéce décrite d'Afrique du Sud a été signalée à Madagascar par Smith de
Tananarive, par Haas de Majunga et par Kuiper de Morondava et Namoroko. Nous y
ajoutons: Antsohihi (Dr. Gaud, 1951); Antsirabe (Perrier de la Bathie). Voir la carte Fig.
23.

Eupera degorteri Kuiper
1954 Byssanodonta degorteri, KUIPER, 94: 42-47; fig. 1-5, р 43.

Cette espéce a été décrite sur des matériaux du Muséum ayant les provenances
suivantes: Cap St. André; riviere Kapiloza; riviere Maningoza; Sahondra; Andravodahy
(dont le type); Morondava. Toutes ces provenances sont de l'Ouest. Nous у ajoutons une
provenance du Nord: Diego-Suarez (Waterlot). Voir notre carte Fig. 24.

374 FISCHER-PIETTE ET VUKADINOVIC

FIG. 24. Distribution de Eupera degorteri Kuiper.

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378 FISCHER-PIETTE ET VUKADINOVIC

ABSTRACT
ON THE FRESHWATER MOLLUSKS OF MADAGASCAR
E. Fischer-Piette and D. Vukadinovic
This work is a complement to that of Starmühlner which appeared in

MALACOLOGIA in 1969. It completes his study by also mentioning lamellibranchs and
by giving additional locations for many gastropods.

AG

ZUSAMMENFASSUNG
ÜBER DIE SÜSSWASSERMOLLUSKEN MADAGASKARS

E. Fischer-Piette und D. Vukadinovic

Diese Arbeit ist eine Ergänzung zu der in 1969 in MALACOLOGIA erschienenen von
Starmühlner. Sie vervollständigt seinen Bericht insbesondere dadurch, dass ausser
Gastropoden auch Lamellibranchier erwähnt werden, und indem für die Gastropoden
zusätzliche Fundorte angeführt sind.

A.G.

RESUMEN
SOBRE LOS MOLUSCOS DE AGUA DULCE DE MADAGASCAR

E. Fischer-Piette y D. Vukadinovic

Este trabajo es complementario al de Starmühlner publicado en MALACOLOGIA en
1969. Completa su estudio mencionando tambien lamelibranquios y dando ubicaciones
adicionales para muchos gaströpodos.

JE.

ABCTPAKT
) ПРЕСНОВОДНЫХ МОЛЛЮСКАХ МАДАГАСКАРА
Е. ФИШЕР-ПЬЕТТ И Д. ВУКАДИНОВИЧ
Эта работа служит дополнением к исследованию Штармюльнера, напечатанного

ологии" в 1969 г. Она выполнена на тех же видах Bivalvia и в ней
указываются дополнительные места нахождения многих Gastropoda.

Z.A.F.

MALACOLOGIA, 1973, 12(2): 379-399

SUBSTRATUM AS A FACTOR
IN THE DISTRIBUTION OF PULMONATE SNAILS
IN DOUGLAS LAKE, MICHIGAN!,?

Philip T. Clampitt

Cranbrook Institute of Science,
Bloomfield Hills, Michigan 48013
USA

ABSTRACT

Study has been made of substratum as a factor in the distribution of 5 species of
pulmonate snails in Douglas Lake, Cheboygan County, Michigan. Quantitative field
sampling, together with laboratory experiments, revealed that adult Physa integra
Haldeman prefer hard substrata such as stones; adult Helisoma antrosa percarinata
(Walker), in contrast, prefer a substratum of sand. When food (algae or detritus) was pre-
sent on both stones and sand in the laboratory, the average distribution of P. integra was
58% on the stones and 8% on the sand (a highly significant difference), while in separate
equivalent experiments an average of 24% of the H. antrosa were on the stones and 39% on
the sand (also significant). Physa parkeri “Currier” DeCamp, Stagnicola emarginata
angulata (Sowerby) and Helisoma campanulata smithi (Baker) all exhibited more com-
plex and varied patterns of distribution as to substratum in the field. In the laboratory, P.
parkeri showed a preference for a stony substratum very similar to that of P. integra when
food was present. The average distribution of H. campanulata was 29% on stones and also
29% on sand when food was present on both. Relationships in the 5 species between sub-
stratum, on the one hand, and depth, wave action, food, oviposition sites, and respiratory
needs, on the. other, are discussed.

INTRODUCTION

Substratum is a significant ecological factor in the distribution of freshwater snails.
After a comparative study of 2 species of aquatic pulmonate snails in Iowa (Clampitt,
1970) and a review of the pertinent literature, I have concluded that this factor deserves
more study than it has so far received.

Hyman (1967), in her summary of the literature on habits and behavior in pulmonate
snails, makes no special mention of substratum with reference to most freshwater forms;
she states only that the freshwater limpets, family Ancylidae, inhabit rock surfaces in
streams and lakes. Boycott (1936), while giving considerable information on the habitats
of British freshwater mollusks, does not describe substratum types in most instances.
Macan (1950) gives some information on substratum and vegetation in relation to the
numbers of gastropod mollusks in Lake Windermere and other bodies of water in the
English Lake District. Elsewhere, Macan (1963) comments more generally both on the
importance of substratum to most freshwater animals, and on the lack of data on the sub-
ject. A recent study of Harman (1972) confirms the importance of substratum in the dis-
tribution of aquatic mollusks.

In a lake well-populated with a variety of species of snails, some reside primarily on the
bottom, others on vegetation, and still other species move freely from one to the other. In
the study cited above (Clampitt, 1970), some populations of Physa integra Haldeman
(Pulmonata: Physidae) were concentrated on stones close to shore, while others were

1 A contribution from the University of Michigan Biological Station and Cranbrook Institute of Science.
2 The work was supported by Cranbrook Institute of Science.

(379)

380

Р. T. GLAMPITT

contined largely to off-shore vegetation; the species appeared to avoid substrata of sand
or mud. P. gyrina Say, an inhabitant of small ponds as well as shallow areas of lakes, was
much less selective as to substratum, being found on living and dead vegetation, stones,
mud and sand.

The substratum on which a snail moves provides food and oviposition sites, and may
afford protection against such physical and biological factors as wave action and preda-
tion. For pulmonate snails dependent on atmospheric oxygen, the
‘substratum’ —whether it be stones, fallen logs, vegetation, or some other
material—may provide a surface on which the snails can crawl upward to reach the air-
water interface. It is reasonable to assume that different snail species will have different
behavior patterns and ecological requirements, and can therefore be expected to show
different patterns of distribution with respect to substratum. The study described here

was undertaken to test this assumption.

Douglas Lake, Cheboygan County,
Michigan, (45°35’ N. lat., 84°40’ W. long.)
was chosen as the site of the study. This
lake has a rich molluscan fauna, including
several pulmonate snail species which are
widely distributed in the lake. Although a
review of the considerable background in-
formation available on the lake and on
various of its molluscan inhabitants 15
beyond the scope of this paper, the
following studies are pertinent: H. B.
Baker (1912, 1914), Welch (1927),
Eggleton (1931, 1935), Cheatum (1934),
Cort (1936a,b), Moore (1939), Cort, et al.,
(1940, 1941), Moffett (1943), Wilson
(1944), Young (1945), Neel (1948), Gan-
non & Brubaker (1969), Gannon & Fee
(1970), and Bazin & Saunders (1971).

Five species of pulmonate snails were
chosen to receive major emphasis in this
study. These are Physa integra Haldeman?
and Р. parkeri “Currier” DeCamp in the
family Physidae; Stagnicola emarginata
angulata (Sowerby) (=Lymnaea e.
angulata Say), Lymnaeidae; and Helisoma
antrosa percarinata (Walker) (=H. anceps
percarinata (Menke)) and H. campanulata
smithi (Baker), Planorbidae. These species
are the most common of the larger
pulmonate snails in Douglas Lake.

The study consisted of 2 major parts: (1)
distribution of each species in the

field—related to substratum
characteristics, depth, and distance from
shore—as revealed by quantitative
sampling at selected locations, and (2) sub-
stratum “preference” as revealed by
laboratory experiment. The work reported
here is the first of a series of investigations
on the ecology, life history and behavior of
Douglas Lake pulmonate snails, being
done at the University of Michigan
Biological Station.

QUANTITATIVE FIELD SAMPLING
METHODS

Quantitative sampling of snails was
done directly by hand. А circular
“sampling loop, constructed of heavy
steel wire and enclosing a М m? area, was
set on the substratum and the enclosed
area was searched carefully for snails. A
face mask and snorkel were used regularly
to aid collecting; SCUBA gear was used at
depths of 2 m or more. Adult snails of the 5
species studied could be seen and collected
readily using this method, as could
juveniles 5 mm or more in greatest shell
dimension.

The sampling was done along transects
at carefully selected sites positive for
snails, at locations in Douglas Lake in-
dicated in Fig. 1. Quantitative sampling
was confined for purposes of this study to

3 The Douglas Lake forms which I have designated as Physa integra were apparently mis-identified by Goodrich
(1932) and Cheatum (1934) as P. зауй crassa Walker. 1 was able to collect a few living P. зауй crassa from
Higgins Lake, Roscommon County, Michigan, the type locality, on July 2, 1970. Examination of characteristics
of both shells and male genitalia clearly establishes that the Higgins Lake forms and those from Douglas Lake
are different entities, belonging not only to different species but to different subgenera (for criteria, see Clam-
pitt, 1970, p. 119-121). In contrast, the lowa P. integra studied earlier (Clampitt, 1970) and those of Douglas
Lake are very similar forms which I believe to be conspecific.

SUBSTRATUM AND FRESHWATER SNAILS 381

М.
Fishtail
Bay
b
с
БОЕ, que Пе В
М
Grapevine d
Parc
ad
a
km Si.
0 0. РО Fishtail
и Вау
0 ORS UM Biol.
mi A ESfiatiion

FIG. 1. Douglas Lake, Cheboygan County, Michigan: approximate location with respect to Great
Lakes region of North America (inset) and of transects (a-d) used for quantitative field sampling of

snail populations.

the eastern part of the lake—i.e., the
North and South Fishtail Bay areas.
Furthermore, only fairly open parts of the
lake, exposed at times tofairly heavy wave
action and characterized by a substratum
of cobbles, gravel, or sand, and with slight
to moderate growth of vegetation, were in-
cluded; data were not collected from the
few more sheltered and pond-like portions
of the lake with heavy vegetative growth
and substrata of silt.

Each transect chosen showed fairly con-
sistent substratum characteristics at any
given depth. These are described below
under “Results.” The transects ran
perpendicular to the lake shore, and
extended usually from the shore to
maximum depths (distances) positive for

snails. A series of stations along each
transect was sampled; the several stations
reflected changes in substratum with in-
creased depth and distance from shore.
Sampling at each station was along a
narrow strip totalling 10 sq. m, running
parallel to shore. Each sample, in turn,
contained snails from a 1 m? area.

The data are presented graphically in
this paper as the average number of snails
per m2, of each of the dominant species, at
each station along the transect. Data were
recorded at each station not only on sub-
stratum, but also on depth and distance
from shore. Temperature data, and data
on shell sizes—reflecting life history
stages—were also collected, and are to be
reported in a later paper.

382 РТ. CLAMPITE

RESULTS the shallow water adjacent to shore, to
Transect “a,” South Fishtail Bay: sand (with scattered stones and pebbles)
The substratum along this transect (Fig. | overlain by a thin layer of flocculent
2c) changed from algae-covered cobblesin organic detritus. The detritus layer
25
a June 30 - July 9, 1969 Transect a.
N
=
>
п
—|
<
Z
п

NO.

b 25 Physa Stagnicola
May 18 - 21, 1970 integra emarg. angul.

N
= 20 Ph
SS (Q ysa Helisoma
m м parkeri antr.. peras
=.
<
Z
п
O
72
DEPTH,
DISTANCE, | 3 - 4 12 19 24
M
SUBSTRA= 13
TUM
I \ \
0 / 7 р \ \
с >
DS
E
=
ee 10
a

FROM

DISTANCE SHORE,

FIG. 2. Quantitative sampling data from transect “a,” South Fishtail Bay. a € b, numbers of adult
snails per m? in July 1969 and May 1970, respectively; average numbers shown in cross-hatched or
shaded bars, range of numbers per m? by vertical lines. c, bottom profile and substratum
characteristics.

SUBSTRATUM AND FRESHWATER SNAILS 383

became gradually thicker with increased
depth and distance from shore. Rooted
vegetation along this transect was sparse to
absent. Beginning at about 30 m from
shore (depth 2 m when the data were
collected), the slope of the bottom in-
creased, so that at about 45 m from shore
the water depth was 5 m. At the times of
sampling most of the snails were confined
to water little more than 1 т deep, and the
data in Fig. 2 are limited to these areas.

Snail density data are shown in Fig. 2
for June 30-July 9, 1969, and May 18-21,
1970. In 1969 (Fig. 2a) there was a rather
definite zonation for 2 species: Physa in-
tegra were found in greatest numbers on
the cobbles adjacent to shore, averaging
5/т? here. Helisoma antrosa were
decidedly most abundant in the detritus-
covered sand, in water 0.9 m deep, 12 m
from shore; they averaged up to 18/m? in
this area. Again in May, 1970 (Fig. 2b), P.
integra showed much the highest den-
sity—averaging 20/m2—in the cobble area
adjacent to shore. Sampling done later in
1970 revealed heavy mortality of P. integra
adults during June and July; by mid-July
the adults had been almost entirely
replaced by tiny juvenile snails.

The other 3 species were fewer in
number and showed less clear zonation.
Stagnicola emarginata, for example, ex-
hibited a more scattered distribution
pattern through both cobble and sand sub-
stratum areas in July 1969 (Fig. 2a); in
1970, this species was quite rare, not only
along this transect but elsewhere in the
lake. Both Physa parkeri and Helisoma
campanulata (the latter not shown in Fig.
2) were low in numbers and rather
scattered in distribution along transect
“a” during both seasons.

Transect “b,” North Fishtail Bay:

The substratum adjacent to shore at
transect “b” (Fig. 3c) was sand, with a
limited amount of detritus and growth of
algae. At about 10 m from shore, at a
depth of 0.9 m, was a sharp drop-off.
Below the drop-off were gradually т-
creasing amounts of detritus upon the
sand; a dense growth of rooted vegetation

(Potamogeton, Myriophyllum, Vallisneria,
etc.) at 2-3 m; a gentler slope at a depth of
5-6 m, on which was deposited a very fine,
dark-colored layer of detritus; coarser
detritus at 7 m; and increasing amounts of
silty detritus at 9 m depth and slightly
below, where the bottom again leveled off.

Snail density data are shown in Fig. 3 (a
& b) for July 12, 1969, and July 22-24,
1970. As at transect “a, the snail density
and distribution data differed greatly in
the 2 years. In July 1969, numbers of
Helisoma antrosa averaged 12 or more per
m? in water 0.1 m deep, within 1 m of
shore; their numbers dropped off sharply
to 0 in water 0.9 m deep, 10 m from shore.
The few Physa integra which were present
were also in very shallow water. In 1970,
few snails of any species were found above
the drop-off area. The numbers of Н. cam-
panulata on the fine silty substratum at 5.5
m depth—average 5/m?—was something
of a surprise; this species elsewhere seem-
ed to be most prevalent (e.g., see Fig. 5) on
sand in water less than 1.0 m deep.

Transect “c,” North Fishtail Bay:
Characteristics of the substratum along
transect “с” аге summarized, together
with bottom profiles, in Fig. 4. A broad
shoal, mostly of sand but containing varia-
tions which could make considerable dif-
ference in the lives of snails populating the
area, extended from shore outward to a
distance of about 150 m. At the edge of the
shoal, at about 2 m deep, was a steep drop-
off extending to a depth of more than 10
m.
Snail density data from July 1969 are
shown in Fig. 5. Helisoma antrosa pop-
ulations averaging 7-9 snails/m? were pre-
sent on a substratum of soft sand overlain
by an algae-covered “crust” of con-
solidated sand grains (Fig. 4) at a depth of
0.9-1.1 m, 65-100 m from shore. Densities
of this species were much lower at other
stations with different substratum condi-
tions. H. campanulata were present in
greatest numbers, averaging 2-3/m?, on
fine sand 0.7 m deep and 40 m from shore;
the presence of ripple marks indicated that
the bottom was disturbed by periodic wave

384

action here. Physa integra and Sıugnicola
emarginata were more scattered in their
aistribution. On July 30, 1969, juvenile P.
parkeri (not shown in Fig. 5) were found in
fair numbers—up to 5 or 6/m2—all along
the transect between 6 and 160 m from
shore, at depths ranging from 0.5 to 5.0 m.

а Transect b.

HT. CLAMEPEITT

Juvenile and some adult H. antrosa were
similarly widely distributed, but with
highest densities—10 or more/m?
—between 1.0 and 2.0 m depth. A few
adult H. campanulata were found below
the drop-off at 2, 6 and 9 m depth, and
some juveniles were collected at 2 and 3 т

Physa integra

15
Helisoma
= m July iZ 1969 = ants) spiere :
= Helisoma
I 5 IM) campanulata
<
Z
n 0
b o
25
0
DEPTH,
M
DISTANCE, 4 8 Il 12 14 22 30
M
SUBSTRA- =]
Tun AY
С 0
2
=
Y
dE
=
a
us 6
=
8
10 20 30
№ DISTANCE FROM SHORE, М

FIG. 3. Transect “b” quantitative data, North Fishtail Bay. a € b, numbers (average and range) of
adult snails per m? in July 1969 and July 1970, respectively. c, bottom profile and substratum
characteristics.

SUBSTRATUM AND FRESHWATER SNAILS 385

DISTANCE FROM SHORE, METERS
0 20 40 60 80 100 120 140 160 180
à \ AE — АЕ = + — 1

/
/ soft sand,,”
4
и а | дае -соуеге 4
3 fine sand, crust, patches
ripple marks, of rooted plants
u slight surface
œ 4
wu crust
EE
uy
= 18
ЕЕ
= 6
a
us
a

Transect c.

soft sand, Е
flocculent _- 7
organic 3
debris

sand,” 7
debris /
/

fairly clean

some organic

sand,
organic

increasing
debris, „I

rooted plants 24

. Y
still more

debris h

sand,
organic

Y
sand, silty, grayish-

flocculent
debris Zi

green,
organic

very silty sand 2

FIG. 4. Transect “c”, North Fishtail Bay area—bottom profile and substratum characteristics.

depth, on the same date.

During the spring and summer of 1970
transect “с” was again sampled. The
numbers of most species in this area were
greatly reduced from those of 1969.
However, on July 22, 1970, the numbers of
Helisoma antrosa averaged 2-3 / пл? at 7 т
depth and about 1/m? at both 5 and 9 m
depth below the drop-off. On August 14,
1970, Physa integra juveniles were found
in numbers averaging 7/m? at 0.5 m
depth, 50 m from shore, on soft sand, at
that time covered with an algae crust;
these numbers decreased gradually both
closer to and farther from the shore where
substratum changes also occurred.

Transect “d,” Big Shoal:

The “Big Shoal” extends from the east
shore of Douglas Lake westward across the
mouth of South Fishtail Bay nearly to
Grapevine Point (Fig. 1). The substratum
was mostly sand, with variations from
shore outward (Fig. 6b) which could affect
the snail populations inhabiting the area.
At 0.45 m depth (at the time of sampling),

15 m from shore, the substratum was clean
sand with distinct ripple marks, indicating
frequent disturbance by wave action. The
ripple marks faded out and a sparse mix-
ture of Chara and a small Potamogeton sp.
appeared between 30 and 50 m from shore
at a depth of 0.5-0.55 m. The sand became
very soft under foot at 60 m from shore,
0.65 m deep, then much firmer again at 90
m out, 0.8 m deep. At about 130 m from
shore, where the water depth was 1.2 m,
the substratum was fine sand with a slight
‘crust’ forming on the surface, and a very
small amount of loose organic detritus.
The slope of the bottom increased tem-
porarily from a depth of 1.2 m at 132 m to
1.5 m at 147 m from shore. Along with this
more rapid change in depth were changes
in the amounts of loose organic detritus,
dead clam shells and stones, all of which
increased in quantity.

Snail densities at transect “d” on July 9-
11, 1970, are shown in Fig. 6a. Most
notable were the high densities—reaching
more than 50/m? at 1.4 depth—of
Helisoma antrosa in a relatively narrow

386 Р. T. CLAMPITT

a 15 Physa integra
3 Stagnicola
emarg. angul.
N
>=
10 Helisoma
>
anfr-perc.
п
—
< Не! 15 ота
zZ campanulata
un
© 5
Z

FROM

Transect c.

July 12 - 16, 1969

65 100 150

SIHIORE,

LS

METERS

Ss

FIG. 5. Transect “c” quantitative data, North Fishtail Bay area. a, numbers (average and range) of
adult snails per m? in July 1969. b, bottom profile and substratum characteristics (see also Fig. 4).

zone, 132 to 147 m from shore at depths of
1.2-1.5 m. As indicated above, the sand
was covered with increasing amounts of
loose organic detritus, dead clam shells
and stones as depth increased from 1.0 to
1.6 m. Also, in what was otherwise a flat
shoal area, the zone of greatest abundance
of snails of this species was in the area
which sloped downward relatively rapidly.
In contrast, H. campanulata was dis-
tributed rather evenly and much more
sparsely along transect “4.” The соп-
trasting distributions of these 2 congeneric
species suggests that they may differ con-
siderably in their behavior and ecological
requirements.

LABORATORY EXPERIMENTS
METHODS

The procedures described here were
designed to test experimentally the
behavior of the snail species on which
quantitative field data had been obtained,
as this behavior pertained to the character
of the substratum and to potential sources
of food associated with different sub-
stratum types.

The basic experimental chamber was an
oval-shaped plastic container, 50 x 30 cm;
the bottom of one half was covered with a
layer of stones and the other with a layer of
sand 2 cm deep (Fig. 7). Space was left in

SUBSTRATUM AND FRESHWATER SNAILS 387

the center of the chamber for insertion of a
dish 8 cm in diameter; this would contain
the snails released at the beginning of an
experiment. The chamber was filled to a
total depth of 10 cm with lake water.
Water temperatures averaged 21.3°C
(range, 19°-24°C). Overhead fluorescent
lights provided continuous, uniform il-
lumination of moderate intensity (averag-

a 60 Transect d.

50

S Helisoma
= =
antr. erc.
~ 40 Р
п
> Helisoma
O campanulata
Zz
п
о 20
7
10
0
DEPTH»; 0.45 0105. 058 Ir
M
er 15 60 90 120

en

2 50
DISTANCE

оу 9 = Pl

FROM

ing 100 footcandles) in the experimental
chamber.

At the beginning of each experiment, a
dish containing water and 20-50 snails of a
single species—the number depending on
the size of the species—was placed in the
center of the chamber. After Y hour,
locations of all snails—whether on stones,
sand, or elsewhere—were recorded at 15-

1970

100 150
SHORE, М

FIG. 6. Transect “d’ quantitative data, Big Shoal. a, numbers (average and range) of adult snails
per m2. b, bottom profile and substratum characteristics.

388 Pt. CLAMPITT

Rete

STONES SAND

K 50 cm А

FIG. 7. Experimental chamber for substratum
preference experiments.

minute intervals for a 14-hour period,
after which the experiment was ter-
minated.

From these data on locations of snails at
different time intervals, computations
were made of the average numbers of
snails located on stones and on sand during
the course of an experiment. Enough
replicate experiments were done on each
species so that experimental data from at
least 200 snails of that species—yielding
some 1200 position recordings in all—were
obtained in a particular set of experiments.
Individual snails were used only once in a
set of experiments.

To test the response of the snails to sub-
strata including as well as excluding a
potential source of food (similar to that
available in the lake), 4 sets of experiments
were done on each species, as described
above, with the following variations:

(1) washed stones vs. washed sand (no

food on either);

(2) algae-covered stones vs.
sand (food on stones only);

(3) washed stones vs. sand with an algal
crust or layer of organic detritus
(food on sand only);

(4) algae-covered stones vs. sand with
algal crust or organic detritus (food
on both stones and sand).

The washed stones were obtained initially
from dry land above the lake; other sub-

washed

stratum materials—with and without
food—were collected from the lake itself,
in areas where 1 or more of the species un-
der study also lived successfully.

RESULTS

The data from these experiments are
presented in Fig. 8 as follows: in “a,” the
snails were given a “choice” between
washed stones and washed sand; in “b,”
between algae-covered stones and washed
sand; in “c, between washed stones and
sand with an algal crust or layer of organic
detritus; and in “d,” between algae-
covered stones and sand with an algal crust
or layer of organic detritus.

Fig. 8a reveals, in Physa integra, a
decidedly more positive orientation
toward the stones than toward the sand
when food was absent from both—21%
compared with 8%, on the average.
Helisoma antrosa percarinata, in contrast,
showed an average distribution of 28% on
the sand and 15% on the stones. The dif-
erences within both species were signifi-
cant; for P. integra, p<.01 and for H. an-
trosa, p<.05.* It will be noted that well
over 50% of the snails of all 5 species were
neither on the stones nor on the sand in
this experimental situation. Some of these
snails—here and in other sets of ех-
periments—moved along the sides of the
experimental chamber, some crawled on
the water surface film, some crawled on
the backs of other snails, and some remain-
ed in or returned to the central dish from
which they had been “released.”

Fig. 8b reveals rather clearly the
tendency of most of the species to concen-
trate most heavily on stones when food was
present there but lacking from the sand.
This tendency was most pronounced in the
2 Physa species; the average distribution of
P, integra was 56% on stones and only 2%
on sand, and in P. parkeri, 61% on stones
and 5% on the sand. In both species, the
differences were highly significant;
p<.001. In contrast, an average of 32% of
the Helisoma antrosa were on the algae-
covered stones as compared with 25% on

4 Tests of significance were done using the t distribution.

SUBSTRATUM AND FRESHWATER SNAILS

the washed sand. This difference was of
doubtful significance; .4>p>.3.

When food was present on the sand, but
not on the stones (Fig. 8c), only Physa in-
tegra continued to show a“ preference’ for
the stones, averaging 27% as compared
with 17% on sand; this preference was of

389

responding figures for P. parkeri were 18%
and 24% (of borderline significance,
.2>p>.1). Those for Helisoma antrosa
were 16% on stones and 42% on sand, and
for H. campanulata, 15% and 39%, respec-
tively. Both of these latter were signifi-
cant; p<.005 for H. antrosa and p<.001

doubtful significance; .3>p>.25. The cor- for H. campanulata. (No data were
STONES SAND
Year oft total
аи» 80 60 40 20 0 20 40 60 80
ol T | И
pied iid) CRC
Pee: AG HTT + wn
О ея. ES
food food
Het ars pos Ss
Н. с. A
Pls i NE
Pos COR СС СС es
Ев АА 23
food
H. a. p. food К ES
Н. с. ES
Pha Für, HER
PAGE no HI food
C
H. a. p. food A
He EAU
eee UE
d Bi tp); UC food
H. p. food К
Е. SMC

let total
population

80 60

80

20

FIG. 8. Substratum preference, as revealed by laboratory experiment, in 5 species of snails (in-
dicated by initials: P. i. = Physa integra, etc.). Data are given as percentages of the total population
situated on stones (to left of heavy vertical line) and on sand (to right of this same line); horizontal
bars represent mean distribution, and horizontal lines—extending into and from the bars—the
range of distribution within a set of experiments. No population totals 100% because some snails, at
any one time, were neither on stones nor on sand, but were located elsewhere in the experimental
chamber (see text). Each bar represents the collective distribution of 200 snails over a 12-hour
period, involving some 1200 position recordings. Numbers of snails used in a single experimental
replicate were: Physa integra, 50; P. parkeri, 20; Stagnicola emarginata, 25; Helisoma antrosa, 40;
Н. campanulata, 40. Four sets of experiments (a through d) were done, using stones and sand with

or without food in 4 combinations.

390 P. T. CLAMPITT
STONES SAND
a EE | | = | т | | 1 T T T a]
PHYSA INTEGRA

no food

food KKK

Boe i ATT

по food

food ЕО

HELISOMA ANTR. РЕКЕ.

по food

food КК
по food tl:
food KE

a E A eS he GR à LR |!

sa
WLW LON mye

к] по

80 60 40 20

% of total population

FIG. 9. Substratum preference, in the laboratory, of the 2 most common and abundant of the larger
pulmonate snails of Douglas Lake, Physa integra and Helisoma antrosa percarinata (the same data,
differently grouped, as given for these 2 species in Fig. 8).

collected for 5. emarginata in this or the
following set of experiments because living
specimens were unavailable. )

The most meaningful comparisons
among species are provided in Fig. 8d,
where food was present both on the stones
and on the sand. This probably best
reflects the usual situation in nature where
both substratum types are available. Both
Physa species exhibited a clear preference
for the algae-covered stones even when
food was also present on the sand; for P.
integra, the averages were 58% of the snails
on stones, 8% on sand; in P. parkeri, 55%
and 12%, respectively. Both “ preferences’
were highly significant; p<.001. Under
these same conditions equal numbers of
Helisoma campanulata gathered on stones
and on sand—29% on each. On the other
hand, 39% of H. antrosa gathered on the
sand, as compared with 24% on the stones.

This difference was significant; p<.02.
Results of the substratum “preference”
experiments on Physa integra and
Helisoma antrosa are presented separately
as Fig. 9, which shows the contrasting
behavior of these 2 species over substrata
of stones and sand. In all 4 sets of
experiments P. integra showed а “pref-
erence for stones over sand, especially in
experiments where food was present in the
stones. Helisoma antrosa showed “‘pref-
erence for the stones over the sand (32%
to 25%) only when food was present on the
stones and absent from the sand, and even
this behavior was subject to considerable
variation (and is of doubtful significance;
.4>p>.3). The apparent preference by P
integra for stones and of H. antrosa for
sand was consistent with the patterns of
distribution of these species in the field
(Figs. 2-6). The other 3 species studied all

SUBSTRATUM AND FRESHWATER SNAILS 391

appeared to have somewhat more varied
patterns of distribution in the field rela-
tive to substratum, and their behavior in
these laboratory experiments (Fig. 8) was
similarly variable.

DISCUSSION

The data presented in this study show
that Douglas Lake populations of Physa
integra and Helisoma antrosa percarinata
present contrasting distributions as to sub-
stratum; adult P. integra prefer stones,
while sand is preferred by H. antrosa.
Laboratory experimental data confirm
these findings. These 2 species are
“specialists, to a greater degree than are
the other 3 species studied, in utilizing 2
types of substratum—stones and sand,
respectively,—both of which are amply
available in Douglas Lake. Not surprising-
ly, therefore, these 2 species are the most
common and abundant of the larger
pulmonate snails in the lake.

Physa parkeri, Stagnicola emarginata
angulata, and Helisoma campanulata are
also widespread in their distribution in
Douglas Lake, but their numbers are
fewer, and they are less clearly identifiable
with particular substratum types. P.
parkeri was widely dispersed over both
stones and sand in the field; in the
laboratory, however, it revealed a strong
preference (closely paralleling that of P.
integra) for stones when food was present
there. From field and laboratory data
taken together, I conclude that all 3 of the
above species are more “generalists” in
their behavior with regard to substratum.
Broad sandy shoal areas, frequently inter-
spersed with stones and other hard sur-
faces, again provide very suitable habitats
for these 3 species at widespread locations
in Douglas Lake.

It is beyond the scope of this paper to
review the literature as it relates to the
various habitats and substratum types oc-
cupied in other bodies of water by the
species studied here. A few examples will
suffice to illustrate the difficulty of
generalizing on the subject. Physa integra,
for example, has been reported from a
variety of types of habitats—creeks, rivers,

brooks, and lakes—on boulders, gravel,
sand, clay, mud and on vegetation (F. C.
Baker, 1928; Goodrich, 1932; Goodrich &
van der Schalie, 1939, 1944; Dawley, 1947;
Clampitt, 1970). P. parkeri has been
reported only from Michigan and only
from a few lakes, inhabiting both sheltered
bays and open or exposed areas (Baker,
1928; Goodrich, 1932; Cheatum, 1934).
Stagnicola emarginata has been found (in
Lake Huron at Mackinac Island) “in
numbers on stones, weedy boards, and
wharf supports close to the surface”
(Goodrich, 1932). Stagnicola emarginata
angulata, according to Cheatum (1934), is
“ordinarily found in exposed littoral
regions, clinging tightly to rocks, or buried
in the sand or mucky bottom.” Helisoma
antrosa, according to F. C. Baker (1928), is
“primarily a river and creek species, not
living in the large lakes’; Dawley (1947),
however, reports that it is very common in
both lakes and rivers in all parts of
Minnesota, and Goodrich (1932) reports
similar habitats for the species all over
Michigan. Goodrich € van der Schalie
(1939) report that this species occurs in
brooks, creeks, rivers, lakes and ponds in
Michigan's Upper Peninsula. Goodrich
(1932) adds: “It may be found clinging to
sticks and stones. In the Great Lakes, it has
exploited a feeding ground of diatoms and
algae on concrete piers and pine spiles. It
can endure the heavy pressure of water in
swift rapids.” Baker (1928) describes H.
antrosa percarinata as “a form of large,
deep lakes or bays of larger lakes. On the
shore of Sturgeon Bay [Wisconsin] it oc-
curs in deep water on rocks near shore.”
Of the same form, Cheatum (1934) states
that it “occurs widely in lakes,’ and is
“found in sheltered vegetation zones and
in exposed littoral regions. ” Baker (1928)
describes typical H. campanulata in
Wisconsin as a species of lakes, with
habitat situations including rock bottom,
sand bottom with vegetation, submerged
logs, and mud bottom in a marshy area, in
water varying from .3 to 1 m deep.
Goodrich & van der Schalie (1944) state
that this species is “apparently intolerant
of domestic sewage and in course of dis-

392 P. T. CLAMPITT

appearance in Indiana. Cheatum (1934)
says of H. campanulata smithi that it is
“commonly found in exposed areas of
Douglas Lake; frequently in sheltered
situations. |

From the above, it can be concluded
that there is considerable adaptive plastici-
ty in most of these species which, as
emphasized by Hunter (1961, 1964), is
characteristic of freshwater snails general-
ly. Therefore, what applies for a particular
species in one aquatic situation may not
necessarily apply for the same species in
other situations. Conclusions from this
study pertain specifically to Douglas Lake,
and are likely to be generalizable only in
part to other bodies of water.

Some anatomical and behavioral
peculiarities—as these pertain both to sub-
stratum and depth distribution—of certain
of the Douglas Lake species should be
noted. The shells of Helisoma cam-
panulata smithi in Douglas Lake are
characterized by a “sculpture of coarse
riblets”” (Е. С. Baker, 1928). As a result of
this structural reinforcement, the shell of
adult specimens is extremely durable; this
is evidenced by the large proportion of
dead shells of this species which remain
unbroken when washed ashore, in con-
trast with the broken fragments of shells
left behind by most other species. Fair
numbers of living H. campanulata (e.g., at
transects “с” and “d,” Figs. 5 & 6) were
often found in very shallow water on a
sand substratum; when wave action was
heavy, the living animals often could be
seen to be buffeted about by the waves,
without any apparent ill effects. In con-
trast, the shells of H. antrosa percarinata
are rather fragile and easily broken, es-
pecially during periods of rapid growth of
the animals. The densest, and apparently
healthiest, populations of this species were
in areas protected in 1 of 2 ways: either (1)
wave action was usually slight (as at
transect “b,” Fig. 3), or (2) in the more ex-
posed areas (such as the Big Shoal, transect
“d,” which was often disturbed by heavy
wave action generated by the prevailing
westerly winds), the snails were in water 1
m or more deep where the substratum suf-

fered little disturbance even on the win-
diest days. Another contrast between the 2
Helisoma species concerns their behavior.
Helisoma antrosa frequently exhibited a
tendency to burrow into the sand,
demonstrated both in the laboratory and
in the field. Burrowing at times of es-
pecially heavy wave action could confer
survival value on this species by pre-
venting the snails from being tossed about
by the waves and thereby damaged. None
of the other snails studied showed any pro-
nounced tendency to burrow.

Adult Physa parkeri appeared to survive
successfully in shallow water zones which
were at least occasionally subject to fairly
heavy wave action, even though their
shells are rather thin and fragile for such a
large snail. At transect “а” in South
Fishtail Bay, fair numbers of adult P.
parkeri were present on the stones near
shore and in adjacent sandy areas in late
spring and early summer, where they laid
large numbers of eggs. Few young of this
species appeared to develop in these areas,
however, in contrast to P. integra. The
shells of young P. parkeri are extremely
thin and fragile and are probably unable to
withstand the frequently heavy wave ac-
tion on this and similar shores. On the
other hand, many individuals of this
species were seen to develop very rapidly
in off-shore sandy areas where the water
was deep enough so that the effects of
wave action were slight. Such populations
of juveniles were found at transect “c”
during the summer of 1969 (water depth 1
m or more), and at transect “d” on the Big
Shoat (water depth about 1.5 m), both in
1970 and 1971. In contrast, juvenile pop-
ulations of the much smaller, slower-
growing and less fragile P. integra seemed
to thrive best on the rocks adjacent to
shore (e.g., at transect “a” in South
Fishtail Bay), even though exposed fre-
quently to moderately heavy wave action.

Brief consideration should be given to
the relationship between substratum and
food in the Douglas Lake snails. The clas-
sification by Fox (1960) of marine detritus
feeders into “filterers,” “scrapers” and
“shovelers” is pertinent. Physa integra, as

SUBSTRATUM AND FRESHWATER SNAILS 393

an inhabitant of stones and other hard sur-
faces, could be expected to feed primarily
by scraping edible materials—algae and

associated SAufwuchisi and
detritus— from these surfaces. Helisoma
antrosa, on the other hand, with its

preference for a sandy substratum, might
be more adapted to “shoveling” in the
loose detritus—with its contained
nutrients— which is more characteristic of
its habitat. However, laboratory observa-
tions suggest that both species are capable
of both “scraping” and “shoveling.
Furthermore, examinations of the crop
and stomach of 20 or 30 snails of each of
the 5 species, collected from various
locations, fail to give a clear picture of
selective feeding in any of the species.? It
is not clear whether the slight anatomical
differences in the jaw and radula of these
and other freshwater pulmonate snails (F.
C. Baker, 1928) are significant in feeding.
Also it remains unclear whether the type of
substratum is of greater importance
nutritionally or for reasons relating to
other aspects of the ecology of the various
species. The problem of the relationship
between substratum and food merits
further study.

As for the role of the substratum in pro-
viding oviposition sites, some kind of solid
surface is required by all 5 species for the
deposition of eggs. In both Physa species
and in Stagnicola, stones, sticks, dead
leaves, clam shells, and the shells of other
living snails were all found to be accept-
able sites. Somewhat surprisingly, an addi-
tional acceptable site was the “crust” of
consolidated sand grains, overlain by alee)
growth, which appeared at transect
(Fig. 4) at about 1 m depth during ve
summer of 1969, and which has been
observed during the summer months in ex-
tensive zones on the Big Shoal and else-
where. The 2 Helisoma species utilize sites
similar to those used by the other species,
except that stones with rough surfaces
seem to be unacceptable. On the other

hand, both Helisoma species were es-
pecially prone to deposit their eggs on the
shells of other living snails, of their own or
other species. In sandy areas with few
other sites appropriate for oviposition—a
type of habitat where both the Helisoma
species were frequently found—this
behavior could have adaptive value for the
species, providing a stable surface on
which the embryonic snails can develop
successfully to the hatching stage.
Distribution both as to substratum and
depth has a bearing on the supposed
respiratory requirements of aquatic
pulmonate snails. Hyman (1967, p 625)
repeats the widely held view that
freshwater pulmonates ‘‘or-
dinarily .. . require access to air and die if
kept submersed.” If this were true
generally of lake pulmonates, they could
probably live only in areas where stones,
emergent plants, or other stable surfaces
were available on which they could crawl
upward periodically to reach the water sur-
face for breathing air. None of the 5
species of this study was so restricted in its
distribution. I therefore conclude that the
supposed need for atmospheric oxygen is
greatly exaggerated. There is good
evidence that many lake pulmonates are
well-adapted for remaining submerged,
and that the mantle cavities of these snails
may often be filled with water, rather than
air, throughout their life cycles (Cheatum,
1934; Hunter, 1953, 1964; Clampitt,
1970). I found that Douglas Lake pop-
ulations of adult Helisoma antrosa and H.
campanulata, living in water either 0.5 or
5.5 m deep, had the mantle cavities filled
with water. The same was true of adult
Physa integra living on vegetation at 3 m
depth in an Iowa lake (Clampitt, 1970). It
is undoubtedly true also of many Douglas
Lake populations of P. integra, P. parkeri,
and Stagnicola emarginata, although
further study is required to confirm this.
This is not to say that pulmonate snails
from lakes will not come to the surface and

5 The stomach contents of each species included sand grains (1% to more than 90%), algae (including diatoms,
blue-greens, various unicellular and colonial green algae), moss leaflets, pine pollen, animal material (rotifers,
parts of small crustaceans and insects, oligochaete annelids, etc.) and organic detritus.

394 Р. T. СБАМРИТ

take on atmospheric oxygen when placed
in the shallow water and restricted space of
a laboratory aquarium, or in the field when
they occur on stones which protrude out of
water adjacent to shore, as at transect “a”
along the shore of South Fishtail Bay. Few
situations in lakes, however, provide such
convenient access to the water surface.
There is little evidence that lake-dwelling
populations of pulmonates (except those
living in very shallow water adjacent to
shore or on emergent vegetation) make
periodic trips to the surface for breathing
air. As long as the dissolved oxygen supply
is adequate, the snails can apparently ob-
tain adequate oxygen for their respiratory
needs by direct diffusion through the in-
tegument. In planorbid snails, such as the
Helisoma species, the development of a
pseudobranch aids the process of aquatic
breathing (Е. С. Baker, 1945; Hunter,
1957).

Large annual variations in densities of
certain species, notably Helisoma antrosa
and Stagnicola emarginata, are evident
from the study. Helisoma antrosa showed
a dramatic decline in numbers at transects
“a, “b” and “ce between 1969 and 1970;
unpublished data from the spring and
summer of 1971 reveal a partial reversal of
this trend at transect “a.” At transect “d”
on the Big Shoal, the very high densities of
Н. antrosa (up to 50 per m?) in a well-
defined zone in 1970 (Fig. 6) were not
maintained in that zone in 1971, although
numbers of this species apparently did in-
crease greatly during 1971 in areas 230 to
300 m from shore at the same transect (un-
published data). The drop in population
density of H. antrosa along transect “d”
between 1970 and 1971 was accompanied
by increases in densities particularly of
Physa parkeri, but also of P. integra and H.
campanulata, in the same area. Stagnicola
emarginata was a common species at
transects ‘а’ and “с” in 1969, with den-
sities of from 1-5 snails/m? not being un-
common. In 1970, this species could be
characterized as very rare not only in these
areas but apparently throughout the lake.
During the 1971 season, numbers of S.
emarginata were again on the increase.

The causes of these fluctuations in popula-
tion density are not clear. The fact that in
H. antrosa they were local in extent, in-
volving only limited areas in the lake at
any | time, while in S. emarginata they ex-
tended throughout the lake, suggests
different causes for the fluctuations in
these 2 species. A 10-year study by Hunter
(1961) of annual variations in growth and
density of natural populations of fresh-
water snails in Scotland indicates that
short-term fluctuations in density are not
uncommon even in stable populations, and
also that such variations are useful as an in-
dex of benthic productivity. Hunter at-
tributed the fluctuations in 3 pulmonate
snail species to the severity of winter con-
ditions. In Douglas Lake, changes in lake
level (relating to precipitation) and the oc-
casional occurrence of severe storms which
could so disturb the substratum as to cause
considerable mortality among certain snail
species, are among the climatic factors
which must be considered. Biological fac-
tors, including life histories of the various
species (on which studies are now in
progress), possible seasonal movements
(also being studied), predation, parasitism,
and intra- and interspecific competition
must also be considered.

There is evidence that long-range
changes in the molluscan fauna of Douglas
Lake have occurred, although earlier
quantitative data are largely lacking. H. B.
Baker (1914) reported on the mollusks of
lake pools and in Douglas Lake itself, giv-
ing descriptive terms such as ‘abundant, ”
“common, “frequent” and “rare to in-
dicate relative densities. The species of the
present study were apparently among the
more common and abundant species of
Baker s studies in similar habitats. A proso-
branch snail, Goniobasis livescens, former-
ly absent from Douglas Lake but native to
nearby lakes (Baker, 1912), was sub-
sequently introduced and is now abundant
and ubiquitous; this species, through in-
terspecific competition, could have had a
depressing effect on the numbers of some
pulmonate species. Moffett (1943) made a
quantitative study of the bottom fauna of
the Big Shoal, which included data on

SUBSTRATUM AND FRESHWATER SNAILS 395

pulmonate snails. His findings that both
Helisoma species were “not typical” and
“very rare” in this area do not correlate
with those reported here, especially in the
case of H. antrosa (Fig. 6). This could in-
dicate either that during the particular
year of his studies the numbers of these
particular species were unusually low, or
that the Big Shoal has changed dramatical-
ly in the intervening 28 years. This appears
quite probable in the light of a recent
report by Bazin & Saunders (1971) which,
on the basis of a gradual but steady in-
crease in the hypolimnetic oxygen deficit
in Douglas Lake during the past 50 years,
indicates that the lake has very gradually
become more eutrophic. Such а trend
could be expected to involve an increase in
littoral benthic productivity, reflected (in
part) by an increase in biomass of
pulmonate snails (Hunter, 1961) in the Big
Shoal area and elsewhere.

- А comparison of the distributions of
Physa integra in Douglas Lake and in Lake
West Okoboji (and other lakes nearby) in
Iowa (Clampitt, 1970) is of considerable
interest and of possible significance. In
both lakes, populations of this species were
concentrated in summer in a zone of
cobbles adjacent to shore. Other pop-
ulations in Lake Okoboji, away from shore,
were found almost exclusively on sub-
merged vegetation—Ceratophyllum,
Myriophyllum, various species of
Potamogeton, etc.; the snails appeared to
avoid substrata of sand and silt. In Douglas
Lake, in contrast, nearly all of the P. in-
tegra which were found in somewhat
deeper water (0.5 to 5.0 m deep) away
from shore were on the bottom—on
stones, submerged logs, dead shells, dead
leaves and often on sand—and very few on
living vegetation. This species illustrates
what appears to be a more general con-
trast between the distributions as to sub-
stratum of Lake Okoboji and Douglas
Lake snails. In Lake Okoboji, nearly all
snails of all species living in deeper
water—0.5 m or more—were on vege-
tation whereas in Douglas Lake, they were
nearly all on the bottom. This contrast was
observed independently by a colleague,

Dr. Eugene Stoermer (personal com-
munication) who has done extensive
SCUBA diving in both lakes. I believe that
the relative progress of cultural (i.e., man-
caused) eutrophication in the 2 lakes gives
at least a partial explanation for this con-
trast. Lake Okoboji gives evidence of be-
ing much more eutrophic. Bovbjerg €
Ulmer (1960) reported a drastic decline in
species diversity among gastropod mol-
lusks over a 45-year period in Lake
Okoboji. These investigators noted par-
ticularly the apparent elimination of a
number of species of lymnaeid snails and
of planorbids of the genus Helisoma, since
earlier studies in the area by Shimek (1915,
1935). Among some 11 species of gas-
tropods found in Lake Okoboji in 1960,
only Physa gyrina and P. integra were pre-
sent in really large numbers at widespread
locations in the lake. The decline of the
gastropod fauna was attributed to the
progressive pollution and eutrophication
of this very popular and heavily used lake.
A similar but less drastic decline in the
molluscan fauna of Oneida Lake, New
York, has been reported recently by Har-
mon & Forney (1970), and attributed to
similar causes. Douglas Lake has been
much less subject to human influence dur-
ing the same interval of time, and if
cultural eutrophication has been oc-
curring, as suggested by the work of Bazin
& Saunders (1971), it has been much more
gradual and subtle in its effects. Certainly
the gastropod fauna of Douglas Lake has
not suffered the kind of depletion which it
has undergone in Lake Okoboji. As has
been already suggested, some species,
such as H. antrosa, may actually have in-
creased in biomass in certain areas such as
the Big Shoal, reflecting increased benthic
productivity associated with the very
gradual eutrophication. It seems reason-
able to suppose that the more rapid
eutrophication of Lake Okoboji has led to
changes in the substratum through in-
creased growth of submerged vegetation,
increased quantities of silt in vegetated
zones, reduced productivity by microflora
on the bottom, a corresponding increase in
organic decomposition and consequent

396

reduction in the dissolved oxygen supply
on the bottom. With such changes oc-
curring in more and more of the littoral
regions of the lake, only those species of
snails which are already adapted to living
on the vegetation, or are able to success-
fully make the transition from the bottom
to the vegetation, or are adapted to con-
tinued life under anoxic conditions on the
bottom, will survive. All others will be-
come locally extinct. It seems reasonable
to speculate that P. integra successfully
made the transition from the bottom to the
vegetation in Lake Okoboji, whereas most
of the larger lymnaeid and planorbid
species which were formerly represented
in the lake did not. The questions which
this idea raises warrant further descriptive
and experimental studies on mollusks in a
variety of lake habitats.

ACKNOWLEDGEMENTS

I am grateful to Dr. Warren L. Wittry,
Director of Cranbrook Institute of Science,
and the Board of Trustees of the same in-
stitution, not only for their encouragement
and support of this work, but also for their
generosity in allowing me time away from
the Institute. I wish to thank Dr. Frederick
K. Sparrow, Jr., recently retired as Direc-
tor of the University of Michigan
Biological Station, for providing me with
the opportunity to do research there. Mr.
Michael Gambel, Mr. Marc Harrison and
Mr. Thomas Pinson all gave valuable
assistance with the field work. I am in-
debted to others, notably Dr. Bruce Z.
Lang (University of Michigan Biological
Station and Eastern Washington State
College) and Dr. Henry van der Schalie
(University of Michigan), for their un-
failing interest and encouragement. Dr. V.
Elliott Smith, Cranbrook Institute of
Science, kindly read and offered helpful
criticism of the manuscript.

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20.

ZUSAMMENFASSUNG

DAS SUBSTRAT ALS VERBREITUNGSBESTIMMENDER FAKTOR FUR
LUNGEN-SCHNECKEN IM DOUGLAS LAKE, MICHIGAN

Р. Т. Clampitt

Dem Substrat als verbreitungsbestimmendem Faktor fiir 5 Lungenschnecken-Arten
aus dem Douglas Lake, Cheboygan County, Michigan, wurde eine Studie gewidmet.
Quantitative Aufsammlungen am natürlichen Standort, zusammen mit Laborversuchen,
ergaben, daß adulte Physa integra Haldeman Hartsubstrate wie Steine bevorzugen; im
Gegensatz dazu bevorzugen adulte Helisoma antrosa percarinata (Walker) sandiges
Substrat. Wenn im Laborversuch Nahrung (Algen oder Detritus) sowohl auf Steinen als

398

P/ T° CLAMPITT

auch auf Sand vorhanden war, war die durchschnittliche Verteilung von P. integra: 58%
auf Steinen und 8% auf Sand (Unterschied hoch signifikant), während in entsprechenden
weiteren Experimenten mit H. antrosa sich im Durchschnitt 24% auf dem Steinsubstrat
und 39% auf dem sandigen einfanden (Unterschied ebenfalls signifikant). Physa parkeri
“Currier” DeCamp, Stagnicola emarginata angulata (Sowerby) und Helisoma cam-
panulata smithi (Baker) zeigten in der Natur komplexere und unterschiedlichere Ver-
breitungsmuster, was das Substrat betrifft. Im Labor zeigte P. parkeri, sehr ähnlich wie
P. integra, eine Präferenz für steiniges Substrat, wenn Nahrung vorhanden war. H. cam-
panulata war im Durchschnitt zu 29% auf Steinen und zu 29% auf Sand verteilt, wenn
beide Substrate Nahrung enthielten. Beziehungen bei den 5 Arten zwischen Substrat
zum einen und Tiefe, Wellenschlag, Nahrung, Ablaichsubstrat und respiratorischen An-
forderungen zum anderen werden diskutiert.

C.M.-B.

RESUME

LE SUBSTRAT, FACTEUR DE DISTRIBUTION DES MOLLUSQUES
PULMONES DANS LE LAC DOUGLAS, MICHIGAN

P. T. Clampitt

On a réalisé une étude sur le substrat considéré comme facteur de distribution pour 5
espéces de pulmonés du lac Douglas, Cheboygan County, Michigan. Des échantillon-
nages dans la nature, en méme temps que des expériences au laboratoire ont révélé que
les adultes de Physa integra Haldeman preferent les substrats durs tels que les pierres; au
contraire, les adultes d’Helisoma antrosa percarinata (Walker) préférent un substrat
sableux. Quand de la nourriture (algues et détritus) était présente а la fois sur le sable et
sur les pierres, au laboratoire, la moyenne de P. integra a été de 58% sur les pierres et de

% sur le sable (différence hautement significative), tandis que dans une experience
équivalente mais séparée, une moyenne de 24% de H. antrosa se trouvait sur les pierres et
de 39% sur le sable (significatif aussi). Physa parkeri “Currier” Decamps, Stagnicola
emarginata angulata (Sowerby) et Helisoma campanulata smithi (Baker) ont tous montré
des types de distribution plus complexes et plus variés vis-à-vis du substrat dans la
nature. Au laboratoire, P. parkeri a montré une préférence pour le substrat pierreux trés
similaire а celle de P. integra quand la nourriture était présente. La distribution moyenne
de H. campanulata était de 29% sur les pierres et aussi de 29% sur le sable quand la
nourriture était présente sur chacun d'eux. On aussi discuté, pour les 5 especes, des
relations entre, d'une part le substrat et d’autre part: la profondeur, l'action des vagues,
la nourriture, les lieux de ponte et les besoins respiratoires.

A.L.

RESUMEN

EL SUBSTRATO COMO FACTOR EN LA DISTRIBUCION DE CARACOLES
PULMONADOS, EN EL LAGO DOUGLAS, MICHIGAN

P. T. Clampitt

Se estudiö el substrato en el Lago Douglas, condado de Cheboygan, Michigan, como
un factor en la distribuciön de cinco especies de pulmonados. Muestras cuantitativas y
experimentos en laboratorio revelaron que los adultos de Physa integra Haldeman,
prefieren substratos duros, de piedra; contrariamente, Helisoma antrosa percarinata

SUBSTRATUM AND FRESHWATER SNAILS

(Walker) prefieren fondos de arena. La presencia de alimento (algas o detritos) sobre las
piedras о arena mostró, en el laboratorio, un promedio de 58% en la distribución de P. in-
tegra en piedras y 8% en la arena (diferencia muy significativa), mientras que en otros
experimentos, equivalentes pero separados, H. antrosa mostró solamente 24% de
preferencia por piedras, y 39% de arena. Р. parkeri “Currier” DeCamp, Stagnicola
emarginata angulata (Sowerby) y Helisoma campanulata smithi (Baker) tienen patrones
de distribución más complejos y variados con respecto a los substratos naturales. En el
laboratorio P. parkeri mostró preferencia por un substrato de piedra, muy similar al de P.
integra cuando habia alimento presente. El promedio de distribución de H. campanulata
fue de 29% en piedras y tambien 29% en arena cuando ambos ofrecian alimento.
Relaciones de las cinco especies entre substratos por una parte, y produndidad, acción de
oleaje, alimento, sitios de ovoposición y necesidades respiratorias por la otra, se discuten
en el trabajo.

J.J.P.

ABCTPAKT

CYBCTPAT, КАК ФАКТОР, ВЛИЯЮ НА РАСПРОСТРАНЕНИЕ
МОЛЛЮСКОВ PULMONATA
В ОЗЕРЕ ДУГЛАС, МИУИГАН

П.Т. KISMIMT

Изучался субстрат, как фактор, влияющий на распространение 5 видов
моллюсков из Pulmonata (озеро Дуглас, Чебойган, Мичиган). Сбор
количественных проб, вместе с лабораторными экспериментами показал, что
взрослые Physa integra Haldeman предпочитают твердый субстрат (камни);
взрослые Helisoma ат тоза percarinata (Walter), напротив, предпочитют песок.
Если пища (водоросли или детрит) имелись в лабораторных условиях или на
песке, среднее распространение P. integra составляло 58% на камнях и 8% Ha
песке (очень значительное различие), в то время как в отдельных
эквивалентных экспериментах, в среднем 24% Н. antrosa были на камнях и 30%
- на песке (различия также значительные). Physa parkeri “Currier”? DeCamp,
Stagnicola emarginata angulata (Sowerby) и Нейзота campanulata smithi (Baker) все
имеют более сложное и изменчивое распространение, связанное не только с
природным субстратом. В лабораторных условиях Р. parkeri предпочитает
каменный субстрат, подобно Р. integra (если пища имеется). В среднем,
распространение H. campanulata на 29% связано с камнями и на 29% - ec
песком, если пища имеется тут и там. В статье обсуждается отношение 5
видов моллюсков к субстрату, глубине, действию волн, пище, местам
откладки яиц и потребностям дыхания.

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INDEX TO SCIENTIFIC NAMES

abbreviata, Coralliophila, 315, 329
Abra, 6, 47, 77
aequalis, 47, 77
abyssicola, Volutocorbis, 309, 310
Achatina, 168, 189, 206, 207
Actinonaias, 97-113
cavinata, 97-113
ligamentina, 100
acuta, Paludomus, 134
adamsi, Seila, 27, 30, 39, 40
Adula, 269, 272, 273, 274, 277
adusta, Ampullaria, 349
adustus, Penion, 314, 321
aequalis, Abra, 47, 77
Aequipecten, 39, 40
irvadians, 39, 40
Aetheria, 369
elliptica, 369
Aforia, 310
goodei persimilis, 310
Agriolimax, 206
albula, Maoritomella, 305
Alcithoe, 301, 310, 315, 316, 318, 319, 321
arabica, 301, 310, 315, 316, 319, 321
Alectrion, 313
aoteanus, 313
alexandrina, Biomphalaria, 115-122
alexandrina watsoni, Biomphalaria, 115-122
alluaudi, Planorbis, 365
alluaudi, Tropidiscus, 365
alternatum, Bittium, 24-30, 39, 40
amaena, Cleopatra, 351, 352
Amalda, 304, 310, 313
australis, 310, 313
amarula, Helix, 359
amarula, Melania, 359
amarula, Thiava, 359, 360
ambiguus, Xymene, 310
Amblema, 97-113
plicata, 97-113
Ameria, 364
lirata, 364
americanus, Modiola, 284, 291
amouretta, Harpa, 310
Ampelisca, 21, 38
Amphipholis, 39, 40
squamata, 39, 40
Ampullariidae, 123, 124, 175, 186, 187, 188,
189, 206, 207
Ampullaria, 124, 125, 146, 147, 168, 186-189,
205-207, 348-350
adusta, 349

canaliculata, 124, 125, 146, 147, 168, 189, 205

cecillii, 349, 350
depressa, 124, 205, 206
filosa, 350
gigas, 147, 187-189, 205, 206
gvasseti, 348, 349
hanleyi, 349
largillierti, 349
madagascariensis, 349
ovum, 349
polita, 124, 147, 186, 188
simplex, 349
subscutata, 349
urceus, 187, 189
Amygdalum, 50, 51, 54, 64, 65, 88, 91
papyrid, 50, 51, 54, 64, 65, 88, 91

(401)

Anachris, 13-46
avara, 22, 26-29, 36, 39, 40
avara similis, 13-46
translivata, 36, 37
Anadara, 13-46, 51, 54, 59, 60, 61, 88, 91
ovalis, 51, 54, 59, 61, 62, 88, 91
transversa, 13-46, 51, 54, 59, 60, 62, 88, 91
anceps percarinata, Helisoma, 380
Ancilla, 304
Ancillista, 304
cingulata, 304
Ancylidae, 379
Ancylus, 366
modestus, 366
angulata, Lymnaea emarginata, 380
angulata, Stagnicola emarginata, 379-399
angusta, Segmentina, 365
angustus, Segmentorbis, 365, 367
Anisus, 364, 365
crassilabrum, 364, 365
annulata, Nucula, 25
Anodonta, 97, 100, 104, 109, 110
cygnea, 97, 100, 109, 110
Anodontinae, 97
Anodontoides, 110
ferrussacianus, 110
Anomia, 24, 27, 29, 39, 40, 51, 54, 67, 68, 88
simplex, 24, 27, 29, 39, 40, 51, 54, 67, 68, 88
antiqua, Neptunea, 310, 313
antrosa percarinata, Helisoma, 379-399
aoteanus, Alectrion, 313
aoteanus, Nassarius, 313
apertus, Caillaudia, 365
apertus, Gyraulus, 365, 366
apertus, Planorbis, 365
apiculata, Chaetopleura, 13-46
arabica, Alcithoe, 310, 315, 316, 319, 321
Arbacia, 39, 40
punctulata, 39, 40
Archaeogastropoda, 186-188, 206, 295-297, 299,
301
Architaenioglossa, 123
Arcidae, 59
Arcuatula, 283, 291
arcuatula, Modiola, 283
avenaria, Mya, 47, 48, 83, 88, 90
argentea, Thuiaria, 51
Argopecten, 24, 26, 27, 29, 47, 67, 88, 90
irvadians, 24, 26, 27, 29, 47, 67, 88, 90
Arion, 206, 207
Ariophanta, 188, 206
Artemia, 109
aspera, Pirena, 357
Aspidobranchia, 186
Asprella, 310
mucronatus, 310
Asterias, 39, 40
forbesi, 39, 40
Astrangia, 39, 40
danae, 39, 40
Atrina, 291
rigida, 291
audeberti, Doryssa, 357
aurea, Venerupis, 225-245
auricularia, Lintricula, 309, 318
auricularia, Olivancillaria, 309, 318
auriculata, Neripteron, 342
auriculata, Neritina, 342, 344

402 MALACOLOGIA

Busycon, 24, 26, 27, 30, 39, 40, 309, 321
canaliculatum, 24, 26, 27, 30, 39, 40, 309

australiensis, Peristernia, 310
australis, Amalda, 310, 313

australis, Baryspira, 310, 313 contrarium, 309
australis, Microvoluta, 310 Byssanodonta, 373
Austrofusus, 314, 321 degorteri, 373

glans, 314, 321 ferruginea, 373
Austromitra, 302, 309, 320 Caelatura, 368

rubiginosa, 309 geayi, 368
avara, Anachris, 22, 26-29, 36, 39, 40 madagascariensis, 368
avara similis, Anachris, 13-46 malgachensis, 368
Babylonia, 313 Caenogastropoda, 296
balthica, Macoma, 1, 52, 55, 74-76, 88, 90 caffra, Nevita, 342
Bankia, 85, 88 caffra, Neritina, 342

gouldi, 85, 88 Caillaudia, 365
Barnea, 51, 54, 83, 84, 88, 90, 91 apertus, 365

truncata, 51, 54, 83, 84, 88, 90, 91 calcitrans, Chaetoceros, 226
Baryspira, 310, 313 caldwelli, Nautilina, 364

australis, 310, 313 caldwelli, Planorbis, 364
bavayi, Pyrgophysa, 364 californianus, Tagelus, 1-11
Bedeva, 310 Calyptraea, 188

hanleyi, 310 camerunensis, Biomphalaria, 115-122

camerunensis manzadica, Biomphalaria, 115
bengalensis, Neritina, 340 campanulata smithi, Helisoma, 379-399
betafoense, Pisidium, 372 canaliculata, Ampullaria, 124, 125, 146, 147,
biangulata, Paludina, 356 168, 189, 205
bicarinata, Melania, 356 canaliculata, Pomacia, 188, 189
biconica, Microvoluta, 314 canaliculatum, Busycon, 24, 26, 27, 30, 39, 40,
bimaculata, Navicella, 346 309
Biomphalaria, 115-122, 214, 367, 368 Cancellaria, 299, 310, 321
alexandrina, 115-122 Cancellariacea, 295, 300, 304, 307, 323, 324
alexandrina watsoni, 115-122 Cancellariidae, 299, 304, 306, 308, 309, 310,
camerunensis, 115-122 311, 315, 317, 323

bengalensis, Nerita corona, 340

camerunensis manzadica, 115
madagascariensis, 367, 368
pfeifferi, 115-122, 368

sudanica tanganyicensis, 115-122

Bithynia, 188, 214

Bittium, 24-30, 39, 40
alternatum, 24-30, 39, 40

Bivalvia, 1, 109, 265, 283

boothi, Philbertina, 305

borbonica, Cimber, 346

borbonica depressa, Navicella, 346

borbonica, Navicella, 346

borbonica, Patella, 345

borbonica, Septaria, 345-347

borboniciensis, Septaria, 346

Borsonia, 305

Borsoniinae, 305

Botula, 273

Brachidontes, 64, 88, 91
recurvus, 64, 88, 91

brevispina, Clithon, 339

brevispina, Neritina, 339

brevispina, Ophioderma, 39, 40

Buccinacea, 295, 296, 302, 308, 315, 325, 330

Buccinidae, 295-331
Buccinulidae, 325
Buccinulum, 314

Buccinum, 299, 307, 309, 310, 312, 313, 316,

321, 356
flumineum, 356
undatum, 309, 310, 313

Bullia, 302

Bulinus, 119, 363, 364
liratus, 364
madagascariensis, 364
mariei, 363, 364

cancellata, Daphnella, 305
cancellata, Tevebra, 305
Cancilla, 310
capense, Sphaerium, 373
Cardiidae, 70
Carditidae, 67
Cardium, 371
casertanum, 371
carinata, Actinonaias, 97-113
carinulata, Paludina, 353
cavoliniana, Polymesoda, 68, 88
casertanum, Cardium, 371
casertanum, Pisidium, 371, 372
caudata, Eupleura, 13-46
cecillei, Pachylabra, 350
cecillii, Ampullaria, 349, 350
cecillii, Pila, 349, 350, 351
celata, Cliona, 39, 40
Cenodagreutes, 305, 306
Cephalopoda, 188
ceramicum, Vasum, 310
Cerastoderma, 27, 30, 39, 40
pinnulatum, 27, 30, 39, 40
Ceratodes, 124
Ceratophyllum, 395
Cerithidea, 361, 362
decollata, 361, 362
Cerithiopsis, 27, 30, 39, 40
subulata, 27, 30, 39, 40
Cerithium, 361
decollatum, 361
Chaetoceros, 226
calcitrans, 226
Chaetopleura, 13-46
apiculata, 13-46
Chama, 90

INDEX, VOL. 12 403

congregata, 90
Chara, 385
chevalieri, Segmentina, 365
Chione, 7
Chlorella, 58
Cimber, 346
borbonica, 346
cinerea follyensis, Urosalpinx, 247-249, 253, 256,
257, 259
cinerea, Hastula, 305
cinerea, Urosalpinx, 26, 27, 29, 39, 40, 247-263
cingulata, Ancillista, 304
clausa, Natica, 24, 27, 30, 36, 38-40
Clavatulinae, 305
Clavinae, 300, 305, 308, 319
Cleopatra, 350, 352, 353, 354
amaena, 351, 352
colbeaui, 352
grandidieri, 353, 354
mangoroensis, 352
cleopatra, Melania, 350
Cliona, 39, 40
celata, 39, 40
Clithon, 339-341
brevispina, 339
longispina, 340
madecassina, 340, 341
rhyssodes, 340
spiniperda, 340, 341
Clypeolum, 340, 341
pulligera knorri, 340, 341
coacta, Melania, 358
coerulescens, Hastula, 310
coerulescens, Impages, 310
colbeaui, Cleopatra, 352
colbeaui, Paludina, 352
Colubraria, 304, 327, 328
maculosa, 327
muricata, 327
sowerbyi, 327
Colubrariidae, 302-331
Columbariidae, 307
Columbarium, 305, 310, 329
pagodum, 310
Columbellidae, 328
Colus, 314
gracilis, 314
Coluzea, 305, 306, 329
mariae, 329
spiralis, 329
Cominella, 307, 314
Cominellidae, 325
Comitas, 305
onokeana, 305
onokeana vivens, 305
commersoni, Nerita, 361
Conacea, 295-331
Concholepas, 303
peruviana, 303
Congeria, 47, 51, 54, 68, 69, 88, 90
leucophaeta, 47, 51, 54, 68, 69, 88, 90
congregata, Chama, 90
Conidae, 299, 305, 310, 311
Conorbiinae, 305
consimilis, Neritilia, 348
consimilis, Neritina, 348
contrarium, Busycon, 309
conularis, Imbricaria, 319

Conus, 307, 310, 313, 318, 319
lividus, 307
mediterraneus, 312, 318, 319
mucronatus, 310
convexa, Crepidula, 24, 27, 29, 39, 40
cookii, Navicella, 345, 346
Coralliophila, 303, 307, 315, 329
abbreviata, 315, 329
Coralliophilidae, 329
Corbicula, 265-281, 369-372
madagascariensis, 369, 371, 372
manillensis, 265-281
sikorae, 371
Corbiculidae, 68
cornuarietis, Marisa, 123-210
cornula, Melania, 359
cornuta, Melania, 359
corona bengalensis, Nerita, 340
corona, Melongena, 309
costata, Cyrtopleura, 52, 55, 84, 85, 88, 91
crassa, Physa sayi, 380
crassa, Pseudoliva, 310
crassilabrum, Anisus, 364, 365
crassilabrum, Gyraulus, 365
crassilabrum, Planorbis, 364, 365
Crassinella, 27-29, 32, 34, 35, 39, 40
mactracea, 27-29, 32, 34, 35, 39, 40
Crassostrea, 48, 65, 66, 88, 247-249
virginica, 48, 65, 66, 88, 247-249
crennularis, Inquisitor, 310
crenulata, Pterygia, 310
Crepidula, 13-46, 146, 168, 206, 214, 215, 219
convexa, 24, 27, 29, 39, 40
fornicata, 13-46
plana, 24, 26-29, 39, 40
cretaceus, Plesiotriton, 328
cuneata, Rangia, 47, 53, 56, 82, 83, 88, 90
cuneiformis, Martesia, 47, 84
cybele, Melania, 359
Cyclas, 372, 373
ferruginea, 373
madagascariensis, 373
Cyclope, 302, 310, 313
neritea, 310, 313
Cyclostoma, 356
unicolor, 356
cygnea, Anodonta, 97, 100, 109, 110
Cyllene, 310
lyrata, 310
Cymatiidae, 304, 327
Cyrtopleura, 52, 55, 84, 85, 88, 91
costata, 52, 55, 84, 85, 88, 91
dalei, Liomesus, 310
danae, Astrangia, 39, 40
Daphnella, 305
cancellata, 305
Daphnellinae, 305
debauxiana, Melanatria, 357
debeauxiana, Pirena, 356, 357
debilis, Splendrillia, 305
decollata, Cerithidea, 361, 362
decollata, Melania, 361
decollata, Pirenella, 361
decollatum, Cerithium, 361
decollatus, Potamides, 361
degorteri, Byssanodonta, 373
degorteri, Eupera, 373, 374
demissus granosissimus, Mytilus, 284, 286, 290

404 MALACOLOGIA

demissus, Modiolus, 64, 88, 91, 283-293
demissus, Mytilus, 283, 284
Dentalium, 213-215, 219
depressa, Ampullaria, 124, 205, 206
depressa, Navicella, 345
depressa, Navicella borbonica, 346
desetangsii, Scabricola, 310
Diluculum, 310, 311, 315
inopinatum, 310
Diotocardia, 186
Diplomeriza, 310
duplicata, 310
Diplothyra, 84
smithii, 84

directus, Ensis, 22, 27, 30, 39, 40, 52, 55, 79, 88

discus, Dosinia, 47, 71
divisus, Tagelus, 27, 30, 79
Domiporta, 310
Donacidae, 77
Donax, 47, 52, 55, 77, 78, 88-90
gouldi, 1, 7
variabilis, 47, 52, 55, 77, 78, 88-90
Doryssa, 357
audeberti, 357
Dosinia, 47, 71
discus, 47, 71
Dreissena, 265-281
polymorpha, 265-281
siamensis, 266
Dreissenidae, 68
Drillia, 310
umbilicata, 310
Drupa, 307
dubius, Taron, 314, 318
duclosiana, Pseudanachis, 310
duisabonis, Melania, 356
duplicarinata, Proneptunea, 310
duplicata, Diplomeriza, 310
duplicatus, Polinices, 26, 30, 39, 40
edouardi, Pisidium, 371

edulis, Mytilus, 47, 48, 63-65, 88, 90, 247, 268,

269, 273, 284-288
Egeria, 4
radiata, 4
Elara, 346
suborbicularis, 346
electa, Limnaea, 363
elliptica, Aetheria, 369
elliptica, Etheria, 369
elliptica, Navicella, 345, 346
emarginata angulata, Lymnaea, 380
emarginata angulata, Stagnicola, 379-399
Ensis, 22, 27, 30, 39, 40, 52, 55, 79, 88
directus, 22, 27, 30, 39, 40, 52, 55, 79, 88
Epidirona, 305
gabensis, 305
erinaceus, Ocenebra, 308, 313, 316
Etheria, 369
elliptica, 369
Eupera, 373, 374
degorteri, 373, 374
ferruginea, 373
Eupleura, 13-46
caudata, 13-46
eximia, Navicella, 346
fasciata, Venus, 225-245
Fasciolaria, 206
Fasciolariidae, 295-331

Ferrissia, 366, 367
modesta, 366, 367
ferruginea, Byssanodonta, 373
ferruginea, Cyclas, 373
ferruginea, Eupera, 373
ferruginea, Limosina, 373
ferruginea, Sphaerium, 373
ferrussacianus, Anodontoides, 110
filosa, Ampullaria, 350
flava, Fusconaia, 97-113
Florimetis, 1-11
obesa, 1-11
fluminea, Melanatria, 356-358, 361
fluminea, Pirena, 356, 357
flumineum, Buccinum, 356
follyensis, Urosalpinx cinerea, 247-249, 253,
256, 257, 259
forbesi, Asterias, 39, 40
fornicata, Crepidula, 13-46
fortunei, Limnoperna, 265-281
fortunei, Modiola, 266
fortunei, Volsella, 266
Fulgerca, 328
fulgetrum, Neritina, 342
Fulgur, 206
Fungiacava, 268
Fusconaia, 97-113
flava, 97-113
Fusidae, 327
Fusinidae, 327, 329
Fusinus, 327
gabensis, Epidivona, 305
gagates, Neritaea, 343
gagates, Neritina, 342, 343, 345
gagates, Vittina, 342, 343
galbana, Isochrysis, 226
Galeodidae, 302, 305, 307, 309, 321, 325-327
Gastropoda, 109, 124, 213
geayi, Caelatura, 368
geayi, Nodularia, 368
geayi, Unio, 368
geayi, Zairia, 368
Gemma, 50, 52, 55, 72, 88
gemma, 50, 52, 55, 72, 88
gemma, Gemma, 50, 52, 55, 72, 88
Geukensia, 283, 284
gibberula, Pyrene, 310
gibberula, Strombina, 310
gigas, Ampullaria, 147, 187, 188, 189, 205, 206
glans, Austrofusus, 314, 321

globosa, Pila, 124, 125, 128, 146, 147, 168, 169,

187-189, 205

Goniobasis, 394

livescens, 394
goodei persimilis, Aforia, 310
goudotiana, Melanatria, 357
gouldi, Bankia, 85, 88
gouldi, Donax, 1, 7
gouldiana, Pandora, 22, 24, 26, 27, 29, 39, 40
gracilis, Colus, 314
gvandidieri, Cleopatra, 353, 354
grandidieri, Paludomus, 353

gvanosissimus, Mytilus demissus, 284-286, 290

Granulifusus, 310

niponicus, 310
granulosa, Pirena, 356
gvasseti, Ampullaria, 348, 349
gvasseti, Lanistes, 349

INDEX, VOL. 12 405

gvasseti, Lanistes olivaceus, 348, 349 johnsoni, Pisidium, 371, 372
grasseti, Lanistes ovum, 347 junghuhni, Navicella, 346
gvasseti, Meladomus, 349 junonia, Scaphella, 310
gvasseti, Meladomus olivaceus, 349 knorri, Clypeolum pulligera, 340, 341
Gyraulus, 365, 366 knorri, Nerita, 341
apertus, 365, 366 knorri, Neritina, 341
crassilabrum, 365 knorrit, Neritina pulligera, 340
gyrina, Physa, 380, 395 knorrii, Neritina, 341
Haedropleuva, 319 lacustris, Modiola, 266
septangularis, 319 Laevicardium, 22, 24-29, 32, 35, 39, 40, 52, 55,
Haliotis, 146, 186, 206, 297, 299 70, 88, 90
Haloginella, 310 mortoni, 22, 24-29, 32, 35, 39, 40, 52, 55, 70,
philippinarum, 310 88, 90
hanleyi, Ampullaria, 349 lamarckii, Melanopsis, 356
hanleyi, Bedeva, 310 lamarckii, Pirena, 356
hanleyi, Pachylabra, 349 lamellata, Physa, 364
Harpa, 310, 313, 330 Lampsilinae, 100
amouretta, 310 Lampsilis, 97-113
Harpidae, 303-331 ovata ventricosa, 99
Hastula, 305, 310, 320 radiata luteola, 100
cinerea, 305 radiata siliquoidea, 97-113
coerulescens, 310 Lanistes, 347, 348, 349
hedleyi, Peculator, 314 gvasseti, 349
Helisoma, 379-399 olivaceus grasseti, 348, 349
anceps percarinata, 380 ovum, 349
antrosa percarinata, 379-399 ovum gvasseti, 347
campanulata smithi, 379-399 ovum plicosus, 349
Helix, 207, 359 ovum striata, 349
amarula, 359 plicosus ovum, 348
Heterodontida, 67 striatus, 349
Heterogastropoda, 296 lapillus, Nucella, 308, 313, 315, 316
hildebrandti, Physa, 364 lapillus, Thais, 258, 259
hildebrandti, Planorbis, 365 largillierti, Ampullaria, 349
Hindsia, 303 largillierti, Pachylabra, 349
Hivudo, 108 latevalis, Mulinia, 26, 30, 52, 56, 81, 82, 88
medicinalis, 108 Leptodesma, 38
Hormospira, 310 leucophaeta, Congeria, 47, 51, 54, 68, 69, 88, 90
maculosa, 310 Leucozonia, 314, 316, 318
hovarum, Limnaea, 363, 364 nassa, 314
hovarum, Radix, 363, 364 leufroyi, Philbertina, 305
hyalina, Lyonsia, 22, 26, 27, 30, 39, 40, 52, 55, ligamentina, Actinonaias, 100
86, 88, 90 limatula, Yoldia, 13-47, 59, 88
Ilyanassa, 213-223, 310, 313 Limax, 168, 188, 207
obsoleta, 310, 313 Limnaea, 363, 364
Imbricaria, 319 electa, 363
conularis, 319 hovarum, 363, 364
Impages, 310 Limnoperna, 265-281
coerulescens, 310 fortunei, 265-281
incisa, Nephtys, 21, 38 Limosina, 373
inconstans, Xenostrobus, 269, 276 ferruginea, 373
incrassatus, Nassarius, 318 lineata, Navicella, 346
inopinatum, Diluculum, 310 lineata, Septaria, 346, 347
Inquisitor, 310 lingulata, Pirena, 356
crennularis, 310 Lintricula, 309, 318, 320
integra, Physa, 379-399 auricularia, 309, 318
Iredalula, 310, 327 Liomesus, 310
striata, 310, 327 dalei, 310
ivvadians, Aequipecten, 39, 40 lirata, Ameria, 364
irradians, Argopecten, 24, 26, 27, 29, 47, 67, 88, lirata, Physa, 364
90 livatus, Bulinus, 364
Ischadium, 283, 284, 285, 289, 291 livatus, Isidora, 364
recurvum, 283, 284, 285, 289, 291 Lithophaga, 268, 269, 273
Isidora, 364 Littorina, 146, 168, 188, 299
livatus, 364 Littorinacea, 320
madagascariensis, 364 livescens, Goniobasis, 394
Isochrysis, 226 lividus, Conus, 307
galbana, 226 longispina, Clithon, 340

johnsoni, Melanatria, 357 longispina, Neritina, 340

406 MALACOLOGIA

longispina, Paranerita, 340 Marginellidae, 295-331
Lora, 316, 320 mariae, Coluzea, 329
travelliana, 316 mariei, Bulinus, 363, 364
turricula, 320 mariei, Pyrgophysa, 364
Loxonematacea, 302 marina, Zostera, 58, 90
Lucina, 47, 52, 55, 68, 69, 88, 90 Marisa, 123-210
multilineata, 47, 52, 55, 68, 69, 88, 90 cornuarietis, 123-210
luhdorffi, Parabathytoma, 305 martensi, Meteutria, 310
Lunarca, 24, 26, 27, 30, 39, 40 Martesia, 47, 84
ovalis, 24, 26, 27, 30, 39, 40 cuneiformis, 47, 84
lunata, Mitrella, 22, 24, 26, 27, 29, 39, 40 masoni, Schistosoma, 115, 119
luteola, Lampsilis radiata, 100 maura, Pivena, 356
lutheri, Monochrysis, 226 medicinalis, Hivudo, 108
Lunatia, 27, 30 mediterraneus, Conus, 312, 318, 319
triseriata, 27, 30 Meladomus, 349
Lymnaea, 109, 214, 219, 380 grasseti, 349
emarginata angulata, 380 olivaceus grasseti, 349
Lymnaeidae, 380 ovum plicosus, 349
Lyonsia, 22, 26, 27, 30, 39, 40, 52, 55, 86, 88, 90 Melanatria, 356-361
hyalina, 22, 26, 27, 30, 39, 40, 52, 55, 86, 88, debauxiana, 357
90 fluminea, 356, 357, 358, 361
Lyonsiidae, 86 goudotiana, 357
lyrata, Cyllene, 310 johnsoni, 357
Macoma, 1, 4, 6-8, 13-46, 47, 52, 55, 74-76, 77, madagascariensis, 357
88, 90 Spinosa, 356, 357
baltica, 7, 52, 55, 74-76, 88, 90 Melania, 168, 350, 356, 359, 361
mitchelli, 47, 52, 55, 56, 76, 77, 90 amarula, 359
nasuta, 1, 4, 6-8 bicarinata, 356
phenax, 88 cleopatra, 350
secta, 6-8 coacta, 359
tenta, 13-46, 77, 88, 90 cornula, 359
mactracea, Crassinella, 27-29, 32, 34, 35, 39, 40 cornuta, 359
Mactridae, 80 cybele, 359
maculata, Terebra, 306 decollata, 361
maculosa, Colubraria, 327 duisabonis, 356
maculosa, Hormospira, 310 madagascariensis, 356
madagascariense, Sphaerium, 373 thiarella, 359
madagascariensis, Ampullaria, 349 tuberculata, 361
madagascariensis, Biomphalaria, 367, 368 Melanoides, 361
madagascariensis, Bulinus, 364 tuberculatus, 361
madagascariensis, Caelatura, 368 Melanopsis, 356
madagascariensis, Corbicula, 369, 371, 372 lamarckii, 356
madagascariensis, Cyclas, 373 Spinosa, 356
madagascariensis, Isidora, 364 Melongena, 309, 313, 327, 328
madagascariensis, Melanatria, 357 corona, 309
madagascariensis, Melania, 356 melongena, 309
madagascariensis, Pachylabra, 349, 350 melongena, Melongena, 309
madagascariensis, Paludina, 353 Melongenidae, 295, 310, 311, 314, 327
madagascariensis, Paludomus, 352, 353 Mercenaria, 27, 30, 70, 71, 88
madagascariensis, Physa, 364 mercenaria, 27, 30, 70, 71, 88
madagascariensis, Pirena, 356, 357 mercenaria, Mercenaria, 27, 30, 70, 71, 88
madagascariensis, Pisidium, 371 Mesogastropoda, 123, 175, 186, 187, 295-298,
madagascariensis, Planorbis, 367 301, 327
madagascariensis, Unio, 368 mestayerae, Ratifusus, 305, 327
madecassina, Clithon, 340, 341 Meteutria, 310
madecassina, Neritina, 339 martensi, 310
Magilidae, 302, 303, 306-309, 314-316, 321, 326, Metula, 328
329 Microciona, 39, 40
Magilus, 303, 329 prolifera, 39, 40
malgachensis, Caelatura, 368 Microvoluta, 310, 314
malgachensis, Unio, 368 australis, 310
Mangelia, 316, 319 biconica, 314
Mangeliinae, 305 Microvolutidae, 301, 307, 330, 331
mangoroensis, Cleopatra, 352 mitchelli, Macoma, 47, 52, 55, 56, 76, 77, 90
manillensis, Corbicula, 265-281 Mitracea, 325
manzadica, Biomphalavia camerunensis, 115 Mitrella, 22, 24, 26, 27, 29, 39, 40
Maoritomella, 305 lunata, 22, 24, 26, 27, 29, 39, 40

albula, 305 Mitridae, 299-331

INDEX, VOL. 12

modesta, Fervissia, 366, 367
modestus, Ancylus, 366
Modiola, 266, 283-293
americanus, 284, 291
arcuatula, 283
demissus, 64, 88, 91, 283-293
fortunei, 266
lacustris, 266
modiolus, 27, 30
plicatula, 283
squamosus, 284, 291
modiolus, Modiolus, 27, 30
Mohnia, 310
mohnia, 310
mohnia, Mohnia, 310
moniliata, Paludina, 352
Monochrysis, 226
lutheri, 226
Monodonta, 300
Monotocardia, 186
morio, Pugilina, 310
morio, Semifusus, 310
morrhuana, Pitar, 22, 26, 27, 29, 39, 40
mortoni, Laevicardium, 22, 24-29, 32, 35, 39, 40,
52, 55, 70, 88, 90
Morula, 307
mucronatus, Asprella, 310
mucronatus, Conus, 310
Mulinia, 26, 30, 52, 56, 81, 82, 88
lateralis, 26, 30, 52, 56, 81, 82, 88
multilineata, Lucina, 47, 52, 55, 68, 69, 88, 90
multilivata, Paludina, 353
Murex, 303, 308, 310, 313, 329
pecten, 310
tenuispina, 310
trunculus, 308
Muricacea, 295, 296, 300, 312, 314, 324, 325,
328, 329
muricata, Colubraria, 327
Muricidae, 299-331
Muricinae, 328
musica, Voluta, 310
Mya, 47, 48, 83, 88, 90
avenaria, 47, 48, 83, 88, 90
Myacidae, 83
Myobarbum, 331
Myriophyllum, 383, 395
Mytilacea, 265
Mytilidae, 63, 276, 283, 291
Mytilopsis, 276
Mytilus, 47, 48, 63-65, 88, 90, 214, 215, 219, 247,
268, 269, 273, 274, 283
demissus, 283
demissus demissus, 284
demissus granosissimus, 284, 286, 290

edulis, 47, 48, 63-65, 88, 90, 247, 268, 269, 273,

284-288
Nacella, 299, 319
nassa, Leucozonia, 314
Nassariidae, 213, 295-331
Nassarius, 13-46, 215, 301, 307, 313, 316, 318
aoteanus, 313
incrassatus, 318
obsoletus, 36, 215, 313
pygmaeus, 318
reticulatus, 301, 313, 318
trivittatus, 13-46
vibex, 24, 30, 39, 40

nasuta, Macoma, 1, 4, 6-8
Natica, 24, 27, 30, 36, 38-40
clausa, 24, 27, 30, 38-40
Nautilina, 364
caldwelli, 364
navalis, Teredo, 85, 86, 88
Navicella, 345, 346
bimaculata, 346
borbonica, 346
borbonica depressa, 346
cookii, 345, 346
depressa, 345
elliptica, 345, 346
eximia, 346
junghuhni, 346
lineata, 346
porcellana, 346
suborbicularis, 345, 346
tessellata, 346
Nematoglossa, 323
Neogastropoda, 295-338
neozelanicum, Scrinium, 305
Nephtys, 21, 38
incisa, 21, 38
Neptunea, 310, 313, 321
antiqua, 310, 313
Neptuniidae, 325
Nereis, 214
Nerineacea, 296
Neripteron, 342
auriculata, 342
Nerita, 340-342, 346
caffra, 342
commersoni, 361
corona bengalensis, 340
knorri, 341
psorica, 361
pulligera, 341
vangiana, 346
Yubella, 341
tuberculata, 361
turrita, 342
viridis, 346
Neritacea, 297, 320
Neritaea, 343
gagates, 343
neritea, Cyclope, 310, 313
Neritidae, 297
Neritilia, 348
consimilis, 348
Neritina, 339-344, 345, 346, 348
auviculata, 342, 344
bengalensis, 340
brevispina, 339
caffra, 342
consimilis, 348
fulgetrum, 342
gagates, 342, 343, 345
knorri, 341
knorrü, 341
longispina, 340
madecassina, 339
pulligera, 341, 343
pulligera knorri, 340
vhyssodes, 340
rubella, 341
souverbiana, 348
spiniperda, 340

407

408

stumpffi, 341
truncata, 341
turrita, 342
viridis, 346
niponicus, Granulifusus, 310
nitida, Parasmittina, 39, 40
Nodularia, 368
geayi, 368
Noetia, 52, 56, 62, 63, 88, 91
ponderosa, 52, 56, 62, 63, 88, 91
norwegicus, Volutopsis, 321
Nucella, 308, 312, 313, 315, 316, 317
lapillus, 308, 313, 315, 316
Nucula, 13-46, 58
annulata, 25
proxima, 13-46, 58, 88
Nuculanidae, 59
Nuculidae, 58
obesa, Florimetis, 1-11
obsoleta, Ilyanassa, 310, 313
obsoletus, Nassarius, 36, 215, 313
obtusa, Retusa, 22, 24, 30, 39, 40
obtusispira, Physa, 364
Ocenebra, 308, 313, 316
erinaceus, 308, 313, 316
Ocenebrinae, 328, 329
Oenopota, 316
travelliana, 316
Oliva, 304, 309, 310, 313, 318, 319
sayana, 309, 310, 313, 318, 319
tehuelchana, 304
Olivacea, 325
olivaceus grasseti, Lanistes, 348, 349
olivaceus grasseti, Meladomus, 349
Olivancillaria, 309, 316, 318, 320
auricularia, 309, 318
Olivella, 307, 308, 310, 313, 318, 319, 330
verreauxü, 310, 313
Olivellinae, 308
Olividae, 299-331
onokeana, Comitas, 305
onokeana vivens, Comitas, 305
Ophioderma, 39, 40
brevispina, 39, 40
Opisthobranchia, 308
Ostreidae, 65
ovalis, Lunarca, 24, 26, 27, 30, 39, 40
ovata ventricosa, Lampsilis, 99
ovoideus, Turbinella, 310
ovum, Ampullaria, 349
ovum grasseti, Lanistes, 347
ovum, Lanistes, 349
ovum, Lanistes plicosus, 348
ovum plicosus, Lanistes, 349
ovum plicosus, Meladomus, 349
ovum striata, Lanistes, 349
Pachylabra, 349, 350
cecillei, 350
hanleyi, 349
largillierti, 349
madagascariensis, 349, 350
simplex, 349
subscutata, 349
pagodum, Columbarium, 310
Paladmetidae, 323
Paludina, 124, 146, 206, 352, 353
biangulata, 356
carinulata, 353

MALACOLOGIA

colbeaui, 352
madagascariensis, 353
montliata, 352
multilirata, 353
trabonjiensis, 353
Paludomus, 352, 353
grandidieri, 353
madagascariensis, 352, 353
Pandora, 22, 24, 26, 27, 29, 39, 40
gouldiana, 22, 24, 26, 27, 29, 39, 40
papyria, Amygdalum, 50, 51, 54, 64, 65, 88, 91
Parabathytoma, 305
luhdorffi, 305
Paradmete, 310
typica, 310
Paranerita, 340
longispina, 340
Parapisidium, 372
reticulatum, 372
Parasmittina, 39, 40
nitida, 39, 40
Paratrophon, 310
quoyi quoyi, 310
parkeri, Physa, 379-399
Patella, 146, 148, 345
borbonica, 345
Patellacea, 297
pauliani, Pisidium, 372
paupercula, Strigatella, 319
paxillus, Paxula, 310
Paxula, 310
paxillus, 310
pecten, Murex, 310
Pectinidae, 67
Pectinobranchia, 186
Peculator, 314
hedleyi, 314
Penion, 314, 321
adustus, 314, 321
percarinata, Helisoma anceps, 380
percarinata, Helisoma antrosa, 379-399
Peristernia, 310
australiensis, 310
Perna, 273
Persicula, 310
persicula, 310
persicula, Persicula, 310
persimilis, Aforia goodei, 310
peruviana, Concholepas, 303
Pervicacia, 306
tristis, 306
Pervicaciidae, 325
Petricola, 53, 56, 73, 88, 272
pholadiformis, 53, 56, 73, 88
Petricolidae, 73
pfeifferi, Biomphalaria, 115-122, 368
Phenatoma, 305, 310
rosea, 305, 310
bhenax, Macoma, 88
Philbertina, 305
boothi, 305
leufroyi, 305
purpurea, 305
philippianus, Trophon, 308
philippinarum, Haloginella, 310
philippinavum, Volvarina, 310
Pholadidae, 83
pholadiformis, Petricola, 53, 56, 73, 88

Phos, 303, 327

Photidae, 327

Phyllocoma, 304

Physa, 146, 364, 379-399
gyrina, 380, 395
hildebrandti, 364
integra, 379-399
lamellata, 364
livata, 364
madagascariensis, 364
obtusispiva, 364
parkeri, 379-399
sayi crassa, 380

Physidae, 379

picta, Polystira, 310

Pila, 124, 125, 128, 146, 147, 168, 169, 187-189,

206, 207, 349-351
cecillii, 349-351

globosa, 124, 125, 128, 146, 147, 168, 169,

187-189, 205
virens, 124
Pilidae, 123
pinnulatum, Cerastoderma, 27, 30, 39, 40
Pirena, 356, 357
aspera, 357
debeauxiana, 356, 357
fluminea, 356, 357
gvanulosa, 356
lamarckii, 356
lingulata, 356
madagascariensis, 356, 357
maura, 356
plicata, 356
sinuosa, 356
Spinosa, 356, 357
Pirenella, 361
decollata, 361
Pisidium, 371-373
betafoense, 372
casertanum, 371, 372
edouardi, 371
johnsoni, 371, 372
madagascariensis, 371
pauliani, 372
planatum, 371
reticulatum, 372
Pitar, 22, 26, 21, 29, 39, 40
morrhuana, 22, 26, 27, 29, 39, 40
plana, Crepidula, 24, 26-29, 39, 40
planatum, Pisidium, 371
Planorbidae, 115, 380
Planorbis, 146, 206, 364, 365, 367
alluaudi, 365
apertus, 365
caldwelli, 364
crassilabrum, 364, 365
hildebrandti, 365
madagascariensis, 367
simpliculus, 365
trivialis, 364, 365
plebius, Tagelus, 53, 57, 78, 79, 87, 88, 90
Plesiotriton, 328
cretaceus, 328
plicata, Amblema, 97-113
plicata, Pirena, 356
plicatula, Modiola, 283
plicosus, Lanistes ovum, 349
plicosus, Meladomus ovum, 349

INDEX, VOL. 12

plicosus ovum, Lanistes, 348
Poirieria, 310

zelandica, 310
Polinices, 26, 30, 39, 40

duplicatus, 26, 30, 39, 40
polita, Ampullaria, 124, 147, 186, 188
Polymesoda, 68, 88

caroliniana, 68, 88
polymorpha, Dreissena, 265-281
Polystira, 310

picta, 310
Pomacia, 187, 189

canaliculata, 188, 189
Pomatias, 146, 168, 188
ponderosa, Noetia, 52, 56, 62, 63, 88, 91
Pontiothauma, 305
porcellana, Navicella, 346
Potamides, 361

decollatus, 361
Potamogeton, 383, 385, 395
Prionodontida, 59
prolifera, Microciona, 39, 40
Proneptunea, 310

duplicarinata, 310
Propebela, 320

turricula, 320
Propidiscus, 365

trivialis, 365
Prosobranchia, 146, 169, 206, 297
Protobranchia, 58
Protothaca, 7
proxima, Nucula, 13-46, 58, 88
Pseudanachis, 310

duclosiana, 310
Pseudoliva, 310

crassa, 310
Pseudolivinae, 330
psorica, Nerita, 361
Pteroconchida, 63
Pterygia, 310

crenulata, 310
Pugilina, 310

morio, 310
pulex, Xenostrobus, 269, 276
pullastra, Venerupis, 225-245
pulligera knorri, Clypeolum, 340, 341
pulligera knorri, Neritina, 340
pulligera, Nerita, 341
pulligera, Neritina, 341, 343
Pulmonata, 109, 379
punctulata, Arbacia, 39, 40
purpurea, Philbertina, 305
Purpuridae, 328
Pusia, 310
pygmaeus, Nassarius, 318
Pyrene, 310

gibberula, 310
Pyrenidae, 302-331
Pyrgophysa, 364

bavayi, 364

mariei, 364
pyrum, Turbinella, 319
quoyi quoyi, Paratrophon, 310
Quoyula, 303
Rachiglossa, 295-331
vadiata, Egeria, 4
radiata luteola, Lampsilis, 100
radiata siliquoidea, Lampsilis, 97-113

409

410 MALACOLOGIA

Radix, 363, 364 similis, Anachris avara, 13-46
hovarum, 363, 364 simplex, Ampullaria, 349
Rangia, 47, 53, 56, 82, 83, 88, 90 simplex, Anomia, 24, 27, 29, 39, 40, 51, 54, 67,
cuneata, 47, 53, 56, 82, 83, 88, 90 68, 88
rangiana, Nerita, 346 simplex, Pachylabra, 349
rangiana, Smaragdia, 348 simpliculus, Planorbis, 365
Rapanidae, 329 simpliculus, Tropidiscus, 365
Rapidae, 329 sinuosa, Pirena, 356
Rapininae, 328, 329 Smaragdia, 346, 348
Ratifusus, 305, 327, 328 rangiana, 348
mestayerae, 305, 327 souverbiana, 348
reticulatus, 305, 327 viridis, 346, 348
recurvum, Ischadium, 283, 284, 285, 289, 291 smithi, Helisoma campanulata, 379-399
recurvus, Brachidontes, 64, 88, 91 smithii, Diplothyra, 84
reticulatum, Parapisidium, 372 Solecurtus, 4
reticulatum, Pisidium, 372 scopula, 4
reticulatus, Nassarius, 301, 313, 318 Solemya, 13-46, 53, 56, 58, 87, 88
reticulatus, Ratifusus, 305, 327 velum, 13-46, 53, 56, 58, 87, 88
Retusa, 22, 24, 30, 39, 40 Solemyidae, 58
obtusa, 22, 24, 30, 39, 40 Solen, 53, 56, 80, 87
rhyssodes, Clithon, 340 viridus, 53, 56, 80, 87
rhyssodes, Neritina, 340 Solenidae, 79
rigida, Atrina, 291 solidissima, Spisula, 27, 30, 47, 48, 53, 57, 80,
Rissoacea, 320 81, 88-91, 251, 256, 257
rosea, Phenatoma, 305, 310 souverbiana, Neritina, 348
rubella, Nerita, 341 souverbiana, Smaragdia, 348
rubella, Neritina, 341 sowerbyi, Colubraria, 327
rubiginosa, Austromitra, 309 Speightiidae, 325
Rupia, 48, 90 Sphaerium, 372, 373
Sabellaria, 214, 215, 219 capense, 373
Sanguinolariidae, 78 ferruginea, 373
sayana, Oliva, 309, 310, 313, 318, 319 madagascariense, 373
sayi crassa, Physa, 380 spiniperda, Clithon, 340, 341
Scabricola, 310 spiniperda, Neritina, 340
desetangsii, 310 spinosa, Melanatria, 356, 357
variegata, 310 spinosa, Melanopsis, 356
Scaphella, 310 Spinosa, Pirena, 356, 357
junonia, 310 spiralis, Coluzea, 329
Schistosoma, 115, 119 Spisula, 27, 30, 47, 48, 53, 57, 80, 81, 88-91,
mansoni, 115, 119 251, 256, 257
Scissurellidae, 301 solidissima, 27, 30, 47, 48, 53, 57, 80, 81,
scopula, Solecurtus, 4 88-91, 251, 256, 257
Scrinium, 305 Splendrillia, 305
neozelanicum, 305 debilis, 305
Scrobicularia, 6 squamata, Amphipholis, 39, 40
secta, Macoma, 6-8 squamosus, Modiola, 284, 291
securis, Xenostrobus, 267, 276 Stagnicola, 379-399
Segmentina, 365 emarginata angulata, 379-399
angusta, 365 Stenoglossa, 295, 322, 323
chevalieri, 365 striata, Iredalula, 310, 327
Segmentorbis, 365, 367 striata, Lanistes ovum, 349
angustus, 365, 367 Striatella, 361
Seila, 27, 30, 39, 40 tuberculata, 361
adamsi, 27, 30, 39, 40 striatula, Venus, 225-245
Semelidae, 77 striatus, Lanistes, 349
Semifusus, 310 Strigatella, 307, 319
morio, 310 paupercula, 319
septangularis, Haedropleura, 319 Strombina, 310
Septaria, 297, 345-347 gibberula, 310
borbonica, 345-347 stumpffi, Neritina, 341
borboniciensis, 346 suborbicularis, Elava, 346
lineata, 346, 347 suborbicularis, Navicella, 345, 346
suborbicularis, 346 suborbicularis, Septaria, 346
tessellata, 346 subscutata, Ampullaria, 349
Septifer, 275 subscutata, Pachylabra, 349
siamensis, Dreissena, 266 subulata, Cerithiopsis, 27, 30, 39, 40
sikorae, Corbicula, 371 Subulitacea, 296, 301

siliquoidea, Lampsilis radiata, 97-113 sudanica tanganyicensis, Biomphalaria, 115-122

INDEX, VOL. 12 411

Tagelus, 1-11, 27, 30, 53, 57, 78, 79, 87, 88, 90 byrum, 319
californianus, 1-11 Turbinellidae, 299-331
divisus, 27, 30, 79 Turbinellinae, 326, 328
plebius, 53, 57, 78, 79, 87, 88, 90 turbinellum, Vasum, 316
tanganyicensis, Biomphalaria sudanica, 115-122 turricula, Lora, 320
Taron, 307, 314, 318 turricula, Propebela, 320
dubius, 314, 318 Turriculinae, 305
tehuelchana, Oliva, 304 Turridae, 300-331
Tellina, 6, 53, 57, 74, 88, 90 Turrinae, 305
agilis, 53, 57, 74, 88, 90 turrita, Nerita, 342
Tellinacea, 1 turrita, Neritina, 342
tenta, Macoma, 13-46, 77, 88, 90 turrita, Vittina, 342
tenuispina, Murex, 310 Typhinae, 328
Terebra, 305 typica, Paradmete, 310
cancellata, 305 umbilicata, Drillia, 310
maculata, 306 undatum, Buccinum, 309, 310, 313
Terebridae, 299-331 unicolor, Cyclostoma, 356
Teredinidae, 85 unicolor, Viviparus, 356, 357
Teredo, 85, 86, 88 Unio, 368
navalis, 85, 86, 88 geayi, 368
tessellata, Navicella, 346 madagascariensis, 368
tessellata, Septaria, 346 malgachensis, 368
Thaididae, 328, 329 Unionidae, 97
Thaidinae, 328, 329 urceus, Ampullaria, 187, 189
Thais, 258, 259, 321 Urosalpinx, 26, 27, 29, 39, 40, 247-263
lapillus, 258, 259 cinerea, 26, 27, 29, 39, 40, 247-263
Theodoxus, 297 cinerea follyensis, 247-249, 253, 256, 257, 259
Thiara, 359, 360 Uttleya, 304
amarula, 359, 360 Vallisneria, 383
thiarella, Melania, 358 variabilis, Donax, 47, 52, 55, 77, 78, 88-90
Thuiaria, 51 variegata, Scabricola, 310
argentea, 51 Vasidae, 326, 328
Tolema, 303 Vasinae, 326, 328
Tonnacea, 296, 297, 327 Vasum, 310, 315, 316, 328
Toxoglossa, 295, 322, 323, 325 ceramicum, 310
trabonjiensis, Paludina, 353 turbinellum, 316
translivata, Anachris, 36, 37 velum, Solemya, 13-46, 53, 56, 58, 87, 88
transversa, Anadara, 13-46, 51, 54, 59, 60, 62, Venericardia, 47, 68
88, 91 tridentata, 47, 68
travelliana, Lora, 316 Veneridae, 70, 225-245
travelliana, Oenopota, 316 Venerupis, 225-245
Treses, 7 aurea, 225-245
tridentata, Venericardia, 47, 68 pullastra, 225-245
Triphoridae, 300 ventricosa, Lampsilis ovata, 99
triseriata, Lunatia, 27, 30 Venus, 225-245
tristis, Pervicacia, 306 fasciata, 225-245
trivialis, Planorbis, 364, 365 striatula, 225-245
trivialis, Propidiscus, 365 verrucosa, 225-245
trivialis, Tropidiscus, 365 verreauxii, Olivella, 310-313
trivittatus, Nassarius, 13-46 verrucosa, Venus, 225-245
Trochidae, 297, 301 Vexilla, 308, 310, 319, 320
Trophon, 308 taeniata, 310
philippianus, 308 Vexillidae, 299-331
Trophoninae, 309, 320, 328 vibex, Nassarius, 24, 30, 39, 40
Tropidiscus, 365 virens, Pila, 124
alluaudi, 365 virginica, Crassostrea, 48, 65, 66, 88, 247-249
simpliculus, 365 viridis, Nerita, 346
trivialis, 365 viridis, Neritina, 346
truncata, Barnea, 51, 54, 83, 84, 88, 90, 91 viridis, Smaragdia, 346, 348
truncata, Neritina, 341 vividus, Solen, 53, 56, 80, 87
trunculus, Murex, 308 Vittina, 342, 343
tuberculata, Melania, 361 gagates, 342, 343
tuberculata, Nerita, 361 turrita, 342
tuberculata, Striatella, 361 Vitularia, 306
tuberculatus, Melanoides, 361 vivens, Comitas onokeana, 305
Tubifex, 109 Viviparus, 124, 146, 356, 357
Turbinella, 305, 310, 319, 321, 328 unicolor, 356, 357

ovoideus, 310 Volemidae, 327

412 MALACOLOGIA

Volsella, 266
fortunei, 266
Voluta, 310
musica, 310
Volutacea, 295, 296, 303, 325, 330
Volutidae, 299-331
Volutocorbis, 309, 310, 316
abyssicola, 309, 310
Volutomitridae, 295-331
Volutomitrinae, 330
Volutopsis, 321
norwegicus, 321
Volvarina, 310
philippinarum, 310
watsoni, Biomphalaria alexandrina, 115-122

Xancidae, 328
Xenostrobus, 267, 269, 276
inconstans, 269, 276
pulex, 269, 276
securis, 267, 276
Xymene, 310
ambiguus, 310
Yoldia, 13-47, 59, 88
limatula, 13-47, 59, 88
Zairia, 368
geayi, 368
zelandica, Poirieria, 310
Zeugobranchia, 297
Zostera, 48, 58, 90
marina, 58, 90

Vol. 12, No. 2

#

CONTENTS

E. S. DEMIAN and F. YOUSIF

Embryonic development and organogenesis in the snail
Marisa cornuarietis (Mesogastropoda: Ampullariidae). 2
Ш. Development of the circulatory and renal systems. ..... e SUR

E. S. DEMIAN and F. YOUSIF

Embryonic development and organogenesis in the snail

Marisa cornuarietis (Mesogastropoda: Ampullariidae).

IV. Development of the shell gland, mantle and

respiratory OrganS ....... A A A cate bo ..

J. ‚N. CATHER
Regulation of apical cilia development by the polar lobe of

imnanassa (Gastropoda,-Nassarüdae)... ору о eee

M. L. M. LE PENNEC

М. В. CARRIKER and H. H. CHAUNCEY

Effect of carbonic anhydrase inhibition on shell penetration fy a
by the muricid gastropod Urosalpinx cinerea ...... 1 1040 da 24

ds B. MORTON

Some aspects of the biology and functional morphology of
the organs of feeding and digestion of Limnoperna fortune
= (Dunker) (Bivalvia: Mytllacea); Save ue ala he siete fe AL AA

S. K. PIERCE '

2 The rectum of “Modiolus” demissus (Dillwyn) (Bivalvia:
Mytilidae): A clue to solving a troubled taxonomy..... Fisk oes JE
7)

М. Е. PONDER

Е
tr 4 The origin and evolution of the Neogastropoda ............. aire
“A

E. FISCHER-PIETTE and D. VUKADINOVIC

Sur les mollusques fluviatiles de Madagascar....... N
o ó

AE CLAMPITT
| ¿ Substratum as a factor in the distribution of pulmonate
AN snails in Douglas Lake, Michigan. .... wa tae TR a sale tee due) US

3 Published at the Museum of Zoology, The University of Michigan, Ann Arbor, п.
HAUT Michigan 48104, U.S. A. , by the Institute of Malacology y by à à». ae

a e DE $ "4 É ; ñ | ; À TAN 4 CEA
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