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VOL. 11 E 1971-1972

MALACOLOGIA

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

Internationale Malakologische Zeitschrift

MALACOLOGIA, VOL. 11

ANG 14 7
HARVARO NEW NAMES
UNIVERS!

GASTROPODA

Problacmaea, Golikov & Kussakin, 1972, 288
mosakalevi (Problacmaea), Golikov & Kussakin, 1972,

CEPHALOPODA

aspera (Galiteuthis), Filippova, 1972, 400
knipovitchi (Moroteuthis), Filippova, 1972, 392
Kondakovia, Filippova, 1972, 395

longimana (Kondakovia), Filippova, 1972, 395

zt

290

MALACOLOGIA, VOL. 11

CONTENTS

Abbreviated titles of scientific publications and place names to be used in

literature citations in MALACOLOGIA............

F. R. BERNARD

The genus Thyasira in western Canada (Bivalvia: Lucinacea). .....

D. BOLTOVSKOY

Pteropodos Thecosomados del Atlantico sudoccidental..........

D. S. BROWN, G. OBERHOLZER and J. A. VAN EEDEN

The Bulinus natalensis/tropicus complex (Basommatophora:
Planorbidae) in south-eastern Africa:

I. Shell, mantle, copulatory organ and chromosomenumber.......

D. S. BROWN, G. OBERHOLZER and J. A. VAN EEDEN

The Bulinus natalensis/tropicus complex (Basommatophora:
Planorbidae) in south-eastern Africa:

II. Some biological observations, taxonomy and general discussion. . .

P. CHANLEY and J. D. ANDREWS

Aids for identification of bivalve larvae of Virginia....

A. S. ELWELL and M. J. ULMER

Notes on the biology of Anguispira alternata

(Stylommatophora: Endodontidae). .

R. M. FELDMANN

First report of Hercoglossa ulrichi (White, 1882)
(Cephalopoda: Nautilida) from the Cannonball Formation

(Paleocene) of North Dakota, U.S.A.

J. A. FILIPPOVA
New data on the squids (Cephalopoda: Oegopsida)

from the Scotia Sea (Antarctic)....

A. GOLIKOV and O. KUSSAKIN

Sur la biologie de la reproduction des patelles de la famille

.. . 0000 . owe ee

. . . . . . . . ee ee © .

Tecturidae (Gastropoda: Docoglossa) et sur la position

systématique de ses subdivisions. .

H. M. LAWS

The chromosomes of some Australasian Paryphantidae.....

ET.

LO

Compatability and host-parasite relationships between species of the
genus Bulinus (Basommatophora: Planorbidae) and an Egyptian
strain of Schistosoma haematobium (Trematoda:Digenea).. .

222

e... oc.

. 415

. 365

LA

. 141

Ce

. 199

. 407

. 391

. 287

. 225

MALACOLOGIA, VOL. 11

CONTENTS (cont.)

W. F. PONDER

The morphology of some mitriform gastropods with special reference

to their alimentary and reproductive systems (Neogastropoda)....... 295
D. B. RAO, M. C. VENKATASUBBAIAH, R. S. REDDY, A. N. RAJU, P. V. RAO

and K. S. SWAMI

Metabolism of brooding young from aestivating adults of the banded

pond snail ‘Viviparus: dengalenstsy.) aie. mejia an
Q. J. STOBER

Distribution and age of Margaritifera margaritifera (L. ) in

a Madison River (Montana, U.S.A,):mussel.bed..... . 0 Lt OR
P. YOKLEY, Jr.

Life history of Pleurobema cordatum (Rafinesque 1820)

(Bivalvia: Unionacea) . . 0501819 . . . . оо оф 00 Фо ee O ¡0 0, 0: je CO МУ ОО 351
C. M. YONGE

On functional morphology and adaptive radiation in the bivalve
superfamily Saxicavacea (Hiatella (=Saxicava), Saxicavella,
Panomya, Panope, Cyrtodaria) x! «wis civ ore еее aan AL

iv

Le
/OL.11 NO. 1

\ SEPTEMBER 1971

аа
| уе

OCT 22 i971

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| | Frais A TOT
(4 HARVARD
UNIVERSIA

MALACOLOGIA

| в -

nternational Journal of Malacology

_ Revista Internacional de Malacologia

Journal International de Malacologie
Международный Журнал Малакологии

- Internationale Malakologische Zeitschrift

MALACOLOGIA

GENERAL EDITOR MANAGING EDITOR
C. J. BAYNE S. K. WU
Department of Zoology Museum of Zoology
Oregon State University University of Michigan
Corvallis, Oregon 97331, U.S.A. Ann Arbor, Michigan 48104, U.S.A.

EDITORIAL ASSOCIATES

ANNE GISMANN, General Editor E. PERISHO KAWAMURA, Secretary
R. NATARAJAN, Associate Editor for India J. B. BURCH Editor-in-Chief
* * * LS * * * * *

MALACOLOGIA, the international journal of molluscan research, is a multilingual publica-
tion dealing with all aspects of the study of mollusks, including morphology, ecology, evolution
and fossil record, classification, distribution, physiology, biochemistry, cytology, genetics,
parasitism, ete. MALACOLOGIA is published by the Institute of Malacology, 1336 Bird Road,
Ann Arbor, Michigan, U.S.A. The Sponsor Members of this Institute, also serving as editors,
are listed below.

N. F. SOHL, President E. G. BERRY
R. ROBERTSON, President-Elect J. В; BURCH
J F. ALLEN Vice-President M. R. CARRIKER
C. R. STASEK, Secretary G. M. DAVIS
K. J. BOSS, Treasurer A. G. SMITH
* * * * * * * * *

Increasing production costs regrettfully have necessitated increasing subscription prices.
Beginning with Vol. 13 (1972) subscription price per volume for North American institutions
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MALACOLOGIA MALACOLOGIA MALACOLOGIA

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PONT

P. O. AGOCSY
Magyar Nemzeti Müzeum
Baross U. 13
Budapest, VIII. , Hungary
E. E. BINDER
Muséum d’Histoire naturelle
1211 Geneva 6
Switzerland
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Technische Universitat
Braunschweig
Braunschweig, Germany
A. H. CLARKE, JR.
National Museum of Canada
Ottawa, Ontario
Canada
E. S. DEMIAN
Department of Zoology
Ain Shams University
Abbassia, Cairo, Egypt, U.A.R.
C. J. DUNCAN
Department of Zoology
University of Liverpool
Liverpool L69 3BX, England
Z. A. FILATOVA
Institute of Oceanology
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Mus. Nat. d’Hist. Natur.
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National Science Museum
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Tokyo, Japan
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Department of Biology
University of Waterloo
Waterloo, Ontario, Canada
K. HATAI
Inst. Geology & Paleontology
Tohoku University
Sendai, Japan
N. A. HOLME
Marine Biological Assoc. U.K.
The Laboratory, Citadel Hill
Plymouth, Devon, England
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Naturhistoriska Museet
Goteborg 11
Sweden
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Los Angeles County Museum
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A. M. KEEN
Department of Geology
Stanford University
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M. A. KLAPPENBACH
Museo Nacional Historia Natural
Casilla de Correo 399
Montevideo, Uruguay
Y. KONDO
Bernice P. Bishop Museum
Honolulu, Hawaii 96819
U.S.A.
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Marine Biological Laboratory
Gronnehave, Helsingor
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N. ODHNER
Evertebratavdelningen
Naturhistoriska Riksmuseet
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Carnegie Museum
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The Australian Museum
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Auckland Institute
and Museum
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R. D. PURCHON
Chelsea College of Science and
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C. P. RAVEN
Zoölogisch Laboratorium
Rijksuniversiteit
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U.S. National Museum
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Institute of Marine Research
Biological Lab. , Bulevardi 9 A
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Marine Biological Station
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India
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Zool. Inst. der Universitat Wien
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Rijksmuseum v. Natuurl. Historie
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Western Australian Museum
Perth, W. Australia
Australia
C. M. YONGE
Department of Zoology
The University
Edinburgh EH9 3JT, Scotland
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A. ZILCH
Senckenberg-Anlage 25
6 Frankfurt am Main 1
Germany

HORACE BURRINGTON BAKER
(1889-1971)

With deep regret we report the death of Dr. Horace Burrington
Baker on March 11, 1971. He was a member of the Editorial
Board of MALACOLOGIA and for many years was also involved
with the editorship of The Nautilus. From 1920 until his retire-
ment in 1959 as Professor Emeritus of Zoology, Dr. Baker was
at the University of Pennsylvania. From 1925, he was also a
Research Associate or Fellow at the Academy of Natural Sciences
of Philadelphia. Dr. Baker is best known for his studies of land
and freshwater gastropod anatomy.

MALACOLOGIA, 1971, 11(1): 1-44

ON FUNCTIONAL MORPHOLOGY AND ADAPTIVE RADIATION IN THE BIVALVE
SUPERFAMILY SAXICAVACEA (HIATELLA (=SAXICAVA), SAXICAVELLA,
PANOMYA, PANOPE, CYRTODARIA)

C. M. Yonge =

University of Glasgow
Scotland

ABSTRACT

Study has been made of species of the 5 genera constituting the superfamily
Saxicavacea, namely Hiatella sp. , Saxicavella jeffreysi, Panomya ampla, Pano-
pe generosa and Cyrtodaria siliqua, all except the last in life as well as in dis-
section and after sectioning. They are shown to constitute a natural group of
bivalves with modification, especially of the pallial characters, permitting an
interesting range of adaptive radiation. Essentially isomyarian (except Saxica-
vella) with a very reduced heterodont dentition, they have a massive external
opisthodetic ligament with, except in Cyrtodaria, a greatly reduced anterior outer
ligament layer. Mantle fusion is intimate. It involves, apart from Saxicavella,
complete fusion of the periostracal secreting epithelia. This is responsible for
the thick periostracum covering the siphons and other projecting pallial tissues
and for the important secondary extensions to the primary ligament. The pedal
gape is small. The mantle cavity is extended posteriorly forming a post-valvular
extension into whichthe ctenidia pass. There is striking hypertrophy of the pallial
muscles with the muscle attachments often as broad as those of the adductors.
This, together with gaping valves whichcannot accommodate the retracted poste-
rior regions, is a conspicuous feature of the last 3 genera. The relative regions
occupied by the post-valvular extension and the siphons differ very strikingly
between the externally very similar Panomya and Panope. Ctenidia and ciliary
currents are similar throughout with Panope and Cyrtodaria alone possessing
plicate (although still homorhabdic) ctenidia. In all but Saxicavella, massive
mucous glands occur on either side of and behind the pedal gape. The moder-
ately developed foot is associated with byssal attachment in the epifaunal Hia-
tella (which may also bore into rock) and Saxicavella; a reduced foot with slow
vertical penetration into soft substrates in Panomya and Panope; and a much
larger foot with horizontal movement through such substrates in Cyrtodaria
where alone the anterior territory of the mantle/shell is the larger. Other or-
gans of the viscero-pedal mass are essentially similar in all genera. A highly
significant feature inthe Saxicavacea is the development of high pressures within
the mantle cavity. The intimate pallial fusion with hypertrophied orbital muscles,
the post-valvular extension and the massive external, convex ligament are all
associated with this and provide the means of boring in Hiatella and of burrowing
in the infaunal Panomya, Panope and Cyrtodaria. Although differing from other
genera in being heteromyarian and with less intimate pallial fusion, Saxicavella
has the same pattern of form, including hinge and ligament, as the other genera
and is rightly included in the superfamily.

lPresent address: Department of Zoology, West Mains Road, Edinburgh EH9 3JT, Scotland.

(1)

2 C. M. YONGE

CONTENTS
Page Page
PEBOBUETIONT daa a ue 2 Organs in the Mantle Cavity.... 22
Ciliary Currents’ < ..2.. RES 23
E RAL CHARACTERS: 2.2 . - .-.. . 2
A a oN - Visceropedal Mass. ... oe 24
о E a a PAÑOPE . a o 24
Species Examined ............ 4 Sa irate
Е | Distribution... 2. 24
Habitat and Habits 2. 2.222.000. 4 Habitat and Habit 95
External Appearance and Shell... .6 E я Bi Da d Shell . ; 95
Hinge and Ligament 00.00. iaa i AS Da a ee
Е Hinge and Ligament . . sa. 26
Mantle Martens ere et ue. 10 :
Е 2 Mantle Margins..... 2 zen 29
Organs in the Mantle Cavity....10 : '
> Organs in the Mantle Cavity..... 29
Ciliary Current. Hr. 11 iy
Visceropedal Mass 12 Ciliary Currents...) ieee 30
EY Visceropedal Mass. . al
SARICAVEBRFA Fd. Rennen ere ons 13
Habitat and Habils ne ner et 13 en Et à ri
External Appearance:and Shelly. ...14 5° as LAA ee
External Appearance and Shell . . . 32
Hinge and Ligament . ..... 2... 15 Е :
: Hinge and Ligament . 2... ne 33
Mantle Mar pins: a cine 15 5
M Mantle Margins’. „2... A 35
Organs in the Mantle Cavity..... 16 3 Е
ane Organs in the Mantle Cavity..... 35
Ciliaryve CUrrents ising oot RER 16 Л
Visceropedal Mass 16 Visceropedal Mass. CE 39
AN: Fr ER Habitat and Habits . . nee
DANOMTAN A cure’ о tete: 16
DESTLIDUCION: eat 18 DISCUSSION... onerosa 37
Bapitatand: Habs ива 19
External Appearance and Shell... 20 ACKNOWLEDGEMENTS... 00m... 39
Hinge and Ligament: :. ле... 22
Mantle’Marginsen a lis 22 LITERATURE:GITED "PRE 39
INTRODUCTION itive isomyarian to a heteromyarian or,

The Bivalvia are most suitably sub-
divided into a series of superfamilies,
the “Stirps” of Thiele (1935), each pos-
sessing a pattern of well defined char-
acters. In the mantle/shell these include
external form with the relative extent
of anterior and posterior territories
(Yonge, 1955) and consequent effects on
the ligament; also the extent of mantle
fusion (Yonge, 1957) with effects on the
siphons where these occur. In the en-
closed body, or viscero-pedal mass,
they include form of the foot and, where
the byssus is retained into adult life,
possible reduction of the anterior por-
tion of the body. This change involves
reduction of the anterior territory of the
mantle/shell and change from the prim-

beyond that, to a monomyarian condition
(Yonge, 1953). The nature of these char-
aracters and the directions in which they
can be modified determine habit and
habitat. Exploitation of particular habi-
tats may be successfully accomplished
by a variety of possible routes, a fact
which explains the frequency of conver-
gence within the Bivalvia. For instance,
representatives of no less than 6 super-
families (including the Saxicavacea) have
independently acquired the structural
modifications necessary for deep bur-
rowing although representatives of only
2 of these (again including the Saxi-
cavacea) have become further special-
ised for boring into rock.

The Saxicavacea form an excellent
example of a superfamily. Asdescribed

ADAPTIVE RADIATION IN SAXICAVACEA 3

below, modifications of a basic pattern
have fitted species of its 5 constituent
genera both for epifaunal life leading to
rock boring and for infaunal life leading
to penetration, in the case of Panope, to
depths unequalled by any other deep bur -
rowing bivalves.

According to Stanley (1968) this super -
family appears during the Mesozoic
when, following more intimate fusion of
the mantle margins (Yonge, 1958), si-
phons were first acquired and so deep
burrowing and “siphon feeding” became
possible. His further statement that
most members of this group “occupy
cavities in hard substrata” requires
qualification.

GENERAL CHARACTERS

Lamy (1923) and Thiele (1935) have
summarized, largely on conchological
considerations, the main characters of
the Saxicavacea. The solid, more or
less elongated and often irregular shell,
which usually gapes posteriorly, has
concentric ribbing and is covered with
a thick periostracum. The ligament is
external, the cardinal tooth is small or
degenerate and there are no lateral teeth.
The adductor impressions are often ir-
regular with the line of pallial attachment
discontinuous or irregular witha distinct
pallial Sinus. The mantle is largely
united with an opening for the small foot
and extended into large siphons covered
by thick periostracum. The ctenidia
are united posteriorly, have either
smooth or plicate lamellae and very dis-
similar demibranchs.

It should be added that the Saxicavacea
are essentially isomyarian. Although the
byssus is retained into adult life in Hia-
tella and Saxicavella, only inthe latter is
there some reduction of the anterior half
of the body and of the anterior territory
of mantle/shell involving reduction of the
anterior adductor, i.e., some tendency

towards the heteromyarianism fully ex-
hibited by the more extensively byssally
attached Mytilacea and Dreissenacea
(Yonge & Campbell, 1968). Apart from
this, modification inform - and so in habit
-is due entirely to changes in the
mantle/shell; the proportions of the en-
closed viscero-pedal mass remain un-
changed as they do in the elongated
Solenacea (Yonge, 1952a; Owen, 1959).
Changes in the growth gradients around
the mantle margin produce aposteriorly
elongated shell with an even more elon-
gated mantle cavity. There are conse-
quent effects on the ligament which be-
comes opisthodetic. Maximum degree
of fusion of the mantle margins results
in general coverage of free surfaces,
including the siphons, with periostracum.
The functional significance of these char -
acters will become apparent in the
course of this paper.

These major characters are pos-
sessed by species of 5 genera, namely
Hiatella Daudin 1801 (= Saxicava Fleu-
riau de Bellevu 1802), Saxicavella Fi-
scher 1878, Panomya Gray 1857, Panope?
Menard de la Groye 1807, Cyrtodaria
Daudin 1799. Hiatella is much the com-
monest genus with species, most nu-
merous in colder seas, in both northern
and southern hemispheres. These occur
in shallow water, intertidally, and nor-
mally on, or boring into,a rocky sub-
strate. The little known Saxicavella,
although byssally attached, occurs on
soft substrates from moderate to great
depths. Panomya, a deep burrower,
occurs in moderate to considerable
depths in both the North Atlantic and
the North Pacific. Panope, the largest
of all deep burrowers, occurs inter-
tidally and in shallow depths in the same
oceans but also around Australia and
New Zealand. Cyrtodaria, ahighly mod-
ified more superficial burrower, is also
present in both northern oceans. Sin-
gularly little is known about species of

2Panope has a few months priority over Panopea (Dall, 1912).

4 C. M. YONGE

FIG. 1. Hiatella sp.

Intact animal viewed from left side with siphons fully extended. For

lettering onthis and subsequent figures see opposite page.

all these genera other than the first.
Fortunately the commonest, Hiatella,
is almost the least modified and forms
a good starting point for this survey of
the Saxicavacea.

HIATELLA

Species Examined.

While 3 species, Hiatella arctica, H.
gallicana (rugosa) and H. pholadis have
been described in both the North Atlan-
tic and the North Pacific, the question
of specific identity, at any rate between
the 2 first, is unusually obscure. At
one time H. gallicana was thought al-
ways to bore into rock while H. arctica
“nestled”, attached by byssus threads,
in crevices or in old borings. But while,
as shown by Lebour (1938) and Jorgen-
sen (1946), there are certainly 2 post-
larval forms, shell characters in the
adult would seem to depend entirely on
habit. This has been shown by Hunter
(1949) who considers that both species
may bore and so lose the spines on the
shell (see Fig. 1), formerly regarded as
diagnostic of H. arctica. In the Clyde

Sea Area he found that the shell form
attributed to H. gallicana is commonest
both among boring and non-boring indi-
viduals. For this reason, the specimens
obtained from Millport and examined,
largely for ciliary currents, in life are
referred to as Hiatella sp.; this also
appears the safer procedure when deal-
ing with sections prepared from small
individuals collected at Friday Harbor
and elsewhere in Puget Sound and locally
considered to be H. arctica, although
Quayle (1960) in his account of the inter-
tidal bivalves of British Columbia would
apparently regard them as H. gallicana.
The larger, and clearly valid, species
H. pholadis which, at any rate in British
Columbia (Quayle, 1960), occurs mainly
in the boring of pholads in intertidal
and subtidal regions, has been examined.

Habitat and Habits.

Hunter (1949) described the activity of
young individuals following settlement on
a rock surface and, as a result of their
strong “low thigmo-taxis”, their even-
tual byssal attachment in crevices, Sub-
sequently animals may either remain

ADAPTIVE RADIATION IN SAXICAVACEA

KEY TO LETTERING ON FIGURES

A anus

AAD anterior adductor

AOL anterior outer ligament layer

AOM epithelium secreting anterior outer
ligament layer

APR anterior pedal retractor

AU auricle

AX ctenidial axis

BM branchial muscle

BY byssus

CG cerebro-pleural ganglion

CN cavity of nymphal ridge

GE clear periostracum

CT ctenidia

DD digestive diverticula

E exhalant current

EA exhalant aperture

ES exhalant siphon

F foot

FIF fused inner mantle folds

FIOF fused inner surfaces of outer
mantle fold

FMF fused middle mantle folds

G gonad

GL pallial mucous gland

GO opening of gonad to exterior

I inhalant current

ID inner demibranch

IA inhalant aperture

IF inner fold of mantle

IL inner ligament layer

IOF inner surface of outer mantle fold

IS inhalant siphon

K kidney

L ligament

LP labial palp

M mouth

MF middle mantle fold

MG mid-gut

attached by the byssus, i.e., live as
“nestlers”, or else excavate a boring.
Their final habitat depends on the nature
of the rock, in Hunter’s words, “Those
settling on a Smooth surface of soft
homogenous rock will bore; those on a
hard but creviced rock surface will
become byssally attached non-boring
adults.”

The process of boring demands no such
structural modifications of shell and
foot as are found in the Pholadidae and

MI mantle isthmus

N nymphal ridge

O oesophagus

OC outer calcareous layer after
decalcification

OF outer mantle fold

OOF outer surface of outer mantle fold

P periostracum

PAD posterior adductor

PC pericardium

PEG pedal ganglion

PG periostracal groove

PGA pedal gape

PL pallial line

PM pallial muscle

POL posterior outer ligament layer

POM epithelium secreting posterior

outer ligament layer

PPR posterior pedal retractor

PS pallial sinus

PSE epithelium secreting periostracum

PVE post-valvular extension

R rectum

RO renal opening

S stomach

SE branchial septum

SI siphonal extension

SO socket

SR siphonal retractors (scar)

SS style sac

E tooth

LU calcareous tubercles

U umbo

UIOF united inner surfaces of outer
mantle fold

V valve

VE ventricle

VF valvular flap

VG visceral ganglion

the Gastrochaenidae. Boring is carried
out by the valves which are forced apart
by water pressure within the mantle
cavity. Hunter has shown that this is
essentially the same as the protective
reaction which is provoked in attached
animals by mechanical stimuli or change
in light intensity. As shown in Fig. 2
these live, ventral side uppermost, in
narrow crevices fastened to both walls
by byssus threads. The siphonal and
pedal openings are closed andthe siphons

6 C. M. YONGE

B

FIG. 2. Hiatella sp. A, Animal attached by
byssus threads in the base of an empty bar-
nacle shell: B, in boring, with post-valvular
extension gripping the walls (after Hunter,
1949).

then withdraw, forcing water into the
mantle cavity (enlarged as described
later) and forcing the valves apart. By
this means the shell is wedged tightly
against the walls of the crevice. The
only difference in boring is that the ani-
mal is not attached by byssus but grips
the walls of the boring by lateral dis-
tension of the region at the base of the
siphons here designated the post-valvu-
lar extension of the mantle cavity (Fig.
1, PVE) the volume of which it signifi-
cantly increases, The boring is circu-
lar in cross section indicating that the
animal must constantly change position
within it, i.e., unlike Botula which bores
while byssally attached (Yonge, 1955).
In Hiatella, it should be noted, the
initial epifaunal habit, made possible
owing to retention into adult life of the
byssus (Yonge, 1962b), has beenfollowed
by change to a rock boring habit with
accompanying loss of byssal attachment.

External Appearance and Shell.

The general appearance of a non-boring
individual is shown in Fig. 1. The shell,

which gapes posteriorly, is usually most
irregular with hardly 2 specimens. the
same (as described and figured by Hun-
ter, 1949); in this case it is very regu-
lar. It is essentially equivalve (many
individuals are not) with 2 conspicuous
posteriorly running ribs bearing low
Spines. It is inequilateral with the area
of the posterior territory of the mantle/
Shell about twice that of the anterior
territory. As indicated in Fig. 1, itis
everywhere covered with very thick
periostracum (P) as are all exposed
pallial tissues, i.e., dorsally at either
end of the ligament, posteriorly over
the post-valvular extension and the si-
phons, and along the entire length mid-
ventrally. The siphons are relatively
short, at least half of the tissues extended
posteriorly consisting of the post-valvu-
lar extension (Fig. 1, PVE) of the mantle
cavity containing the posterior portion of
the ctenidia (see Fig. 7). In a real
sense the mantle cavity is too large to
be contained within the valves. The
important functional consequences of this
have already been mentioned. The in-
halant siphon (IS) is about twice the
length of the exhalant siphon (ES) with
consequent wide separation of the 2 cur-
rents. The external opisthodetic liga-
ment (IL, POL) forms a rounded mass
posterior to the anteriorly inclined um-
bones (U).

The internal surface of the shell
(Fig. 3) is marked with the impressions
of the adductors (AAD, PAD) and of the
pedal (and byssal) retractors the ante-
rior of which is separately inserted
(APR), the. posterior one (PPR) merged
with that of the adductor (PAD). The
pallial line (PL) is interrupted but thick,
indicating considerable development of
the orbital muscles. The pallial sinus
(PS) is deep with large muscle inser-
tions on the dorsal and ventral sides,
indicating the presence of 2 sets of
powerful siphonal retractors (SR) by
means of which the thick siphons, with
periostracal covering thrown into crin-
kled folds, are effectively, if not quite
completely, withdrawn within the pos-

ADAPTIVE RADIATION IN SAXICAVACEA 7

APR

FIG. 3. Hiatella sp.

terior margins of the shell.
Hinge and Ligament.

Although the anterior territory is
reduced, the hinge line remains parallel
to the antero-posterior axis, i.e., there
is no tendency towards heteromyaria-
nism. The hinge is very simple with a
reduced heterodont dentition. In small
shells only, there is a single small
cardinal tooth on the right valve fitting
into a socket between 2 still smaller
teeth on the left valve. In adult shells
teeth are lost.

The ligament, highly characteristic of
the superfamily, is large, external and
markedly opisthodetic. It is shown in-
tact from the dorsal aspect, in longitu-
dinal section and from the ventral aspect
in Figs. 1, 3, and 7 respectively and dia-
grammatically in Fig. 5. It is situated
posterior to the umbones (U) and is
covered with thick periostracum (P) to
which it is intimately united at both
ends (see Figs. 1, 5, 7). Beneath it is
composed in almost equal parts of thick
inner ligament layer (IL) and of poste-
rior outer ligament layer (POL) which
extends over this and forms a broad

AOL ee
PS

RED,

SR

Interior of right valve showing ligament and muscle scars.

band posterior to it, i.e., over the epi-
thelium which secretes it. Anterior
outer ligament layer (AOL), as shown in
section in Fig. 4b, c and also diagram-
matically in Fig. 5, is reduced to negli-
gible amounts. The 5 layers described
in the ligament by Hunter consist of the
superficial periostracum together with
subdivisions of posterior outer andofin-
ner ligament layers due probably to dif-
ferences in physical properties (and so
in staining reactions) associated with
compression or extension. The margin
of the valves posterior to the umbones
is curled inward formingnymphalridges
(Fig. 3, N). The result is to carry the
area of union with the ligament from the
inner to the dorsal surface as shown in
section in Fig. 4. The convex external
ligament so formed permits wide sepa-
ration of the valves.

Details of ligamental structure, in-
cluding the presence of the extremely
reduced and certainly functionally negli-
gible anterior outer ligament layer (AOL)
are shown in Fig. 4a-g. The presence
of thick periostracum (P) anterior to
the ligament is shown in a, over it in
b-f and posterior to it ing. Itis se-

8 С. М. YONGE

UIOF

FIG. 4. Hiatella sp. Transverse sections through ligament. a, anterior to ligament; b, through
region of anterior outer ligament layer lying between diverging ends of inner ligament layer;
c, showing diverging ends of posterior outer ligament layer; d, full development of inner and
of posterior outer ligament layers; e, posterior outer ligament layer only; f, near posterior end
of posterior outer ligament layer; g, posterior to ligament showing fused periostracum.

ADAPTIVE RADIATION IN SAXICAVACEA 9

FIG. 5. Hiatella sp. Ligament.

creted by the united inner surfaces of
the outer mantle folds (UIOF). Anteri-
orly (b, c) the inner ligament layer (IL)
with the mantle isthmus (MI) and the
posterior outer ligament (POL) are split
for a short distance (see also in Fig. 5).
The major regions of the ligament are
shown in sections d and e, made respec-
tively through the middle of the length
of the inner ligament with posterior
outer ligament above it, and through the
latter exclusively in the region behind.
As shown in f and also in Fig. 5, the
posterior surface of this layer (POL)
is crescentric, the margins taking the
lead in backward extension under the
periostracum.

The ligament in Hiatella (andthrough-
out the Saxicavacea) is characteristically
displaced well behind the umbones. This
would appear to be afurther consequence
of the growth gradients responsible for
the posterior pallial enlargement already
noted. The anterior outer ligament
layer is greatly reduced. But this is
not because the ligament is opisthodetic
(as, of course, it is). For instance in
the etheriid Bartlettia (Yonge, 1962a)
where the ligament is probably even
more opisthodetic but where it originates

Diagrammatic views of ligament.
showing positions of umbones and teeth, inner margins of nymphal ridges indicated by broken
lines; below, longitudinal section, arrows indicating direction of growth of ligament layers.

Above, viewed dorsally,

well to the anterior of the umbones,
this layer is almost as large as the
posterior outer layer and forms an im-
portant part of the functional ligament.
The extension posteriorly between the
umbones of periostracal secreting sur-
faces (UIOF) probably accounts for the
overgrowth and resorption of the teeth
(better observed in Panope). The ante-
rior splitting of the ligament super-
ficially resembles conditions in the Lu-
cinacea and Veneracea (Allen, 1958;
Ansell, 1961) where it is attributed to
the action of a small tangential com-
ponent in shell growth [as fully repre-
sented in Glossus (Isocardia) and in the
Chamidae (Owen, 1953: Yonge, 1967)].
This is very probable in these bivalves
with rounded shells. But in Hiatella the
dorsal margins of the valves are straight
and the ligament elongated. As indicated
by Hunter, there is some antero-poste-
rior rocking of the valves on a dorso-
ventral axis running through the middle
of the ligament and the anterior split-
ting of the ligament may well be associ-
ated with this. Hunter stated that this
rocking assists the process of boring as
it probably does. Primitively (and ex-
clusively in individuals which do not

10 C. M. YONGE

bore) it appears to be concerned with
protection. It permits the withdrawal
into the posterior gape of the post-
valvular pallial extension and of the
bulk of the siphons. Both are massive
and covered with thick periostracum.

Mantle Margins.

These are fused, apart from the pedal
gape (Fig. 7 PGA) and the siphonal
openings. As indicated in transverse
section (Fig. 6), unionisintimate involv-
ing the inner and middle folds with the
consequent union in the mid-line of the
inner, periostracal-secreting, surfaces
of the outer marginal fold, i.e., repre-
senting Type ‘C’ (Yonge, 1957). This is
the reason why all exposed pallial sur-
faces are covered with periostracum.
Hunter (1949) has described and figured
the condition around the walls of the
pedal gape with the periostracal groove
running along the middle of these. The
2 valves are united ventrally by the cross
fusion of the radial pallial (orbital)
muscles (Fig. 6, PM) which are broadly
attached to the shell (Fig. 3, RL). Hun-
ter notes the formation in this way of
a muscular floor to the mantle cavity
which can act as an additional adductor.
Both of the siphonal openings are ringed
by the free middle and inner folds with
numerous tentacles arising from the
former surrounding each opening. The
inhalant opening has also an inner ring
of tentacles arising from the inner fold
but this is represented by a membrane
around the exhalant opening (see Fig.
1). The network of filtering tentacles
around the inhalant opening forms what
Morse (1919) in his account of living
Saxicava rugosa described as a “perfect
brush”. These tentacles and other ex-
posed tissues are coloured pink.

Organs in the Mantle Cavity

The appearance of an animal viewed
from the left side after removal of the
left valve and mantle fold is shown in
Fig. 7. The 2 adductors (AAD, PAD)
which, according to Hunter, cancontract
either together or alternately, are sim-

ilar in size, although the anterior mus-
cle is displaced ventrally. The foot (F)
with the large byssus threads (BY) issu-
ing at its base, is relatively large with
the posterior retractors (PPR) larger
than the anterior pair (APR); it is long,
slender and constantly active in young
animals according to Morse (1919) but
it shows little activity in the adult.

The elongated ctenidia (CT), non-
plicate and homorhabdic, extend behind
the posterior adductor into the post-
valvular extension to terminate at the
base of the siphons (they do not pass
into these). Similar post-valvular ex-
tensions occur in the Teredinidae and
also in the posteriorly elongated telli-
nacean, Solecurtus, but are formedinthe
latter by fusion of the inner mantle
margins only (Yonge, 1949).

The ctenidial axes are attached to the
sides but not to the posterior surface of
the visceral mass (there is a space here
through which water can be forced from
1 chamber to the other). Behind this
the gills are united by way ofthe ascend-
ing lamellae of the inner demibranchs.
These are not united to the visceral
mass except in the region anterior to
the shorter outer demibranch. This is
united for its entire length by way of the
ascending lamellae to the mantle surface;
it has a short supra-branchial extension
anteriorly. As recorded by Atkins
(1937), the lamellae are flat and homor-
habdic. There is a marginal groove
along the free margin of the inner demi-
branchs only. The palps (LP) are of
moderate size.

Conspicuous glandular areas, origi-
nally noted by Pelseneer (1911), extend
along either side of the mid-ventral
region of the mantle cavity. Hunter
found larger areas in boring thaninnon-
boring individuals; he thought this might
be due to “continued contact stimuli”,
due to the passage over them of ground
particles of rock. But in the non-boring
individuals, which alone were examined
in the course of this research,the glan-
dular areas could hardly have beenmore
extensive, as shown in Figs. 6 and 7

ADAPTIVE RADIATION IN SAXICAVACEA 11

PL

FIOF

FIG. 6. Hiatella sp. Transverse section through floor of mantle cavity showing complete fu-
sion of the mantle margins with periostracum extending between the valves: indicating also, the
presence ot glandular areas.

Une PPR

2mm.

APR 7 229 VE

2

ep,

ALU №” ZE PVE

<=

AAD— TEA

FIG. 7. Hiatella sp. Animal lying in right valve after removal of left valve and mantle lobe,
siphons partially withdrawn. Arrows indicate direction of respiratory and feeding currents;
broken arrows, currents on undersurfaces; feathered arrows, cleansing currents.

(GL). Similar glands occur throughout Ciliary Currents.
the Saxicavacea (and also in other super-

families); they do not appear to have As shown in Fig. 7 and already de-
any specific connexion with rock boring scribed by Atkins (1937), frontal cilia
but to be solely concerned with consoli- carry particles from the outer andinner

dation of the pseudofaeces. surfaces of the outer demibranch to the

12 C. M. YONGE

FIG. 8.

axis, but on the inner demibranch cilia
beat towards the marginal groove. Oral-
ward currents are restricted to these
2 routes. This disposition of ctenidial
currents corresponds to Atkins’ Type
C and occurs in the majority of eula-
mellibranchs. Atkins further reported
that the ctenidia in Hiatella are sensitive
and contract both antero-posteriorly and
dorso-ventrally.

The palps perform their normal selec-
tive function. Material rejected from
them or from the ctenidia collects on
the mantle surface and is carried (see
feathered arrows in Fig. 7) mid-
ventrally to the base of the inhalant
siphon where pseudofaeces (PS) accu-
mulate. Hunter writes of vortices here
and anterior to the pedal gape. He adds
that at regular intervals, of from 3 to
6 minutes, sharp contractions of the
adductors, with an accompanying with-
drawal of the foot and partial closure of
the pedal opening, cause expulsion of
pseudofaeces through the inhalant siphon,
as in the great majority of other bivalves.

Visceropedal Mass.

The anatomy of species of Hiatella
(Saxicava) has been briefly described by
Pelseneer (1911) with important addi-
tions by Hunter (1949). Only a general

Hiatella sp. View from left side showing internal anatomy.

account is now necessary to provide a
basis of comparison with the other
genera here considered. General struc-
ture is indicated in Fig. 8. The foot and
pedal (also byssal) muscles have already
been described. In the alimentary canal,
the oesophagus (O), as noted by Pelse-
neer, is unusually long in probable con-
sequence of the general posterior elon-
gation. Purchon (1958) has fully de-
scribed both structure and ciliary cur-
rents within the stomach which he in-
cludes within his Type IV. The same
pattern is found in the other genera.
The surrounding mass of digestive di-
verticula (DD) open by way of 9 ducts on
the left (3 via the left pouch), and by 2
ducts on the right side. The style sac
(SS), united with the mid-gut, opens
postero-ventrally and the gut coils ante-
rior to it and below the oesophagus
before passing posteriorly and thendor-
sally to traverse the ventricle (VE),
emerging as the rectum (R) and opening
at the anus (A) behind the posterior
adductor. The pericardium (PC) with
the enclosed heart (AU, VE) is dis-
placed somewhat posteriorly, as are
the kidneys (K). A pericardial gland
extends over the ventricle and adjacent
regions of the auricles (White, 1942).
Sexes are separate with the gonad (G)

ADAPTIVE RADIATION IN SAXICAVACEA 13

FIG. 9. Saxicavella jeffreysi. Shell, viewed from left.

when fully developed (as it is not in
Fig. 8) extending posteriorly over the
pericardium. The gonoduct (GO) opens
into the exhalant cavity just anterior to
the renal aperture (RO). The positions
of the cerebro-pleural and pedal ganglia
(CG, PEG) are shown in Fig. 8; the mas-
sive fused visceral ganglion (VG) lies
below the posterior adductor. A detailed
account of the nervous system is given
by Hunter who describes a pair of si-
phonate ganglia connected by pallial
nerves with the visceral ganglion and
also with the pallial ring and from which
branching nerves extend into the siphons.
However, neither in any specimen of
Hiatella nor in any other species of the
Saxicavacea could the presence of these
ganglia be confirmed.

SAXICAVELLA

This genus, of which Saxicavella jef-
freysi Winckworth was examined, has
been regarded by Thiele (1935) as a sub-
genus of Hiatella (Saxicava). Study of
the animal, however, reveals differences

which must be considered as generic.
This is apparently the first account of
anything beyond the shell in any species
of this somewhat rare genus. Unfortu-
nately living animals sentfrom Plymouth
were moribund when received, so that
only meagre information about conditions
in life could be obtained.

Habitats and Habits.

Information about habitat comes from
Holme (1959 and correspondence). Saxi-
cavella jeffreysi, with other species of
the genus, is sublittoral occurring on
soft substrates, both on clean sand and
on soft mud, probably in both (and cer-
tainly in the latter) attached by a sparse
byssus to shell fragments. In its mode
of attachment, sub-littoral habitat andin
its comparative rarity, this species
recalls the myacean, Sphenia binghami
(Yonge, 1951a). Under aquarium condi-
tions individuals were observed by Holme
to settle within empty valves of Spisula
indicating a habit like that of “nestling”
Hiatella. The species is widely, though
sparsely, distributed between the Ca-

14 С. М. YONGE

FIG. 10. Saxicavella jeffreysi.

4mm.

View from
posterior end showing inhalant and exhalant
apertures.

FIG. 11. Saxicavella jeffreysi.

2-5mm.

Interior of right valve showing ligament and muscle scars.

nary Islands and Gilbraltar in the south
and Bergen in the north according to
Jeffreys (1865) and Lamy (1923) who
refer to it as Panopea plicata and Saxi-
cava plicata respectively. Massy (1930)
states that it occurs in depths of between
9 and 1,207 fathoms.

External Appearance and Shell.

There are no siphons and the external
appearance, apart from the protruding
byssus threads, is that of the shell
shown in Fig. 9. This is small, never
exceeding 1 cm in length, and smooth.
It is markedly inequilateral with the
hinge line inclined anteriorly with con-
sequent reduction in depth of the ante-
rior territory, and enlargement of the
posterior, territory. This species is, to
some extent, heteromyarian.? The pro-
minent umbones face inwards. Internally

3The difference between Saxicavella and Hiatella resembles that between Cardita variegata and

C. ventricosa in the Carditacea (Yonge, 1969).

ADAPTIVE RADIATION IN SAXICAVACEA 15

24)

Y)

APR

AAD

TT,
N: 7
1) yt Li

PAD

Anm LD
| | Mm
I

4mm.

FIG. 12. Saxicavella jeffreysi. Animal viewed from left side after removal of left valve and

mantle lobe.

(Fig. 10) the anterior adductor scar is
a little smaller than that of the poste-
rior adductor; those of the small pedal
retractors are about equal in size. The
pallial line is barely detectable and
there is no sinus. Externally there is
a thin but well developed periostracum.
There is no posterior gape although the
valves do separate widely (see Fig. 11).

When expanded, byssus and sometimes
foot (Fig. 12) protrude through the pedal
gape (PGA). The appearance posteriorly
is shown in Fig. 11, the rounded inhalant
and exhalant openings almost flush with
the surrounding tissues.

Hinge and Ligament.

These are essentially as in Hiatella.
A small cardinal tooth has been reported
as present in the right valve but this is
usually absent in adult shells and none
was seen. The ligament (Fig. 10) is not
situated so far posterior to the umbones
as in Hiatella but, as revealed in trans-
verse section, has the same structure,
i.e., split anteriorly, with reduced ante-

rior outer, and very thick inner and.
posterior outer, layers. It isattachedto
prominent nymphal ridges (N).

Mantle Margins.

Here a significant difference from
Hiatella is revealed, fully adequate to
justify generic separation. As shown in
Fig. 12, while the general surface of the
exposed mantle tissues is covered with
periostracum, there is not complete
union alongthe mid-line ventrally. There
is a wide area of naked tissue [fused
inner mantle folds (FIF)] between and
around the inhalant and exhalant openings
(Fig. 11, IA, EA). Conditions aroundthe
mantle margins are indicated in the
sections shown in Fig. 13a-f. Anterior
to the pedal gape (a), there is fusion
only of the inner mantle folds (FIF) with,
of course, complete separation of all 3
folds (IF, MF, IOF) around the gape (b).
Fusion then proceeds in stages, first
(c) the union of the inner folds (FIF),
and then (d) of the middle mantle folds
(FMF). But there is never, as there is

16 C. M. YONGE

in Hiatella and in all other Saxicavacea,
complete union of the periostracal se-
creting surfaces present on the inner
surface of the outer mantle folds (IOF).
This is shown in d and e, the latter
indicating the beginning of separation of
the middle mantle folds which becomes
pronounced further posteriorly where
this fold enlarges to form the small
tentacles shown from the posterior as-
pect in Fig. 11. Dorsally there is com-
plete fusion of the periostracal secreting
surfaces and the same intimate union of
periostracum and ligament as in Hia-
tella. But the absence of complete ven-
tral union [i.e., fusion of Type B not C,
(Yonge, 1957)] of these surfaces sepa-
rates Saxicavella from the remaining
Saxicavacea.

The inhalant and exhalant openings
(Figs. 11, 12) are simple and bounded
exclusively by inner mantle folds bearing
no tentacles. They are separated by
some distance from the common sur-
rounding ring of short tentacles on the
middle mantle lobes (MF) outside which
is the line of the inner surface of the
outer mantle fold (OF) marking the limit
of periostracal secretion.

Organs in the Mantle Cavity.

The disposition of these is shown in
Fig. 12. All the organs are essentially
as in Hiatella. The great extent ante-
riorly of the inner demibranch (ID) is
notable and also posteriorly the great
space available owing to enlargement of
this region of the mantle cavity due to
heteromyarianism. But there is no
extra-valvular extension - only the po-
tentiality for this in the extensive (but
not complete) periostracal investment
of the exposed mantle tissues. The en-
largement of the posterior territory is
here, as in other, more heteromyarian,
genera, associated with byssal fixation
and involves a wide separation of inhal-
ant and exhalant currents (see Fig. 11).

Ciliary Currents.

Unfortunately the specimens were re-
ceived in too poor a condition for these
to be followed apart from the cleansing

currents indicated on the foot in Fig. 12.
But the ctenidia resemble those of the
other Saxicavacea (of which this genusis
certainly a member) and there is unlikely
to be any difference in what is, in any
case, a very Standard pattern.

Visceropedal Mass.

The general anatomy of S. jeffreysi is
shown in Fig. 14 which permits direct
comparison with conditions in Hiatella
(Fig. 8). In that genus the posterior
end is drawn out with a post-valvular
extension and large siphons. Here
the anterior end is reduced and the pos-
terior end enlarged in depth, a typical
heteromyarian condition (although here
with relatively little reduction of the
anterior adductor). This is associated
with byssal attachment on flat, open
substrates as inthe Mytilacea and Dreis-
senacea (Yonge & Campbell, 1968), and
in Sphenia (Yonge, 1951) and Entodesma
(Yonge, 1952b) (Myacea and Adesmacea
respectively). All are without,or with
very short, siphons in contrast to Hia-
tella which attaches in confined spaces
to become either a “nestler” or a borer
and has long siphons. The 2 pedal (and
byssal) retractors (APR, PPR) are ap-
proximately equal. The gut is very
Similar with long oesophagus and united
style sac and mid-gut although the latter
has no anterior coils but passes imme-
diately in a postero-dorsal direction.
The pericardium (PC), ventricle (VE)
and kidney (K) are somewhat more pos-
teriorly placed than in Hiatella, this
owing to the enlargement of the posterior
territory and so of the posterior half
of the visceropedal mass. The gonoduct
(GO) opens immediately anterior to the
renal pore (RO) but the extent of the
gonad is unknown. There are the usual
nerve ganglia (CG, VG), the pedal gan-
glia not being visible in this whole mount
of a small specimen.

PANOMYA
This, with the 2 succeeding genera,

is infaunal, a deep burrower in soft
substrates in contrast to the byssally

ADAPTIVE RADIATION IN SAXICAVACEA 17

1mm
FIG. 13. Saxicavella jeffreyST. Tansverse sections Tou ventral margins of mantle.

a, anterior to pedal gape; b, through pedal gape; c, immediately posterior to pedal gape show-
ing fusion of inner folds; d, showing fusion of middle folds of mantle; e, showing initial separa-
tion of middle folds; f, showing wide separation of middle folds. N.B. absence of fusion of

outer folds.

attached, or secondarily boring, Hiatella primarily due to the complete protective
and Saxicavella. Their highly success- covering provided by thick periostracum
ful exploitation of this mode of life is and to the exceptionally extensive areas

18 C. M. YONGE

CG

AAD

PGA

3mm

FIG. 14. Saxicavella jeffreysi. Internal anatomy viewed from left side.

of extruded pallial tissues, ventrally and
to some extent anteriorly, as well as
posteriorly.

Distribution

Species of this interesting but little-
known genus occur in the North Atlantic
and the North Pacific. Although long
known, the Atlantic Panomya arctica*
(Lamarck 1818) has rarely been taken
except as empty valves which mayreach
lengths of over 9 cm. It is a deep bur-
rower living often at considerable depths
and most unlikely to be taken intact by
a dredge. One of the few figures, if not
the only figure, of the intact animal [as
Panopaea norvegica; see Iredale (1915)
for synomymy] with extended “siphons”
is contained in Forbes & Hanley (1853)
and is here reproduced in Fig. 15. Itis
known to occur in soft, largely muddy,
substrates to considerable depths. The
shell is well described and figured by
Tebble (1966) who gives its distribution

as “from Iceland, and the Lofoten Is-
lands, to the British Isles, and down the
Atlantic coast of America to Chesapeake
Bay, and in the N. Pacific around the
Behring Straits”.

In the North Pacific a large variety,
turgida, of this species was described
by Dall (1916) from the Aleutians as far
eastward as the Shumagins with the
still larger species, P. beringiana, in
the eastern Behring Sea. The common-
est Pacific species, P. ampla, ranges
from the Arctic Circle as far south as
Puget Sound and also occurs in the Sea
of Okhotsk and off the north of Japan.
It is much the same size as P. arctica
but differs (Dall, 1895) “by its much
more heavy and rude shell, with a more
expanded posterior region and flatter,
more irregular valves.” Specimens
were collected and animals observed in
life at Friday Harbor. This account of
the genus is therefore based on exam-
ination of this species.

4Panomya spengleri Valciennes 1839 is preferred by Lamy (1923) to prevent confusion with

Hiatella (Saxicava) arctica.

ADAPTIVE RADIATION IN SAXICAVACEA 19

FIG. 15. Panomya norwegica.
Forbes & Hanley, 1853).

/ Gi a
War У

My Lo 4N!
— Ly:

‚II

+ ON CK

A S VONT
ie
SE DAS ANOS

FIG. 16. Panomya ampla.

Above, from left side; below, ventral aspect.

Animal with expanded siphons viewed from left side (from

DR 9215 D)

IN LE or =
I 5;

Dotted line indicates

posterior end of post-valvular extension (containing ctenidia).

Habitat and Habits.

On 2 occasions a total of 8 specimens
of Panomya ата (Fig. 16) was dredged
in a bottom of thick clay-like mud at a
depth of about 15 fathoms in Griffin Bay
at the south end of San Juan Island, Wash-
ington; the cut siphons of another indi-
vidual and some empty shells were also
taken. On other occasions the upper
region of a siphon together with many
cut siphons of the similarly infaunal

Mya truncata were dredged in mud at
Similar depths. The intact animals lived
well in aquaria where they readily bur-
rowed in mud from their normal habitat,
presumably largely by ejection of water
through the pedal opening, with the rela-
tively small foot being of only minor
assistance. When closed the tips of the
siphons are indistinguishable from the
surrounding mud but they become appar -
ent when they open (Fig. 17) owing to
the internal red colour then revealed.

20 C. M. YONGE

FIG. 17.

Panomya ampla.
siphons emerging on surface of substrate.

Appearance of

The surrounding tentacles normally ex-
tend over the surface of the mud but the
openings occasionally rise above this,
especially when extruding water. This
is done with great power through the in-
halant opening. Water containing pseudo-
faeces was sometimes shot for several
feet clear of the small aquarium tank.
The siphons are very sensitive. They
close immediately after particles of any
size or in unusual quantity enter. The
membrane surrounding the exhalant si-
phon constantly changes to reduce or
enlarge the area of the opening.

External Appearance and Shell.

The appearance of a fully extended
specimen of P. ampla viewed from both
lateral and ventral aspects is shown in
Fig. 16. The total “siphonal extension”
is some 3 times the length of the valves
within which it cannot be withdrawn.
The mantle tissues also extend anteriorly
while ventrally the valves are separated
by a distance almost equal to their depth
so that the appearance in section is that
of a somewhat rounded triangle. Every-
where the exposed tissues are covered
with a very dark, thick and much wrin-

AAD

3cm

FIG. 18.

Panomya ampla (A) and Panope
generosa (B). Interior of right valves show-
ing ligament and muscle scars.

kled periostracum with numerous ad-
herent sand grains. The pedal gape
(PGA), only some 5 mm long in the
specimen figured, is centrally placed and
directed ventrally. Despite the fact that
it must be deeply embedded in mud, the
opening in several specimens was sur-
rounded by colonies of minute Polyzoa.
Their presence indicates how frequently
the siphons extend. The pedal gape
was observed from time to time to
dilate forming acircular opening through
which water was shot out following sud-
den contractions of the hypertrophied
orbital muscle which forms the thick
floor of the mantle cavity. Following
extrusion of water, these tissues remain
contracted for some time although the
valves are always widely separated.

In an animal of shell length 4 cm, the
“siphonal extension” was 11 cm long.
Subsequent dissection revealed that the
ctenidia reached to within 1.5 cm of the
tip, i.e., that 86% of the extension re-

ADAPTIVE RADIATION IN SAXICAVACEA 21

FIG. 19. Panomya ampla.
ventral, aspect.

presented post-valvular extension of the
mantle cavity (up to PVE in Fig. 16).
This is a striking development from con-
ditions in Hiatella. The siphonal open-
ings separate only slightly (Fig. 17).
They are surrounded by an area of
clear periostracum (CP) without adher-
ent sand grains. This tucks in when the
siphons close and contract.

The shell valves gape widely at both
ends. Each is roughly rectangular and
distinguished from those of Panomya

Hinge and ligament;

above, viewed from dorsal; below, from

arctica by the truncated posterior mar-
gin (cf. Figs. 15, 16). They are mark-
edly inequilateral with the posterior
territory about 3 times the area of the
anterior; the umbones (U) face inwards;
the external ligament (L) is very prom-
inent. The thick chalky shell is covered
with a black periostracum which readily
flakes off. Internally the muscle inser-
tions are highly characteristic (Fig. 18,
A). The pallial line (PL) is as broad as
the adductor scars (AAD, PAD) and is

22 C. M. YONGE

separated into a number of separate
scars. The insertions of the siphonal
retractors (SR) are as large or larger
than those of the adductors. There is a
pallial sinus into which only a very lim-
ited proportion of the posterior tissues
can be withdrawn. Although completely
enclosing the visceral mass (except
ventrally), the shell in this genus may
best be regarded as providing attach-
ment for the massive pallial muscles
the contraction of which will force out
water, either through the pedal opening
in association with burrowing or through
the inhalant siphon in connexion with
cleansing.

Hinge and Ligament.

These exhibit the now familiar char-
acters. Although lost in older specimens,
the cardinal teeth, 2 on the left and 1 on
the right valve (Fig. 19, T), are initially
well developed. The ligament arises
just posterior to them dnd to the um-
bones. The hinge line is straight and
the ligament unusually long as well as
broad (Figs. 18,19). It is attached lat-
erally to very conspicuous nymphs (N)
which largely obscure it when viewed
from the ventral aspect (Fig. 19, lower).
Sections could not be made so that the
extent of the anterior outer ligament is
uncertain but both the inner layer and
the posterior outer layer are very thick
with periostracum extending over them.
The function of this ligament appears to
be to hold the valves firmly together, as
an opening thrust is unnecessary. Sep-
aration of the valves is caused by water
pressure generated in the mantle cavity
following contraction of the siphonal re-
tractors, the siphons and the pedal gape
being closed (as in Hiatella but on a
larger scale).

Mantle Margins.

Complete fusion occurs as in Hiatella
apart from the 3 openings. There is
great hypertrophy of the orbital (pal-
lial) muscles which form a thick floor
to the mantle cavity as shown cut through
in Fig. 20, PM. The walls of the pedal

gape (Fig. 21) consist of the extended
(and unciliated) surface of the middle
mantle fold (MF) which bears a con-
Spicuous band of orange pigment (see
Fig. 20) just within the periostracal
groove which extends a little way within
the outer opening. The inner opening is
bounded by lips formed from the inner
mantle fold (IF). This same fold bears
tentacles around the inhalant, and forms
a very mobile membrane around the
exhalant, siphon (Fig. 17); the middle
fold (MF) which extends around and be-
tween the siphons bears numerous pap-
illa-like tentacles.

Organs in the Mantle Cavity.

These are shown in Fig. 20. The vis-
ceral mass is Strikingly globular with a
firm muscular coat. The foot (F) has
relatively well developed retractors
(APR, PPR) and so presumably has some
function although burrowing appears
largely due to extrusion of water through
the pedal gape. The exceptionally long
ctenidia, of which about the anterior */;
is shown in Fig. 20, are similar to those
of Hiatella, the inner demibranch being
the larger and alone extending between
the long palps (LP) which are extensively
attached to the mantle. Probably cor-
related with the strains they encounter
when the powerful muscles contract,
the non-plicate lamellae are unusually
loose and wide. The axial region is
exceptionally wide (Fig. 20) with thick
strands of longitudinal muscle visible
below the epidermis. The axisis attached
to the sides but not to the posterior
face of the visceral mass. The inner
demibranchs are nowhere attached to
this but unite with one another posterior
to it. A space is thus left through which
water can pass from 1 branchial cham-
ber to the other when the massive pal-
lial muscles contract, otherwise the
ctenidia would rupture. Periodic surges
of water were observed following con-
tractions of the siphonal muscles. These
caused dilation of the ctenidia with pas-
sage of water from exhalant to inhalant
chamber. There is no supra-axial ex-

ADAPTIVE RADIATION IN SAXICAVACEA 23

PPR
eM SS PS
AAD I = Qe ; |
SIR SHE Yi) GE, ee
ne RUT 7 4 aS
=F 7 nr UMR
Sie N, 7
= К IN / И Y) YA a
ANS SU pe / M, —\\
CES x к ISA Y Hf, ul
E O Nat UN elie ES
a >> == = ee
NEU OR CANSO

FIG. 20. Panomya ampla. Animal viewed from left side after removal of left mantle and valve.

Arrows as before.

tension of the outer demibranch. Mar-
ginal grooves are present on all demi-
branchs. As in Hiatella, there is a very
large pallial mucous gland (Figs. 20,
21, GL) on the floor of the mantle cavity
on either side of the pedal gape but
extending both anterior and posterior to
this. The anus (A) reaches for ап excep-
tional distance behind the posterior ad-
ductor to discharge faeces into the
proximal region of the long post-valvular
extension.

Ciliary Currents.

On the ctenidia these are essentially
as in Hiatella. There is anexceptionally
powerful oralward flow along the wide
axial regions and others along the 4
marginal grooves. All frontal ciliacar-
ry particles to the free margins of the
demibranchs except those on the upper
2/; of the inner surface of the outer
demibranchs which beat towards the
axis (see broken arrows on OD in Fig.
20). Cleansing currents on the visceral
mass and mantle lobes carry particles

Р ОЕ
Panomya ата.
transverse section through pedal gape show-
ing position of mantle folds and glandular

FIG 21" Diagrammatic

areas. Arrows showing direction of lateral
currents; crosses showing region of posteri-
orly running currents.

postero-ventrally into the midventral
channel. As shown in Fig. 21, cilia
beat away from the lips of the pedal
gape and over the surface of the massive
mucous gland (GL) and then posteriorly
into the midventral channel (see feath-
ered arrows in Fig. 20). Here pseudo-
faeces massed in mucus from these
glands pass to the posterior end of the
long post-valvular extension to be ex-
pelled from time to time through the

24 C. M. YONGE

inhalant opening following muscular con-
tractions (with pedal gape closed).

Visceropedal Mass.

There is nothing significantly different
from conditions in the other 2 genera.
There is here no effect of byssal fixation.
The “body”, i.e., the region between the
anterior and posterior retractors is very
symmetrical partly because it is unin-
fluenced by the post-valvular extension,
this being relatively less elongated than
in Hiatella. The oesophagus is long and
the mid-gut thrown into a complex series
of folds ventral to it and anterior to the
style-sac which is large and curves well
forward. The stomach resembles that
of Hiatella. No information was obtained
about reproduction and the nervous sys-
tem calls for no comment. It becomes
clear that it is the pallial, and not the
visceropedal, characters which vary sig-
nificantly in this superfamily.

PANOPE
Distribution.

This remarkable genus, which com-
prises the largest of all deep burrowing
bivalves, includes the North Pacific
“seoduck”?, Рапоре generosa Gould
which was studied personally at Friday
Harbor. It is now becoming rare, at
any rate intertidally, and the specimens
examined were mostly kindly provided
by Dr. F. L. Hisaw. The genus contains
more species and has a much wider dis-
tribution than Panomya (with which it
has frequently been confused). There
would appear to be 9 valid species
of which Lamy (1923) lists 7 with sev-
eral varieties. In the eastern Atlantic,
Panope glycymeris (=aldrovandi) Born,
occurs in the Mediterranean with var.
rugosa extending into the open Atlantic
off Portugal and also, according to
Nicklés (1950), south to Dakar. Along

the American Atlantic coasts, P. bitrun-
cata Conrad, which is a member of the
Carolinian faunal province, occurs from
Cape Hatteras to the borders of Mexico
(Johnson, 1956; Robertson, 1963), while
P. abbreviata Valenciennes occurs inthe
southern hemisphere off Patagonia. In
the North Pacific, P. generosa Gould
ranges from Alaska as far south as San
Diego, while P. globosa Dall is present
still further south in the Gulf of Cali-
fornia (Keen, 1958). On the west Pa-
cific, P. generosa and also P. japonica
A. Adams occur off Japan. In the South
Pacific, P. zelandica Quoy & Gaimard
occurs off New Zealand as described
by Bucknill (1926), to which should be
added P. smithae Powell from deeper
water [see Powell (1950) who also gives
fuller information about P. zelandica;
both species attain lengths of about 5
inches]. P. natalensis (=australis)Wood-
ward, the 1 species so far recorded
from the Indian Ocean, off Natal, occurs
off the southeast coasts of Australia. It
is described also by Macpherson & Ga-
briel (1962), who refer to it as P. aus-
tralis and state that it occurs to depths
of some 8 fathoms. Anarrower species,
P. angusta Hedley, is stated by them to
occur off Queensland.

Species of this genus thus inhabit
temperate waters in both northern and
southern hemispheres in the Atlantic
and the Pacific and, off Natal, in the
Indian Ocean. Panope angusta in the
southern Pacific and P. globosa and P.
bitruncata, in the northern Pacific and
Atlantic respectively, extend into the
margins of the tropics. The mediter-
ranean, Р. glycymeris is probably the
largest species, shells taken off Sicily
reaching lengths of 10 or 11 inches
(Valenciennes, 1839), followed by the
much better known North Pacific P.
generosa which is up to 9 inches long.
Moreover the massive siphons which

5According to Quayle (1960), “the name ‘geoduck’ or ‘geoduc’ is said to derive from the Nis-

qually (Indian) phrase for ‘dig deep’ ”.

ee

ADAPTIVE RADIATION IN SAXICAVACEA 25

cannot be withdrawn within the valves
are at least 3 times the length of the
shell which therefore represents not
more than М the length of the living
animal. With the exception of P. smithae
which occurs in coarse shelly deposits
at depths down to 70 fathoms (Powell,
1950), species of Panope appear all to
be subtidal, as noted and discussed by
Robertson (1963). They burrow in sand
or mud at the lowest tidal levels and in
shallow water, i.e., in regions where it
is only occasionally possible to dig them
while they burrow too deeply to be taken
in the dredge. These facts probably
explain the apparent rarity of most spe-
cies. There are many fossil species
ranging from the Pleistocene as far
back as the mid-Jurassic.

The following discussion is concerned
mainly with Panope generosa. Surpris-
ingly little is known about this species,
despite its relatively enormous size -
with its great siphons it attains a total
length of 3 ft - and highly edible qualities
which have resulted in its virtual ex-
tinction between tide marks as a result
of digging. It has long been a protected
species in the State of Washington where
it may now only be collected in small
numbers exclusively by means of hand
or spade.

Habitat and Habits.

The 3 specimens examined had been
dug at low water of spring tides at Gar-
rison Bay, San Juan Island. In British
Columbia, Quayle (1960) states that it
occurs in sand and mud beaches in
protected bays, burrowing to depths of
3 ft and ranging from the intertidal to
deep water. C.E. Lindsay (Shellfish
Laboratory, Quilcene, Washington) in
conversation with the author stated that
Panope generosa occurs on all types of
bottom, gravel, sand or mud, being
commonest below the lowest tidal levels.
By diving it can be found at depths down
to 50 ft and be excavated by the use of
a powerful water jet. Large specimens
attain weights of up to 13 lb with a pos-
sible maximum of 20 lb. Milne & Milne

(1948) who describe the methods of
digging, which involve the use of an L-
shaped board pointing upshore to pre-
vent water draining into the hole, state
that this may have to be 4 ft deep before
the siphons can be securely grasped.
Distribution is stated to be very local
with colonies no more than 12 yards
across containing 60 to 100 individuals.
But such colonies must now be very
rare indeed.

Sexes are separate and spawning oc-
curs in late April or early May (Quayle,
1960). Almost nothing is known about
the life history, though Milne & Milne
(1948) state that in the following year
the young “resemble worms inthe mud.”
They are then 3 to 5 inches long with
a “cylindrical wormlike body three-
quarters of an inch in diameter”. Even
at this stage the valves, about the size
of a finger nail, cannot close, the pair
being “hinged together to form a paper-
thin saddle over the vital organs at the
creature’s anterior end”. For the next
4 years the animals work themselves
deeper and become recognizable as
clams. Fifteen or 16 years is stated as
a not unusual age. On what basis these
statements are made is not clear but
they may well be correct. Six preserved
specimens of shell length between 2.3
and 2.8 cm (see Fig. 22) with contracted
Siphons of around twice these lengths
were examined at Quilcene. They had
been collected by Mr. Lindsay from
gravel and were said by him to be very
active at that size, rapidly reburrowing
when exposed.

External Appearance and Shell.

The general appearance of Panope
generosa, as displayed in the smallest
of the 3 adult specimens, is shown,
viewed laterally, ventrally and, of the
anterior half only, dorsally in Figs. 23,
A-C. The precise dimensions of the
Specimen figured were: shell length
8.5 cm, depth 6.5; length of siphon
9.5 cm, maximum width (base of siphons)
6.0, width of mantle exposed ventrally,
4.5 cm. This specimen was contracted,

26 C. M. YONGE

ES
Ss

=> = EAN ===." ==
AAA A Р

Р

FIG.

22. Panope genevosa.

men 2.6 cm long. Above, viewed from left
side; below, ligament etc. from dorsal as-
pect.

Young speci-

probably to the fullest possible extent.
The largest specimen, of shell length
13.5 cm, measured 58 cm when expand-
ed, possibly although not certainly, to
its fullest extent. Since the largest ani-
mals have a shell length of some 23 cm
they presumably attain an expanded
length of at least 1 m. In this specimen
the diameter of the siphonal extension
was 8 cm at the base tapering to 3.5 cm
at the tip of the siphons.

In Panope hypertrophy of the extra-
valvular mantle tissues has been car-
ried to a greater extent even than in
Panomya. As shown in the figures,
even when fully contracted, not only is
there a great siphonal extension but the
tissues protrude for a considerable dis-
tance both anteriorly and ventrally. When
viewed from the ventral aspect (Fig.
23 B) the shell valves are seen to be
widely separated, by a distance equi-
valent to the depth of the valves (10.5 cm
in the case of the large specimen which

had a maximum circumference of 36.5
cm). Owing to this ventralward bulging,
the cross section of the animalis almost
circular as shown in Fig. 27. The
small, somewhat dumb-bell shaped, ped-
al gape (PGA) is antero-ventrally sit-
uated (Figs. 20, A,B). All exposed tis-
sues are covered with thick brown per-
iostracum, darkest around the distal
region of the siphonal extension.

Although attaining much greater size,
the thick shell resembles that of Pano-
mya as shown in Fig. 18 where shells
of the 2 genera are compared. The
valves are truncated, a condition which
develops during growth (cf. Figs. 22,
23A), and gape widely at both ends.
Externally they are concentrically ridged
(Fig. 23A) and greyish white with a thin
yellow periostracum. The umbones are
more centrally placed than in Panomya
(cf. Figs. 18A, B), i.e., the anterior and
posterior territories are not very dis-
Similar in area. The major internal
difference is the even thicker,and every-
where continuous and very deeply im-
pressed, pallial insertions in Panope.
No other bivalve has such massive orbi-
tal muscles; they form the exceptionally
thick muscular floor of the mantle cav-
ity shown in section in Fig. 27 (PM).
With the anterior and posterior adductors
(AAD, PAD) and the siphonal “retrac-
tors” (SR) they form a continuous band
of muscle (see scars in Fig. 18B) the
function of which is to control the volume
of the mantle cavity (including, of course,
its posterior extensions); the valves can-
not be appreciably drawn together, they
serve as the regions of muscle attach-
ment, no longer as a Significant pro-
tection.

Hinge and Ligament.

The centrally placed hinge carries a
single cardinal tooth in each valve.
These are shown (T) with sockets (SO)
into which they fit from the ventral
aspect in Fig. 24. That of the right side
is viewed dorsally in Fig. 25. Unlike
Panomya, these teeth are not lost during
growth. The external opisthodetic liga-

ADAPTIVE RADIATION IN SAXICAVACEA 27

FIG. 23. Panope generosa. A, viewed from left side (only partially expanded); B, ventral
aspect; C, dorsal aspect.

28 C. M. YONGE

FIG. 24.

Panope generosa. Hinge and ligament from ventral aspect.

FIG. 25. Paxope generosa.
ligament and teeth.

ment is rounded (Figs, 22,23C). It is
relatively much shorter thanin Panomya
but otherwise very similar with the
Same massive inner and posterior outer
ligament layers (IL, POL). The former
is opaque white and lamellate, and it
frequently contains calcareous tubercles
(Fig. 24,TU) which also occur on the
inner surface of the valves. The poste-
rior outer layer is darker with less ob-

Hinge region of right valve viewed from dorsal aspect showing

vious lamellation. The ligament merges
at each end into the thick periostracum
(P) which also covers it and with which
it is functionally associated, holding the
valves firmly together against the pres-
sures generated in the mantle cavity by
the contraction of the powerful pallial
muscles, There is a prominent nymphal
ridge (Fig. 25, N) to the dorsal surface
of which the ligament is attached as

ADAPTIVE RADIATION IN SAXICAVACEA 29

U Е ROL
PPR
APR A N P

Авм\ NU

LPE Pb hf <
AAD SAN MO AA > o >

S AOL GEN

Aa i ОШ PC 1 Où

IN) SS) À
SO LZ, oa

MN 47 ss

ON JE 7 Y

S

NT =

tm

P

!

1
FIG. 26. Рапоре generosa.
mantle. Arrows as before.

shown in section in Fig. 27.
Mantle Margins.

These are fully fused as in all Saxi-
cavacea apart from Saxicavella. The
unique degree of hypertrophy of the
cross-fused pallial muscles has already
been noted. In the animal of shelllength
10 cm, the floor of the mantle cavity was
1.5 cm thick and 2.5 cm thick at the base
of the siphons. Periostracum does not
extend within the pedal gape, the opening
of which is guarded by mobile lips (inner
mantle folds) between which water is
expelled in sudden jets when the siphonal
and other pallial muscles contract.

Careful observations were made in
situ of the siphonal openings of 2 spec-
imens barely covered with water at low
spring tides at Turn Island near Friday
Harbor. The tip of the fused siphons
was some 5 cm long by 2.4 cm wide.
When fully expanded the inhalant opening
was slightly the larger, about 1.3 cmin
diameter. Both were round and funnel-

ee
ZT Timm

Te
>
wees

4cm

Animal viewed from left side after removal of left valve and left

Shaped but, unlike Panomya, without
either inner or outer tentacles. A band
of brown pigment was present just within
the exhalant opening and streaks of red-
dish brown coloration, extending some-
what deeper, in the inhalant opening.
With both siphons widely open, a strik-
ingly powerful current was directedfrom
the exhalant opening which was directed
obliquely to one side by a bending of
the extremity of the tube. This current,
which broke the surface of the water
above, is certainly the most powerful
of its kind personally observed, due, as
it must be, purely to ciliary action.

Organs in the Mantle Cavity.

These are shown in Fig. 26 whichalso
indicates, in longitudinal section, the
relatively immense thickness of the
pallial muscle (PM) and also the very
anterior position of the pedal gape (PGA).
The visceral mass is very rotund with
a short, pointed and anteriorly directed
foot (F) with small anterior and poste-

30 C. M. YONGE

5cm.

FIG. 27. Panope generosa. Transverse
section through centre of ligament as indi-
cated by dotted line in Fig. 26, showing
rounded visceral mass with enormous devel-
opment of ventral pallial muscle and conse-
quent reduction of mantle cavity. Arrows as
before with dots indicating position of oral-
ward currents and the cross indicating re-
gion of posterior current carrying pseudo-
faeces.

rior retractors (APR, PPR). As in
Panomya, it is clearly an organ of very
limited function. The palps (LP) are
long and the ctenidia (unlike Panomya)
markedly plicate (although homorhabdic)
with, as usual, the 2 demibranchs widely
separate anteriorly. The outer is the
smaller and has no marginal groove.
Despite external appearances, the cte-
nidia only extend for a short distance
posterior to the valves where they are
attached to the septum (SP) separating
the inhalant and exhalant openings. They
doubtless contract to the minimum when
the mantle cavity is opened, as in Fig. 26,
but even when fully relaxed they cannot
extend much posterior to the valves.
Thus, in striking contrast to Panomya,
and also to Hiatella, the post-valvular
extension would here appear to consist
of the fused siphonal tubes.

As indicated in transverse section in

Fig. 27, the outer demibranchs (OD) are
firmly attached by their free margins
to the visceral mass and for their
entire length. The axis (AX), very
broad anteriorly, is attached to the vis-
ceral mass except posteriorly; there
the inner margins of the inner demi-
branchs (ID) are united, becoming at-
tached to the visceral mass only for
the posterior Ys of this. More ante-
riorly, in the region shown in Fig. 27,
they are free, the unattached margins
forming a kind of valvular flap (VF).
This permits water to pass from the
exhalant siphon into the inhalant cavity
which, as in Panomya,is essential for
the ejection of water’ through the pedal
opening during burrowing. At other
times application of these flaps against
the sides of the visceral mass will
maintain the functional separation of
inhalant and exhalant chambers.

Very large pallial mucous glands
(Figs. 26, 28, GL), -in an animal of shell
length 10 cm they were 5.5 cm long and
1.0 cm wide - extend on either side of
the pedal gape. The rectum (Fig. 26, R)
stretches unattached for some distance
behind the adductor with the anus (A)
carried well into the basal region of the
exhalant siphon. The faeces, observed
expelled in situ, are not consolidated
into the firm pellets formed in many
bivalves. They consist of a continuous
greenish mass with a diameter of about
0.35 mm contained within a transparent
mucous sheath with a firm inner mem-
brane, forming long cylinders with an
overall diameter of around 0.5 mm.
Since the length of these faecal threads
is many times the length of the posterior
regions of the gut, they must be formed
in coils but it is uncertain precisely
how or where. These non-compacted
threads are light and have so great a
surface area that they are easily car-
ried up the long siphon in the exhalant
current.

Ciliary Currents.

As shown in Figs. 26 and 27, frontal
cilia on the outer demibranch carry
particles around the margin into the |

ADAPTIVE RADIATION IN SAXICAVACEA 31

FIG. 28. Floor of mantle

Panope genevosa.
cavity showing opening of pedal gape with
glandular areas on either side. Arrows indi-
cate direction of ciliary currents.

oralward current on the axis. On the
inner demibranch currents beat towards
the marginal groove as in the other
genera. Currents on the palps are nor-
mal. The general direction of the
cleansing currents on the surface of the
visceral mass and mantle is indicated
by the feathered arrows in Figs. 26 and
27. Particular interest centres on the
region of the pallial mucous glands, the
currents in this region, more complex
than those in Panomya, being shown in
Fig. 28. Particles embedded in mucus
are carried marginally to join poste-

| riorly directed currents on either side.
| These join with similarly directed cur-

rents diverging from the sides of the
pedal gape to form the median ventral
current (x) shown laterally in Fig. 26
and in section in Fig. 27. It occupies a
groove which continues along the entire
length of the inhalant siphon. The cili-
ated epithelium lining the groove is white
in contrast to the remainder of the
Siphonal wall, which is light brown and

unciliated. Pseudofaeces are carried
by cilia up this siphon although doubt-
less ejected through the opening by
periodic muscular contractions.

Visceropedal Mass.

Nothing requires significant comment,
internal structure being essentially the
same as inthe other genera. However,
in contrast to the unusual length of the
siphons, the visceropedal mass becomes
even more rounded and equilateral than
in Panomya (cf. Figs. 20, 26). The ex-
tension of the shell to accommodate the
post-valvular extension and the siphons
with consequent effects on the contained
visceropedal mass, noted in Hiatella and
which was reduced in Panomya, is here
almost completely lost.

CYRTODARIA
Distribution.

This genus is no less remarkable
than Panope and is, not excluding Saxi-
cavella, the least known genus of the
Saxicavacea. It is northern and com-
prises Cyrtodaria siliqua (Spengler,
1793)-the “Northern Propeller Shell”
and C. kurriana Dunker, 1862. The
former is confined to the North Atlantic,
where the genus probably originated.
The latter iscircumpolar, including East
Greenland (Ockelmann, 1958), being a
member of the high arctic community.
It is confined to shallow water. Much
has been added to knowledge about the
distribution and history of both of these
species by Nese (1965).

Attention is here confined to Cyrto-
daria siliqua but, unfortunately, entirely
to preserved material kindly supplied
by Dr. W. J. Clench and Dr. J. A. Allen.
This animal occurs on bottoms, usually
of fine sand, down to depths of 150 m
although usually between 50 and 150
(Nesis, 1965), or shallower according to
Bousfield (1960). It extends from the
Arctic to Georges Bank off Cape Cod
(Allen, 1965). It is obviously extremely
common Since it is often the most abun-
dant animal in the stomachs of demersal
fish such as cod and haddock; however,

32 C. M. YONGE

FIG. 29.

Cyrtodaria siliqua. Preserved specimen. A, viewed from left side; B, from ventral

aspect. Note approximation of valves anteriorly and wide gape posteriorly.

owing to its infaunal habit, it has rarely
been taken alive. Knowledge of its ap-
pearance in life and what may be deduced
about its habits is confined, so far as
can be determined, to the observations
of Morse (1919) on“Glycymeris siliqua”.
But, in this instance it will be more
convenient to discuss structure before
dealing with these observations and their
implications.

External Appearance and Shell.

Of the 2 specimens initially examined,
both from the Agassiz Museum, Har-
vard, 1 came from Grand Bank and the
other from Ipswich Bay, Massachusetts.
The shells were respectively 10.3 and
8.3 cm long, 3.2 and 2.9 cm wide and
4.2 and 3.8 cm in height. In their state
of complete contraction (Figs. 29,30) the
massive fused siphon (SI) covered, like
all exposed tissues, with thick dark

periostracum projects as a round-ended
mass with only the barest indication of
terminal openings. It cannot be with-
drawn between the widely gaping poste-
rior margins of the valves. But, in
striking contrast to the preceding ge-
nera, there is no anterior gape. When
the shell “closes” the anterior margins
of the valves meet and the animal forms
an anteriorly directed wedge as shown
ventrally and dorsally in Figs. 29B and
30A. The former reveals the diminish-
ingly wide area of ventral separation of
the valves. The pedal gape (PGA) is
situated at the anterior end.

The massive shell is covered every-
where, except in old shells around the
umbones where it becomes worn off, by
a dark brown to black periostracum. It
differs from all the preceding genera in
that the anterior territory is larger
than the posterior territory (cf. the

|

ADAPTIVE RADIATION IN SAXICAVACEA 33

4cm.

PAD

FIG. 30. Cyrtodaria siliqua. A, preserved specimen viewed from dorsal aspect; B, interior
of valves with ligament viewed from ventral aspect, inner ligament split at either end.

areas anterior and posterior to the um-
bone (U) in Fig. 29A). This initially
indicates a different habit, namely active
forward movement through the substrate
in contrast to the passive vertical pos-
ture of Panomya or Panope. The dif-
ference is comparable, inthe Tellinacea,
with that between the continuously active
Donax and the passively deep buried

_ Solecurtus (Yonge, 1949). Pallial attach-
_ ments (Fig. ЗОВ) are broad and are con-
| tinuous with those of the adductors, not
| unlike conditions in Panope (Fig. 18B)
| but with no pallial sinus. The anterior

Scar is elongated and much the larger.
Hinge and Ligament.

At any rate in the adult, there are no

teeth. The ligament (Fig. 29, L), exter-
nally more prominent, is of the same
general form as in the other genera
from which it differs in the presence of
a relatively large region of anterior
outer ligament (Figs. 31, 32, AOL). This
is also extended laterally into cavities
anterior to the nymphal ridges (Fig. 31
CN). The periostracum also extends
into these cavities then passing forward
and around the anterior end of this por-
tion of the ligament. The impression
obtained is of an anterior extension of
the primary ligament pushing its way
into the anterior area of fused perio-
stracum. This enlargement of the ante-
rior ligament layer is associated with
that of the anterior territory of the shell.

34 C. M. YONGE

PSE

FIG. 31. Cyrtodaria siliqua. A, ligament viewed in median longitudinal section from left side;
B, mid-dorsal tissues responsible for secreting primary and secondary ligament, viewed from
above.

PG ee A

PGA

FIG. 32. Cyrtodaria siliqua. Animal (preserved specimen) partially dissected, viewed from
left side.

The inner (IL) and the posterior outer areas of secretion (viewed laterally in
(POL) ligament layers are thick, the Fig. 31B) consist of a laterally extended
former distinctly white and glistening, anterior outer surface of the outer

the latter very dark. The underlying mantle folds (AOM), an elongated mantle

ADAPTIVE RADIATION IN SAXICAVACEA 35

FIG. 33. Cyrtodaria siliqua.
anatomy, especially the gut.

isthmus (Fig. 32 MI) and a broad, band-
like posterior outer surface of the outer
mantle folds (POM) [cf. conditions in
the Etheriidae (Yonge, 1962a)].

Over this primary ligament extends
the customary thick layer of perio-
stracum (P) which, asinthe other genera
unites the valves both dorsally and ven-
trally. The ligament is attached later-
ally to very prominent nymphal ridges
(N). The whole structure of primary
and secondary (periostracal) ligament
serves, as in Panope and Panomya, to
hold the valves together against the
great internal pressure generated in the
mantle cavity when the adductor, pallial
and siphonal muscles contract with the
siphonal openings closed.

Mantle margins.

These are essentially as in Panomya
and Panope. It appears from the obser-
vations of Morse (1919) that tentacles
encircle both siphonal apertures (Fig.
34) but these could not be seen in these
contracted specimens. Although so well
protected by periostracum, the siphons
(which cannot be withdrawn within shel-
ter of the valves) are frequently bitten
off by fish and doubtless have corre-
sponding powers of regeneration. The

Preserved specimen viewed from left side showing internal

pedal gape (PGA) is large in correlation
with the size of the foot, and the border-
ing areas occupied by the middle and
inner folds are wider than in Panomya
and Panope. It is flanked internally by
pallial mucous glands (Fig. 32, GL).

Organs in the Mantle Cavity.

These are shown in Fig. 32 but, owing
to lack of living specimens, without any
indication of ciliary currents. The
enlargement of the anterior territory is
immediately apparent with the elongated
anterior adductor extending far forward.
The ctenidia, plicate andhomorhabdic as
in Panope, pass back into the post-
valvular extension but not to the same
extent as in Panomya. The outer demi-
branch (OD) ends well short of the large
palps (LP) and the impression gained is
that the mouth with the palps and inner
demibranchs (ID) have been carried
anteriorly but the outer demibranchs
have not. A well developed branchial
muscle (BM) is inserted just anterior to
the anterior pedal retractor (APR). The
anteriorly situated pedal gape with flank-
ing glandular areas has been mentioned.

Visceropedal Mass.

The very large foot is anteriorly di-

36 C. M. YONGE

rected and clearly capable of elongated
extension through the pedal gape. Both
retractors (APR, PPR) are well devel-
oped. In the gut the oesophagus (Fig. 33,
O) is exceptionally long, a further con-
sequence of forward extension, the stom-
ach and style-sac (S, SS) resemble those
of the other genera but the mid-gut is
carried anteriorly and thrown into a
series of coils, doubtless to permit
extension when the footis protruded. The
rectum traverses the ventricle (Fig. 32,
R, VE) and the anus (A) is not carried
clear of the posterior adductor. Details
of the heart, pericardium and left kidney
are shown in Fig. 32 with the positions
of the 3 major nerve ganglia. Much of
the visceral mass is occupied by gonad
(Fig. 33, G).

Habitat and Habits.

In his description of a living specimen,
dredged in Portland Harbor (Maine),
Morse (1919) refers to the expanded
animal as presenting “a remarkable
appearance. The mantle and bulbous
siphonal end were extended far beyond
the edge of the shell” (Fig. 34). The
siphons (Fig. 35B) he noted as unusual
in that the opening of the exhalant si-
phon is the larger. The valvular mem-
brane is “surrounded by papillae, long
and short ones alternating, white in
color”. The inhalant opening “is small
and surrounded by long slender papillae
crowded together and curving inward.
The whole appearance indicates that the
siphons must extend to a great length,
perhaps three times the length of the
shell.” He describes the foot as being
long, “somewhat carinated, and capable
of extending up and down in various
directions.” His drawings of the expanded
animal, shown in Figs. 34 and 35A, indi-
cate only very partial expansion and
the foot is unlikely to assume, when it
is under the substrate, the upward cur-
vature shown. The great extension of
the periostracally covered tissues, pos-
teriorly, ventrally and also to some
extent anteriorly (Fig. 34) resembles

FIG. 34. Cyrtodaria siliqua. Animal ex-
panded showing upwardly directed foot and
massive siphon. (From Morse, 1919.)

FIG. 35. Cyrtodaria siliqua. Left, living
animal viewed from dorsal aspect; right,
expanded siphonal openings. (From Morse,
1919.)

conditions in Panomya and Panope. Gen-
eral impressions are of a bivalve adap-
ted for horizontal movement through the
sandy substrate. The form of the.shell
is well adapted for this, so is the en-
larged foot, while the elongated siphons
probably turn upwards near the tip so
that the apertures open clear of the sub-
strate in which the animal lies horizon-
tally extended. This is the only genus
of the Saxicavacea which is active.

ADAPTIVE RADIATION IN SAXICAVACEA 37

DISCUSSION

As the foregoing descriptions of spe-

cies of the 5 genera indicate, the Saxi-
cavacea represent a natural group with
a complex of fundamental characters
which distinguishes them from other
eulamellibranch bivalves and which has
also permitted the appearance of an
interesting diversity of adaptive radia-
tions.

The significant structural features

are those of the mantle/shell and of the
foot. They comprise:

№

. There

With the exception of Saxicavella,
all are isomyarian with the hinge
line parallel to the ventral margins
of the shell.

. There is a reduced heterodont den-

tition with no more than one tooth in
each valve and these often lost in
the adult.

is a massive opisthodetic
primary ligament situated behind
the umbones with large inner and
posterior outer ligament layers and,
with the exception of Cyrtodaria, a
greatly reduced anterior outer layer.

. Both anteriorly and posteriorly the

primary ligament is extended sec-
darily by unusually thick fused per-
iostracum.

. The ligament is inserted laterally

on to the upper (morphologically
inner) surface of uprolled nymphal
ridges so that a particularly well
developed, convex external ligament
is formed.

. Again with the exception of Saxica-

vella, mantle fusion is of Type C,
i.e., with complete fusion of peri-
ostracal secreting surfaces on the
inner surface of the outer mantle
folds. Hence the siphons and all
exposed pallial surfaces are covered
with a usually especially thick and
darkly pigmented periostracum.

. Also with the exception of Saxica-

vella, there is a striking hyper-
trophy of the orbital (pallial) mus-
cles, the attachments of which to

10.

fale

12.

13.

. There

the shell valves are often as broad
as those of the adductors between
which they extend.

. The mantle cavity is extended poste -

riorly with formation of a post-val-
vular extension (even better devel-
oped in the Adesmacea, notably the
Teredinidae) into which the ctenidia
pass, often far beyond the posterior
margin of the valves.

is an increasing tendency,
starting in Hiatella but highly devel-
oped in Panomya, Panope and Cyrto-
daria, for great distension of the
periostracally covered pallial tis-
sues outside the confines of the shell
valves, not merely posteriorly in
connection with the siphons but also
ventrally and anteriorly. The valves
increasingly come to provide the
means of pallial attachment rather
than of protection, the valves gaping
extensively in all but Saxicavella and
Hiatella.

There is usually very great devel-
opment of siphons in association
with that of the post-valvular exten-
sion of the mantle cavity, but there
is a notable difference in the rela-
tive proportions of the 2 in the ex-
ternally very similar Panomya and
Panope.

There are essentially similar cteni-
dia and ciliary currents (the com-
mon eulamellibranch Type C, of
Atkins, 1937) throughout although
with increasing separation of inner
and outer demibranchs and the devel-
opment of powerful, separately in-
serted branchial muscles in Panope
and Cyrtodaria in association with the
need to withdraw the far extended,
and here alone plicate, ctenidia.
Again with the exception of Saxica-
cavella, there are massive pallial
mucous glands on either side of the
pedal gape; cleansing currents ap-
pear to be similar in all genera.

A moderately developed foot is as-
sociated with byssal attachment in
epifaunal Hiatella and Saxicavella, a

38 C. M. YONGE

TABLE 1. Relationships of form and habit within the Saxicavacea: reduced heterodont dentition;
external opisthodetic ligament; intimate pallial fusion.

Byssally Attached
1

also
boring

1
1
|
1
SAXICAVELLA *
|
|, HIATELLA

IA | А,

Epifaunal

Posterior Territory larger

PANOMYA PANOPE

Horizontal Burrowing

Type B Fusion

Type C Fusion

CYRTODARIA

Infaunal

Anterior Territory
larger

reduced foot with slow vertical pene-
tration of soft substrates in Panom ya
and Panope and a much enlarged
foot with horizontal movement in
Cyrtodaria, the 3 last being infaunal.

14. Apart from the extent to which the
mid-gut coils, which appears related
to habit, there are no significant
differences in the visceral organs
between the 5 genera.

Certain important functional consid-
erations emerge. Apart from Saxica-
vella, great hydrostatic pressures are
generated in the mantle cavity. These
are due to contraction of the powerful
pallial muscles with accompanying clo-
sure of the siphons and, except where
necessary for movement, the pedal gape.
Dorsally pressure is contained by the
powerful primary ligament assisted by
its secondary periostracal extensions
in both directions. Apart from Saxica-
vella and Hiatella this is clearly the
major function of the ligament; reduction
or absence of hinge teeth is associated
with lack of need for close approxima-
tion of the closed valves. Formation of
the arched external ligament is partic-
ularly effective in furnishing resistance
against internal pressure. Hydrostatic

pressure is essential in the boring pro-
cess of Hiatella |as probably also in
Platyodon (Yonge, 1951b) but not in
other rock borers such as Lithophaga
(Yonge, 1955) or the pholads]. It is no
less important in the vertically down-
ward movement through an often dense
substrate in Panomya and Panope, where
the foot is small, in a process which
takes the latter to unique depths. In
Cyrtodaria it may be assumed to be of
very similar assistance in forward
movement, the animal being possibly
anchored by dilation of the post-valvular
extension and siphons while the wedge
shaped anterior end is carried forward
with accompanying pedal extension. Pre-
cise knowledge of the process would be
of great interest.

Saxicavella differs most from the
general pattern having on the one hand
a more primitive type of mantle fusion
(Type B instead of C) and on the other
in being the sole heteromyarian, a con-
sequence -although notaninevitable con-
sequence (e.g., Hiatella) - of byssal at-
tachment (Yonge & Campbell, 1968).
Nevertheless the pattern of hinge and
ligament and of general form are those
of the Saxicavacea and it is rightly to

ADAPTIVE RADIATION IN SAXICAVACEA 39

be included in this superfamily.

Adaptive radiation has therefore in-
cluded byssal attachment and a “nest-
ling” habit in Saxicavella and Hiatella
with resultant acquisition of a boring
habit in the latter. These genera are
epifaunistic; the remaining 3 are in-
faunal. Panomya and Panope exhibit
interesting convergence with Mya (Mya-
cea) and with Tresus (Schizothaerus)
and Lutraria (Mactracea) being highly
specialised vertically disposed deep bur -
rowers. Cyrtodaria, associated with
Panope in possessing plicate ctenidia,
is uniquely adapted for horizontal move-
ment. In this genus alone is the ante-
rior territory larger than the posterior
territory of the mantle/shell with the
anterior outer ligament layer forming
a Significant proportion of the primary
ligament. Relationships, both in terms
of structure and of habit are summarized
my Dable 1.

ACKNOWLEDGEMENTS

The bulk of the observations on living
animals were made at the Friday Harbor
laboratory of the University of Wash-
ington, Seattle, during the summers of
1959 and 1969. Specimens of Hiatella,
Panope and Panomya were all studied
there. The author records his gratitude
to Dr. R. L. Fernald, the Director, and
to Dr. Dixy Lee Ray for much help and
many facilities. He also wishes to thank
Mr. N. A. Holme of the Marine Biologi-
cal Laboratory, Plymouth for specimens
of Saxicavella jeffryesi with notes on
their habitat in the English Channel, to
Dr. W. J. Clench ofthe Agassiz Museum,
Harvard, for preserved specimens of
the North Atlantic Crytodaria siliqua and
to Dr. J. A. Allen of the Dove Marine
Laboratory of the University of New-
castle for additional specimens of this
most interesting species.

sections were prepared and figures
drawn by Miss J. I. Campbell whose
Salary, as Research Assistant, was cov-
ered by a grant from the Science Re-
search Council. Acknowledgements are

At Glasgow :

also made to the United States Education
Commission in the United Kingdom for
award of a Fulbright Travel Grant.

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ADAPTIVE RADIATION IN SAXICAVACEA 41

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ZUSAMMENFASSUNG

UBER FUNKTIONALE MORPHOLOGIE UND ADAPTIVE RADIATION BEI DER
MUSCHEL- SUPERFAMILIE SAXICAVACEA (HIATELLA (=SAXICA VA),
SAXICAVELLA, PANOMYA, PANOPE, CYRTODARIA)

C. M. Yonge

Einige Arten der 5 Gattungen, die die Superfamilie Saxicavacea bilden, nämlich
Hiatella sp., Saxicavella jeffreysi, Panomya ampla, Panope generosa und Cyrtodaria
siliqua sind untersucht worden, alle ausser der letzten sowohl lebend als auch anat-
omisch. Es wird gezeigt, dass sie eine natürliche Muschelgruppe mit Modifikation
besonders der Mantelcharaktere bilden und ein interessantes Beispiel für adaptive
Radiation geben. Sie sind ursprünglich Isomyarier (ausser Saxicavella) und haben
eine sehr reduzierte heterodonte Bezahnung, ein starkes Äusseres opistodetisches
Ligament mit einem äusseren Ligamentlager, das nur bei Cyrtodaria nicht vorn
reduziert ist. Die Mantelverwachsung erstreckt sich, abgesehen von Saxicavella,
auch auf die Epithelien, die das Periostrakum ausscheiden, denn das dicke Perio-
strakum bedeckt die Siphonen und andere hervorstehende Teile des Mantels und
bildet dicke sekundäre Verlängerungen des primären Ligamentes. Der Fusschlitz ist

42

C. M. YONGE

klein. Die Mantelhôhle ist nach hinten ausgedehnt und bildet eine Verlängerung
hinter den Schalen, in die die Kiemen einrücken. Die Mantelmuskeln sind auffallend
stark entwickelt, die Muskelansätze oft ebensobreit wie die der Adduktoren. Dies,
sowie klaffende Schalen, die nicht die rückwärtigen Teile bedecken können, ist ein
auffälliges Merkmal der letzten 3 Gattungen. Die relativen Körperregionen, die von
der Verlängerung hinter den Schalen und den Siphonen eingenommen werden, unter-
scheiden sich sehr auffällig bei Panomya und Panope, die sonst äusserlich einander
ähnlich sind. Die Kiemen und die Wimperströme sind bei Panope und Cyrtodaria
durchaus Ähnlich, diese beiden allein haben gefaltete (obgleich noch homorhabdische)
Kiemen, Bei allen ausser Saxicavella sind grosse Schleimdrüsen an jeder Seite und
hinter dem Fussschlitz vorhanden. Der mässig entwickelte Fuss ist bei der epifaun-
ischen Hiatella (die auch in Felsen bohren kann) mit Byssus-Anheftung verbunden
ebenso bei Saxicavella; ein reduzierter Fuss, der langsam senkrecht in weiches
Substrat eindringt, bei Panomya und Panope, und ein viel grösserer Fuss mit waage-
rechter Bewegung durch solche Substrate bei Cyrtodaria, bei der allein das Vorterteil
des Mantels und der Schale das grissereist. Andere Organe der Viscero-Pedal-Masse
sind in allen Gattungen im wesentlichen Ähnlich. Ein sehr bedeutsames Merkmal bei
den Saxicavaceen ist die Entwicklung starken Druckes innerhalb der Mantelhöhle.
Die enge Mantelverwachsung mit den Uberentwickelten Mantelmuskeln, die Ver-
längerung hinter den den Schalen und das massige äussere konvexe Ligament sind
alle damit verbunden und ermöglichen es Hiatella, zu bohren, und Panomya, Panope
und Cyrtodaria, zu graben. Obwohl Saxicavella sich von den anderen Gattungen
dadurch unterscheidet, dass sie herteromyarisch ist und ihre Mantelränder nicht so
fest verwachsen sind, hat sie dieselbe Grundform, einschliesslich Schlossplatte und
Ligament, wie die anderen Gattungen, und wird zu Recht in dieselbe Superfamilie
gestellt.
B. 2.

RESUME

MORPHOLOGIE FONCTIONNELLE ET RADIATION ADAPTATIVE CHEZ LES
SAXICAVACEA (HIATELLA, (=SAXICAVA), SAXICAVELLA, PANOMYA,
PANOPE, CYRTODARIA).

C. M. Yonge

Des études ont été entreprises sur des espéces appartenant a 5 genres de la Super-
famille des Saxicavacea, à savoir: Hiatella sp., Saxicavella jeffreysi, Panomya ampla,
Panope generosa et Cyrtodaria siliqua, toutes sauf la dernière ayant été étudiées sur
le vivant tant pour les dissections que pour les coupes. Elles sont apparues comme
constituant un groupe naturel de bivalves avec des modifications, en particulier des
caractéres du manteau, qui ouvrent un intéressant domaine de radiation adaptative.
Essentiellement isomyaires (excepté Saxicavella) avec une dentition hétérodonte trés
réduite, elles ont un épais ligament opisthodéte externe avec, excepté chez Cyrto-
daria, une couche ligamentaire antérieure externe très réduite, La fusion des lobes
du manteau est intime entrainant, sauf pour Saxicavella, une fusion complete des
épitheliums secrétant du periostracum, un épais periostracum recouvrant les siphons
et les autres tissus palléaux saillants et constituant d’épaisses extensions secondaires
par rapport au ligament primaire. L’ouverture pédieuse est petite. La cavité
palléale s’étend postérieurement constituant une extension post-valvulaire dans la-
quelle passent les cténidies, Il y a une frappante hypertrophie des muscles palléaux
dont les attaches musculaires sont souvent aussi larges que celles des adducteurs,
Ceci, en même temps que les valves baillantes ne peuvent ajuster les régions posté-
rieures contractées, est un fait marquant des 3 derniers genres. Les régions rela-
tives occupées par l’extension post-valvulaire et les siphons different de facon
frappante entre Panomya et Panope, pourtant trés similaires extérieurement. Les
cténidies et la ciliature sont partout similaires avec seulement Panope et Cyrtodaria
qui possèdent des cténidies repliées (bien qu’encore homorhabdiques). Il y a chez

ADAPTIVE RADIATION IN SAXICAVACEA

tous, sauf Saxicavella, de grosses glandes muqueuses de chaque côté et en arrière
de l’ouverture pédieuse. Le pied, modérément développé, est en relation avec l’attache
byssale chez les épigés Hiatella (qui peut aussi perforer les roches) et Saxicavella;
le pied, réduit, a une lente pénétration verticale dans les substrats meubles chez
Panomya et Panope; le pied, plus large, a un mouvement horizontal à travers de tels
substrats chez Cyrtodaria, où c’est seulement la zone antérieure du manteau/coquille
qui est la plus large. Les autres organes de la masse viscéro-pédieuse sont tout
a fait similaires dans tous les genres, Un fait hautement significatif chez les Saxica-
vacea c’est le développement des fortes pressions à l’intérieur de la cavité palléale.
L’intime fusion palléale avec des muscles orbitaires hypertrophies, l’extension post-
valvulaire et l’épais ligament externe convexe sont en relation avec ce fait et appor-
tent les moyens de forer chez Hiatella et de fouir chez les hypoges Panomya, Panope
et en ayant une fusion palléale moins intime, Saxicavella a, y compris pour la char-
niere et le ligament, le m@me aspect morphologique que les autres genres et est, a
juste titre, inclus dans la Superfamille.
ASE:

RESUMEN

SOBRE LA MORFOLOFIA FUNCIONAL Y RADIACION ADAPTIVA EN LOS
SAXICAVACEA (HIATELLA, (=SAXICAVA), SAXICAVELLA, PANOMYA,
PANOPE, CYRTODARIA)

C. M. Yonge

Se estudiaron las siguientes especies correspondientes a los cinco géneros que
constituyen la superfamilia Saxicavacea: Hyatella sp., Saxicavella jeffreysi, Panomya
ampla, Panope generosa y Cyrtodaria siliqua; con excepción de la última, las demás
especies se observaron en vivo, asi como en disección y cortes. Ellas demuestran
constituir un grupo natural de bivalvos con modificación, especialmente los carac-
teres paleales, permitiendo una interesante amplitud en radiaciónadaptiva. Esencial-
mente isomiarios (excepto Saxicavella) con dentición heterodóntica muy reducida,
tienen un ligamento opistodético masivo, excepto en Cyrtodaria, con la capa ligamental
externa anterior grandemente reducida. La fusión del manto es íntima. Esta integra
- excepto en Saxicavella - el epitelio secretor del periostraco. A esto se debe el
engrosamiento del periostraco cubriendo los sifones y la importantes extensiones del
ligamento primario así como otras de los tejidos paleales. La abertura pedal es pe-
queña. La cavidad paleal se extiende posteriormente formando una extensión post-
valvular dentro de la cual pasan las branquias. Existe una notable hipertrofia de los
músculos paleales, con la zona de adherencia con frecuencia tan ancha como la de
los adductores. Esto, junto con las valvas hiantes las cuales no pueden acomodar las
contraídas regiones posteriores, es un aspecto conspicuo delos tres últimos géneros.
Las regiones ocupadas por la extensión post-valvular y los sifones, difieren muy
marcadamente entre -aunque muy Similares extrioemente- Panomya y Panope. Bran-
quias y corrientes ciliares son del todo similares con Panope y Cyrtodaria sólo posee
branquias plegadas (aunque todavia homorhabdicas). En todos, pero no en Saxicavella,
aparecen masas glandulares mucosas a cada lado y detrás de la abertura pedal. El
pie moderadamente desarrollado se asocia con adherencias del byssus en Hiatella
(que es epifaunal pero también puede taladrar rocas) y Saxicavella; es reducido, con
penetración vertical corta en substratos blandos, en Panomya y Panope; mucho más
grande, con movimientos horizontales en el substrato, en Cyrtodaria en la cual la
portión anterior, de manto-concha, es la mayor, Demás órganos de la masa viscero-
pedal son esencialmente similares en todos los generos, Un aspecto de altas presio-
nes dentro de la cavidad paleal. La íntima fusión paleal con músculos orbitales
hipertrofiados, la extensión post-valvular y el ligamento externo convexo y masivo,
se asocian a esto y provee el medio perforador en Hiatella y excavador en Panomya,
Panope y Cyrtodaria. Aunque difieren de otros géneros por ser heteromiarios y con
menor fusión paleal, Saxicavella tiene el mismo patrón formativo, incluyendo char-
nela y ligamento, como los otros, y es correctamente incluído en la superfamilia.

J.J. P.

43

44

C. M. YONGE
ABCTPAKT

O ФУНКЦИОНАЛЬНОЙ МОРФОЛОГИИ И АЛАПТИВНОЙ PAIMAIMM У SAXICAVACEA
(HIATELLA (SAXICAVA), SAXICAVELLA, PANOMYA, PANOPE, CYRTODARIA).

K.M. MOHT
Изучались виды из 5 родов двустворчатых моллюсков, вхолящих в
налсемейство Saxicavacea, а именно На еИа sp., Saxicavella jeffreysi, Pano-
mya ampla, Panope generosa И Cyrtodaria siliqua. Все, кроме последней
исследовались прижизненно, а также путём вскрытия и после Hero. Эти
моллюски * составляют естественную группу, обладающую модификациями,

особенно в строении мантии, что позволяет говорить об известной степени
адаптивной радиации. Будучи изомиарными моллюсками (кроме Saxicavella ),
с очень редуцированным гетеродонтным замком, они имеют массивный наружный
опистодетный лигамент и (кроме Cyrtodaria ) сильно-редуцированный передний
слой лигамента. Мантия сростается изнутри (кроме Saxicavella), имея также
полное сростание периострака, покрывающего сифоны и другие выросты
мантийнои ткани и образующего толстые вторичные выросты. Ножное мантийное
зияние небольшое. Мантийная полость тянется назад, образуя поствальвулярное
впячивание, куда входят ктенидии. Имеется сильная гипертрофия мантийных
мускулов и их места прикрепления часто также широки, как у аддукторов.
Это, а также заднее зияние сторвок, которое не может обеспечить полное
втягивание заднего отдела тела, составляет характерные черты трёх
последних (из перечисленных выше) родов. Соответственные части тела,
занятые пост-вальвулярным выростом и сифонами очень сильно отличаются у
весьма сходных снаружи Panomya и Panope. Ктенидии и ресничные токи У
всех сходны, несмотря на то, что Рапоре и Cyrtodaria одни только обладают
пликатными (хотя и гоморабдическими) ктенидиями. У всех (кроме Saxicavella )
имеются массивные слизистые железы, расположенные с обоих сторон и позади
HOXHOTO зияния. Умеренно-развитая нога связана с наличием биссуса у
эпифаунной Hiatella, которая может также вбуравливаться в скалыи У
Saxicavella; редуцированная Hora, связаная со способностью лишь медленного
вертикального опускания в мягкий грунт, имеется у Рапотуа и Рапоре;
гораздо более крупная нога, обеспачивающая горизонтальное продвижение в
таком субстрате имеется у Cyrtodaria, У которой лишь передний отдел
мантия/ раковина более крупный. Остальные органы висцерально-педального
отдела весьма сходны у всех родов. Весьма важныму Saxicavacea у является
способность повышать давление внутри мантийной полости. Связанные с зтим
внутреннее сростание мантии с гипертрофированными орбитальными мускулами,
пост-вальвулярное выпячивание и массивный наружный лигамент, дают
возможность сверления у На еИа и закапывания инфаунных Panomya, Рапоре
и Cyrtodaria. Хотя Saxicavella и отличается от остальных родов Saxicavacea
тем, что имеет гете ромиарные аддукторы и менее глубокое внутреннее
сростание мантии, она обладает теми же чертами строения, включая замок и
лигамент, как и остальные рода, т.е. имеет право быть включенной в данное
надсемейство. :

Z. A. Е.

MALACOLOGIA, 1971, 11(1): 45-119

AIDS FOR IDENTIFICATION OF BIVALVE LARVAE OF VIRGINIA!
Paul Chanley? and J. D. Andrews?
ABSTRACT

Larvae of 23 species of marine bivalves inhabiting the “mid-north Atlantic”
coastal area of the U.S.A. have been grown in the laboratory. These species
have been described comparatively to aid planktologists in identifications.

Identification aids include: 1) Comparative photomicrographs of larvae of
representative sizes and ages. 2) Graphs of length-height relationships of
prodissoconch shell for interspecific comparison of larvae throughout develop-
ment. 3) Tables of dimensions and umbonal shapes of larvae. 4) Keys to
straight-hinge and umbonate larvae. 5) Graphs and tables of spawning seasons
and geographic distribution of species. 6) Brief descriptions of each species.

Combined use of all these aids is recommended for identification of larvae.
Since advanced larvae are usually easier to identify than early ones, workers
should begin with umbonate larvae and progress to smaller individuals by com-

parison. Frequently abundant species can be identified by population characters
such as average length-height relationship.

INTRODUCTION

Bivalve larvae constitute an impor-
tant and distinctive part of the marine
plankton community (Thorson, 1946).
Yet detailed studies of their distribution
and behavior have been hampered by
the inability of investigators to identify
species in plankton samples.

There are numerous reasons for this
difficulty: 1) Larval stages of a ma-
jority of species have never been de-
scribed, and many existing descriptions
are incomplete. 2) Larvae in preserved
plankton samples must be identified
mostly by shell characters. 3) Larvae
may appear similar at comparable stages
of development, hence no satisfactory
criteria for identification have been
developed. 4) Most published accounts
are of one or a few species and the
interspecific comparisons needed for
identification are difficult. This is

particularly true when comparing the
descriptions of investigators whose ter-
minology and descriptive emphasis are
different. 5) Some descriptions of bi-
valve larvae are based on erroneous
identifications, or juveniles rather than
larvae. Rearing larvae from known
parents in the laboratory eliminates
this problem but authors employing this
technique have usually described a li-
mited number of species with little
attempt at interspecific comparisons.

In contrast to the immense literature
on adult mollusks and their shells,
information on larvae is scarce. Al-
though larvae of a number of species
from Europe, North America, and Japan
have been described, few papers are
useful for identification of planktonic
specimens.

In Europe, Loven (1848) observed
Spawning and early embryology of 3
species and tentatively identified plank-

1
Contribution No. 322 from the Virginia Institute of Marine Science.

| rein Institute of Marine Science, Wachapreague, Virginia, U.S.A. Present address:
Shelter Island Oyster Company, Greenport, L.I., New York 11944, U.S. A.

3
Virginia Institute of Marine Science, Gloucester Point, Virginia, U.S. A.

46 CHANLEY AND ANDREWS

tonic larvae of 6 others. Borsiak
(1909) described several planktonic lar-
vae but only identified a few. Odhner
(1914) also identified planktonic larvae.
Kändler (1926) and Lebour (1838) iden-
tified larvae by rearing captured plank-
tonic larvae to recognizable stages in
the laboratory. Lebour also reared
some species past metamorphosis from
artificially fertilized eggs. Her brief
key to larval Cardium is the first key
to bivalve larvae. Werner (1939) de-
scribed only a few species of plank-
tonic larvae, but the descriptive detail
and effectiveness of his definitions have
influenced the terminology and tech-
niques of most subsequent investigators.
He suggested that the length-height re-
lationship and hinge-line length could
be useful in identifying bivalve larvae.

Jgrgensen’s (1946) comprehensive re-
port includes descriptions of about 50
species taken in plankton samples and
an exhaustive literature review. In
addition, he captured planktonic larvae
and reared them in the laboratory.
Rees (1950) also described planktonic
larvae of a large number (78) of spe-
cies. His report includes diagrams,
summary tables of hinge structures and
photomicrographs of larval valves ar-
ranged by families. Although many of
his identifications are tentative, Rees’
work is notable as the first attempt to
classify many larvae by family char-
acters. Zakhvatkina (1959), relying
heavily on the work of Rees and others,
described in detail 28 species of lar-
vae and constructed a key for their
identification. Her methods and sources
of larvae are not given.

In Japan, Miyazaki (1935; 1936) reared
larvae of 10 species in the laboratory,
with no attempt at interspecific compar-
isons. In a later literature review
(1962), he classified 200 species into 20
types on the basis of “definitely re-
cognizable charactersitics of prodisso-
conchs.” He suggested classifying lar-
vae by type of development (incubatory,
egg mass, protobranch, glochidium,
etc.). Imai and his colleagues (see

literature cited) have described the lar-
vae of a number of species they reared
in outdoor tanks. Yoshida (see litera-
ture cited) has grown larvae of several
species in the laboratory. Although
he has made comparative studies (1953;
1957), his descriptions have usually been
published separately.

The earliest work dealing with North
American species is that of Stafford
( 1912). He described planktonic larvae
and observed that the length-height re-
lationship and hinge-line length could
be used to identify straight-hinge larvae.
Sullivan (1948), also working with plank-
tonic larvae, grouped species by shape
and listed distinctive characteristics.
Loosanoff & Davis (1963) and Loosan-
off, Davis & Chanley (1966) described
larvae reared in the laboratory from
known parents. They emphasize the
length-height relationship, but their ap-
proach is descriptive rather than com-
parative.

The purpose of the studies reported
here is to present data obtained from
laboratory-cultured bivalve larvae to
facilitate identification of planktonic lar-
vae. Photomicrographs are supplemen-
ted by tables and graphs of dimensions
and seasonal occurrence of larvae. Keys
and brief descriptions have also been
included. Because only data from lab-
oratory-cultured larvae of known parents
have been used, coverage is limited
to 23 species representing 16 families.
These species are about half those oc-
curring in Virginia (Wass, 1965).

These identification aids are intended
for use in mid-North Atlantic estuarine
areas of the U.S.A., though oceanic
species frequently found in inshore wa-
ters are included. Geographic variations
in occurrence and seasonal distribution
are common but there is no evidence of
morphological variation indifferent geo-
graphical populations.

Detailed descriptions of 5 species
(Barnea truncata, Rangia cuneata, Noe-
tia ponderosa, Donax variabilis, Lyon-
sia hyalina) have been published sepa-
rately (Chanley, 1965a; 1965b; 1966;

IDENTIFICATION OF BIVALVE LARVAE 47

1969; Chanley & Castagna, 1966).
TERMINOLOGY *

Most marine bivalve larvae develop
a shell, secreted as a unit by the
Shell gland, within 18-30 hours after
fertilization of eggs. This first shelled
stage is called Prodissoconch I (Prod I)
(Werner, 1939). The shells of Prod I
are uniform in texture with the dorsal
margin or hinge forming a straight
line. They can be recognized in empty
valves at all stages of larval develop-

ment. Stages with additional shell,
deposited by the mantle, are called
Prodissoconch II (Prod II). The shells

of Prod II are sharply delineated from
that of ProdI and show growth lines.
The differences in appearance between
Prod I and Prod II can be seen in many
of the photomicrographs of larval hinge
structure (Figs. 9, 15B, 21, 25, 27C and
D, 33, 39 and 44D).

For purposes of identification, larvae
are separated into 2 groups by shape.
Early stages are D-shaped (Prodlas well
as Prod II), “straight-hinge” larvae and
later stages are “umbo” larvae. Straight-
hinge larvae are defined as those having
a hinge line at least half the total length
(maximum anterior-posterior dimen-
sion). Umbo larvae are those with a hinge
line less than half the total length or
with well developed umbos (Fig. 1).

Total length in Prod I larvae is usu-
ally 15-30 u greater than hinge-line
length. Hinge-line length is a Prod I
measurement and an important identifi-
cation aid for straight-hinge larvae be-
cause it does not increase appreciably
during the larval development of most
species. It ranges from 35 to over
100 u.

The hinge line becomes obscured in
umbo larvae, and shape of umbos be-
comes an important characteristic. Um-
bonal shapes are illustrated in Fig. 1.
Umbos tend to be “round” and “indis-
tinct” in early development. Though

*See also glossary at end of paper.

never prominent in some species, e.g.,
Aequipecten irradians and Rangia cune-
ata, they do become conspicuous inmost
bivalve larvae.

Umbos may appear continuous with
the rest of the shell, as in the “round,”
“proadly rounded” and“angular” types,
or discontinuous, as in the “knobby”
and “skewed” types (Fig. 1). The broad-
ly rounded umbo is common and well
illustrated by most larval venerids.
Some species of larvae with this type
of umbo do not go through the round
or indistinct stage. Less common is
the angular umbo exemplified by Mul-
inia lateralis. Knobby umbos, such as
those found in pholads and anomiids,
are also common. Frequently other
types of umbos become knobby just
prior to metamorphosis. The skewed
umbo is a variant of the knobby type
and is found only in the genus Cras-
sostrea. Intermediate and transitional
shapes occur frequently.

Relative length and shape of anterior
and posterior ends of valves can also
be used to identify larvae. Relative
lengths of ends can be estimated from
an imaginary perpendicular line drawn
from the middle of the hinge to the
ventral margin (Fig. 1). Valve ends
may be nearly equal in length and shape
or one end may be either appreciably
longer, or more pointed, or both.

Slope and length of anterior and pos-
terior shoulders are importantfeatures.
Usually the point of sharpest turn or
“break” in the contour of larval shapes
occurs at a higher level on the posterior
shoulder (Fig. 1). Shoulders may be
straight or rounded. Umbos and shoul-
ders may comprise from И to more
than 12 total height (maximum dorso-
ventral dimension).

Distinctive characteristics such as
coloration, texture and thickness of valve
edges are subtle and difficult to describe
but useful in identification of larvae.
With practice, size, shape, umbo type
and special characteristics are inte-

48 CHANLEY AND ANDREWS

TABLE 1. Sources of data for identification aids relative to the larvae of 23 bivalves occurring

in Virginia

Е Own
Species

Aequipecten irradians Lamarck
Anadara transversa (Say)
Anomia simplex Orbigny
Barnea truncata (Say)
Crassostrea virginica Gmelin
Cyrtopleura costata (L.)
Donax variabilis Say

Ensis directus Conrad

Gemma gemma (Totten)
Laevicardium mortoni (Conrad
Lyonsia hyalina Conrad
Mercenaria mercenaria (L.)
Modiolus demissus Dillwyn
Mulinia lateralis (Say)

Mya arenaria (L.)

Mytilus edulis L.

Noetia ponderosa (Say)
Petricola pholadiformis (Lamarck)
Pitar morrhuana Linsley
Rangia cuneata (Gray)

Spisula solidissima (Dillwyn)
Tellina agilis Stimpson

Teredo navalis L.

1 4 »4 »4 DA MMM мм

>

м

rs“

Observations

Observations of
Loosanoff, Davis & Chanley (1966)

X
Xx
X

grated by the eye, and recognition of
similar larvae in a sample is possible.
One must always be conscious of size
of larvae, and frequent measurements
with an ocular micrometer are strongly
recommended.

Hinge structure and internal anatomy
can be used to help identify larvae but
have not been considered comparatively
in this report. They are difficult to
observe in whole preserved larvae and
are usually impractical for routineiden-
tifications in plankton samples.

MATERIALS AND METHODS

All descriptions are of larvae reared
in the laboratory from known parents.
In addition to the material obtained by
personally rearing larvae, data and pho-
tomicrographs from Loosanoff et al.

(1966) are also presented (Table 1). Mod-
ified techniques of Loosanoff & Davis
(1963) were used in obtaining and cul-
turing larvae.

Cultured larvae were examined daily
and samples were regularly preserved
for measurements and photomicro-
graphs. Dimensions were determined
by measuring at least 10 larvae at each
5 и length interval to the nearest 5 y.
Most photomicrographs are of freshly-
preserved whole larvae. Occasionally
it was necessary to photograph living
specimens. This was accomplished by
diluting culture water with distilled wa-
ter in a Sedgwick-Rafter counting cham-
ber until larvae ceased movement.

Larvae were preserved in a seawater
solution of 10% sugar, 1% formalin and
.05% sodium bicarbonate (Carriker,
1950a; 1950b). A reference collection

IDENTIFICATION OF BIVALVE LARVAE 49

Umbo Stage

Dorsal
Straight-Hinge Stage
Anterior
Shoulder

Posterior Umbo
\

Straight-Hinge Line uns: --Depth---

1
-d--

r
р
|
р

—

\

=
Posterior Anterior =
) | | =
| | | | |
; Latin) Ent a NS 2 Г
r--Length---
¡Posterior | Anterior !
End N End
Ventral
Umbonal Shapes
Knobby Skewed
Round or Indistinct Broadly Rounded Angular

FIG. 1. Diagrammatic illustration of terminology used to describe dimensions and shapes of
bivalve larvae. The posterior end is usually blunter and shorter than the anterior and has a
higher shoulder. Length of ends is compared by imagining a perpendicular line through the
larva as shown in top center figure.

of many species of various sizes has come.
been assembled for comparative work. Species have been listed phylogenet-
Additions to this collection will be wel- ically in Figs. 2 and 4 to facilitate

20 CHANLEY AND ANDREWS

comparison between closely related spe-
cies. In other figures and in the tables,
species have been listed alphabetically
for convenience.

RESULTS

The identification aids devised include
comparative photomicrographs, tables
of seasonal and geographic distribution,
tables and figures of dimensions, keys
and specific descriptions. They are
designed for use with either live or
well preserved larvae. Combined use
of these aids is recommended.

Shape and dimensions are emphasized
in the present account. Both are influ-
enced by larval position with respect
to the viewer. Consequently, it is
imperative that larvae should be in
analogous positions. For easiest iden-
tification they should lie on one side
with both ends in the same plane.

Straight-hinge and eariy-umbo larvae
are usually more abundant in plankton
samples than those with well developed
umbos. Advanced larvae are usually
more easily identified. Therefore, it is
advisable to work with them first. With
experience, smaller larvae of the same
species can then be identified by com-
parison. Frequently a few species will
be particularly numerous and identifi-
cations can be made by population char-
acteristics (e.g., average length-height
relationship).

Comparative Photomicrographs (Fig. 2)

Photomicrographs of larvae are the
most useful of all aids because they
give a more accurate portrayal of shape
and proportions than can be conveyed
verbally or with drawings. Pictures
used in composite figures were cutfrom
photomicrographs of groups of larvae.
Larvae are arranged by size andoriented
to facilitate easy comparisons, Arrange-
ment is in phylogenetic order. Occa-
Sionally unrelated larvae appear to be
Similar in size and shape. For this
reason, all photomicrographs for a giv-
en size should be examined.

It was not possible to orient all photo-
graphs uniformly with anterior ends al-

ways to the right or left because some
of the earlier work was completed be-
fore the need for such orientation was
realized. No attempt has been made
to arrange larvae by chronological age
because rate of larval development var-
ies considerably withtemperature, qual-
ity and quantity of food, and numerous
other culture conditions. Only shapes
should be compared since texture or
darkness may reflect photographic var-
iation rather than larval appearance.

Distribution (Tables 2 and 3; Fig. 3)

The larvae of many species could not
be reared in the laboratory because
adults could not be induced to spawn
and their stripped gametes failed to
develop normally. Of these species, 9
are common and must be considered
in identifying specimens from plankton,
These are listed with their distribu-
tions and probable appearance of larvae
in Table 2.

Knowing the origin of field collections
can aid in identification of larvae. Some
species are limited to Chesapeake Bay
and its tributaries, whereas others are
found in oceanic water or seaside bays.
The distribution and relative abundance
of species included in this report are
shown in Table 3, These descriptions
refer to the Chesapeake area, and es-
tuarine species in Virginia may be
oceanic in other areas, or vice versa.

A knowledge of the season of sample
collection also helps in identifying lar-
vae. Some species spawn in spring and
others in fall. Spawning seasons have
been determined or estimated from his-
tological and gross examination of go-
nads, spawning response in the labora-
tory and published accounts. Spawning
seasons have not been adequately de-
fined for many species. Geographic
and annual variations occur in well-
known species. Consequently, season-
ality of reproduction is defined only
broadly (Fig. 3).

Dimensions (Tables 4 and 5; Fig. 4)

Larval identifications are facilitated
by measuring total length, height and
hinge-line length. These dimensions

IDENTIFICATION OF BIVALVE LARVAE 51

Anadara Noetia Modiolus Mytilus Aeguipecten
LENGTH transversa ponderosa demissus ire ans

60

70

° e $
- |, €

100
| 10
120

130

140

150

160

170 3

FIG. 2. Comparative photomicrographs of larvae of 23 bivalves. (Photographs of all but 8
species, Noetia ponderosa, Tellina agilis, Donax variabilis, Rangia cuneata, Barnea truncata,
Cyrtopleura costata, Lyonsia hyalina and Gemma gemma, are from Loosanoff, Davis € Chanley,
1966.) Lengths are in u.

52 CHANLEY AND ANDREWS

LENGTH Anomia Crassostrea Laevicardium Mercenaria Pitar

simplex virginica mortoni mercenaria morrhuana

50

60 S

70 & $

so ® e

о e a
100 E) Y \ É

a
110 »
120 a ES
130 £ ®
4

150
160
170

FIG. 2. (continued)

IDENTIFICATION OF BIVALVE LARVAE 53

LENGTH Petricola
50

60
70
80 ®
90 o
100
110

120

130

140

150

то XA

FIG. 2. (continued)

Tellina

Pholadiformis agilis

Donax ley nsis Spisula
variabilis directus solidissima

54 CHANLEY AND ANDREWS

LENGTH ,Mulinia Rangia Mya Barnea Cyrtopleura
lateralis cuneata arenaria truncata costata
50
E
60 @ =

70 A |
80 =
Ko

®
®

90 |
100 >

110 ® cy
20 м |

130 œ

140 @ $

150 = @

160

QO e

170

FIG. 2. (continued)

IDENTIFICATION OF BIVALVE LARVAE

Teredo Lyonsia
LENGTH navalis hyalina
50

60

MO

FIG. 2. (continued)

180

190

200

210

220

230

240

250

260

ero

280

290

300

Teredo
navalıs

310

320

330

340

350

360

370

380

390

400

55

56 CHANLEY AND ANDREWS

Anadara Noetia Modiolus Mytilus Aequipecte
LENGTH >ransversa ponderosa demissus edulis pat '

180
190
200
210
220
230
240
250
260
270
280
290

300

FIG. 2. (continued)

IDENTIFICATION OF BIVALVE LARVAE 97

Anomia Crassostrea Laevicardium Pitar

LENGTH simplex
180

190
200

210

220

230

240

250

260

270

280

290

300

FIG. 2. (continued)

virginica mortoní Mercenaria morrhuana

pe mercenaria
, № J)

58 CHANLEY AND ANDREWS

LENGTH Gemma Petricola Tellina Donax Ensis
gemma pholadıformis agılis variabilis directus

180

190
200
210
220
230
240
250

260

270

280

290

300

FIG. 2. (continued)

IDENTIFICATION OF BIVALVE LARVAE 59

Spisula Mulinia Mya Barnea Cyrtopleura
LENGTH so/lidissima lateralis arenaria truncata costata
180 des

190

200

210

220

230

240

250

260

270

280

290

300

FIG. 2. (continued)

60 CHANLEY AND ANDREWS

Species

Aequipecten trradians
Anadara transversa -------------
Anomia simplex
Barnea truncata A A =
Crassostrea virginica
Cyrtopleura costata
Donax variabilis
Ensis directus
Gemma gemma
Laevicardium mortoni
Lyonsia hyalina

Mercenaria mercenaria
Modiolus demissus
Mulinia lateralis

Mya arenaria

Mytilus edulis

Noetia ponderosa
Petricola pholadiformis
Pitar morrhuana

Rangia cuneata — PR

Spisula solidissima
Tellina agilis
Teredo navalis

------ Estimated

FIG. 3. Spawning seasons in Virginia of 23 species of bivalves.

TABLE 2. Distribution and appearance of larvae of 9 bivalves common in Virginia but not in-

cluded in this report

Distribution of Adults

(Salinity) Appearance of Larvae

Species

Anadara ovalis (Bruguiere) Above 15% Probably similar to other

larval Arcidae

Above 5% in Chesapeake
Bay and its trubutaries

Brachidontes recurvus
(Rafinesque)

Probably similar to other
larval Mytilidae

Above 5% in Chesapeake
Bay and its tributaries

Amygdalum papyria (Conrad) Probably similar to other

larval Mytilidae

Patchily abundant in Unknown

rivers at 10%, and lower

Congeria leucophaeta
(Conrad)

Macoma balthica (L. )

Above 5% in Chesapeake
Bay and its tributaries

Described as pale with low
reddish indistinct umbo. Dirt
frequently sticking to shell

Macoma phenax (Dall) Chesapeake Bay and its Unknown

tributaries

Macoma tenta Say
Tagelus plebeius (Solander)
Bankia gouldi Bartsch

Above 10%
Above 10%o

Above 10% in Chesapeake
Bay and its tributaries

Unknown
Unknown

Probably similar to Teredo
navalis but with height not
exceeding length

IDENTIFICATION OF BIVALVE LARVAE 61

TABLE 3.

Distribution and abundance of adult bivalves of 23 species in Virginia

дМм —————

Distribution

Species (Salinity) Abundance

Aequipecten ivvadians Lamarck

Anadaya transversa (Say)

Anomia simplex Orbigny
Barnea truncata (Say)
Crassostrea virginica Gmelin
Cyrtopleura costata (L. )

Donax variabilis Say
Ensis directus Conrad

Gemma gemma (Totten)

Laevicardium mortoni (Conrad)

Lyonsia hyalina Conrad

Mercenaria mercenaria (L.)
Modiolus demissus Dillwyn

Mulinia lateralis (Say)

Mya arenaria (L.)

Mytilus edulis L.

Noetia ponderosa (Say)

Petricola pholadiformis
(Lamarck)

_ Pitar morrhuana Linsley

Rangia cuneata (Gray)

Spisula solidissima (Dillwyn)

Tellina agilis Stimpson

Teredo navalis L.

High salinity seaside bays

Above 10% in Chesapeake
Bay and its tributaries

Above 10%
Above 10%p
Above 6%

Above 10%p

Ocean beaches
Above 10%

Above 10%

Above 10% in sand

Above 10% > in Chesapeake
Bay and its tributaries

Above 15%
Above 5%o
Above 10%

Above 5%

Inlets between barrier
islands and mouth of
Chesapeake Bay

Above 17.5%o
Above 10%

Oceanic, in seaside bays

Less than 15%. in James,
Potomac and Rappahannock

rivers and in Back Bay
Oceanic and in seaside bays

Above 18%

Above 10%o

| Rare

Common

Common

Common, abundant in patches
Abundant

Scarce to common

Common to abundant in
patches in summer
Common to abundant

Common to abundant in
patches but rare on seaside

Common to abundant in spring
and early summer: Rare in
seaside bays

Scarce to abundant in patches

Abundant
Abundant

Common to abundant; scarce
in seaside bays

Abundant in Chesapeake Bay
and its tributaries but scarce
in seaside bays

Scarce to common

Common

Common to abundant in
patches

Very rare

Abundant in these areas

Common

Common to abundant in
patches

Common

62 CHANLEY AND ANDREWS

=
= = < <
= < ш x ш
CATEGORIES &ч7195„ 2225 D dos <0 8
LOS Dore a = = ош = On
o A ES AN E] INIA
(in microns) ACES Tes A AS A eee
21900 O A AS ACI A
A к <= з ош анозх а з<ча оо <но
a ae
e |
60 © |
- 50
e e © Má
e e
o за
70 o o о. @ - во
o.
e A é 60
Oo e
Ces o o al
o e
- 80
= By
Oo 292
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| Фо оо ee ey} ap ees
| o ® © [ : "Y a
90 Oe Fae
age. De de =
р
у 51190
E =
' 4100
ES и 170
® J 1
©
O As o : - 80| 5
> o. e e ee | sE
e... ete ee
100 >. ФФ: 1°
нм
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(TU 1
Bazar @ ;100
14
' 3110
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9. À ' MINIMUM
it - т 4 90 1
р f 1
$ Фо .... Фо | - о © wean
HO Br ' р . Ù 1100 E i MAXIMUM
eee 4 STRAIGHT EARLY UMBO
ean HINGE UMBO
= № 7110
р >
4120

FIG. 4. Comparative length-height relationships of 21 species of bivalve larvae. At least 10
larvae were measured to the nearest 5 y at each 5 y length interval. Solid circles indicate mean
height.

63

IDENTIFICATION OF BIVALVE LARVAE

V3H1SOSSVHI
003431
VINONV
VINyYv8

УНП 371404145
VINITOW
VIONVY
N3193d1Nn83V
39113

VAW

vINSIAS
VNI711731
VvI1091413d
VIUVN3IY3N
SISN3

XVNOQ
WNIOYVINA3VA
SNTILAW

SN 1OIGOW
VIL3ON
УЗУДУМУ

(in microns)

”
zw
pe
So
zo
>
JI4

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= z
ız 2
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oe, =
x
0-13
E
EE
KIT
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FIG. 4.

(continued)

CHANLEY AND ANDREWS

64

V3H1S0SSvVH9I
003431
VINONV
VINYvVE
VYUNIIdOLYAD
VINIING
VIONVY
N3193dINOIV
YVlid

VAN

VINSIdS
VNI77131

LENGTH
CATEGORIES
(in microns)

MINIMUM
® bu
MAXIMUM
EARLY UMBO
UMBO

3120

4130

(continued)

FIG. 4.

65

IDENTIFICATION OF BIVALVE LARVAE

wauisossvyd
003431
VINONV
ЕСА
VININIOLYA
VINIINN
N3193d4IN03v
YVLid
VAN
vINSIAS
VNI77131
109154133
VIUYVN3IY3W
SISN3
XVNOQ
NNIOUVIIAIVTI

æ
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1H913H

150

160

LENGTH
CATEGORIES
(in microns)

180

170

180

190

(continued)

FIG. 4.

Fig. (Page |)

CHANLEY AND ANDREWS

66

4180|
4230)

V341S0SSvVH9
ViNyvg
VUNITAOLYAD
VINITNW

vun

vINSIAS
VNI9731
VISVN3943N
SISN3

XVNOg
ANIOUVIIA3WA
SN TUILAM
SNTOIOmN
VuVOVNY

т

LENGTH
ICATEGORIES

|
|
|

(in microns)

230

Е

[мхи U
UMBO

Y3H1S0SSvVH9
003431
VIWONY
ViNyva
VUN3I4OLHAD
VINITNM
N319341N03v
VAN
vinsids
VNI7731
VIHYN3O43M
SISN3

xVNOO
ANIONVILA3WA
SNTILAM

SN T0I00M
VIL3ON
VUVOVNY

LENGTH
CATEGORIES |
(м microns)

4160|
4170
+180
4220)
2170 |
4180,
4190
+210
-220

4

(continued)

—

200
210

FIG. 4.

67

IDENTIFICATION OF BIVALVE LARVAE

SNOYOIMN NI

4190
4200

3210

о о

о
m +
y u
T

3220
260
4270

le]
Qu
T

3210

4220)
4230

240

4250

4260

V3Y1S0SSVH9
VINUVE
vun31dO1HAI
VINSIdS
SI9N3

SA MILAN

SNTOIGOW

vuvavnv| —_&———_

T T T T

LENGTH
CATEGORIES
(in microns)

260

270

MINIMUM
MEAN
MAXIMUM
UMBO

SNOYOIW NI

1H913H

- 180
3190

4200

4210
1220
30

[o]
+
N
=

4250

o
©
T

4210
4220

4230

4240

ie

4

V3Y1SOSSVYO
VINYve

УУП 319401345
vVINSIAS
VNITI31L
SISN3
ANIOYVIIA3VA

LENGTH
CATEGORIES
(in microns)

T

$

@ -250

(continued)

FIG. 4.

= ya |
LENGTH = ye
FE ER om LENGTH o
CATEGORIES| & 35 7 ао | CATEGORIES =
GBRicrons)) 2 228 22 | CHANLEY AND ANDREWS | 2
< 5 я = 2 (in microns) a
|< 33335 | z
== +
JE
3210 MINIMUM
+ ou.
4220 | MAXIMUM
UMBO
4230 300
4240
280 +
Ф
2
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=
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23
ee 310
290 270
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4300
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FIG. 4. (continued)

Fig. (Page 7)

MYTILUS
BARNEA

CRASSOSTREA

240

250

260

270

280

290

300

310

320

IN MICRONS

HEIGHT

IDENTIFICATION OF BIVALVE LARVAE

69

TABLE 4. Hinge line, minimum and maximum lengths (inp) of straight-hinge bivalve larvae. *

Species

Aequipecten irvadians 85
Апааата transversa 70
Anomia simplex 60
Barnea truncata 55
Crassostrea virginica 65
Cyrtopleura costata 60
Donax variabilis 70
Ensis directus 85
Laevicardium mortoni 80
Mercenaria mercenaria 100
Modiolus demissus 105
Mulinia lateralis 60
Mya атепалта 85
Mytilus edulis 90
Noetia ponderosa 80
Petricola pholadiformis 70
Pitar movrhuana 70
Rangia cuneata 75
Spisula solidissima 80
Tellina agilis 75
Teredo navalis 70

Total Length
Minimum Maximum

Hinge-line Length
Minimum Maximum

140 55 65
140 60 70
110 45 55
100 40 50
100 45 50
95 35 40
120 50 60
155 70 75
130 60 65
155 70 80
175 | 80 90==
100 40 50
135 55 60
175 75 Sons
160 65 80
125 55 65
125 55 65
135 55 65
130 55 60
105 45 50
105 40 50

*Gemma gemma and Lyonsia hyalina larvae are not included because they do not go through a

typical straight-hinge stage.

**Hinge line may be as short as 65 u in very young larvae.

have been measured to the nearest 5 y.
Minimum length and hinge-line length
are given in Table 4. Both are Prod I
characters useful in identification be-
cause they are relatively constant. In
Table 5 total lengths of larvae at dif-
ferent umbonal stages and maximum
larval lengths are shown. Maximum
planktonic size at metamorphosis is
variable and planktonic juveniles occur
(not included in this report). Juveniles
can sometimes be recognized by ab-
sence of a velum, by a clear area
around the foot, and by dissoconch shell
growth. These characters are not al-
ways readily apparent in preserved or
quiescent specimens.

The length-height relationship (Fig.
4) is another important identification
character. Height ranges from 70 u
less than length in some Arcidae to
greater than length in some Ostreidae
and Teredinidae. This ratio quickly

guides an experienced planktologist to
pertinent groups of larvae, though it
is seldom distinctive for individual spe-
cies. It is especially effective when
stage of development is considered.

Keys

Only characteristics that can readily
be determined in living or well pre-
served larvae have been included in the
keys because their purpose is to serve
as a practical aid to identification. As
a result, artificial characters have been
used and some basic structures ignored.
This “artificiality” has the inherent dis-
advantage of grouping unrelated species
and requiring considerable revision of
the keys whenever data for previously
unidentified species become available.
Consequently, these keys represent a
preliminary attempt at practical identi-
fication rather than a stable approach
to classification of bivalve larvae.

70 CHANLEY AND ANDREWS

TABLE 5.
at metamorphosis.
type to another. *

er CR A ee ИИ
Round or Broadly
Species | Indistinct | Rounded un. EN Skewed
р E Umbos Umbos Umbos
Umbos Umbos |
se EEE
Aequipecten ivradians 120-200
Anadara transversa 130-140 135-320
Anomia simplex 90-120 | 90-215
Barnea truncata 90-125 | 110-315
Crassostrea virginica 80-105 95-120 115-350
Cyrtopleura costata 70-115 110-300
Donax variabilis 100-120 100-200 180-340
Ensis directus 135-195 200-275 200-275
Laevicardium mortoni 110-170 150-245
Mercenaria mercenaria 140-235
Modiolus demissus 150-240 200-305
Mulinia lateralis 90-150 130-240 200-240
Mya arenaria 110-200 170-210
Mytilus edulis 150-305 260-305
Noetia ponderosa 145-165 160-210
Petricola pholadiformis 110-185
Pitar morrhuana 110-150 140-185
Rangia cuneata 110-175
Spisula solidissima 110-200 135-275
Tellina agilis 90-135 130-250
Teredo navalis 105-130 115-200

Length of larvae in u and shape of umbos. Largest length given is approximate size
Overlapping measurements indicate transitions from one umbo

*Larvae of Gemma gemma and Lyonsia hyalina are not included because they do not develop an
umbo.

Umbonal shapes have been catego-
rized. These categories are illustrated
in Fig. 1 and defined in the glossary.
Familiarity with this classification is
essential. Umbonal shape changes grad-
ually during development. Therefore,
many species have been listed several
times to cover transitions and inter-
mediate stages. Where length ranges
are give, they refer to larval length
only during a particular stage of devel-
opment (as shown in Tables 4 and 5),
not the complete length range.

Color and texture are used as char-

.acters if they are distinctive under
varied conditions of lighting and pre-
servation. Subtle distinctions are pos-
sible with experience.

The terminology is defined in the
glossary and illustrated in Fig. 1.

KEYS TO BIVALVE LARVAE
OF VIRGINIA

1 D-shaped with hinge line straight
and more than half total length
.. Key to Straight-Hinge Larvae

Not D-shaped, or with hinge line
less than half total length..... 2
Hinge line, if evident, less than
half total length; dorsal margin
rounded or with distinct umbo;
no central indentation. . . . .

2 (1)

Oval, without definite straight-
hinge line or umbos, frequently
with central indentation of dorsal
margin, gray, black or opaque. .3
3.(2) Length 150-180, u... «nl

IDENTIFICATION OF BIVALVE LARVAE 74

Length greater than 245 u.....
Е Gemma gemma

Key to the Straight-Hinge Larvae
1 Hinge-line length less than 60 u

ас Ses ce TT 2
Hinge-line length 60 » or more
ENTE IA, E TAMOS 5 1033
2 (1) Hinge-line length less than 50 u*
ER TABA AA ee PO ER 3
Hinge-line length 50-60 y. .... 8
3 (2) Shoulders round with gradual
transition*to hinge; 209% 25... +

Shoulders straight with angular
transition to hinge, usually pink

or purple: in hinge “area...
N ete Sua à Barnea truncata
Cyrtopleura costata

4 (3) Posterior end blunter than ante-
rior; posterior shoulders drop-
ping from hinge more rapidly
Ehaneanterior is Ls. oe. Le 5
Ends nearly symmetrical..... 6

5 (4) Dark, heavy shell and margin. .
ne Crassostrea virginica
Light, pale shell and margin...

Acide fe I IS Mulinia lateralis

6 (4) Dark, heavy or opaque...... $
Light, pale and fragile; usually
with clear area under center of
slightly rounded hinge line....
StR ar à . Anomia simplex

7 (6) Texture heavy, dark band around
shell margin, frequently opaque
when preserved. . Teredo navalis
Texture lighter, dark band less
pronounced. Usually pale pink or
purple пеар ее...
A, EA Tellina agilis

8 (2) Anterior end more pointed than
POSTEO e oo ce oe el, 9
Ends almost equally rounded. . 11

9 (8) Pale andfragile. Shoulders slight-
AU ев

Not pale and fragile. Shoulders
strateht DEINER oe 10

10 (9) Dark and heavy. Shoulders long
ee ae Petricola pholadiformis

Not dark and heavy. Shoulders
short. ..... . .Pitar morrhuana

118), Pale and Iragilen me Zilk.
ay Seay’ By ER .Anomia simplex

Not pale and fragile..; 2)... 12

12 (11)Shoulders nearly straight.....
He ie ue: ater cv . Pitar morrhuana
Shoulders rounded...... Donax
variabilis, Spisula solidissima

Mya arenaria or Laevicardium

mortoni
13 (1), “HingerlineiG0=70 jie) Re oe 14
Hinse line overs 70. en acest 17

14 (13)Dark and heavy, usually distinctly
brown. Height 10-30 y less than
length. Shoulders rounded. (Ar-
eidae)s 24. IPRA hee Gee 15
Neither dark nor heavy, Height
5-20 » less than length. Shoul-
ders ‘straights. SOMME Ur 16

15 (14)Ventral margin round, almost
forming semicircle with ends. .
а HE JA .Noetia ponderosa
Ventral margin curved but not
round, not forming semicircle
with ends. . . Anadara transversa

16 (14)Pale. Gradual transition from
shoulders to hinge; anterior end
much more pointed than poste-
LIO Y Aequipecten ivvadians
Neither dark nor pale. Angular
transition from shoulder tohinge.
Anterior end slightly more pointed
than posterior. . Pitar morrhuana

17 (13)Dark and heavy; usually distinctly
brown Er . .Noetia ponderosa
Neither dark nor heavy; without
distinctivexcolor a En 16

18 (17)Shoulder-hinge transition grad-
ual, almost continuous curve.,.

MASTERS is idiyectus

Shoulder-hinge transition angular

*Crassostrea virginica, Anomia simplex, Tellina agilis, Barnea truncata, Cyrtopleura costata,
Mulinia lateralis and Teredo navalis are very similar at lengths of 75 y and less.

72

1

3 (2)

4 (1)

5 (4)

7 (4)

8 (7)

CHANLEY AND ANDREWS

Modiolus demissus,
Mytilus edulis,
Mercenaria mercenaria

ee a” fo! natale" ele

Key to the Umbonate Larvae

mbes ‘skeweds. en tn Br
Е er Crassostrea virginica

Umbos angular: to DR ar 2
Umbos broadly rounded...... +
Umbos knobby: а. 11
Umbos round or indistinct... .21

Posterior end blunt, dropping al-
most vertically from shoulder to
ventral margin; umbos high with
shoulders sloping steeply.....
he = D ror Mulinia lateralis
Ends almost equally rounded; um-
bo low with shoulders sloping
Prague Her Ba 3
Length 180-2304. . Mya arenaria
Length 215-2100. 2220208 2.

Ends of nearly equal length... 7
Anterior end more pointed than
posterior; shoulders and umbos
about 1/2 total height. ....... 6
Ends nearly equally rounded.
Shoulders and umbos about 1/3
total height. . . .Donax variabilis
Dark and heavy; umbos broad;
shoulders Slope steeply. Poste-
rior shoulder straight. Length
EOS LR cee A te te: 280
ae Bee Petricola pholadiformis
Not dark or heavy. Umbos nar-
row. Shoulders slope gradually;
posterior shoulders rounded at
lengths to 185 y but straight in
larger larvae..... Spisula solid-
issima or Laevicardium mortoni
Length 130 y or less. Heavy
shell margin with dark rim. . .8
Length 140 р or more. Not unu-
sually dark or heavy. ....... 9
Umbos with distinct pink or pur-
ple color... .Cyrtopleura costata

or Barnea truncata
No pink or purple color. Fre-
quently opaque when preserved

9 (7)

10 (9)

11 (1)

12 (11)Length less than 125 u.

IAS ne CU Teredo navalis
Shoulders rounded. .........
EN Pitar morrhuana
Shoulders straight. 2". 10
Length 140-235 u. Umbos broad.
Shoulders slope steeply.......
D Le Mercenaria mercenaria
Length 200-275 y. Umbos narrow.
Shoulders slope gradually.....
Ensis directus

Ends of nearly equal length. . .15
Inequi-
. Crassostrea virginica
10

valve. ..
Length greater than 125 y...

13 (12)Shoulders straight. Shoulders and

14(13)Dark with heavy outline.

umbo about / total height. Length
greater than 200 u... 2. и
EEE EUER . Mulinia lateralis
Shoulders round. Shoulders and
umbo either {/; total height or
more than//total height. .... 14
Faint
pink or purple color in umbo.
Shoulders slope steeply. Shoul-
ders and umbo more than total
height. Length 130-250 u.....
Oe thee DS SR Tellina agilis
Color not distinctive. Shoulders
slope gradually. Shoulders and
umbo about 7; total height. Length
Over 130 y... Donax variabilis

15 (11) Anterior end more pointed than

16 (15) Dark brown.

¡o AA atime .16
Ends nearly equally rounded. .19
Anterior end red-
dish-brown. Flattened dorso-
ventrally. Length much greater
than height. (Arcidae)...2 2. 17
Color not distinctive. Egg-shaped
except for knobby umbo. (My-
tilidaeho ооо 18

17 (16) Ventral margin nearly straight.

Shoulders long. Ends sharp.
Length 135-320 u....... A
ме Anadara transversa
Ventral margin rounded. Shoul-
ders short. Ends blunt. Length
160-210 u... .Noetia ponderosa

18 (16) Ventral margin nearly straight.

Umbo broad and conspicuous.

IDENTIFICATION OF BIVALVE LARVAE 73

Length 200-305 jue. а
ee ee .Modiolus demissus
Ventral margin rounded. Umbo
narrow andinconspicuous. Length
260-305 u.... Mytilus edulis
19(15)Heavy shell margin with dark
zim...bquivalven... feces) 200, 20

Pale and fragile. Inequivalve.
Frequently with byssal notch on
antero-ventral margin when
length exceeds 175 u. Length
902219. u... Anomia simplex
20(19) Round. Height usually 5-10 u
less than length; never exceeding
length. Pink or purple in umbo.
Ence 110-315 ar 4. 2%
RAS EL Barnea truncata

or Cyrtopleura costata

Oval. Height usually exceeding
length when length is greater

than 140 y. Shell margin with
pronounced dark rim. Frequently
opaque when preserved. Length
119-2202u.., ; Teredo navalis

21 (1) Anterior end longer than poste-

Ends of nearly equal length. . 25
22 (21) Anterior end more pointed than
ВРЕТ Е MN ee 7 23
Ends nearly equally rounded. .31

23(22)Dark. Length 80-105 y. Inequi-
valve. ... Crassostrea virginica
Pale. Equivalve, ......... 24

Color not distinctive. Equivalve.
Пере greater than 110 u.....

He ee Laevicardium mortoni

or Spisula solidissima

24 (23) Anterior end forming apex of
triangular-shaped larva. Umbos

flat at lengths from 120-150 u,
becoming rounded from 150-200 u
RS GE Aequipecten irradians
Anterior end not as sharply point-

ed. Larva not triangular. Umbos
.Mulinia lateralis
25 (21) Anterior end more pointed than
POSTRE eS econo wee Re 26

Ends nearly equally rounded. . 29

| 26(25)Heavy. Elongated or dorso-ven-
| trally compressed. Distinctively
| brown. Anterior end frequently
| reddish brown. (Arcidae)... 27

Not distinctively colored or dor-

so-ventrally compressed... . 28

27 (26) Ventral margin almost straight

ee ere Anadara transversa

Ventral margin rounded......

a PEAR SU Noetia ponderosa

28 (26) Developmental state of the fol-
lowing:

length 110-2150 и...

IDEEN, Pitar morrhuana

Length: 1359-19 un. na.

Ele. ER .Ensis directus

Length. 150-240 и...

RE Re a ee Modiolus demissus

Length 150-305 u... ee...

. .. Mytilus edulis

29(25)Dark and heavy; shell margin

with dark rim.. ..Tellina agilis

Not dark. Without dark rim

around shell margin....... 30

30(29) Pale. Length 90-120 y. Inequi-

Valve. a. pooh Anomia simplex

Not pale. Length greater than

Оо Equiyalver a... 23. 31

31 (30) Umbos high. Length 110-220 y

... Mya arenaria

Length 110-175 u

.Rangia cuneata

telle, (eue. © 6

Umbos по.

СИС УСК gel er le

SPECIFIC DESCRIPTIONS

Valid, or recently accepted, generic
and specific names, as listed by Vokes
(1967), have been used in these descrip-
tions. Other generic and specific names
that have been used by the authors of
the references cited are enclosed in
parentheses.

Family Arcidae

Literature: Arca noae L. (Odhner,
1914); Anadara broughtonii (Schrenk)
(Yoshida, 1953; Kan-no & Kikuchi, 1962;
Kan-no, 1963); A. granosa L. (Pathan-
sali, 1964); A. subcrenata (Lischke) (Yo-
shida, 1937a; 1957);A. (Arca) transversa
(Say) (Loosanoff & Davis, 1963; Loosan-
off et al., 1966).

Anadara transversa (Say)

Dimensions: Total length 70-320 u
Height 15-20 y less than length; increas-

Le CHANLEY AND ANDREWS

2004 . va © ®

ЕТС. 5.
with shell incompletely formed.

anterior end left.

ing to 70 u less than length with growth.
Hinge line about 64 u. Metamorphosis
at 215-320 р; usually 240-260 u.

Shape: Dorso-ventrally compressed.
Low elongate outline. Umbos round or
indistinct from 130 to 170 u; knobby
above 170 u. Ends of nearly equal
length; anterior more pointed than pos-
terior.

Other Characters: Distinctly brown;
anterior end frequently reddish brown,
especially in late stages. Eyespot ap-

Composite photomicrographs of larval Noetia ponderosa.
BIO OZ
sions are given in y under the individual larvae to the right.

120х105
©)
135 X110

>

180х150
a e
m (+) 200X155
Age in days: A. 1. Some

D. 20. E. 26. F. 30. Length x height dimen-

These larvae are arranged with

pearing at about 225 u; becoming con-
Spicuous with increasing size.

Distribution: Adults, common in Vir-
ginia in Chesapeake Bay and tributaries
with salinity above 15%, spawned in
laboratory in late spring and early sum-
mer.

Comparison to Other Species: Elon-
gate appearance, distinct brown color,
and length-height reltionship distin-
guish Arcacean larvae. Noetia pon-
derosa has longer hinge line, shorter

IDENTIFICATION OF BIVALVE LARVAE 75

тт
000410011

FIG. 7. Schematic diagram of the develop-

ment of the internal anatomy of larval Noetia

ponderosa. The key to the symbols used in

this drawing and in all remaining drawings is
as follows:

B AA, aa or AM - anterior adductor muscle

А or a - anus

AF or af - apical flagellum

B or BG or b - byssus gland

BS or bs - byssal spur

df - developing foot

E or e - pigmented eyespot

F or f - foot

G or g - gut

GL or gl - gills

H - heart

h - heel of foot, byssal spur

L or 1 - liver or digestive diverticulae

M or m - mouth

PA or pa - posterior adductor muscle

r - reddish-brown color

RM - retractor muscles

ST or st - statocyst

S - stomach

V or v - velum

VR, vr or vm - velar retractor muscles

shoulders, blunter ends, broader umbo
and more rounded ventral margin.

Family Noetiidae

Literature: Noetia ponderosa (Say)
(Chanley, 1966)

FIG. 6. Hinge structure of larval Noetia Noetia ponderosa (Say)

ponderosa. Length of larval shell: A. 80 u. (Figs. 5, 6, 7)

В. 120u. С. 1554. D. Separate valves

175 и. Dorsal view with left valve on top. Dimensions: Total length 80-210 u.

Anterior end to the right. Height 15-20 y less than length, increas-

76 CHANLEY AND ANDREWS

110 X 80

u

LS

130 X110

155Х [20

170 X 150

190 x 170

200X 180

230x220

FIG. 8. Composite photomicrographs of larval Mytilus edulis. Age in days: A. 1. B. 2. C. 6.
D. 9. E. 16. F. Larger larvae also 16 days old. Length x height dimensions are given in u
under the individual larvae to the right. These larvae are arranged with anterior end right.

FIG. 9. Hinge structure of Mytilus edulis larva 225 u long. Anterior end below. Left photo-
graph is dorsal view, right is ventral view.

IDENTIFICATION OF BIVALVE LARVAE а

1054

FIG. 10. Schematic diagram of the development of the internal anatomy of larval Mytilus edulis.

See caption for Fig. 7 for key.

ing to 55 „ less than length. Depth
increasing from 25 to 70 « less than
length. Hinge line usually 75-80 u (65-
ТО y in one-day-old larvae). Metamor-
phosis at 185-210 u.

Shape: Umbos indistinct to broadly
rounded at 150-160 „; broad knob in
larger sizes. Ends of nearly equal
length, with anterior more pointed above
130 u.

Hinge: Taxodont teeth. increasing
from 4-6 at either end of hinge line,
as larvae develop. Tooth areas about
25 u long; separated by undifferentiated
35 „ central area.

Other Characters: Distinctly brown.
Anterior end darker reddish-brown in
umbonate stages. Apical flagellum in
early larvae. Indistinct eyespot at about
180 u; becoming conspicuous with con-
tinued growth.

Distribution: Adults common at sa-
linities above 17.5%; spawned in spring,
Summer and fall.

Comparison to Other Species: Com-
pared under Anadara transversa.

Family Mytilidae

Literature: Unidentified sp. (Odhner,
1914; Rees, 1950); Adula simpsoni
(Marshall) (Rees, 1950); Brachidontes

senhausi (Reeve) (Yoshida, 1937b; 1953);
Crenella decussata (Montagu) (Jgrgen-
sen, 1946); Modiolus (Modiola) adriatica
(Lamarck) (Jérgensen, 1946); М. demis-
sus (Dillwyn) (Sullivan, 1948; Loosanoff
& Davis, 1963; Loosanoff et al., 1966);
M. (Modiola) modiolus (L.) (Jgrgensen,
1946; Rees, 1950; Newell & Newell,
1963). Musculus (Modiolaria) discors
(L.) (Thorson, 1935); M. (Modiolaria)
niger Gray (Thorson, 1935); M. (Modio-
laria) marmorata (Forbes) (Lovén, 1848;
Jorgensen, 1946; Rees, 1950); Mytilus
californianus Conrad (Breese, Mille-
mann & Dimick, 1963); M. crassistesta
Lischke (Miyazaki, 1936; Yoshida, 1936;
1953); М. edulis (L.) (Borisiak, 1909;
Delsman, 1910; Stafford, 1912; Matthews,
1913; Field, 1923; Kändler, 1926; Nel-
son, 1928; Werner, 1939; Jgrgensen,
1946; Sullivan, 1948; Rees, 1950; Cos-
tello et al., 1957; Breese et al., 1963;
Newell & Newell, 1963; Loosanoff &
Davis, 1963; Bayne, 1965; Loosanoff
et al., 1966).

Mytilus edulis L.
(Figs. 8, 9, 10)

Dimensions: Total length 90-305 y.
Height 25-35 y less in straight-hinge
larvae; 15-20 u less than length in um-

78 CHANLEY AND ANDREWS

FIG. 11. Composite photomicrographs of larval Aequipecten irradians.
Ba 2. С. 50 1351). Ds 501550). Е. 1.

Age in days: А. 1.

F. 11. Length x height dimensions are given in

u under the individual larvae to the right. These larvae are arranged with anterior end left.

bonate larvae. Depth 50 y less than
length in early stages; increasing to
115 «x less than length with growth.
Hinge line usually 75-85 y (65 y in one-
day-old larvae). Metamorphosis from
215 to 305 y but juveniles frequently
planktonic.

Shape: Early straight-hinge larvae
appear chopped off along long hinge line.
Umbos appearing at about 150 y; rounded
at first but projecting above shoulders

as inconspicuous broadly rounded knob
after 260 y. Anterior end much more
pointed than posterior. Ends of nearly
equal length or anterior end slightly
longer.

Hinge: No definite hinge teeth during
larval period. Faint irregularities sug-
gesting pending taxodont dentition at both
ends of hinge line.

Other Characters: Color not distinc-
tive. Apical flagellum present but in-

IDENTIFICATION OF BIVALVE LARVAE 79

FIG. 12. Dorsal view of hinge of larval Aequipecten irradians.

AEQUIPECTEN IRRADIANS

FIG. 13. Schematic diagram of the development of the internal anatomy of larval Aequipecten
irvadians. See caption of Fig. 7 for key.

80 CHANLEY AND ANDREWS

260 X 240

FIG. 14. Composite photomicrographs of larval Crassostrea virginica. Age in days: A. 4.
B. 6. C. 10. D. 14. E. 19. F. 23. Length x height dimensions are given in u under the indi-
vidual larvae to the right. These larvae are arranged with anterior end right.

conspicuous in young larvae. Eyespot conspicuous umbo, less curved ventral
5-7 u in diameter in larvae after 205 y. margin and proportionately less height.
Distribution: In Virginia adults li-

mited to high-salinity cool water. Spawn- Modiolus demissus Dillwyn

ing season probably late fall or early Dimensions: Total length 105-325 u.
spring. Height 15-30 y less (usually 20-25 и)

Comparison to Other Species: Dis- in straight-hinge larvae; 25-40 u less
tinguishing characteristics of mytilid than length in umbonate larvae. Hinge
larvae are long hinge line, egg shape, line usually 80-90 и. Metamorphose
inconspicuous umbos and large size. from 220 to 305 u.

Modiolus demissus larvae with more Shape: Round umbos form at about

IDENTIFICATION OF BIVALVE LARVAE 81

FIG. 15. Hinge structure of Crassostrea virginica larvae. Anterior end is to the left. A. Dor-
sal view of shell 70 u long. В. Dorsal view of shell 105 р long. С. Internal view of valves 265 u
long.

FIG. 16. Schematic diagram of the development of the internal. anatomy of larval Crassostrea
virginica. Figure of umbo larvae on right is from Galtsoff (1964). See caption of Fig. 7 for key.

82 CHANLEY AND ANDREWS
90 X 80

100 X 90

©

110 X 100

®

120 X 110

140 X 120

150 X 130

170 X 140

190 X 150

200 X 170

FIG. 17. Composite photomicrographs of larval Laevicardium mortoni. Age indays: A. 1
(about 90 u). В. 7 (о 1151). С. 7 (120-140 u). D. 7 (135-155 u). E. 7 (160-180 u). Е. 10
(to 200 u). Length x height dimensions are given in р under the individual larvae to the right.
These larvae are arranged with anterior end right.

160 y, becoming knobby and conspicuous through September.

at about 200 u. Ends of nearly equal Comparison to Other Species: Com-

length; anterior much more pointed than pared under Mytilus edulis.

osterior. ‹ мн

° Other Characters: Color not distinc- ВЕ

tive. Eyespot present from 200 u. Literature: Unidentified sp. (Rees,
Distribution: Adults abundant at sa- 1950); Aequipecten (Pecten) irradians

linities above 5%. Spawning from June Lamarck (Risser, 1901; Belding, 1910;

IDENTIFICATION OF BIVALVE LARVAE 83

FIG. 18. Hinge structure of larval Laevicardium mortoni. Internal view showing ligament at
the posterior (upper) end of otherwise undifferentiated hinge line. Valves are 170 u long.

100 u

FIG. 19. Schematic diagram of the internal anatomy of larval Laevicardium mortoni. See cap-
tion of Fig. 7 for key.

84 CHANLEY AND ANDREWS

260 X 225

FIG. 20. Composite photomicrographs of larval Mercenaria mercenaria. Age in days: A. 2.
В. 3. С. 11. D. 6 (different brood). E. 11. Е. 16. Length x height dimensions are given in u
under the individual larvae to the right. These larvae are arranged with anterior end left.

Wells, 1927; Gutsell, 1930; Costello (Pecten grandis Solander)(Stafford, 1912;
et al., 1957; Loosanoff & Davis, 1963; Posgay, 1950; Merrill, 1961; Bourne,
Sastry, 1965; Loosanoff etal., 1966); 1964).

Lima sp. (Lebour, 1937; Rees, 1950); : у
Pecten opercularis (L.) (Fullarton, 1890; ns gern ua a Lo
Jorgensen, 1946); P. (Chlamys) striatus (Figs. 11, 12, 13)

(Müller) (Jorgensen, 1946; Rees, 1950); Dimensions: Total length 85-200 y.
P. septemradiatus Müller (Jorgensen, Height 10-20 y less than length (usually
1946); P. tenuicostatus Mighels (Drew, 15 y). Depth 50-70 y less than length.
1906); P. tigrinum Muller (Jérgensen, Hinge line about 60 y. Metamorphosis
1946); Placopecten magellanicus Gmelin from 175 to 200 y.

IDENTIFICATION OF BIVALVE LARVAE 85

FIG. 21. Hinge structure of larval Mercenaria mercenaria 180 u long.

ligament. Posterior end is left.

Shape: Low, rounded, poorly-defined
umbo appearing at about 125 и; remain-
ing inconspicuous throughout develop-
ment. Anterior end more pointed and
longer than posterior. Larvae triangu-
lar with anterior end apex of triangle.

Hinge: Toothed area 10-15 » long
with 3 taxodont teeth at each end of
hinge line. Central hinge area (about
35 y long) undifferentiated.

Other Characters: Pale, fragile. In-
conspicuous eyespot developing at 150-
180 u.

Distribution: Rare and only in sea-
side bays of Virginia. Spawning spring
and summer.

Comparison to Other Species: Pointed
anterior end, indistinct umbo and pale
appearance are distinctive.

Family Anomiidae

Literature: Anomia aculeata Müller
(Stafford, 1912; Sullivan, 1948);A. lisch-

Interior view showing

kei Dautzenberg & Fischer (Miyazaki,
1935); A. patelliformis L. (Jgrgensen,
1946); A. simplex (ephippium) (D'Orbig-
ny) (Odhner, 1914; Rees, 1950; Loosan-
off, 1961; Loosanoff & Davis, 1963;
Loosanoff etal., 1966). A. squamula
L. (Lebour, 1938; Jorgensen, 1946; Rees,
1950). Monia squama (Gmelin) (Rees,
1950).

Anomia simplex D’Orbigny

Dimensions: Total length 60-215 u.
Height from 15 y less (in small larvae)
to 10 y more than length (in large lar-
vae). Hinge line about 50 y. Metamor-
phosis at 180-215 u.

Shape: Inequivalve. Right valve al-
most flat with poorly developed umbo.
Umbo round in left valve from 90 to
110 р; becoming prominent knobby pro-
jection in larger larvae. Ends nearly
symmetrical. Irregularity (byssal notch)
frequently on antero-ventral margin of

86 CHANLEY AND ANDREWS

FIG. 22. Composite photomicrographs of lar-
valGemma gemma. A. Young larvae stripped
from adult. Length 245-270 u. B. Larvae
recently released from adult. Length 310-
340 и. С. Still larger larvae that were
stripped from adult. Length 360-390 y.

®

Hinge structure of larval Gemma
Interior view of open valves.

FIG. 23.

gemma.

larvae above 180 u.

Other Characters: Pale and fragile.
Eyespot sometimes appearing at 115 y;
usually present at 180 u.

Distribution: Adults common at sa-
linities above 10%. Spawning season
late summer and early fall in Virginia.

Comparison to Other Species: Early
straight-hinge larvae similar to Cras-
sostrea virginica, Mulinia lateralis and
pholads. Anomia simplex and C. vir-
ginica are the only bivalve in Virginia
with inequivalve larvae. Pale color,
unskewed knobby umbo, length-height
relationship and byssal notchdistinguish
larvae of A. simplex.

Family Ostreidae

Literature: General (Bernard, 1898;
Borisiak, 1909; Boury, 1928; Davaine,
1853; Hori & Kusakabe, 1926; Huxley,
1883; Ranson, 1948; 1951; 1960; Voisin,
1931); Crassostrea angulata (Lamarck)
(Amemiya, 1926); C. commercialis (Ire-
dale & Roughley) (Roughley, 1933); C.
gigas Thunberg (Cahn, 1950; Davis, 1950;
Fujita, 1934; Hori, 1926; Imai & Hata-
naka, 1949; Imai et al., 1950b; Loosan-
off & Davis, 1963; Loosanoff et al.,
1966; Seki, 1938); C. rhizophorae (Guild-
ing) (Galtsoff, 1964); C. virginica Gmel-
in (Amemiya, 1926; Belding, 1909; 1912;
Brooks, 1880; 1905; Carriker, 1951;
Costello et al., 1957; Davis, 1950; Galts-

IDENTIFICATION OF BIVALVE LARVAE 87

FIG. 24. Composite photomicrographs of larval Petricola pholadiformis.

ETC. AO D. 12. Е. 14,
vidual larvae to the right.

Зо 1155

off, 1964; Imai et al., 19506; Jackson,
1888; Loosanoff & Davis, 1963; Loosan-
off et al., 1966; Medcof, 1939; Menzel,
1954; 1955; Needler, 1924; 1941; New-
combe, 1946; Prytherch, 1924; 1934;
Ryder, 1883; Stafford, 1909; 1912; 1913;
1914; Stenzel, 1964; Sullivan, 1948;
Wells, 1920a; 1920b; 1927); Ostrea den-
selamellosa Lischke (Cahn, 1950, Seki,
1930; Seno, 1929); O. edulis L. (Ame-
Miya, 1926; Cole, 1937; 1938; 1939;

105 X 90

120 X 100

200u 175 X 155

F

Age in days: A. 2.

Length x height dimensions are given in u under the indi-
These larvae are arranged with anterior end right.

Danton, 1917; Erdmann, 1935; Galts-
off, 1964; Hagmeier, 1916; 1931; Horst,
1882; 1883; Imai, Sakai & Okada, 1952;
Jackson, 1888; Korringa, 1941; Loosa-
noff & Davis, 1963; Loosanoff et al.,
1966; Mazzarelli, 1923; Walne, 1956;
Yonge, 1926; 1960); O. equestris Say
(Menzel, 1954; 1955); O. frons L. (Men-
zel, 1954; 1955); О. lurida Carpenter
(Davis, 1949; Galtsoff, 1964; Hopkins,
1937; Hori, 1933; Imai etal., 1954;

88 CHANLEY AND ANDREWS

FIG. 25. Hinge structure of larval Petricola
pholadifovmis. Dorsal view of larval valves
170 u long showing ligament. Anterior end
is right.

Loosanoff & Davis, 1963; Loosanoff et
al., 1966); О. lutaria Hutton (Hollis,
1963); O. taurica Krynicky (Borisiak,
1909; Zakhvatkina, 1959); Pycnodonta
hyotis (L.) (Galtsoff, 1964).

Crassostrea virginica Gmelin
(Figs. 14, 15, 16)

Dimensions: Total length 60-350 u.
Height 10 y less, increasing to equal
at 90-100 р; eventually exceeding length
by as much as 15y. Depth 35-40 u
less than length; increasing to 100 u
less than length in late stages. Hinge
line usually 45-50 u. Metamorphosis
from 310 to 350 u.

Shape: Inequivalve. Umbolessdevel-

® Ar

- 100 X 85

®
НО X 95

FIG. 26. Composite photomicrographs of larval Tellina agilis. Age in days: A. 1. B. 4. C. 7.
Length x height dimensions are given in u under the individual larvae to

D. 10. E. 12. F. 15.
the right. These larvae are arranged with anterior end right.

| FIG. 28.

IDENTIFICATION OF BIVALVE LARVAE 89

EIG. 27.
agilis.
of valves 110 u long.
valves about 130 u long.
D. Valves 250 u long

Hinge structure of larval Tellina
Anterior is right. A. Internal view
B. Dorsal view of

C. Dorsal view of
valves 195 u long.
showing ligament.

oped in right valve; round at 80-100 u;
knobby at 85-125 и; skewed and posteri-
orly directed above 125 y. Anterior end
longer, more pointed than posterior.
Posterior shoulder more curved than
anterior.

Hinge: 2 hinge teeth 8 u wide at
each end of hinge line.

Other Characters: Dark and heavy.
Eyespot appearing at about 260 u.

Distribution: Adults abundant at sa-
linities above 5%. Spawning from late
May to November.

Comparison to Other Species:
comparison under Anomia simplex.

Family Cardiidae

See

Literature: Tentative identifications
(Rees, 1950); Laevicardium (Cardium)
crassium (Gmelin) (Lebour, 1938; New-
ell & Newell, 1963); Cardium echinutum
L. (Lebour, 1938; Newell & Newell,
1963); C. edule L. (Lebour, 1938; Jgr-
gensen, 1946; Newell & Newell, 1963);
C. exiguum (pygmeum) Gmelin (Loven,
1848; Jgrgensen, 1946); C. minimum
Reeve (Jgrgensen, 1946); C. ovale (fas-
ciatum) Sowerby (Jgrgensen, 1946; New-
ell & Newell, 1963); С. scabrum Phil-

ZEN
= SR \ A

Schematic diagram of the development of the internal anatomy of larval Tellina agilis.
See caption of Fig. 7 for key.

90 CHANLEY AND ANDREWS

we

HO
ade €

С

ЕТС. 29.

Composite photomicrographs of larval Donax variabilis.

Age in days: A. 2. -B. 8

С. 12. D. 19. E. 19. Е. 22. Length x height dimensions are given in y under the individual
larvae to the right. These larvae are arranged with anterior end left.

ippi (Newell & Newell, 1963); Fulvia
mutica (Reeve) (Yoshida, 1953); Laevi-
cardium mortoni (Conrad) (Loosanoff
& Davis, 1963; Loosanoff et al., 1966).

Laevicardium mortoni Conrad
(Figs. 17, 18, 19)

Dimensions: Total length 80-245 u.
Height 10-20, less in straight-hinge
larvae; up to 45 y less than length in
umbonate larvae. Hinge line 60-65 u

long. Metamorphosis from 205 to 245 y
(usually 210-230 u).

Shape: Round umbos developing at
about 120 y; becoming broadly rounded
at about 150 u. Anterior end longer,
more pointed than posterior. Anterior
shoulder longer than posterior.

Hinge: Undifferentiated except for
irregularity at posterior end near liga-
ment.

Other Characters: Color not dis-

IDENTIFICATION OF BIVALVE LARVAE 91

EIG. 30.
variabilis. Anterior end is up. A. Dorsal
view of valves 85 u long. B. Internal view of
valves 97 u long. C. Internal view of valves
140 u long. D. Internal view of valves 275 u
long.

Hinge structure of larval Donax

tinctive. Apical flagellum conspicuous.
No eyespot.

Distribution: Adults commoninChes-
apeake Bay and its tributaries where
salinity is above 10%. Spawning season
probably in early summer.

Comparison to Other Species: Early
stages are similar to several species.
Long anterior end and comparatively
great difference between length and
height distinguish later stages. Tellina
_ agilis larvae also with long anterior
_ end but with knobby umbos and darker
| color.

Family Veneridae

Literature: Seven species tentatively
| identified (Rees, 1950); Gemma gemma
| Totten (Sullivan, 1948); Gouldia minima

(Montagu) (Nikitin & Turpaeva, 1957);
Mercenaria campechiensis Gmelin (Loo-
sanoff & Davis, 1963; Loosanoff et al.,
1966); M. mercenaria L. (Stafford, 1912;
Belding, 1912; 1931; Sullivan, 1948; Loo-
sanoff & Davis, 1950; 1963; Carriker,
1956; 1961; Costello et al., 1957; Loosan-
off, 1959; Loosanoff et al., 1966); Mere-
trix lusoria Hamaguri (Yoshida, 1953);
M. meretrix L. (Yoshida, 1941); M
yudis (Вой) (Nikitin € Turpaeva, 1957;
Zakhvatkina, 1959); Pitar morrhuana
Linsley (Sullivan, 1948; Costello et al.,
1957; Loosanoff & Davis, 1963; Loosan-
off et al., 1966); Paphia staminea Conrad
(Fraser, 1929); Saxidomus giganteus
Deshayes (Fraser, 1929); Tapes procli-
vis Milaschewitsch (Nikitin & Turpaeva,
1957); T. semidecussata Reeve (also
known as Paphia philippinorum and Ve-
nerupis philippinorum) (Miyazaki, 1934;
1935; 1936; Yoshida, 1935; Cahn, 1951;
Loosanoff & Davis, 1963; Loosanoff et
al., 1966); variegata Sowerby (Yo-
shida, 1960); Venerupis pullastra (Mon-
tagu) (Quayle, 1952); Venus gallina L.
(Jgrgensen, 1946; Nikitin & Turpaeva,
1957; Zakhvatkina, 1959); V. ovata Pen-
nant (Jgrgensen, 1946): V. striatula (Da
Costa) (Ansell, 1962).

Mercenaria mercenaria L.
(Figs. 20, 21)

Dimensions: Total length 100-235 y.
Height 10-30 y less; usually 20-25 u
less than length but frequently only 15 y
less near metamorphosis. Depth usual-
ly 60-65 » less than length. Hinge line
70-80 y. Metamorphosis from 175 to
235 и, but usually 210-225 y.

Shape: Broadly rounded umbos devel-
oping at about 150 u. Anterior end
slightly more pointed than posterior.
Ends of nearly equal length. Anterior
shoulder longer than posterior.

Hinge: One small anterior tooth in
each valve; large posterior ligament.

Other Characters: Color not distinc-

tive. Conspicuous apical flagellum.
No eyespot.
Distribution: Adults abundant where

salinity is above 15%. Spawning pri-

92 CHANLEY AND ANDREWS

100 u

FIG. 31.
bilis. See caption of Fig. 7 for key.

marily in June and July but continuing
until November.

Comparison to Other Species: The
long hinge line with resulting late umbo
development is usually distinctive. Ear-
ly larvae have proportionately greater
height than mytilids. Mytilid umbos

are not broadly rounded.

Gemma gemma Totten
(Figs. 22, 23,)

Dimensions:
Height 40-80 y less than length.

Shape:

Oval.

Total length 245-390 u.

No distinct straight-

Schematic diagram of the development of the internal anatomy in larval Donax varia-

AAA HA O a

IDENTIFICATION OF BIVALVE LARVAE 93

FIG. 32. Composite photomicrographs of larval Ensis directus.
Length x height dimensions are given in u under the individual larvae
These larvae are arranged with anterior end left.

BED. 10:
to the right.

№. 17. Е 5.

hinge ог umbo Stage.

Other Characters: Dark, opaque, non-
pelagic. Larval development entirely
internal. Released as juvenile 340-
390 u long.

Distribution: Common where salinity
is above 10% .in Chesapeake Bay and
its tributaries.

Comparison to Other Species: Simi-
lar to larval Pandoracea but much lar-

105 X 85

120 X 10C€

145 X 115

160 X135

200х165

240x200

Age in days: A. 2. В. 4. С.

ger and non-pelagic.
Pitar morrhuana Linsley

Dimensions: Total length 70-185 u.
Height 10-20 y (usually 15 y) less than
length. Hinge line 55-65 м. Meta-
morphosis from 165 to 185 u.

Shape: Umbos round at 110 y, be-
coming broadly rounded about 145 u.
Ends nearly symmetrical. Shoulders

94 CHANLEY AND ANDREWS

>»
u
y
=
Я
e

À
=
$

RY

à
y Y

FIG. 33. Hinge structure of larval Ensis
directus. Dorsal view of valves 235 u long
with anterior end at bottom.

rounded.
Other Characters: Color not distinc-

tive. Apical flagellum present. No
eyespot.

Distribution: Rare in seaside bays
of Virginia.

Comparison to Other Species: Hinge
line is shorter and umbos develop at
smaller size than in larval Mercenaria
mercenaria. Ends are nearly equal in
length while in Laevicardium mortoni
anterior end is longer than posterior.
Shoulders slope less steeply than in
Petricola pholadiformis.

Family Petricolidae

Literature: Petricola lithophaga (Ret-
zium) (Zakhvatkina, 1959); P. pholadi-

formis Lamarck (Sullivan, 1948; Rees,
1950; Loosanoff & Davis, 1963; Loosan-
off et al., 1966).

Petricola pholadiformis Lamarck
(Figs. 24, 25)

Dimensions: Total length 60-185 u.
Height 5-10 y less in earliest stages.
Usually 15 y less than length below
150 y and 20 y (maximum 25) less in
larvae. Depth 45-70 y less than length.
Hinge line 50-60 u. Metamorphosis
from 165 to 185 u.

Shape: Broadly rounded umbos de-
veloping at about 110 y. Anterior end
slightly longer than posterior; ends
nearly equally rounded. Shoulders
straight and sloping steeply.

Hinge: Hinge line undifferentiated
except for broad depression in right
valve above hinge line near anterior
end and slight irregularity at posterior
end of hinge line. Ligament appears
slightly posterior to center of hinge
line when larvae are about 170 y long.

Other Characters: Color not dis-
tinctive. Shell heavier than in most
clam larvae; margin dark. No pig-
mented eyespot.

Distribution: Adults common where
salinity is above 10%. Spawning April
through September.

Comparison to Other Species: Early
straight-hinge P. pholadiformis larvae
are similar to many other species.
Distinguishing characters of later stages
include length of hinge line, heavy shell,
steep slope of shoulders, length-height
relationship and small size at meta-
morphosis.

Family Tellinidae

Literature: Gastrana fragilis (Linné)
(Zakhvatkina, 1959); Macoma balthicaL.
(Werner, 1939; Jgrgensen, 1946; Sul-
livan, 1948); M. calcarea (Chemnitz)
(Thorson, 1936); Tellina balaustria L.
(Odhner, 1914); T. crassa Pennant (New-
ell & Newell, 1963); T. donacina L.
(Zakhvatkina, 1959); T. fabula Gronov
(Zakhvatkina, 1959; Newell & Newell,
1963); Т. agilis (tenera) Stimpson (Sul-

FO ИИ

IDENTIFICATION OF BIVALVE LARVAE 95

FIG. 34. Schematic diagram of the development of the internal anatomy of larval Ensis directus
(from Loosanoff et al., 1966). See caption of Fig. 7 for key.

livan, 1948); T. juvenalis Hanley (Miya-
zaki, 1938); Tellina sp. (Loven, 1848;
Borisiak, 1909; Rees, 1950).

Tellina agilis Stimpson
(Figs. 26, 27, 28)

Dimensions: Total length 75-250 u.
Height 10-15 р less in straight-hinge
stages to as much as 30 u less than
length at metamorphosis. Depth 30-90 u
less than length. Hinge line 45-50 u.
Metamorphosis from 200 to 250 u.

Shape: Umbos round from 90 to 135 u
but knobby in larger larvae. Anterior
end longer than posterior. Shoulders
long and slope steeply. Shoulders and
umbos comprising over 1/2 total height.

Hinge: Numerous minute irregular

teeth extend over the entire hinge line.

Other Characters: Heavy larvae with
faint purple or rose color in umbos.
Dark shell margins. At least one con-
Spicuous apical flagellum. No pigmented
eyespot.

Distribution: Common where Salinity
is above 10%. Spawning season begin-
ning in April or May but its duration
unknown.

Comparison to Other Species: Rela-
tive height of shoulders and umbos is
distinctive. Color resembles pholads
but length-height relationship and long
anterior end are distinctive. Laevicar-
dium mortoni has long anterior end but
with proportionately greater length,
broadly rounded umbo and no distinctive

96 CHANLEY AND ANDREWS

“FIG. 35. Composite photomicrographs of larval Spisula solidissima. Age in days: A. 1.
ОН iss

C. 19. D. 10. (different brood).
under the individual larvae to the right.
color.

Family Donacidae

Literature: Donax vittatus (Da Costa)
(Rees, 1950); D. venustus Poli (Zakhvat-
kina, 1959).

Donax variabilis Say
(Figs. 29, 30, 31)

Dimensions: Total length 70-340 u.
Height usually 15-20 „ less in straight-

270 X 245

B. 12.
Length x height dimensions are given in u

hinge larvae; 25-35 » less than length
in umbo stages; to 50 u less at meta-
morphosis. Depth 40-60 less "than
length, increasing to 170 y less at meta-
morphosis. Hinge line 50-60 y. Meta-
morphosis 275-340 u.

Shape: Umbos round from 100 to
120 u; broadly rounded 120-200 u; knobby
over 170 u. Ends equally rounded below
250 u; posterior more pointed in larger
larvae. Anterior end longer than poste-

IDENTIFICATION OF BIVALVE LARVAE 97

FIG. 36. Hinge structure of larval Spisula
solidissima. Anterior end is left. A. Dor-
sal view of separated valves 215 u long. B.
Interior view of opened valves 260 u long.
Ligament visible in right (lower) valve near
posterior end of hinge line.

rior. Ventral margin well rounded,
forming semicircle with ends.

Hinge: Irregularly shaped teeth over
entire hinge length.

Other Characters: Color not dis-
tinctive. Apical flagellum present (2
in large larvae). No pigmented eyespot.

Distribution: Adults with mature ga-
metes common on ocean beaches in
Virginia from July to November.

Comparison to Other Species: Low
umbo and gradually sloping shoulders
are distinctive. Dentition is similar to
Tellina agilis but large teeth are more
numerous and evenly distributed.

Family Solenidae

Literature: Cultellus pellucidus (Pen-
nant) (Kändler, 1926; Lebour, 1938; Jor-
gensen, 1946; Rees, 1950; Newell &
Newell, 1963); Ensis directus (Conrad)
(Sullivan, 1948; Costello et al., 1957;
Loosanoff & Davis, 1963; Loosanoff et
al., 1966); E.ensis (L.) (Rees, 1950;
Newell & Newell, 1963); E. siliqua (L.)
(Lebour, 1938; Rees, 1950; Newell &
Newell, 1963); Solen gouldi Conrad (Yo-
shida, 1939; 1953).

Ensis directus (Conrad)
Figs. 32, 33, 34)

Dimensions: Total length 85-270 u.
Height 10-15 y less in straight-hinge

100 u

FIG. 37. Schematic diagram of the development of the internal anatomy of larval Spisula

solidissima. See caption of Fig. 7 for key.

98 CHANLEY AND ANDREWS

FIG. 38. Composite photomicrographs of larval Mulinia lateralis.
D. Lengths 135-175 u.

Lengths 85-100 u. С. Lengths 90-120 u.
stage; 15-20 u less in early umbo and
25-40 y less than length in late umbo
stages. Depth 55-130 y less than length.
Hinge line 70-75 u. Metamorphosis
from 220 to 270 u.

Shape: Umbos variable inappearance,
never projecting prominently; usually
rounded from 135 to 195 y; broadly
rounded or angular above 200 u. Ends
of equal length; anterior more pointed
than posterior. Anterior shoulder longer
than posterior.

CA

175х160

240х225

A. Lengths 65-75 и. В.
Е. Lengths 159-195 u.

Hinge: Small tooth at each end of

hinge line in right valve. Anterior
tooth directed posteriorly; posterior
tooth laterally.
Other Characters: Color not distinc-
tive. Apical flagellum present. Small
indistinct pigmented eyespot sometimes
visible above 185 u.

Distribution: Adults common where
salinity is above 10% , spawning March
to mid-June.

Comparison to Other Species: Long

IDENTIFICATION OF BIVALVE LARVAE 99

FIG. 39. Hinge structure of larval Mulinia
lateralis. Ventral views with anterior end
right. Upper valves are 190 y long with no
ligament. Lower valves are 215 y long and
have a faint ligament near the posterior end
of the hinge line.

hinge line is similar to Mercenaria
mercenaria but umbo not as high or
broad. Shoulders slope more gradually.
Spisula solidissima larvae have shorter
hinge line, proportionately greater
height, longer anterior end and lack
hinge teeth.

Family Mactridae

Literature: Lutraria lutraria (L.)
(Rees, 1950); Mactra corallina (Mon-
tagu) (Rees, 1950; Newell & Newell,
1963); M. sachalinensis Schrenk (Kino-
shita & Hirano, 1934; Imai et al., 1953);
M. sulcatoria Reeve (Miyazaki, 1936);
M. veneriformis Reeve (Miyazaki, 1936);
Mactra sp. (Lovén, 1848); Mulinia late -
yalis Say (Sullivan, 1948; Loosanoff et

al., 1966); Rangia cuneata Gray (Fair-
banks, 1963; Chanley, 1965b); Spisula
elliptica (Brown) (Rees, 1950; Newell
& Newell, 1963); S. solidissima (Dill-
wyn) (Sullivan, 1948; Rees, 1950; Loo-
sanoff, 1954; Costello et al., 1957; New-
ell & Newell, 1963; Loosanoff & Davis,
1963; Loosanoff et al., 1966); S. subtrun-
cata (da Costa) (Kändler, 1926; Jorgen-
sen, 1946; Rees, 1950; Nikitin & Tur-
paeva, 1957; Zakhvatkina, 1959).

Spisula solidissima (Dillwyn)
(№523. 35: 36,37)

Dimensions: Total length 80-275 u.
Height usually 15-20 u less but up to
25 » less than length in large larvae.
Depth increasing from 55 u less than
length to 115 y less at metamorphosis.
Hinge line 55-60 и. Metamorphosis at
220-275 u.

Shape: Round umbos appearing at
110 y, never high, broadly rounded after
135 и. Anterior end longer and more
pointed than posterior. Shoulders round-
ed, sloping gradually. Anterior longer
than posterior.

Hinge: Undifferentiated except faint
suggestion of single tooth at either end
of hinge line. At metamorphosis a
large tooth develops internally anterior
to the hinge line in the left valve and a
posterior ligament develops.

Other Characters: Color not distinc-
tive. No pigmented eyespot. Con-
Spicuous apical flagellum.

Distribution: Adults common in o-
ceanic water and near barrier islands.
Spawning April through early June, pos-
sibly again in fall.

Comparison to Other Species: Com-
pared under Ensis directus.

Mulinia lateralis Say
(Figs. 38, 39)

Dimensions: Total length 60-240 y.
Height usually 10 y (5-15 „) less below
175 и and 15-20 y less than length at
later stages. Depth from 35 to 100 u
less than length. Hinge line usually

100 CHANLEY AND ANDREWS

96 x 88 ,

119 X 106 ®

à.

y
Er
RK
An
e >

153X138

И"? . +

от

176 X160 ME

A hy oo

FIG. 40. Composite photomicrographs of larval Rangia cuneata. Age in days: A. 1. B. 4.

©. 6: D. 7.

40-45 y; may reach 50 y. Metamorpho-
sis from 185 to 240 y.

Shape: Rounded umbos at 80-100 u;
becoming higher and angular at 130-
160 y; knobby at lengths over 200 u.
Anterior end longer, slightly more point-
ed than posterior. Shoulders almost
straight; sloping steeply in well umboed
larvae.

Hinge: Undifferentiated except for
faint irregularity at either end of hinge.
Posterior ligament appears at about
200 u.

Other Characters: Usually slightly
pale or light. No apical flagellum or
pigmented eyespot.

Distribution: Adults common where
salinity is above 8% in Chesapeake
Bay and its tributaries, scarce on sea-
side. Spawning April to November.

Comparison to Other Species: Early
straight-hinge stage is similar to Cras-
sostrea virginica, Anomia simplex and

Length x height dimensions are given in u under the individual larvae to the right.
These larvae are arranged with anterior end right.

pholads. Short hinge line, pale color,
and proportionately great height are
distinctive. See comparison under Ran-
gia cuneata.

Rangia cuneata Gray
(Figs. 40, 41, 42)

Dimensions: Total length 75-175 u.
Height usually 10 u less (ranging from
5 to 20 y). Depth increasing from 45
to 65 u less than length. Hinge line
55-65 » long. Metamorphosjs from 160
to 175.

Shape: Round low inconspicuous um-
bos developing at lengths of 120-130 u.
Ends equally rounded. Anterior end
and shoulder longer than posterior.
Shoulder rounded.

Hinge: Undifferentiated.
forming at metamorphosis.

Other Characters: Color not distinc-
tive. No pigmented eyespot. Apical
flagellum present.

Ligament

IDENTIFICATION OF BIVALVE LARVAE 101

FIG. 41. Hinge structure of larval Rangia
cuneata. Ventral views with anterior end
right. Upper valves are 140 u long with no

ligament. Lower valves are 170 u long and
have a faint ligament near the posterior end
of the hinge line.

Distribution: Usually present where
Salinity is below 10% in Back Bay,
James and Rappahannockrivers. Spawn-
ing season probably April to September.

Comparison to Other Species: Com-
paratively great height distinguishes
species from most clam larvae. The
longer hinge line, low rounded umbo,
round shoulders and darker texture dis-
tinguish it from Mulinia lateralis.

Family Myacidae

Literature: Mya arenaria L. (Kellogg,
1901; Stafford, 1912; Belding, 1916;
1930; J¢grgensen, 1946; Sullivan, 1948;
Costello et al., 1957; Loosanoff & Davis,
1963; Loosanoff et al., 1966); M. are-

naria japonica Jay (Yoshida, 1938; 1953);
M. truncata L. (Jgrgensen, 1946; Rees,
1950).

Mya arenaria L.

Dimensions: Total length 85-230 u.
Height usually 15u less (increasing
from 10 to 25 y less than length). Hinge
line 55-60 u long. Metamorphosis from
175 to 230 u.

Shape: Round umbos appear at 115-
120 u; becoming angular above 160 u.
Anterior end longer, more pointed than
posterior. Shoulders rounded; becoming
straight in late stages.

Other Characters: Irregular opaque
spots frequent around margin. Liver
dark brown (dependent to some degree
on food). Color not otherwise distinc-
tive. Apical flagellum present. No
pigmented eyespot.

Distribution: Common in Chesapeake
Bay and tributaries where salinity is
above 5%; scarce in seaside bays.
Spawning season September to Decem-
ber. Possibly minor spawning May and
June.

Comparison to Other Species: Early
umbo larvae are Similar to several
other species. Later, umbos are more
rounded and narrower than in Petricola
pholadiformis and Pitar morrhuana.
Shoulders slope more steeply than Ensis
directus but less steeply than Mulinia
lateralis. Height is proportionately
greater than in Laevicardium mortoni.
Late spawning season is useful in iden-
tification.

Family Pholadidae

Literature: Barnea candida (L.) (Bou-
chard-Chantereaux, 1869; Jgrgensen,
1946; Zakhvatkina, 1959); B. parva (Bonn)
(Lebour, 1938); B. truncata Say (Siger-
foos, 1895; Chanley, 1965a); Parapholas
quadrizonata Spenger (Miyazaki, 1936);
Pholadidea loscombiana Turton (Lebour,
1938); Pholas sp. (Kindler, 1926); P.
dactylus (L.) (Zakhvatkina, 1959); Zir-
faea crispata (L.) (Werner, 1939; Jgr-

102 CHANLEY AND ANDREWS

RANGIA

CUNEATA

100 4

FIG. 42. Schematic diagram of the development of the internal anatomy of larval Rangia cuneata.

See caption of Fig. 7 for key.

gensen, 1946; Sullivan, 1948; Rees, 1950).

Barnea truncata Say
(Figs. 43, 44, 45)

Dimensions: Total length 55-315 u.
Height usually 5-10 u less (0-10 u in
straight-hinge stages; 0-20 и in umbo
larvae). Depth increasing from 20 u
less than length to 80 y less at meta-
morphosis. Hinge line usually 45 u.
Metamorphosis from 250 to 315 y (usu-
ally 270-285 u).

Shape: Umbo first appearing rounded
at 85-95 и; rapidly developing to nipple-
shaped knob projecting above circular
larva. Ends equal; broadly rounded.
Shoulders short, rounded, steeply slop-
ing; anterior slightly longer than poste-
rior.

Hinge: 2 teeth in left valve (5-10 u
wide) fitted at either end of long (20-
25 » wide) central tooth on right valve.
Second tooth (5-10 » wide) on right valve
just anterior to gap for anterior tooth
of left valve. Small posterior tooth

developing in right valve just before
metamorphosis. May be developing
apophysis.

Other Characters: Dark with heavy
dark band around margin of shell; pal-
lial line forming interior margin of
band. In empty valves over 150 u long
adductor muscle scars conspicuously
interrupt pallial line. Pink or purple
color in shell umbos and anterior shoul-
ders (also on ventral margin in late
umbo larvae). Gut frequently outlining
clear circular area in umbo region.
No apical flagellum or pigmented eye-
spot.

Distribution? Common where salinity
is above 10%. Probably spawning May
through September.

Comparison to Other Species: Early
straight-hinge larvae are similar to
Crassostrea virginica and other species
with short hinge lines. They rapidly
develop an angular hinge-shoulder tran-
sition that is distinctly pholad. Dark
heavy appearance and pink umbo are

IDENTIFICATION OF BIVALVE LARVAE 103

FIG. 43. Composite photomicrographs of larval Barnea truncata.

ey

120 X 110

®

140 X 130

280 X 275

Age in days: A. 1. В. 7.

C. 19 with velum extended. D. 22. E. 28 with velum extended. F. 35. Length x height dimen-
sions are given in y under the individual larvae to the right. These larvae are arranged with

anterior end to the right.

distinctive. Tellina agilis has longer
Shoulders. C. virginica is inequivalve
with skewed umbo. Height is greater
than width above 140 y in Teredo naval-
is and margin is darker. Cyrtopleura
costata is generally paler and rounder
with slightly smaller hinge line and

hinge teeth. Individual larvae of these
2 species are usually indistinguishable.

Cyrtopleura costata (L.)
(Figs. 46, 47, 48)

Dimensions: Total length 60-330 u.
Height usually 5-10 y less but from 0

104 CHANLEY AND ANDREWS

FIG. 44. Hinge structure of larval Barnea truncata. Anterior end is up. A, B, C. Dorsal
view of valves 85 y, 160 u and 290 u long. D, E, Е. Open valves 80 u, 130 y and 290 y long.

‚ dark band around margin of shell.
‚ ог purple color in shell on umbos, ante-

IDENTIFICATION OF BIVALVE LARVAE

105

BARNEA TRUNCATA

FIG. 45. Schematic diagram of the development of the internal anatomy of larval Barnea truncata.

See caption of Fig. 7 for key.

to 15 u less in large larvae. Depth
30-70 u less than length. Hinge line
usually 40 u (35-40 x). Pediveligers
from 215 to 330 u. Metamorphosis
usually at about 300 u.

Shape: Circular. Umbos first ap-
pearing at 80 y, becoming rounded nip-
ple-like knobs. Ends equally rounded
but anterior slightly longer than poste-
rior in large larvae. Shoulders rounded
and sloping steeply; anterior slightly
longer than posterior.

Hinge: 2 teeth (anterior 8 и wide,
posterior 5 y wide) on left valve fit at

‚ either end of broad (18 y wide) central

tooth on right valve. Anterior tooth

(5 y wide) on right valve anterior to gap
for anterior tooth of the left valve.

Other Characters: Dark with heavy

Pink

rior shoulder and ventral margin of late
umbo larvae. Gut frequently outlining

clear circular area in umbo. No apical
flagellum or pigmented eyespot. Pedi-
veliger frequently with 1 or 2 gill loops
and excurrent siphon.

Distribution: Common where Salinity
is above 10%. Spawning May through
September.

Comparison to Other Species:
comparison under Barnea truncata.

See

Family Teredinidae

Literature: Bankia anechoensis Roch
(Rancurel, 1965); B. gouldi Bartsch (Nel-
son, 1924); B. indica Nair (Nair, 1956);
B. setacea Tryon (Quayle, 1953; 1956;
Townsley, Richy, Trussell, 1966); Te-
vedo bartschi Clapp (Lane, Tierney &
Hennacy, 1954); Teredo sp. (de Quatre-
fages, 1849; Borisiak, 1909; Lebour,
1938; Rees, 1950); T. japonica Clessin
(Miyazaki, 1935); T. megotara Hanley
(Jg@rgensen, 1946); T. navalis L. (Hat-
scheck, 1881; Sigerfoos, 1908; Grave,

106 CHANLEY AND ANDREWS

FIG. 46. Composite photomicrographs of larval Cyrtopleura costata.

Co 17. Ds 25.

1928; Nelson, 1924; Jgrgensen, 1946;
Sullivan, 1948; Imai et al., 1950a; Lane,
1955; 1961; Costello ef al., 1957; Za-
khvatkina, 1959; Loosanoff € Davis,
1963; Loosanoff et al., 1966); T. norwe-
gica Spengler (Lebour, 1938); T. (Lyro-
dus) pedicellata de Quatrefages (Isham
& Tierney, 1953); T. thomsoni Tryon
(Rancurel, 1965).

Тетеао navalis L.

Dimensions: Minimum length at re-
lease from parent 70-90 y. Maximum
length over 200 y, Height 10-15 y less
than length in early straight-hinge lar-
vae, equal to length at 130-140 y, and
exceeding length in large larvae by as
much as 35y. Depth 35 y less than
length in young larvae; only 15 y less
at metamorphosis. Hinge line 45-50 u.

Age in days: A. 1.
Length x height dimensions are given in y under the individual larvae to the right.
These larvae are arranged with anterior end right.

Metamorphosis at 190 to over 200 u.

Shape: Oval. Maximum diameter,
dorso-ventral after 140 u. Globose.
Rounded umbo obscuring hinge line at
95-100 u. Umbo symmetrical and ra-
pidly becoming knobby. Ends broadly
rounded; symmetrical. Shoulders short,
rounded and sloping steeply.

Other Characters: Dark band around
shell margin with clear band inside.
Thick heavy appearance. Frequently
Opaque when preserved. Short incon-
spicuous apical flagellum present only
in earliest stages. No pigmented eye-
spot.

Distribution: Common where salinity
is above 10%. Larvae present from
June to October (Scheltema & Truitt,
1956).

Comparison to Other Species: Dark

В. 103

IDENTIFICATION OF BIVALVE LARVAE 107

FIG. 47.
pleura costata. Dorsal views of valves with
anterior end left. Length of larval shell:
DTO. В. 145 up. С. 260 p.

Hinge structure of larval Cyrto-

band around shell is more pronounced
than in pholads. This is the only equi-
valve species with height greater than
length.

Family Lyonsidae

Literature: Lyonsia norwegica (Gme-
lin) (Rees, 1950); L. hyalina (Conrad)
(Chanley & Castagna, 1966). Larvae
of a few closely related Pandoridae
have also been described. Pandora
gouldiana (Dall) (Stafford, 1912; Sullivan,

1948); P. inaequivalvis (L.) (Allen, 1961).

Lyonsia hyalina (Conrad)
(Figs. 49, 50, 51)

Dimensions: Total length 155-175 u.
Height 120-130 y. Depth about 85 u.

Shape: Oval with greatest diameter
anterior-posterior. Hinge line indented
in center. No typical straight-hinge or
umbo stage.

Hinge: Undifferentiated except for
U-shaped ligament 15 y long and 11 y
wide.

Other Characters: Dark gray or
black. Opaque. Multiple apical flagella.
No pigmented eyespot.

Distribution: Adults common inChes-
apeake Bay and its tributaries where
salinity is above 10%.

Comparison to Other Species: Re-
sembles only other Pandoracea or Gem-
ma gemma. The latter is not shelled
below 245 y and not pelagic.

DISCUSSION AND CONCLUSIONS

Bivalve larvae are difficult todescribe
and identify because they have relatively
few characteristics that can be quanti-
tatively defined. The problem is fur-
ther compounded by the failure of in-
vestigators to develop a standard ap-
proach to the description of larvae. As
a result, many published descriptions
are incomplete or cannot be compared
to the descriptions of other investiga-
tors.

The authors would like to suggest that
descriptions of laboratory-reared bi-
valve larvae include the following mini-
mal information.

Dimensions - Length, height anddepth
(for straight-hinge, umbo and pediveli-
ger larvae). Also length of the straight-
hinge line. Include ranges and means.

Shape - Umbo (round, broadly round,
angular, knobby, skewed); shoulders
(curved, straight, length, steepness of
slope, anterior compared to posterior);
ends (length, blunt, pointed, anterior

108 CHANLEY AND ANDREWS

FIG. 48. Schematic diagram of the development of the internal anatomy of larval Cyrtopleura
costata. See caption of Fig. 7 for key.

”

FIG. 50. Interior opened valves of larval _
FIG. 49. Larval Lyonsia hyalina. 155-175 u Lyonsia hyalina showing ligament. Length |
long. 1-3 days old. about 160-165 u. About 2 days old.

IDENTIFICATION OF BIVALVE LARVAE 109

100y

LYONSIA HYALINA

FIG. 51. Schematic diagram of the development of the internal anatomy of larvae of Lyonsia

hyalina. See caption of Fig. 7 for key.

compared to posterior); ventral margin
(round, flat, semicircular); relative
height of umbo and shoulders to total
height.

Hinge - Descriptions of teeth and lig-
ament at representative sizes.

Special Characters - Color, byssal
notch, eyespot, apical flagellum, etc.

With such information, it may be pos-
sible to more precisely assess the sys-
tematic position of a species. Although
larval development is presently known
of too few species to permit an analysis
of its significance as a taxonomic aid,
some speculation is possible.

On the basis of the foregoing descrip-
tions, larvae of Lyonsia hyalina differ
so markedly from other larvae that this
species must be widely separated from
the others taxonomically. It is apparent

that larvae of some taxonomic groups
are very similar. For example larval
Arcaceans have a characteristic shape,
color and hinge structure. The simi-
larities between larval Teredinidae and
Pholadidae suggest these families may
be closely related. Hinge similarities
between larvae of Donax variabilis and
Tellina agilis indicate they are related,
although their larvae have little else in
common.

On the other hand, the lecithotrophic
larvae of the venerid Gemma gemma
are more similar to the lecithotrophic
larvae of Lyonsia hyalina than to the
more closely -related planktotrophic lar-
vae of other venerids. This suggests
that influences, other than taxonomic,
are also of importance in determining
larval characters. The view is further

110 CHANLEY AND ANDREWS

supported by Sellmer’s (1967) obser-
vation that small species and species
living in deep or cold water tend to
incubate larvae. Apparently, adult size,
environment and probably other factors
can result in modifications of larval
development that mask taxonomic simi-
larities.

Not until we have more complete
information on larval development in the
bivalves will it be possible to more ac-
curately assess the relationship be-
tween larval development and systema-
tics.

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|

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IDENTIFICATION OF BIVALVE LARVAE 115

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APPENDIX

A GLOSSARY OF THE TERMS USED
TO DESCRIBE BIVALVE LARVAE

Angular - Type of umbo with an almost
pointed apex. Outline is continuous
with straight shoulders.

Anterior end of larva - Usually recogni-
zable by the more gradual slope of
the anterior shoulder from the umbo.
The velum is extended from the ante-
ro-ventral margin of the shell.

Apical flagellum - The long centrally lo-
cated flagellum (or flagella) of the
velum of many species. These fla-
gella are derived from the cilia of
the apex of trochophore larvae.

IDENTIFICATION OF BIVALVE LARVAE 117

Apophysis-An internal finger-shaped
protuberance of the shell.

Broadly rounded - Type of umbo that is
generally round, but somewhat flat-
tened dorsally. The outline is con-
tinuous with the shoulders.

Depth - Maximum distance through the
larva from left valve to right. (Called
thickness or convexity by some au-
thors.)

Dissoconch - Postlarval shell. Usually
sharply delineated from the larval
shell (prodissoconch) and of different
texture.

Dorsal - Hinge side of larvae.

Eyespot - Conspicuous pigment spot evi-
dent near center of the outline of many
species of larvae as they approach
metamorphosis.

Height - Greatest shell distance in the
dorso-ventral plane perpendicular to
the length (Called width by some au-
thors.)

Hinge line - The dorsal area of the shell
where the 2 valves are permanently
attached.

Indistinct- Type of umbo that appears
as gradual curving of the hinge line,
not prominent, outline continuous with
shoulders.

Knobby - Type of umbo with nipple-like
appearance. Outline is discontinuous
with shoulders.

Length - Greatest shell distance parallel
to the hinge line.

Pediveliger - Term proposed by Carri-
ker (1961) to refer to metamorphosing
larvae that possess both functional
foot and functional velum. It is now
widely accepted.

Posterior end-End of larva bearing
the anus. It is usually recognizable
by the higher, steeper slope of the
posterior shoulder.

Prodissoconch- The shelled stages of
bivalve larvae before metamorphosis
and dissoconch growth. Frequently
divided into 2 substages. Prodisso-
conch I (Prod I) refers to the first
Shelled stage in which the shell con-
sists only of shell deposited by the
shell gland. Prodissoconch II (Prod

II) refers to subsequent larval stages
when shell is deposited by the mantle
and growth lines are visible. These
2 terms correspond roughly with the
European designation of veliger and
veliconcha stages. They are frequent-
ly used to refer to the shell only.

Provinculum - Thickened dorsal area of
the shell that bears the hinge teeth,
when they are present.

Punctate - Marked by small dots or
spots.

Round - Type of umbo that appears as a
gradual curving of the hinge line, not
prominent, outline continuous with
shoulders.

Set- To metamorphose from larva to
juvenile. Setting involves loss of
velum and development of foot, byssus
gland, eyespot, gills and siphons, de-
pending on species.

Shoulder -Dorsal aspect of the shell
between the hinge or umbo and re-
spective ends of the shell.

Skewed - Twisted, off center, or asym-
metrical umbo, outline not continuous
with shoulders.

Straight-hinge stage-The earliest shelled
stage of most bivalves. Larvae have
a straight hinge line and are “D”
shaped. This stage persists until
total length is twice the length of the
hinge line. It differs from the Pro-
dissonconch I stage of Werner (1939)
in that it is defined by shape and size
rather than source of shell.

Taxodont -Having numerous similar but
unspecialized adjacent hinge teeth.

Truncate - Ending abruptly, squared or
cut-off appearance.

Umbo-A dorsal swelling of the shell
of older larvae that obscures the
hinge line and usually gives the lar-
vae a distinctive shape.

Umbo stage - The stage of later larval
development when the umbo is prom-
inent. It can be conveniently defined
as beginning when total length is
double the hinge length.

Veliconcha - The bivalve larva after the
shell has grown beyond the original
shell deposited by the shell gland (see

118 CHANLEY AND ANDREWS

prodissonch). In this stage, the shell the Prodissoconch I stage. The term
is marked with growth lines. veliconcha was applied to later stages.

Veliger - Technically a general term, Werner's interpretation and modifi-
meaning with a velum. It is used to cations thereof, have been used by
describe the shelled pelagic stages many European authors.

of gastropod and pelecypod larvae in
this country. Werner (1939) used
this term to describe the stages of
development from fertilization through Ventral - Side of larva opposite the hinge.

Velum-Large conspicuous ciliated swim-
ming organ of pelagic bivalve larvae.

ZUSAMMENFASSUNG
HILFEN FUR DIE BESTIMMUNG VON MUSCHELLARVEN AUS VIRGINIA
P. Chanley und J. D. Andrews

Larven von 23 Arten von Meeresmuscheln, die im mittleren Nordatlantik an der
Küste der Vereinigten Staaten vorkommen, sind im Laboratorium aufgezogen worden,
Sie sind vergleichend bescrieben worden, um den Planktonsammlern die Bestimmung
zu ermöglichen.

Die Bestimmungshilfen enthalten: 1) Vergleichende Mikrofotos der Larven der
wichtigsten Grössen- und Altersstufen. 2) Diagramme der Verhältnisse zwischen
Länge und Höhe der Jugendschale zum Vergleich der Larven verschiedener Arten
im Verlaufe der Entwicklung. 3) Tabellen der Masse und der Wirbelformen der
Larven. 4) Bestimmungsschlüssel für Larven mit gerader Schlossplatte und Wirbel,
5) Diagramme und Tabellen der Fortpflanzungszeiten und geographischen Verteilung
der Arten. 6) Kurze Beschreibungen jeder Art.

Für die Bestimmung der Larven sind diese Hilfen kombiniert zu benutzen. Da
weiter entwickelte Larven gewöhnlich leichter zu bestimmen sind als ganz junge,
sollten die Bearbeiter mit Larven beginnen, die schon einen Wirbel haben und durch
Vergleich zu den kleineren Individuen übergehen. Oft können häufige Arten durch
Populationscharaktere bestimmt werden, so z.B. durch das durchschnittliche Ver-

hältnis zwischen Länge und Höhe.
Ho 725

RESUME
MOYENS POUR L’IDENTIFICATION DES LARVES DE BIVALVES DE VIRGINIE
P. Chanley et J. D. Andrews

Les larves de 23 espèces de bivalves marins habitant la zone côtières “mid-north
Atlantic” des U.S.A., ont été élevées au laboratoire. Ces espèces ont été décrites
comparativement pour aider les planctonologistes dans leurs identifications,

Les moyens d’identification comprennent: 1) Des microphotographies comparées
des larves à des Ages et des tailles représentatifs. 2) Des courbes de relation hauteur/
longueur de la prodissoconque en vue des comparaisons interspécifiques des larves
au cours du développement. 3) Des tables de dimensions et de formes de l’umbo des
larves. 4) Des clés de détermination de larves à charnière droite et celles pourvues
d’un umbo, 5) Des graphiques et des tables de saisons de maturité et de distribution
géographique des espèces.

L'usage combiné de tous ces moyens est recommandé pour l'identification des
larves. Puisque les larves âgées sont plus faciles à identifier que les jeunes, les
chercheurs devraient commencer par les larves pourvues d’un umbo et reconnaître
progressivement les plus petites par comparaison, Souvent les espèces abondantes
peuvent être identifiées par des caractères de population tels que la relation moyenne
longueur-hauteur.

A. L.

IDENTIFICATION OF BIVALVE LARVAE

RESUMEN
IDENTIFICACION DE LARVAS DE BIVALVOS
P. Chanley y J. D. Andrews

Se criaron en laboratoiro larvas de 23 especies bivalvos de la zona costera del
Atläntico medio en Estados Unidos. Para ayudar a los planctologistas en la identifi-
caciôn, se da una descripciön comparada de los siguientes aspectos: 1) microfotos
comparadas de las larvas representado edades y tamafios. 2) graficos de proporciön
longitud-altura de las prodisoconchas para comparaciön interespecifica durante el
crecimiento. 3) tablas de formas umbonales y dimensiones. 4) claves para las char-
nelas y larvas umbonadas. 5) graficos y tablas de las estaciones de desove y distri-
buciön geografica de las especies. 6) descripciön breve de cada especie.

Se recomienda, para la mejor identificaciön de laslarvas, que todos esos elementos
se usen en combinación. Desde que las larvas en estado avanzado son más fáciles de
identificar, el investigador debe comenzar con larvas umbonadas y proseguir con
individuos más y más pequeños por comparación. Con frecuencia, las especies abun-
dantes se pueden identificar por caracteres de población, tales como el promedio

longitud-altura,
J.J. P.

ABCTPAKT

ПОСОБИЕ ДЛЯ ОПРЕДЕЛЕНИЯ ЛИЧИНОК IBYCTBOPUATEX
МОЛЛЮСКОВ ШТАТА ВИРДЖИНИЯ

Tl. ЧЕНЛИ и Дж. SHIPKC

Личинки 23 видов морских двустворчатых моллюсков, обитающих в средней
части прибрежной зоны США, в северной Атлантике, содержались и выращива-
лись в лабораторных условиях. Личинки этих видов были описаны в сравни-
тельном аспекте, чтобы облегчить их определение при обработке проб план-
ктона. 4

Этот определитель включает: 1) Сравнительные микрофотографии личинок
разного возраста и размера. 2) Графики отношения длины и высоты продис-
соконха раковины для внутривидового сравнения личинок в течение их раз-
вития. 3) Таблицы размеров и очертания макушечной части личинки. 4) Клю-
чи для определения личинок с прямым замком и выпуклой макушкой. 5) Гра-
фики и таблицы времени размножения и географического распространения
видов. 6) Краткое описание каждого вида. Рекомендуется комбинированное
использование всех этих показателей для определения личинок.

Поскольку более развитые личинки обычно легче определять, чем более
ранние стадии, следует начинать с личинок с развитой макушкой и посте-
пенно переходить к более ранним стадиям и вести их сравнение. Часто мас-
совые виды могут быть определены по некоторым общим чертам популяции,

таким как среднее отношение длины и высоты.
Z. A. Е.

119

MALACOLOGIA, 1971, 11(1): 121-140

PTEROPODOS THECOSOMADOS DEL ATLANTICO SUDOCCIDENTAL

Demetrio Boltovskoy

Facultad de Ciencias Naturales y Museo
La Plata, Argentina

RESUMEN

El presente trabajo es resultado del estudio de los Pteröpodos contenidos en
56 muestras de plancton (28 barridos horizontales superficiales y 28 verti-
cales, generalmente 200-0 m) obtenidas por elautor en noviembre de 1969 en un

área cuyos limites son: norte: 36°19'S, sur: 38°05'S, este: 42°58 W y oeste: 57

29'W.

o

La fauna fue analizada desde el punto de vista sistemático y distributivo. Se
encontraron en total 9 especies: Limacina helicina, L. retroversa, L. inflata,

L. bulimoides, Clio pyramidata, Cl. cuspidata, Creseis sp.,

Cavolina sp.

Diacria sp. y

Este estudio es una de las primeras investigaciones sobre los Pterópodos de

este parte del Atlántico Sur.

En base a las especies registradas se examina la hidrología superficial de la

zona en Cuestión.

El autor concluye que las 4 masas de agua conocidas para

este sector del Atlántico Sudoccidental pueden ser perfectamente delimitadas
mediante el uso de los Pterópodos hallados, siendo, por consiguiente, estos
moluscos planctónicos excelentes indicadores hidrológicos.

INTRODUCCIÓN

En vista de que son escasísimos los
estudios de esta zona del Atlántico
siendo por ello este trabajo una de las
primeras contribuciones en este sentido,
considero que, pese a su limitación geo-
gráfica, su contenido representa un in-
terés no despreciable para el conoci-
miento del área que abarca.

Existe una breve comunicación de
Scarabino (1967) sobre los Thecosoma-
dos muertos de 3 muestras de fondo de
la plataforma continental uruguaya y una
contribución del autor del presente estu-
dio acerca de los Pterópodos vivos sobre
la plataforma bonaerense (D. Boltovskoy,
en prensa).

En lo que se refiere a las expedi-

| ciones clásicas que motivaron los am-
| plios estudios del mundo orgánico mari-

pocas о ninguna muestra.

| no, en su gran mayoría dedicaron su

atención a zonas ubicadas más al norte

© al sur del Mar Argentino y si bien

cruzaron el mismo, extrajeron aquí muy
La expedi-

ción alemana “Gazelle” recorrió el Mar
Argentino desde el Estrecho de Maga-
llanes hasta Montevideo; sus colecciones
de Pterópodos fueron estudiadas por
Pfeffer (1879) pero, lamentablemente,
los datos de distribución son algo con-
fusos y, frecuentemente, sin indicación
explícita de la localidad. Pelseneer
(1888), en su informe sobre los Pteró-
podos colectados por la expedición
“Challenger”, cita, para esta zona, 3
especies halladas al este de las costas
uruguayas [Clio (Creseis) acicula, C.
pyramidata y Cavolinia inflexa]. El
material de la “Sweddish Antarctic Ex-
pedition” (1901-1903), estudiado por Hu-
bendick (1951), registra numerosas es-
pecies hasta la latitud 32°15'S (long.
50 14'W), los hallazgos siguientes (Spi-
vatella helicina, Procymbulia valdiviae
y Proclio subteves) corresponden a la
latitud 48°27'S (long. 42°36'W) y no hay
registros intermedios.

Mientras que el Atlantico Norte y el
Central y el sector Antartico de este
océano estan relativamente bien estu-

(121)

122

diandos, vemos que todo lo contrario
sucede con su parte sudoccidental.

Las tareas propuestas para el presente
estudio son el conocimiento de las espe-
cies presentes, su abundancia relativa,
su distribuciön geogräfica y la conside-
racion de la posibilidad de su uso en
calidad de indicadores biolögicos.

MATERIAL Y METODOS DE ESTUDIO

El estudio es resultado del análisis
de 56 muestras de plancton (28 barridos
horizontales de superficie y 28 verti-
cales, comunmente 200-0 m), obtenidas
por el autor a bordo del navio oceano-
grafico brasilefio “Almirante Saldanha”
durante los perfiles “Samborombön” y
“Mar del Plata” de la “XLI Comissäo
Oceanografica Costa Sul”. Dicha cam-
pafia tuvo lugar a fines de 1969 y los
perfiles mencionados se realizaron du-
rante noviembre del mismo afio, abar-
cando un sector cuyos limites fueron:
36%19'S y 38°05'S (lat.) y 42°58'W y
57929 W (long.). Latabla 1 brinda todos
los datos referentes a las estaciones y
a la fauna en ellas encontrada.

La red correspondiente a losbarridos
horizontales fue de 100 micrones de
abertura de malla, la vertical de 158
micrones. Inmediatamente de extraído,
el material fue fijado con formol al
10% previamente neutralizado con bó-
rax. A pesar del poco tiempo que tran-
scurrió entre la extracción de las mues-
tras y su estudio, en algunos casos los
caparazones de los moluscos se vol
vieron muy quebradizos y, ocasional-
mente, desaparecieron por completo di-
solviéndose totalmente. Si bien el cuer-
po blando del animal conservaba su forma
primitiva, era imposible de identificar
específicamente.

GENERALIDADES SOBRE
LA FAUNA ENCONTRADA

Se encontraron en total 9 especies,
a saber: Limacina helicina, Г. retro-
versa, L.inflata, L. bulimoides, Clio

D. BOLTOVSKOY

pyramidata, C. cuspidata, Creseis sp.,
Diacria sp. y Cavolinia sp. Las de
apariciôn mas regular fueron Limacina
helicina y L. inflata, aunque en canti-
dad de ejemplares la predominancia
correspondió a Limacina retroversa.
Todas las estaciones (excepto la 2261)
contuvieron Pteröpodos.

Morton (1954) destacó que las migra-
ciones verticales diarias de Limacinidae
tienen un rango mucho mas estrecho
que las de Cavoliniidae. Es muy pro-
bable que la dominancia de los individuos
de la primera familia se deba no sola-
mente a su abundancia en la zona estu-
diada, sino también a la particularidad
que se acaba de mencionar. Esta afir-
mación adquiere más valor aún si se
considera que la mayoría de los Lima-
cina vetvoveysa es un representante
típico de las aguas en cuestión, no sucede
lo mismo con Limacina helicina cuyo
hábitat óptimo se encuentra en la pro-
ximidad de la Convergencia Antártica
(Chen, 1968), ni con Limacina inflata
que es de distribución más septentri-
onal. Por otro lado, especies tales
como Creseis acicula, C. virgula, Clio
pyramidata, etc., que deberían ser re-
lativamente abundantes en esta área, es-
tuvieron prácticamente ausentes o re-
presentadas por muy pocos ejemplares.

Los individuos juveniles constituyeron |

un gran porcentaje del total de la fauna
encontrada. Esto es notable, sobretodo,
en lo referente a los representantes de
la familia Limacinidae y en tal grado
que, en varios casos, fue imposible su
determinación sistemática. Probable-
mente, esto se debe a que no se reali-
zaron barridos verticales profundos.
En muchos grupos de animales planc-

tónicos, entre los cuales se incluyen los |
Pterópodos, los individuos jóvenes tie- |
nen límites migratorios más estrechos

y, generalmente, prefieren capas de
agua superiores a aquellas que habi-

tarán en el estado adulto (Vinogradov, |

1968).
En lo referente a las migraciones
verticales diarias, se registró mayor

|

|

PTEROPODOS DEL ATLANTICO 123

REFERENCIAS

*o 00

А — 06

EST SE

0 —— 9° —

A
ER

0

S
U
2 =
S
3

ESPECIES
A
60

7 KA

DISTRIBUCION

00-0

124 D. BOLTOVSKOY

LAMINA I

Fig. 1 a-c) Limacina helicina (Phipps). Est. 2286 (H)
a) vista frontal,
b) vista ventral,
c) vista dorsal.

Fig. 2 a-b) Limacina retroversa (Fleming). Est. 2286 (H)
a) vista frontal,
b) vista dorsal.

Fig. 3 a-c) Limacina inflata (d’Orbigny). Est. 2269 (H)
a) vista frontal,
b) vista ventral,
c) vista dorsal.

Fig. 4 a-b) Limacina bulimoides (d’Orbigny). Est. 2279 (H)
a) vista frontal,
b) vista dorsal.

Fig. 5 Creseis sp. Est. 2266 (V), protoconcha.
Fig. 6 Diacria sp. Est. 2277 (V), protoconcha.
Fig. 7 Cavolinia sp. Est. 2274 (H), extremo basal.

Fig. 8 a-b) Clio cuspidata (Bosc). Est. 2269 (V)
a) vista ventral,
b) vista lateral.

Fig. 9 Clio pyramidata Linnaeus. Est. 2279 (V), vista ventral.

Fig. 10 Clio pyramidata Linnaeus. Est. 2267 (V), vista ventral
de un ejemplar juvenil.

Riesa Clio pyramidata Linnaeus. Est. 2279 (V), vista dorsal.

PTEROPODOS DEL ATLANTICO 125

9 Escala MM, 31

126 D. BOLTOVSKOY

cantidad de Pterdpodos en las esta-
ciones nocturnas que en las diurnas
(sin diferencias excesivas).

PARTE SISTEMATICA

Por razones de espacio y debido a
que son numerosas en la bibliograffa,
no daré aquilasdescripciones detalladas
de las especies, limitandome a una
breve caracterizaciön de las mismas y
a determinadas observaciones que con-
sidero de interés.

Las listas de sinonimia estan redu-
cidas a las citas originales, a los tra-
bajos que trataron material proveni-
ente del Océano Atlantico y a algunas
obras de importancia general.

Las siglas (H) y (V), luego del número
de estación, significan barrido horizon-
tal y vertical, respectivamente.

Orden THECOSOMATA, Blainville, 1824
Suborden EUTHECOSOMATA Meisen-
heimer, 1905

Familia Limacinidae Gray, 1847
Género Limacina Lamarck 1819
Limacina helicina (Phipps, 1774), s. 1.

Lam.-I, Fig. 1а-с.

Clio helicina Phipps, 1774, A Voyage
towards the North Pole, :195.

Limacina antarctica Pelseneer, 1888,
Rep. Pterop. HMS “Challenger”. 2.
The Thecos., :22, Pl. I, Fig. 3,4.

Limacina helicina Vayssiere, 1915, Moll.
Euptérop. (Ptérop. Thécos), :142, Pl.
VII, Fig. 135-152; Mackintosh, 1934,
Distr. macropl. Atlant. Sector of the
Antarct., Fig. 2j; Tesch, 1946, The
Thecos. Pterop., I. The Atlant., :6,
Fig. 1; Tesch, 1947, Pterop. Thecos.,
:3, Fig. 5A-B; Chen & Be, 1964, Sea-
son. distr. Euthecos. Pterop. west.
North Atlant., :189, Fig. 2a,b; Chen,
1966, Calc. Zoopl. Scotia Sea and
Drake Pass., Fig. 6; Chen, 1968, Zoo-
geogr. Thecos. Pterop. West Antarct.
Ocean, :95, Map 1.

Numerosos autores la separan en.

diferentes especies (Pelseneer, 1888;

Eliot, 1907), variedades (McGowan, 1960)
o subespecies y formas (Spoel, 1967).
Debido a que en mi material tuve una
cantidad relativamente pequefia de ejem-
plares de esta especie (muchos de los
cuales fueron juveniles), y como no he
notado diferencias morfolögicas dignas
de considerarse entre los mismos, pre-
fiero considerar mis hallazgos como
pertenecientes a una especie única, sin
distinciön de categorias inferiores.

Los ejemplares estudiados son, sin
excepciön, individuos tipicos. Poseen
espiras bajas y suturas rectas, aber-
tura de forma subtrapezoidal, umbilico
ancho y profundo, ancho maximo mayor
que la altura y valva fragil de color
amarillento-hialino. Los caparazones
de mayor tamafio presentan una escul-
tura muy tenue en forma de lineas de
crecimiento perpendiculares a las su-
turas.

Distribuciön

Su presencia se registrö en las mues-
tras 2262 (H) y (V), 2263 (H) y (V), 2264
(H), 2266 (V), 2269 (H) y (V), 2270 (V),
2271 (H), 2272 (H), 2273 (H) y (V), 2274
(H), 2276 (V), 2277 (H), 2278 (V), 2283
(V), 2284 (H), 2286 (H) y (V) y 2287 (H)
y (V). Esto la coloca en primer lugar
en cuanto a la regularidad de aparición.
En todos los casos se trató de modera-
das cantidades de ejemplares, general-
mente juveniles (3-4 vueltas).

Esta especie es característica de las
aguas polares y subpolares (Eliot, 1907;
Massy, 1920, 1932; Mackintosh, 1934;
Wiborg, 1955; Spoel, 1967 y Chen, 1968).

Limacina vetroversa
Shale

Lam. Г Fig. 2a,b

(Fleming, 1823),

Heterofursus retroversus Fleming, 1823,
Mém. Wern. Nat. Hist. Soc., :498,
Tab#19, Bic. 2,

Limacina balea Moller, 1841, Proceed.
Tidsskr., 1. Raekke, 3 Bd., :489.

Limacina australis Pelseneer, 1888,
Rep. Pterop. HMS “Challenger”. 2.
The Thecos., :29, Pl. J, Fig 6!

|

PTEROPODOS DEL ATLANTICO

Limacina retroversa Vayssiere, 1915,
Moll. Euptérop. (Ptérop. Thécos.),
:142, Pl. VII, Fig. 156-160, 170 e
171, Pl. IX, Fig. 213-216; Tesch, 1946,
The Thecos. Pterop., I. The Atlant.,
16, «Fig. 2A-G; Chen, 1966, Calc;
Zoopl. Scotia Sea and Drake Pass.,

Fig. 6.

Limacina vetrovevsa, subsp. balea
Tesch, 1947, Pterop. Thecos., :3,
Fig. 6A,B.

Limacina retroversa, subsp. retroversa
Tesch, 1947, Pterop. Thecos., :3,
Fig. 6B,C.

Limacina (Limacina) retroversa forma
balea Spoel, 1967, Euthecos., :47,
Fig. 12,13.

Limacina (Limacina) retroversa forma
retroversa Spoel, 1967, Euthecos.,
:43, Fig. 10,11.

Limacina (Limacina) retroversa forma
australis Spoel, 1967, Euthecos., :48.

Al igual que en el caso anterior, exis-
ten aqui disidencias en cuanto a la pre-
sencia de una sola especie o de varias.
Uno de los criterios, el sostenido por
Möller (1841), Sars (1878), Bonnevie
(1913), Tesch (1913, 1947), Massy (1932)
y Spoel (1967), basandose en el tamafio,
la altura y la cantidad de anfractos de
los individuos, la divide en various gru-
pos con diferentes categorias sistema-
ticas. Por otro lado Boas (1886), Pel-
seneer (1888), Meisenheimer (1905),
Vayssiére (1915), Hsiao (1939), Redfield
(1939) y Chen & Bé (1964), sostienen
que se trata de una misma especie
en diferentes estados de desarrollo.

Si bien el material revisado corres-
ponde en su totalidad a una misma zona,
fue muy grande la cantidad de ejem-
plares examinados y ninguna diferencia
morfolögica de importancia he notado
entre ellos. Por lo tanto seguiré aqui
el criterio del 2° grupo de investigado-
res citados, considerandola como espe-
cie unica.

Se trata de conchillas altas de sutu-
ras casi oblicuas, umbilico conspicuo
y abertura sub-trapezoidal. Se encon-
traron ejemplares de diversos tamafios,
desde juveniles hasta adultos de 7 vuel-

127

tas. Estos últimos presentan suturas
muy profundas y, frecuentemente, no-
tables estrías de crecimiento.
Distribución

Es una especie subpolar. Este cri-
terio lo han ratificado, entre otros,
Schiemenz (1906), Eliot (1907), Paulsen
(1910), Bigelow (1926), Hansen (1960),
Kramp (1961) y Spoel (1967).

Su presencia se registró en las mues-
tras 2264 (V), 2265 (H) y (V), 2267 (V),
2268 (H) y (V), 2269 (H), 2273 (V), 2276
(V), 2284 (V), 2286 (H) y (V) y 2287 (H).
La cantidad de ejemplares, a excep-
ción de un caso, varió de escasa a
normalmente abundante. La excepción
mencionada es la muestra horizontal de
la estación 2286 que consistió casi ex-
clusivamente en Pterópodos perteneci-
entes a esta especie. Aproximadamente
50 m° de agua filtrada dieron por resul-
tado más de 50.000 individuos (mayor -
mente adultos). Este fenómeno se pro-
dujo una sola vez, las estaciones veci-
nas a la 2286 contuvieron pocos o nin-
gún ejemplar de Limacina retroversa.

Mackintosh (1934) destacó la distribu-
ción irregular, manchiforme del planc-
ton en general y de Limacina retroversa
en particular. Quizá una explicación de
este fenómeno, al menos con respecto
a la especie que nos ocupa, sea la si-
guiente observación. La muestra 2286
(H) se tomó a las 23.30 horas y los
moluscos estaban concentrados en la
capa superficial de agua (la cantidad
de individuos obtenida en el barrido
vertical fue muchísimo menor), mien-
tras que las estaciones 2285 (a la ma-
drugada) y 2287 (al atardecer) se reali-
zaron con 5.30 y 6.30 horas de diferen-
cia, respectivamente, con la 2286. Ese
tiempo es suficiente para que los ani-
males desciendan al fondo, cosa que
aparentemente hacen en lugares de poca
profundidad ya que la luz condiciona
que dejen de batir sus “alas” sedimen-
tando naturalmente (Fryer, 1869).

Hay aun otro hecho que creo impor-
tante destacar. Los valores de Og,

NO» y PO4 fueron muy altos (en rela-

ción a las demás estaciones en este

D. BOLTOVSKOY

128

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132 D. BOLTOVSKOY

lugar. Los anälisis correspondientes
evidenciaron 6.66 ml/l de Oo y 0.17
mg/l de NO» (la mayor cantidad de este
nutriente se registro en la vecina esta-
cion 2285: 0.22 mg/l). En cuanto a los
fosfatos, a la profundidad de 90 m
(sobre el fondo) se obtuvo el valor mas
alto: 1.67 mg/l ( en superficie el con-
tenido fue de 0.55 mg/l). Es muy pro-
bable que estos factores influyan en al-
guna medida sobre los Pteröpodos.

Según Spoel (1967), las aguas someras,
debido a la variabilidad de sus condi-
ciones ecológicas, no son favorables
para la vida de los Pterópodos. Sin
embargo, la enorme concentración des-
cripta ocurrió en la plataforma, sobre
una profundidad de 95 m.

Lebour (1932) notó que en el Mar del
Norte Limacina retroversa es una de
las especies más frecuentes y que son
notables sus concentraciones estivales.
Basándose en Hardy, escribe que es muy
importante desde el punto de vista ali-
menticio ya que no solo es depredada
por otros Moluscos y Quetognatos, sino
que constituye del 2 al 17% del alimento
anual total del arenque. Es muy proba-
ble que en el Mar Argentino suceda algo
semejante con respecto a determinados
peces planctófagos. Lamentablemente,
la falta de antecedentes no permite
sacar conclusión alguna en este sentido.

Limacina inflata (d’Orbigny, 1836)
Lam. I, Fig. 3a-c

Atlanta inflata d’Orbigny, 1836, Voy.
Amér. Mérid., Moll. 5(3), :174. (1846,
Atlas, Pl. 12, Fig. 16-19).

Limacina inflata Boas, 1886, Spolia
Atlant., :48, Tab. 3, Fig. 38; Vays-
siere, 1915, Moll. Euptérop. (Ptérop.
Thécos.), :133, Pl. VIII, Fig. 153-155
& 167-169; Tesch, 1946, The Thecos.
Pterop., I, The Atlant., :8, Pl. I, Fig.
1; Tokioka, 1955, Plankt. anim. coll.
Syunkotu-Maru. IV. Thecos. Pterop.,
:61, Pl. VII, Fig.:5,6; Chen € Be,
1964, Season. distr. Euthecos. Pterop.
west. North Atlant., Fig. 2f,g,h.

Limacina (Thilea) inflata Spoel, 1967,
Euthecos., :50, Fig. 17-19.

Los ejemplares encontrados coinciden
totalmente con las descripciones de esta
especie que figuran en d’Orbigny (1836)
y en tratados posteriores. La abertura
es ancha, de forma ovoide y el umbilico
relativamente abierto. El último anfrac-
to es siempre mucho mayor que los
precedentes. Las espiras son muy
bajas, a tal punto que en vista frontal
no se observan las vueltas precedentes
a la última.

Spoel (1967), describiendo la costilla
dorsal de Limacina inflata, observa que
hay casos en que ésta está dividida, en
2 que corren paralelamente para jun-
tarse sólo a nivel del dorso del último
anfracto, en la culminación del cual
forman la protrusión llamada diente de
la abertura. Se encontraron individuos
con una, con dos costillas, y sin ella.

Muchos de los Limacinidae indeter-
minados debido a su extrema juventud
pertenecen, presumiblemente, a esta
especie. Los mayores son totalmente
adultos (hasta 2.5 y 3 vueltas).
Distribución

Esta especie ocupó el 2° lugar (luego
de Limacina helicina) en cuanto a fre-
cuencia de aparición. Se registró en
las siguientes muestras: 2264 (H), 2265
(V), 2266 (V), 2269 (H) y (V), 2270 (H)
y (V), 2271 (H) y (V), 2272 (V), 2273
(V), 2276 (H) y (V), 2277 (V), 2278 (H)
y (V), 2279 (V), 2280 (V), 2281 (H), 2283
(V) y 2284 (H) y (V). Con pocas excep-
ciones, se trató de moderadas cantida-
des de individuos, frecuentemente juve-
niles.

Evidentemente, se trata de una especie
ampliamente distribuída que habita las
aguas templadas y cálidas (Boas, 1886;
Sykes, 1905; Tesch, 1946; Hida, 1957;
Barth et al, 1968, etc.). Pelseneer
(1888) le atribuye una distribución, en el
Atlántico, desde 42°N hasta 40°S, inclu-
yéndola en su “South Atlantic Province”.
Este último autor, Massy (1920) y Hu-
bendick (1951), la registraron cerca de
las costas brasileñas.

De acuerdo a Chen € Ве (1964), el
intervalo térmico de esta especie va de
14 a 28°C y el salino de 35.5% a 36.7%,

PTEROPODOS DEL ATLANTICO 133

Considero que los limites inferiores
deben ser ampliados ya que encontré
Limacina inflata en aguas de 8.4°C y
33.5% de salinidad.

Rampal (1967) destaca que si bien
alcanza mayores profundidades, surango
vertical fluctúa, tanto de día como de
noche, entre los 200 y 0m. Esto con-
tribuiría a explicar el hecho de que, sin
ser una de las especies dominantes,
halla sido registrada en estas muestras
con tanta frecuencia.

Limacina bulimoides (d'Orbigny, 1836)
Lám. I, Fig. 4a,b

Atlanta bulimoides d’Orbigny, 1836, Voy.
Amér. Mérid., Moll. 5(3), :117. (1846,
Atlas, Pl. 12, Fig. 29-31).

Limacina bulimoides Boas, 1886, Spolia
Atlant., :47, Tab. 3, Fig. 36-37;
Vayssiere, 1915, Moll. Euptérop. (Pté-
rop. Thécos. ), :141, Pl. VIII, Fig.
165; Tesch, 1946, Thecos. Pterop.,
I. The Atlant., :9, Pl. I, Fig. 4; Mor-
ton, 1954, Pelagic Moll. Benguela
Current; :171, Fig. 2; Tokioka, 1955,
Plankt. anim. coll. Syunkotu-Maru.
Ev. ~Thecos. Pterop., :62, Pl. VII,
Fig. 9,10; Chen & Be, 1964, Season.
distr. Euthecos. Pterop. west. North
Atlant., Fig. 20,p.

Limacina (Munthea) bulimoides Spoel,
1967, Euthecos., :53, Fig. 21.

Las- descripciones que dieron d’Or-
bigny (1836) e investigadores posterio-
res, concuerdan perfectamente con mis
ejemplares. Las conchillas adultas son
cônicas, con suturas y rostro conspi-
cuos, umbilico cerrado, practicamente
ausente. Se observö el peculiar color
del caparazön: marrön-rojizo, pronun-
ciado sobre todo a nivel de las suturas
y del umbilico. Las notables estrias de
erecimiento, perpendiculares a las su-
turas, son evidentes, mäs que nada, so-
bre el ültimo anfracto.

Distribuciön
Se obtuvo en las siguientes muestras:
2266 (V), 2269 (H), 2271 (V), 2272 (V),

2276 (V), 2279 (V), 2280 (H), 2281 (H) y
2288 (V).

De todas las especies encontradas es
la que demoströ menor tolerancia con
respecto a aguas frias. Las tempera-
turas mas bajas donde fue registrada
oscilaron entre 15 y 16°C.

Hay una concordancia general sobre
su distribución geográfica: es una espe-
cie tropical-subtropical de distribuciön
muy vasta.

Muchos autores (Morton, 1954; Hida,
1957; Spoel, 1967) destacan que Limacina
bulimoides estafrecuentemente asociada
a L. inflata. Aparentemente, dicho fenö-
meno también se registrö en este caso:
7 de las 9 muestras que contenian Lima-
cina bulimoides, tambien presentaron
ejemplares de L. inflata.

Familia Cavoliniidae Fischer, 1883
Género Clio Linnaeus, 1767
Clio pyramidata Linnaeus, 1767, s. 1.

Lam. I, Fig. 9-11

Hyalea lanceolata Lesueur, 1813, Mém.
quel" nov: .€Sp:!. 284, Pl) 5) Fig;

Cleodora pyramidata var. lata Boas,
1886, ySpolia Atlant) ‘69. тар. 5;
Fig. 74,86, Tab. 6, Fig. 96g, 97e,

Tab. 4, Fig. 47.

Cleodora pyramidata Vayssiere, 1915,
Moll. Euptérop. (Ptérop. Thécos.),
:68, Pl. I, Fig. 19-20 (non Fig. 21),
Pl. V, Fig. 92-95 (non Fig. 96), Fig.
97-102, Pl. X, Fig. 226.

Euclio pyramidata Tesch, 1946, Pterop.
Thecos., I. The Atlant., :14, Pl. I,
Fig. 11; Tesch, 1947, Pterop. Thecos.,
:5, Elg.18:

Euclio pyramidata lanceolata Tokioka,
1955, Plankt. anim. coll. Syunkotu-
Maru, IV. Thecos. Pterop., :62, Pl.
VIII, Fig. 11-13.

Clio pyramidata Chen & Be, 1964, Sea-
son. distr. Euthecos. Pterop. west.
North Atlant., Fig. 2r.

Clio pyramidata forma lanceolata Spoel,
1967, Euthecos., :67, Fig. 48,49.

Se trata de una especie connumerosas

134

formas (Spoel, 1967), variedades (Boas,
1886) o subespecies (Tokioka, 1955). A
pesar de aceptar enteramente que bajo
la denominación de “Clio pyramidata”
se encuentran incluidos organismos con
evidentes diferencias morfolögicas entre
si, debido a la falta de material compa-
rativo, evitaré adoptar cualquier cri-
terio con respecto a los subgrupos que
incluye la especie.

En mi material encontré tanto indivi-
duos juveniles como adultos. Estos
últimos fueron ejemplares cuyo largo no
alcanzó los 10 mm, de costillas laterales
fuertemente divergentes. Las estrías de
crecimiento bien conspicuas. Con fre-
cuencia se encontró exclusivamente la
protoconcha, sin embargo, gracias tanto
a su morfología relativamente típica
como a los datos que existen acerca de
su distribución, fue posible determinar
la especie correspondiente.
Distribución

Su distribución es amplísima en todo
el mundo a excepción de las aguas po-
lares. La mayor frecuencia seobserva
en las áreas templadas y templadas-
frías decreciendo (aunque sin desapare-
cer) hacia el Ecuador.

Durante la campaña en cuestión su
presencia se verificó en las siguientes
muestras: 2264 (V), 2266 (V), 2267 (V),
2272 (V), 2275 (V), 2277 (V), 2279 (V),
2280 (V), 2281 (H) y 2285 (V). Los ante-
cedentes que existen con respecto a
hallazgos anteriores cerca del área in-
vestigada, son los correspondientes a
Pelseneer, 1888 (frente a costas uru-
guayas), Massy, 1920, 1932 (frente a
Rio de Janeiro y al noreste de Islas
Malvinas, respectivamente) y Scarabino,
1967 (conchillas vacías sobre la plata-
forma continental uruguaya).

La baja frecuencia de esta especie
tan común, se debe, indudablemente, a
sus migraciones verticales diarias que
llegan a una amplitud de 2000 m (Stub-
bings, 1938). Los pocos ejemplares
que se obtuvieron, correspondieron, a
excepción de un solo caso, a barridos
verticales.

D. BOLTOVSKOY

Clio cuspidata (Bosc, 1802)
Lám. I, Fig. 8a,b

Hyalea cuspidata Bosc, 1802, Hist. Nat.
Coq... et leurs usages., :241, Pl. 9,

Fig. 5-7.

Cleodora cuspidata Boas, 1886, Spolia
Atlant., :81, Tab. L Fig" 2, Tab
Fig. 13, Tab. 4, Fig. .51, Taba

Fig. 87,88; Vayssiere, 1915, Moll.
Euptérop. (Ptérop. Thécos.), :77, Pl.
I, Fig. 16-18, Pl. V, Fig. 103-106,
Pl. X, Fig. 227; Massy, 1932, Moll.
:Gastr. Thecos. and Gymnos. (Pte-
rop.), 2277.

Euclio cuspidata Tesch, 1946, Thecos.
Pterop., 1. The Atlant. 1432s
Fig. 9; Tesch, 1947, Pterop. Thecos.,
5, Pigs 9.

Clio cuspidata Spoel, 1967, Euthecos.,
:73, Fig. 64-67.

El ünico ejemplar encontrado fue un
adulto de 14 mm de alturay 19mm entre
los extremos de las espinas laterales.
La conchilla transparente, hialina, pre-
senta evidentes estrias de crecimiento
de diferente grosor. EI lado ventral
es fuertemente convexo - notablemente
curvada la parte posterior del dorso.
Este ültimo sobrepasa la mitad ventral
y por su parte media corre una costilla
que se proyecta hacia adelante amanera
de espina (en este ejemplar faltaba su
extremo distal). La abertura es muy
alargada en sentido lateral y angosta
dorso-ventralmente.

Sobre la superficie dorso-lateral de
la conchilla, cerca de la protoconcha,
hay una colonia de Hidrozoos. Antece-
dentes de este fenömeno pueden encon-
trarse en Tesch (1946) quien destaca
que es un hecho frecuente que Campa-
niclava cleodorae (Gegenbaur) actue co-
mo epizoico sobre Clio cuspidata.

Distribución

El ejemplar descripto fue hallado en
la estación 2269 (V).

Es una especie típica de las aguas

cálidas, se conoce en el Mediterráneo,
Atlántico, Pacífico e Indico (Spoel, 1967).

|

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PTEROPODOS DEL ATLANTICO

Género Creseis Rang, 1828
Creseis sp.

Man 1, Fie. 5

La falta de ejemplares completos no
permitió establecer la especie a que
pertenece la protoconcha encontrada en
la muestra 2266 (V). Probablemente se
trata de Creseis acicula (Rang, 1828) o
Creseis virgula (Rang, 1828), ambas
ampliamente distribuídas en esta parte
del Atläntico.

Género Diacria Gray, 1847
Diacria sp.

Läm. I, Fig. 6

En la muestra 2277 (V) se hallö una
protoconcha que, probablemente, perte-
nece a un ejemplar de Diacria trispi-
nosa (Blainville, 1821).

Género Cavolinia Abilgaard, 1791
Cavolinia sp.

Läm. I, Fig. 7

En la muestra 2274 (H) se encontrö
el extremo basal de un individuo de
este género. Debido a que esta parte
es muy semejante en varias especies
del género Cavolinia y a que son nume-
rosas las que habitan esta parte del
Atlantico Sur, es imposible determinar
la especie.

CONSIDERACIONES HIDROLOGICAS

El area investigada, debido a sus ca-
racteristicas hidrolögicas particulares,
es de especial interés. Se trata de una
amplia zona de choque de dos masas
de agua de diferentes caracteristicas
fisico-quimicas. Por un lado, desde el
norte avanza la Corriente calida de
Brasil; por el otro, en sentido contra-
rio, las aguas subantarticas de la Corri-
ente Cabo de Hornos y su ramaocciden-
tal, la Corriente de Malvinas. Este
€ncuentro condiciona la existencia de
una muy amplia zona (Zona de Con-
vergencia Subtropical-Subantartica) con
aguas de mezcla en diferentes propor-

135

ciones, y sectores de aguas puras de
tal o cual origen (franjas, manchas y
lenguas). Los limites de esta zona
(especialmente el septentrional) varian
estacionalmente. En verano, еп 5и parte
occidental (precisamente allf donde tuvo
lugar la derrota estudiada), son los pa-
ralelos 35-36°S al norte y 48-49°S al
sur (E. Boltovskoy, 1968). Hacia el
oeste de la Zona de Convergencia hay
una banda de aguas puramente subanar-
ticas pertenecientes a la Corriente de
Malvinas, y entre éstas y la costa se
encuentran las aguas de la Zona Costera
Argentina cuyo débil movimiento tiene
el mismo sentido que la corriente que
las flanquea por el este (E. Boltovskoy,
op. cit.). Por ultimo queda un area
ubicada frente a la desembocadura del
Rio de la Plata (Area de Influencia del
Rio de la Plata) cuyas aguas tienen una
salinidad inferior a lo normal.

De acuerdo a este esquema hidrolö-
gico superficial, estival, presentado por
E. Boltovskoy (1968, :210), durante su
derrota el buque cruzó las siguientes
masas de agua (de oeste a este): 1°-
Area de Influencia del Río de la Plata
(Ests. 2261-62); 2°-Zona Costera Ar-
gentina (Ests. 2263, 2286-88); 3°-Co-
rriente de Malvinas (Ests. 2264 y 2285)
y 4°-Zona de Convergencia Subtropical-
Subantártica (Ests. 2265-2284).

Solo 2 de las 9 especies halladas
tienen su origen en latitudes altas.
Ellas son Limacina helicina y L. retro-
versa, ambas traídas por la Corriente
de Cabo de Hornos y la de Malvinas.
Su presencia es indicio de aguas sub-
antárticas. Las restantes 7 especies,
todas de origen subtropical, evidencian
la presencia de aguas pertenecientes a
la Corriente de Brasil.

En un trabajo donde realiza una zona-
ción de acuerdo ala fauna de Pterópodos,
Meisenheimer (1906), observa: que la
presencia de Limacina inflata en el Mar
Argentino se debe a la “corriente cálida
de Cabo de Hornos”. Su explicación
es la siguiente: la parte de la Corriente
del Oeste de Deriva que, sobre los 40-
45°S, en el Pacífico, avanza en sentido

136

oeste-este, antes de alcanzar las costas
de Chile se divide en 2 ramas: hacia
el norte da la corriente de Humboldt y
hacia el sur una rama que, Siguiendo a
Berghaus (1891), Meisenheimer deno-
mina Corriente de Cabo de Hornos.
Esta ultima, luego de rodear Tierra
del Fuego, avanza hacia el noroeste
poniéndose en contacto con la Corriente
de Malvinas. Sus aguas son las que
traen elementos subtropicales a la zona
en cuestiön.

Si bien existe, evidentemente, cierta
influencia sobre las costas fueguinas y
es probable que algunos hallazgos loca-
les de Limacina inflata tengan ese ori-
gen, me inclino a poner en duda la pre-
sencia de esta especie en toda la Zona
de Convergencia del Mar Argentino como
resultado de esta corriente. En mi
opinion la fuente principal de aporte de
organismos subtropicales a la zona en
cuestión, es la Corriente de Brasil
cuyas aguas, en verano, pueden ser
detectadas, biológicamente, hasta la la-
titud 49°S (E. Boltovskoy, 1968).

En cuanto a Clio cuspidata, segura-
mente en la zona estudiada es relativa-
mente frecuente, sobre todo en verano
cuando la Corriente de Brasil tiene
mayor influencia. El que se halla re-
gistrado una sola vez se debe a que es
una especie batipelagica; Rampal (1967)
destaca que se distribuye a diferentes
profundidades entre 200 y 3500 m.

El analisis global de la fauna en
relaciön al la zonaciön de E. Boltovskoy
(1968), es el siguiente;

La estación 2261, de baja salinidad
(30.62%) evidentemente debido al aporte
de agua dulce por parte del Río de la
Plata, no contuvo Pterópodos. La 2262
(sal: 33.63%) y 2263 (33.60%), cercanas
a las aguas malvinenses puras, contu-
vieron fauna subantártica exclusivamen-
te (Limacina helicina). Desde la est.
2264 (aguas malivinenses) hasta la 2285,
con contadas excepciones, la fauna re-
gistrada fue heterogénea subtropical-
subantártica, predominando el 2° tipo.
Las estaciones 2286 y 2287 (Zona Cos-
tera Argentina; movimiento predominan-

D. BOLTOVSKOY

te de las aguas de sur a norte) contu-
vieron Pterópdos subantárticos sola-
mente y la última (2288), algunos ejem-
plares juveniles de Limacina bulimoides
(subtropical). Este último hallazgo pro-
bablemente se deba a una pequeña rama
occidental de la Corriente de Brasil
que penetra hacia el sur entre la Co-
rriente de Malvinas y la Zona Costera
Argentina a la altura del Area de In-
fluencia del Río de la Plata.

De lo anteriormente expuesto se de-
duce que la distribución de los Pteró-
podos coincide bastante bien con el
esquema hidrológico citado. Por otro
lado, la comparación de estos datos con
los que arrajó el estudio de los Fora-
miniferos de las mismas muestras, de-
mostró una coincidencia muy alta (co-
municación verbal del Dr. E. Boltov-
skoy).

Todas estas consideraciones llevan a
la conclusión que los Pterópodos son
buenos indicadores hidrológicos. La
sensibilidad con respecto a las varia-
ciones de los carácteres físico-quími-
cos del agua (requisito indispensable
para un buen indicador) se apreció en
su ausencia en aguas de baja salinidad
(Est. 2261) y en su distribución acorde
con el tipo de agua. Además, una ilus-
trativa prueba de la sensibilidad de
estos planctontes, la dan los siguientes
fenómenos. En la est. 2268 se regis-
tró un brusco salto térmico del agua
superficial (est. 2267: 17.5%C, 2268:
13.2°C, 2269: 16.6°C) que se reflejó en
los Pterópodos de la estación mencio-
nada de tal manera que mientras que
todas las estaciones vecinas contenían
fauna de mezcla, ésta presentó fauna
subantártica exclusivamente (Limacina
retroversa).

Realizando un diagrama T-S se puede
agrupar a la mayoría de las muestras
en 2 conjuntos ubicados en aguas de
diferentes características termosalinas.
El primero, en aguas de alta tempera-
tura y salinidad, incluyó el 55% de
las muestras y su fauna fue, en casi
todos los casos, de mezcla. El 2° con-

junto, ubicado en aguas de temperatura

PTEROPODOS DEL ATLANTICO 137

y salinidad algo inferiores, agrupo 6
estaciones 4 de las cuales contuvieron
Pteröpodos subantarticos exclusivamen-
te.

Otra ventaja de su uso como indica-
dores hidrolögicos consiste en que son
organismos suficientemente numerosos
en el plancton y su determinaciön sis-
tematica no presenta mayores dificul-
tades.

Ensayos del uso de los Pteröpodos
como indicadores de masas de agua se
pueden encontrar en: Meisenheimer
(1906), Bogorov & Vinogradov (1951),
Hida (1951), Chen € Bé (1964), Rampal
(1965) y Chen (1966a).

AGRADECIMIENTOS

Quiero testimoniar aqui mi agrade-
cimiento a mi padre, Dr. E. Boltovskoy,
cuya permanente ayuda posibilitó la rea-
lización del presente trabajo. Asimismo
agradezco a la Direitoria de Hidro-
grafia e Navegacáo (Brasil) y al Con-
sejo Nacional de Investigaciones Cien-
tíficas y Técnicas (Argentina), entidades
que permitieron que se hiciera factible
mi intervención en la campaña, y a la
plana mayor, tripulación en general y
científicos del NOc Almirante Saldanha.

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ABSTRACT

THECOSOMATOUS PTEROPODS OF THE SOUTHWESTERN ATLANTIC

D. Boltovskoy

The
surface and 28 vertical,

thecosomatous pteropods in fifty-six plankton samples (28 horizontal
generally 200-0 m,
systematical and distributional points of view.

hauls) were studied from the
The zone of collection is

described as follows: North 36°19'S, South: 38°05'S, East: 42°58'W and West:

57°29'W.

Nine species were found: Limacina helicina, L. retroversa,

L. inflata, L.

bulimoides, Clio pyramidata, Cl. cuspidata, Creseis sp., Diacria sp. and

Cavolinia sp.

This is one of the first thorough studies on the pteropods of this part of the

South Atlantic Ocean.

The hydrology of surface waters is discussed on the basis of the results ob-
tained and the author arrives at the conclusion that the 4 water masses known
for this area can be perfectly delimited and thus these mollusks are excellent

hydrological indicators.

140

D. BOLTOVSKOY

ZUSAMMENFASSUNG
THECOSOMATA (PTEROPODA) DES SUDWESTLICHEN ATLANTIK

D. Boltovskoy

Diese Arbeit stellt ein Ergebnis der Untersuchung von Pteropoden (Pteropoda,
Thecosomata) dar. Diese wurden in 56 Plankton-Proben (28 Horizontalfange - Ober-
wasserschicht; 28 Vertikalfänge - die meisten von 200-0 m Tiefe) vom Autor (Novem-
ber, 1969) aus einem Gebiet des Südwest-Atlantiks entnommen, das wie folgt begrenzt
wird: im Norden 36°19'S; im Stiden 38°05'S; im Westen 57°29'W; im Osten 42°58'W.

Es wurden Systematik und Verbreitung der Fauna untersucht; im Ganzen wurden
9 Arten gefunden: Limacina helicina, L. retroversa, L. inflata, L. bulimoides, Clio
pyramidata, Cl. cuspidata, Creseis sp., Diacria sp. und Cavolinia sp.

Diese Untersuchung ist eine der ersten Arbeiten über Pteropoden in diesem Teil
des Südatlantiks.

Auf Grund der vorhandenen Arten konnten Schlussfolgerungen über die Hydrologie
gezogen werden. Der Autor kommt zum Ergebnis, dass die vier Wasserzonen,
die für dieses Gebiet bekannt sind, sich auf Grund der vorhandenen Pteropoden gut
unterscheiden. Daraus folgt, dass diese Mollusken mit Erfolg als biologische,
besser gesagt hydrologische Indikatoren dienen können.

RESUME

PTEROPODES THECOSOMES DU SUD-OUEST DE L’ATLANTIQUE
D. Boltovskoy

Ce travail d’investigation est le résultat de l’étude des Ptéropodes contenus dans
56 échantillons de plancton (28 prélèvements horizontaux superficiels et 28 verticaux,
généralment 200-0 m) obtenus par l’auteur en novembre 1969, dans une aire dont
les coordonnées sont, Nord: 36°19'S, Sud: 38°05'S, Est: 42°58'W et Ouest: 57°39'W.

La faune a été analysée des points de vue systématique et distributif. Neuf especes
ont été trouvées en tout: Limacina helicina, L. retroversa, L. inflata, L. bulimoides,
Clio pyramidata, Cl. cuspidata, Creseis sp., Diacria sp. et Cavolinia sp.

Cette étude est une des premières investigations sur les Ptéropodes de cette partie
de l’Atlantique Sud.

En se basant sur les espéces enregistrées, on a examiné l’hydrologie superficielle
de la zone en question. L’auteur en conclut que les 4 masses d’eau connues pour ce
secteur de l’Atlantique sud-Öccidental, peuvent être parfaitement délimitées par
l’usage des Ptéropodes trouvés. Par conséquent, ces mollusques planctoniques sont
d’excellents indicateurs hydrologiques.

тат изучения Крылоногих (Pteropoda

Thecosomata), 28 горизонтальных-по-
верхностный глубины 200-Ом), собран-
ой части Атлантического океана, в
щие широты и долготы: 36°19" южн.,
систематики и распределения, всего

дов: Limacina helicina, L. retroversa, L. inflata, Г. bulimoides, Clio

pyramidata, CL. | cuspidata, Creseis sp., Diacria sp. и о sp.
Настоящее исследование-одна из первых работ no Крылоногим этой части
К е THO! гидрологии, сделанные
В т к заключению, что четыре
дные четко разграничиваются при
что эти моллюски могут быть

гидрологические, индика-

MALACOLOGIA, 1971, 11(1): 141-170

THE BULINUS NATALENSIS/TROPICUS COMPLEX
(BASOMMATOPHORA: PLANORBIDAE) IN SOUTH-EASTERN AFRICA:
I. SHELL, MANTLE, COPULATORY ORGAN AND CHROMOSOME NUMBER

D.S. Brown”, G. Oberholzer” and J. A. Van Eeden”
ABSTRACT

Bulinus natalensis (Küster) of southern Africa has been regarded as distinct
from or as synonymous with B. tropicus (Krauss) in different recent publications;
some populations have been classified as intermediate. B. natalensis has been
included in the B. truncatus (Audouin) species group, which is associated with
the transmission of human schistosomiasis in northern Africa. Therefore clar-
ification of the taxonomic status and identification of B. natalensis is important.

The present paper describes observations on the shell, mantle and copulatory
organ in 86 samples from populations belonging to the Bulinus natalensis/tropi-
cus complex, collected mostly in Natal province, South Africa, and in one sample
of B. truncatus from Egypt. Quantitative data are given for 4 shell characters
(length of spire, type of columella and umbilicus, presence of periostracal la-
mellae) and 2 anatomical features (mantle pigment and copulatory organ) studied
in nearly 6,000 snails. Length of spire was expressed as a ratio, and other
features were classified in 3-4 categories, each awarded a score of 1, 2, 3, or
4 points. This numerical scoring provided a convenient system for recording
data and evaluating variation.

Many samples had distinctive characters; there were statistically significant
differences in the length of the spire between samples obtained from different
stations onthe same lake shore, and between samples collected at different times
in a locality that underwent a drastic ecological change. However, both intra-
and inter-sample variation is apparently continuous.

A basic haploid number of 18 chromosomes was observed for 17 localities
sampled, in conformity with previous cytological observations on the Bulinus
natalensis/tropicus complex.

There appear tobe no clear differences between the species Bulinus natalensis,
B. tropicus and B. zuluensis, yet for certain features variation is correlated
and shows a geographical pattern. Shells resembling B. natalensis and B, zulu-
ensis were obtained most frequently on the coastal region of Natal; these popu-
lations were generally characterised by the depressed spire, twisted columella,
narrow umbilicus, poorly developed periostracal lamellae and the presence of
some partially or wholly aphallic individuals.

INTRODUCTION

The African freshwater genus Bulinus
is the subject of intensive study because
some species serve as intermediate
hosts in the transmission of human and
bovine schistosomiasis. В. natalensis

(Küster) and B. tropicus (Krauss), both
described from South Africa, have been
regarded either asdistinct species (Con-
nolly, 1939; Mandahl-Barth, 1965) or as
synonyms (Mandahl-Barth, 1957; De
Azevedo etal., 1961). A considerable
number of populations were classified

1 British Medical Research Council, c/o Experimental Taxonomy Section, Zoology Department,
British Museum (Natural History), London, S.W. 7.

Potchefstroom Division of the Bilharzia Research Group of the South African Council for Scien-
| tific and Industrial Research, Potchefstroom University, Transvaal, Republic of South Africa.

(141)

142 BROWN, OBERHOLZER AND VAN EEDEN

as “intermediate” by Brown et al. (1967)
according to the shape of the mesocone
on the first lateral radular tooth. It is
important to resolve the uncertainty sur-
rounding the taxonomic status and iden-
tification of B. natalensis because this
species was included by Mandahl-Barth
(1965) inthe B. truncatus (Audouin) spe-
cies group, members of which are gen-
erally regarded as potential intermediate
hosts of Schistosoma haematobium. Fur -
ther information on B. natalensis is
given by Oberholzer, Brown & VanEeden
(1970) who report on the radula of the
B. natalensis/tropicus complex and by
Brown, Oberholzer & Van Eeden (1971)
who present biogeographical and other
data and discuss the combined findings.

This paper describes the intra- and
inter-population variation in the shell,
mantle pigmentation and copulatory or-
gan observed in nearly 6,000 snailsfrom
86 localities in south-eastern Africa.
One sample of Bulinus truncatus from
Egypt was also studied. The majority
of population samples were collected in
Natal province, Republic of South Africa
(see Brown et al., 1971, for a descrip-
tion of the area). Particular attention
was paid to the districts in Natal that
include the type localities of B. natal-
ensis and B. zuluensis Melvill & Pon-
sonby; both these species and also B.
tropicus are identifiable in our material
(Figs. 3a-f; see also Brown etal.,
1971, Fig. 4). The shell features stud-
ied, spire length, columella, umbilicus
and costulation, were chosen for the
following reasons. According to the
original descriptions, the shells of B.
tropicus, natalensis and zuluensis differ
in the length of the spire, whichis longest
in tropicus and shortest in zuluensis.
The shape of the columella (Fig. 3 e,f)
is characteristic of natalensis according
to Krauss (1848) and Connolly (1939).
Our own experience suggested that an
open umbilicus and lamellae of perio-
stracum were most frequent in popula-
tions resembling B. tropicus. Variation
in mantle pigment may possibly be of
taxonomic value as the genetic inherit-

ance of dark spots has been demon-
strated (De Larambergue, 1939) in Bu-
linus contortus (Michaud). Aphallic in-
dividuals, i.e., lacking the copulatory
organ, have been found almost exclu-
sively in the species groups of В. trunca-
tus and B. natalensis (Mandahl-Barth,
1957, 1965; Brown et al., 1967).

MATERIALS AND METHODS

The snails comprising each population
sample were collected from limited loci
of apparently uniform ecology. Many
habitats, such as farm dams, were so
small that it was possible to reach every
part with a hand-net. In larger water-
bodies each sample was taken from a
restricted area of shore, usually not
exceeding a few square metres. Brief
data on localities are given in Table 1;
samples are referred to by number in
the text. Fuller information about local-
ities is available in the records of the
Snail Research Group of the Council
for Scientific and Industrial Research,
Institute for Zoological Research, Pot-
chefstroom University. The southern
African material studied comprises 52
samples collected by D. 5. Brown and
G. Oberholzer from 1966 to 1967, 12
samples collected in 1967 by P. J. Geld-
enhuys and L. Le Hanie, 11 samples col-
lected by D. S. Brown from 1966 to 1968
and further specimens from 11 samples
originally studied by Brownet al. (1967).
The locality numbers used in the latter
publication are given in Table 1 accom-
panied by the letters BSBN; all other
numbers are accession numbers in the
Institute for Zoological Research, Pot-
chefstroom, where drawings as well as
material have been deposited.

Snails were narcotised with a solution
of menthol in chloral hydrate and fixed
in a hot solution (60°C) of 4% formalde- |
hyde (Van Eeden, 1958). After a few
days the specimens were washed in water
and transferred to a 10:1 mixture of 70% |
ethanol and 10% glycerine. Fixation in |
hot formaldehyde had the effect of loos- |
ening the attachment of the animal to the

TABLE 1.

BULINUS NATALENSIS/TROPICUS COMPLEX I 143

Quantitative data for some features of the shell and anatomy of 86 samples of the

Bulinus natalensis/tropicus complex from south-eastern Africa, and of one sample of B. trun-
catus from Egypt.

10

11

(a)

Locality
and
accession
nos. (a)

Trigo de Morais (M)
1507
Irrigation channel

Lionde (M) 11. 7.67
Pool

Trigo de Morais (M)
11. 9b.67. Pool

Lagoa Uanhlala (M)
21267
Shallow Lake

Xinavane (M)
11. 24. 67
Concrete-lined drain

Lake Sibayi 1 (N)
62.1.66

Lake Sibayi 4(N)
62.4.66

Lake Sibayi 5 (N)
62. 5. 66

Lake Sibayi 7 (N)
62. 7.66

Lake Sibayi 8 (N)
62. 8.66

Lake Sibayi 9 (N)
62. 9. 66

100

100

90

40

100

100

100

15

100

20

1.14

AAA Anatomy
Copu-
Colum-|Umbil-| Costu- Nantie latory
= icus | lation (e) organ.
(e) (e) Abnormal/
Absent
2.3 195 0
Zl 2.3 3.2 1.8 2/1
Це 28 2.8 129 1/5
2.0 2.4 Zool 1.5 0
1.6 lg 25 18 1/1

2.3 2.9 3.4 (Shells only)

2.3 259 3.4 2.5 1/0
2.5 Зы 3.5 2.7 0
2.1 2.7 3.3 2.3 16/6
2.2 2.8 3.0 3.0 0
2.4 2.7 32 2.6 0

The following abbreviations are used: Mozambique (M), Natal (N), Cape Province (CP),
Orange Free State (OFS), Transvaal (T).

Research, Potchefstroom University.
(1967).

reported on by Brown et al.

Accession numbers at the Institute for Zoological
The 11 samples additionally labelled BSBN were

The number of shells examined. Unless indicated otherwise, the number of animals dis-
sected was the same or slightly fewer.

The ratio shell length:aperture length, which is a measure of the spire.

The coefficient of variation for sample mean L:AL, i.e. , standard deviation X 100:(L:AL).

Sample mean scores. For explanation of points awarded see text and legend to Fig. 9.

Eighteen pairs of chromosomes observed.

144

BROWN, OBERHOLZER AND VAN EEDEN

Table 1 (contd. )

Locality

Sample and
no. accession
nos. (a)

12

16

17

is!

19

20

21

f
22

23

Lake Sibayi 10 (N)
62.10. 66

Lake Sibayi 11 (N)
62. 11. 66

Lake Sibayi 12 (N)
62.12.66

Umpangazi lake (N)
62.14.66. Sandy
shore with reeds

Ujengu Pan (N)
62.15.66. Muddy
shore of shallow lake

Mozi Pan (N)
62.16.66. Muddy
shore of shallow lake

Sekunti Pan (N)
62.17.66. Muddy pool

Hluhluwe, Mzinene
river (N) BSBN 33
83.4.67. Muddy pool

Nyalazi (N)
83.7.67. Farm dam

Mtubatuba (N)
BSBN 29. 83.8.67
Farm dam

Bangazi Pan 1,
St. Lucia (N)
83.12.67. Sandy
shore with reeds

Bangazi Pan 2,
St. Lucia (N)
83. 13:67.
Marshy shore

Lake Futululu (N)
83.15.67. Muddy shore

Lake Teza (N)
83.17.67. Muddy shore

Nos.
exam-
ined

(b)

10

100

68

100

100

31

100

100

100

27

18

100

58

Shell Anatomy

1.19

1.10

1.16

4.2

5. 6

4, 4

5. 0

4.2

3.6

4.0

4.9

2.9

2.2

2.3

2.9

2.0

2.5

2.4

2.5

2.3

2.6

2.8

2.3

2.9

2.9

2.4

2.3

2.8

2.7

2.2

2.4

2.4

3.0

3.0

2.6

2.8

Costu-

lation

(e)

2.9

2.9

2.8

Mantle
(e)

2.2

2.0

1.6

2.2

2.0

2.1

1.9

1.8

1.8

Copu-
latory
organ.
Abnormal/
Absent

BULINUS NATALENSIS/TROPICUS COMPLEX I

Table 1 (contd. )

Sample
no .

27

28

29

30

31

32

33

34

35

36

37

38

39

Locality
and
accession
nos. (a)

Pan near Umfolozi
river, Mtubatuba (N)
83.18.67. Shallow

muddy pool

Lake Umzingazi,
Richards Bay (N)
83.23.67. Sandy
shore with reeds

Enseleni river (N)
83.25.67. Slow-flowing
with marshy banks

Lake Cubu (N) 83. 28.67
Sandy shore

Mlalazi dam, Eshowe (N)
30.1.67. Marshy shore

Gingindlovu (N)
30.2.67. Farm dam

Inyezani river,
Gingindlovu (N)
30. 3.67. Marshy pool

Stanger (N)
30.6.67. Farm dam

Stanger (N) BSBN 12
30. 7.67
Slow-flowing stream

Wewe river, Tongaat (N)
30. 9.67. Stony margin
of large dam

Mount Edgecombe (N)
30.11.67. Farm dam

Mhlangana river,
Avoca (N) 30.12.67
Marshy pool

Port Shepstone (N)
30.15. 67
Slow-flowing stream

Glen Rosa (N)
30. 22.67. Farm dam

75

19

86

100

100

76

99

100

100

89

100

62

1.27

4.1

3.6

3.0

3.9

3.3

3.5

5.3

5.0

5.9

ZO

2.1

2.0

2.1

2.3

2.2

2.2

3. 0

3.3

2.9

2.6

2.9

2.1

2.2

2.2

3.1

Costu-
lation

(e)

2.6

1.8

2.2

he)

18

1.6

Copu-
latory
organ.
Abnormal/
Absent

2/0

4/0

(Shells only)

1/1

3/0

2/2

146 BROWN, OBERHOLZER AND VAN EEDEN

Shell Anatomy

Table 1 (contd. )

Locality
Copu-
Sample and
- Costu- latory
no. accession т Mantle
Ft lation (e) organ.
(e) Abnormal/
Absent
40 | Umlazi (N) 30. 24. 67 20 1 30% |452 112.3 35 350 2.0 0
Pool in streambed
ait Ixopo district (N) 74 ME (ESO A 2.0 2.4 Bere 0
30.25.67. Farm dam
42 | Ixopo river, Ixopo 100 (BAD 0202 1.6 1.6 2.0 0
(№) BSBN 18
30. 26.67. Marshy Pool
43 Umzimkulu (N) 100 12925238 221 23 2.3 1.9 0/1
30. 27.67. Farm dam
44 | Umzimkulu district 60 US Net || 223 Sel 2.8 28 0
(N) 30.28.67. Pool
45 |Highflats (N) 29 130016111873 ЗЕ 1.6 Dae 0
30. 31.67. Farm dam
46 |Highflats (N) 92 12.352 1115..00122.4 рр 2.8 2.1 1/0
30. 32. 67. Farm dam
47 Highflats district 100 172407 O 2 2a: 2.8 2.1 1/0
(N) 30.33.67. Pool
48 |Jolivet (N) 69 as 34372222 3.2 245 2.3 0
30. 34.67. Farm dam
49 |Renishaw (N) 97 122491336. 2.5 3.2 3.0 2.0 0
30. 35.67. Farm dam
50! Ixopo district (N) 97 7.282 225 2.4 2.6 252 0
30.36.67. Farm dam
51 Richmond district (N) 89 1.3201 1623210202 1,17 РТ 1.6 3/1
30. 38. 67. Farm dam
52 | Eston (N) 100 137015051116 9 192 2. 8 1.6 0
30.39.67. Farm dam
53 |Wewe river, Tongaat 50 1.36 (| 44} 1.6 1.5 2.4 155 1/0
(N) BSBN 9. 47.4.68
Slow-flowing stream
54 | Ladysmith (N) BSBN 34 100 1235 21/6. 032129 Zul 1.9 2 0
47.5.68. Pool
55 |Harrismith (OFS) BSBN 100 1224 16.20 2.2 2.4 1.0 2. 4 0
68. 47.7. 68. Pool
56 |Harrismith (OFS) ВВМ 62 12.307 MiGs 9) |) 221 2.0 ie 2.0 0

70. 47.19.68. Farm dam

BULINUS NATALENSIS/TROPIC US COMPLEX I

Table 1 (contd. )

Locality
Sample and
no. accession
nos. (a)
57 | Van Reenen (OFS)

58

59

60

61

62

63

64

65

66

67

68

69

70

al

47.8.68. Farm dam

Sani Pass (N)
BSBN 89. 47.9.68
Stagnant ditch

Umtata district (CP)
47.10.68. Farm dam

Ermelo (T) BSBN 87
47.12.68. Farm dam

Harrismith (OFS)
47.13.68. Farm dam

Komatipoort,
Ngwetispruit (T)
BSBN 56. 68. 2. 66
Marshy pool

Kaapmuiden (T)
68. 17. 66
Irrigation channel

Malelane, Buffelspruit
(T) BSBN 54.
68.18.66. Farm dam

Newcastle district
(N) 36.6.67. Pool

Newcastle district
(N) 38.12.67. Pool

Dundee district (N)
38.21.67. Pool

Dundee district (N)
38.26.67. Farm dam

Ladysmith district

(N) 38. 38.67. Farm dam

Estcourt district (N)
38.74.67. Slowly
flowing water in swamp

Newcastle district

(N) 37.15.67. Farm dam

Nos.
exam-
ined

(b)

62

98

80

99

94

100

50

100

78

35

45

99

92

55

46

Shell Anatomy

1. 26

1. 46

1.25

2.1

2.0

2.2

2.4

2.0

2.3

2.1

2.4

1.4

2.4

2.3

2.5

Costu-
lation

(e)

1.8

147
Copu-
Mantle latory
(e) organ.
Abnormal/
Absent
2.2 1/0
JE 0
2.3 0
22 0
220 1/0
1.7 1/0
1.6 0
1.0 0
08) 0
2.4 0
PAS PE 1/0
2.3 1/0
DNS 1/0
1.9 2/0
Qe 0

148

BROWN, OBERHOLZER AND VAN EEDEN

Table 1 (contd. )

Locality

Sample and

no.

72

74

75

76

AT,

78

79
80

81

82

gal

84

85

86

87

| (№) 37. 27. 67.

accession
nos. (a)

Kliprivier district
Farm dam

Kliprivier district
(N) 37.48.67. Farm dam

Kliprivier district
(N) 37.65.67. Farm dam

Bergville (N)
37.75.67. Farm dam

Mooirivier district
(N) 37.109. 67
Slowly flowing stream

Kwa Mashu, Durban
(N) BSBN 63. 47.6.68
Pool in quarry

Umhlatuzani river,
Durban (N) BSBN 2.
47.1.68. Muddy pools

Cairo, Egypt 47.17.68

Bisana (CP) BSBN 7.
47.3.68. Pool

Lydenburg (T)
BSBN 16. 47.18.68
Stream

Newcastle (N) BSBN 6.
47.2.68. Pool

Potchefstroom district
(T) 47.14.68. Pool

Ixopo district (N)
47.16.68. Farm dam

Nottingham Road
district (N)

47.15.68. Farm dam

Frankfort district
(OFS) 47.11.68.
Farm dam

Ifafa Beach (N) Pool

Nos.
exam-
ined

(b)

73

59

51

67

60

46

70

20
20

20

20

20

20

20

20

20

Shell Anatomy

1. 30

4.3

4.6

4.7

3.3

5.1

5. 8

1.6

1.7

1.8

2.2

1.0

2.1

1.2

2.4

Mantle
(e)

2.1

1.7

1.8

Copu-
latory
organ.
Abnormal/
Absent

1/0

1/0

1/0

BULINUS NATALENSIS/TROPICUS COMPLEX I 149

Shell, so that it was usually possible to
extract the animal easily. Empty shells
were numbered and the animals stored
separately. Techniques employed in the
examination of the shell are described
below.

2mm

SHELL
Methods of observation

Between 4 and 100 shells exceeding
4.0 mm length were studied from each
locality. When more than 100 specimens
were collected a sub-sample was se- = Ww Ù
lected that represented the range inindi-
vidual size and included similar num- FIG. 1. Dimensions of the shell illustrated
bers of snails from different parts of for a specimen of Bulinus natalensis from
the size range. In some localities near Lake Sibayi, Natal (7). L=shell length; UL=
the coast Bulinus natalensis was col- ultimate whorl length; AL = aperture length;
lected together with young specimens of W = shell width.

_--R(3) UL/W:124 . RB), L/AL=1:24

-X(61), UL/W=1-25

(0)
O

(61), AL/L- AL =

A --X(13), AL/L - AL =

D
O

5

NUMBER OF SNAILS

o)

15 16 17 18 19

12 3
UL

14 12 13 -4
LAL
30 40

ALL- AL

50 6:0 7:0 8:0 9:0

FIG. 2. Bulinus natalensis/tropicus complex. Frequency distribution of shell ratios in 2
samples: 100 shells from Lake Sibayi, Natal (13), and 97 shells from Harrismith, Orange Free
State (61). The majority of shells from the latter locality have longer spires than do the shells
from the former locality. The ratios given are: (1) Length of ultimate whorl to shell width
(UL:W), a ratio that is almost identical in the 2 samples; (2) shell length to aperture length
(L:AL), that shows a significant difference between the 2 samples; (3) aperture length to spire
{ie AL:(L-AL), a very sensitive index of spire length, in that depressed shells give high
values.

150

B. globosus® (Morelet) that were similar
in the shape of the columella (Brown
et al., 1971, Pl. 1, Fig. 13). The 2 spe-
cies could be separated according to
the more elongated aperture and glos-
sier texture of B. globosus, though the
identity of doubtful snails was confirmed
by the examination of apical sculpture
and the kidney.

Shells were measured with sliding
callipers from drawings made at a
table-top magnification of X 12 by means
of a Wild dissecting microscope equipped
with a drawing tube. Shells were ori-
entated so that all of the spire was visi-
ble, and the outer lip was seen with a
minimum of the outer surface of the
whorl (Fig. 1). Preliminary observa-
tions were made in order to detect any
personal bias in measurements and to
select a ratio as an index of shell shape.

Two observers (Brown and Oberhol-
zer) made 3 replicate sets of drawings
and measurements of 10 shells from
Buffelspruit, Transvaal (64). Measure-
ments were made of shell length (L),
ultimate whorl length (UL), aperture
length (AL) and shell width (W). The
first line constructed on each drawing
(Fig. 1) was a longitudinal axis passing
through the shell apex and the upper
end of the columella; this line passed
along the length of the columella, or cut
across the aperture, according to the
orientation of the ultimate whorl in re-
lation to the rest of the shell. Four
lines were constructed at right angles
to the longitudinal axis passing through:
the apex, the suture at the beginning
of the ultimate whorl, the attachment of
the upper lip to the whorl, and the base
of the aperture. These lines demarcated
the length (L), aperture length (AL) and
the ultimate whorl length (UL). Differ-

3

BROWN, OBERHOLZER AND VAN EEDEN

ences between personal means were
significant for W and UL, but not for L
or AL. The 99% confidence intervals
for the means of L and AL for each of
the 10 shells, calculated from the com-
bined measurements of both observers,
varied between +0.52 and +1.01 (ex-
pressed as percentages of the mean)
and were less than+1.00% for 15 out of
the 20 mean values. This may be re-
garded as an acceptable experimental
error.

A sample of 100 shells having de-
pressed spires (13; Lake Sibayi, Natal),
and a sample of 94 shells generally with
longer spires (61; Harrismith, Orange
Free State), were compared in respect
of the ratios L:AL, UL:W and AL:
(L-AL) (Fig. 2). The sample means for
UL:W were respectively 1.24 and 1.25
and the frequency distributions of the
individual values are practically iden-
tical, but the samples differ clearly in
the means and frequency distributions
of L:AL and AL:(L-AL). The former
ratio, lying between 1 and 2, is pro-
portional to the spire length. The latter
ratio is a more sensitive index of de-
pression of the spire, as it approaches
infinity as (L-AL) tends towards zero,
with the result that values for depressed
shells are very high in comparison with
long-spired shells. However, the distri-
bution of AL: (L- AL) may be extremely
skewed (Fig. 2, sample 13) and such
ratios are unsuitable for simple statis-
tical treatment (Simpson, Roe € Lewon-
tin, 1960). Accordingly, the ratio L:AL
was selected as a satisfactory index of
shell shape for general use.

The columella of each shell was a-
warded a score of 1-4 points according
to whether it was concave, straight,
twisted or twisted and reflected (Fig.

A member of the Bulinus africanus group (Mandahl-Barth, 1957), which is characterised by the

presence of a “truncate” columella, a microsculpture of nodules on the apex and a ridge on the

ventral surface of the kidney.

4 Krauss (1848) described Bulinus natalensis as having a somewhat bent (etwas gebogene) colum-

ella, while Connolly (1939) referred to a “twist”.
which is employed in the present paper.

“twisted”,

Mandahl-Barth (1957, 1965) used the term

BULINUS NATALENSIS/TROPICUS COMPLEX I 151

HHI
ИИ
1] H N | |

i}

|| || \
ШИ т
НУ

y |! \ CIN) | АА UW Vs
If ЛИН | | | A ZI] у AN I If AN NA NIN
) IN й Mi) j I MA

el

N

== 7 /
=== 7 и
ФЕ Y
| e

W

| FIG. 3. Bulinus natalensis/tropicus complex. Columella and umbilicus. Shells representative
of B. tropicus (a, b), B. natalensis (c-e) and B. zuluensis (f). Types of columella: concave
(a); straight (b-d); twisted (e); twisted and reflected (f). Types of umbilicus: open (g); semi-
open (h); rimate (i); closed (j). The scale line represents 5 mm (a-f) or 2.5 mm (g-j).

152 BROWN, OBERHOLZER AND VAN EEDEN

@ № м,
III A MT

Y,

Wat

27
===

== =~

AS N

===

III mn — = AE
AZ
III

\
SS

S =
\

FIG. 4. Bulinus natalensis/tropicus complex. Types of ornamentation: well developed lamellae M
over transverse ribs (a); moderately developed lamellae (b); no lamellae but with some trans- M
verse ribs (c); nearly smooth (d). The scale line represents 5 mm.

3, a-f) The umbilicus was awarded Transverse ornamentation on our shells ©
1-4 points according to whether it was consisted of more or less regular ribs ©
open, semi-open, rimate, or closed (Fig. that were sometimes overlain by lamel-

3, g-j; Brown et al., 1971, Pl. 1, Fig. 15). lae of periostracum varying greatly in

BULINUS NATALENSIS/TROPICUS COMPLEX I 153

LOCALITY 54

50 60 70
SHELL LENGTH IN MM

80 90 100

LOCALITY 77

5.0 60 70 80 90 10 0
SHELL LENGTH IN MM

development; each shell was awarded 1-4
points according to whether it possessed
well-developed lamellae, moderate la-
mellae, ribs but no lamellae, or was
nearly smooth (Fig. 4, a-d; Brownetal.,
2971, Pl. 1, Fig. 16).

Spire length

Intra-sample variation in the ratio
shell length/aperture (L:AL), Some of

our samples showed a tendency for the
spire to be relatively longer in large
shells than in small ones (Fig. 5; local-
ities 68, 77). However, atany particular
shell length there was considerable var-
iation in L:AL and high values were
scattered over much of the size range.
In other samples there was no obvious
correlation between L and L:AL (Fig. 5;
locality 54) perhaps because of a smal-
ler size range.

Sixteen of our samples were each
divided into 2 approximately equal parts,
‚ one containing small shells and the
| other large ones. The mean L:AL for
‚ each sub-sample was calculated and
| differences between the means in each
| pair of sub-samples were subjected to
Га t-test of significance. In all but one
| pair of sub-samples, the mean for the

17}
LOCALITY 68

50 SOTO 80 90 100. mo 120
SHELL LENGTH IN MM

FIG. 5. Bulinus natalensis/tropicus complex.
Ratio between shell length and aperture length
(L:AL) plotted against L for individual shells
in 3 samples: 100 shells from Ladysmith,
Natal (54); 99 shells from Dundee, Natal (68);
48 shells from Kwa Mashu, Durban (77). The
horizontal scales are not uniform.

larger shells was the greater. Differ-
ences were highly significant (P = .01
or less) for 5 samples (e.g., locality
77, Fig. 5), of moderate significance
(P = .01-.05) for 2 samples, and insig-
nificant for 9 samples. For 3 of the
samples in which L:AL was significantly
larger in the bigger shells, mean L:AL
was calculated for shells grouped into
1 mm class intervals of L (Fig. 6); the
ratio increases nearly constantly.

These observations suggest that the
spire becomes relatively longer with
growth in at least some populations
belonging to the B. natalensis/tropicus
complex, though it is possible that nat-
ural selection also plays a part (see
Discussion). Evidently, L:AL for shells
of different sizes should be compared
with caution, yet we believe that com-
parisons between our sample means for
L:AL are meaningful, because many
samples have similar means and ranges
for L (see Fig. 8; 37 samples have mean
L between 6 and 7 mm).

The highest coefficient of variation
(V = standard deviation expressed as a
percentage of the mean) for sample mean
L:AL was 7.8 (46 shells from locality
77, Durban); the majority of our samples

154 BROWN, OBERHOLZER AND VAN EEDEN

16

50 60 70

FIG. 6. Bulinus natalensis/tropicus complex.

(L:AL) plotted against L in 3 samples:
(61); Dundee, Natal (68).
of L.

RN
D bs

NUMBER OF SAMPLES
O

On SB DO œ

307 3:5 14.0 0259050557860 651 70 75
у

FIG. 7. Bulinus natalensis/tropicus complex.
Frequency distribution of the coefficient of
variation (V) for the sample mean values of
the ratio between shell length and aperture
length (L:AL).

had V less than 6.0 (Fig. 7). The maxi-
mum values lie within the range com-
monly obtained, according to Simpson
et al. (1960, in taxonomically homo-
geneous biological material. The distri-

80
SHELL LENGTH

——= e

90 100 110 120 180
IN MM

Ratio between shell length and aperture length
Huhluwe, Natal (19); Harrismith, Orange Free State
Indicated numbers of shells are grouped in 1 mm class intervals

bution of L:AL plotted in relation to L
is shown in Fig. 5 for the most varied
sample (locality 77), and for 2 samples
having the greatest intra-sample ranges
for L:AL (localities 54, 68). These
ranges are 1.16-1.65 (V = 6.03) for 100
shells from Ladysmith, Natal (54) and
1.20-1.70 (V = 6.50) for 99 shells from
Dundee, Natal (68). Part of the varia-
tion in the latter sample is due to the
wide size range included and to the
correlated increase between L:AL andL
(Fig. 6). The contribution from this
source of variation seems to be small
in the sample from locality 54, which
includes a much smaller size range and
has widely scattered values for L:AL
(Fig. 5). On inspection, the distribution
of L:AL in Fig. 5 does not suggest that
there are significant discontinuities in
any sample, though the highest value for
locality 54 is somewhat isolated. In view
of these scatter diagrams and ofthe val-
ues for V it appears that these samples,
though exceptionally variable, should be
regarded as taxonomically homogeneous.

BULINUS NATALENSIS/TROPICUS COMPLEX I 155
5

>
45 LSib15
1:6 92
= 76
72
4
1:5 À 26| | 53
40 44 ai 78

=)
SS п | 3
NE 3
FL
<
uJ
>

13
uJ
=)
a
>
<
и

1-2

22
1-1 25
28

SHO) 60

FIG. 8. Bulinus natalensis/tropicus complex.

70 80 90
SAMPLE MEAN SHELL LENGTH IN MM

58
68
O
51 52
46 oT
81
64
75
83
38

10:0 11:0

Sample mean values for the ratio between shell

length and aperture length (L:AL) plotted against sample mean L. Numbers refer to localities
listed in Table 1. Ranges of L:AL for individual shells are represented by vertical lines; many
samples having the same mean L have overlapping ranges for L:AL, giving continuous lines. A
single mean value is given for 9 samples from Lake Sibayi, Natal (6-14).

Total variation and inter-sample dif-
ferences in the ratio shell length/ aper-
ture length (L:AL). The extreme indi-
vidual values for L:AL obtained from
5,874 shells were 1.00 and 1.77 (Brown
et al., 1971, Pl. 1, Figs. 8 & 12). Values
of 1.08 and 1.70 have been reported for
Bulinus tropicus (Stiglingh, Van Eeden &
Ryke, 1962; Stiglingh, 1966). Sample
means varied between 1.10 (16, Ujengu
Pan, northern Natal) and 1.56 (58, Sani
Pass, Natal).

For a population in which L:AL is re-

lated to L, the mean L:AL for a sample
will be related to mean L and conse-
quently some samples of large shells
have high mean values (Fig. 8). How-
ever, populations with depressed shells
may never reach such a great mean L
as do long-spired populations, and in
this case Fig. 8 would give an exagger-
ated impression of the increase of L:AL
with L. In fact, the 3 highest values of
L:AL (samples 5, 58, 77) occur in the
middle of the range of L, where there
are many Samples of similar mean shell

156 BROWN, OBERHOLZER AND VAN EEDEN

length. Each of these 3 samples was
compared with one having similar mean
L, but a smaller value of L:AL, i.e.,
sample 5 with 85, 77 with 61, 58 with
81; the difference for L:AL in each pair

NUMBER OF SAMPLES
o
e
œ
n
o
w
о
w
e

COPULATORY ORGAN

4 4 L —
14 1.5

1-2 13
MEAN SCORE

FIG. 9. Bulinus natalensis/tropicus complex.
Frequency distributions of sample mean
scores for features of the shell, mantle and
copulatory organ (Table 1). A single mean
value is given for all samples from Lake
Sibayi, Natal (6-14).

of samples is highly significant (P =
<.01). However, statistically signifi-
cant differences in the shell may be
readily demonstrated between popula-
tions of freshwater snails, andthe biolo-
gical importance of such differences
should be evaluated with a knowledge of
many populations. In the present case
there appear to be no discontinuities
suitable for taxonomic purposes, be-
cause of the extensive overlap between
ranges for L:AL in different samples,
and the nearly continuous distribution of
sample mean values for L:AL (Figs. 8,9).

Significant differences in spire length
were found even between some samples
collected from different stations on the
shore of Lake Sibayi, Natal (6-14). The
majority of shells in the 9 samples ex-
amined have depressed spires and sam-
ple mean L:AL varies narrowly between
1.14 and 1.26, yet intra-sample varia-
tion is so small that differences between
some pairs of means are highly signifi-
cant (P =<.01).

A significantdifference in spire length
was observed between 2 samples col-
lected at different times from Tongaat,
Natal:

No. 53, 7 July, 1964, n= 50, mean
L:AL=1.36 (standard deviation 0.0596);
No. 35, 9 May, 1967, n = 100, mean
L:AL=1.27 (standard deviation 0.0633).
The probability of observed difference
in L:AL being obtained by chance is
<0.01. Sample 53 was taken from dense
vegetation in a slowly flowing stream
and sample 35 from stones at the edge
of the small lake that was later formed
by the damming of this stream.
Populations having the most depressed

Key to scores: 1 2 3 4

Columella Concave straight twisted twisted and reflected

Umbilicus open semi-open rimate closed

Costulation well developed moderately no lamellae nearly smooth
lamellae over ribs developed lamellae

Mantle dark medium pale -

Copulatory organ normal abnormal absent -

BULINUS NATALENSIS/TROPICUS COMPLEX I 157

Transvaal

PRETORIA

(0

LESOTHO

SHEPSTONE

Eastern Cape

59

9

e
UMTATA

FIG. 10. Bulinus natalensis/tropicus complex.

\
\. MOZAM (BIQUE

<

SAMPLE MEAN SCORE
© 1.50 - 1.59
(B1.40 - 1.49
O 1.30 - 1.39
@ 120-129
O 110-119

Distribution of samples, showing the sample

mean values for the ratio between shell length and aperture length (L:AL). It is seen that the
lowest values (samples having the most depressed spires) are concentrated near the coast of

Natal. Locality numbers are those given Table 1.

Spires, i.e., mean L:AL<1.20, were found
only in the coastal region of northern
Natal (Fig. 10; Nos. 8-12, 15, 16, 23, 25,
28, 31, 32). However, moderately de-
pressed populations with mean values
for L:AL lying between 1.20 and 1.29

were obtained in eastern Cape (59),
Orange Free State (55), Transvaal (60)
and Mozambique (2), while unusually
long-spired populations having mean
L:AL>1.50 were obtained from eastern
Cape (80), Durban (77), Sani Pass (58)

158 BROWN, OBERHOLZER AND VAN EEDEN

CONCAVE | STRAIGHT TWISTED
COLUMELLA

| TWISTEDREFLECTEN

ZZ m 3

UMBILICUS

LAMELLATE MOD. L | SMOOTH |

FIG. 11. Bulinus natalensis/tropicus com-
plex. Intra-sample variation in 3 shell fea-
tures. Each horizontal bar represents the
number of samples, indicated at the right
margin, in which a particular range of cate-
gories was represented.

and Mozambique (5).
Columella

There were some shells having a
twisted and reflected columella (Fig. 3,
f) in 43 population samples; 23 of these
also contained examples of all the other
3 types of columella, and 20 samples
included shells of either the twisted or
straight types (Fig. 11). Shells having a
concave columella (Fig 3, a) were pre-
sent in 58 samples; 23 of these as al-
ready pointed out also contained exam-
ples of all the other 3 types, 31 samples
included shells with either straight or
twisted types, and 4 samples comprised
straight as well as concave types. Thus,
no sample of shells included less than
2 types of columella, and in every sam-
ple the types represented were in adja-
cent categories, i.e., where there were
3 types they were 1, 2 and 3, or 2, 3 and
4, The types of columella here recog-

nised are connected by continuous vari-
ation, and intra-sample variation seems
to be continuous.

The frequencies of the various types
of columella varied greatly between
samples (Table 1, Fig. 9); the greatest
sample mean score was 3.0 (i.e., a
large proportion of twisted columellae)
for 20 shells from Newcastle, Natal (82)
and the smallest value was 1.4 (i.e., a
preponderance of the concave type) for
98 shells from Sani Pass, Natal (58).
The frequency distribution of the sample
mean scores is nearly continuous with a
marked concentration of values at the
middle of the range (Fig 9). No geo-
graphical pattern was apparent in the
variation of the columella.

Umbilicus

The umbilicus, like the columella, was
highly variable within population sam-
ples, all 4 categories being represented
in 48 samples (Fig. 11). In some sam-
ples the umbilicus was closed in small
shells and open in large ones, but in
other samples the umbilicus was open
or closed over the whole size range.

Mean sample scores (Table 1) varied
between 1.1 (i.e., a large proportion of
open umbilici) in 100 shells from Er-
melo, Transvaal (60), and 3.5 (i.e., a
large proportion closed umbilici) in 20
shells from Umlazi, Natal (40). The
frequency distribution of sample mean
scores is continuous (Fig. 9) showing a
concentration of values near the middle
of the range, and secondary peaks near
each end of the range. Populations hav-
ing a high proportion of closed umbilici
(score 2.6-3.5) were commonest in east-
ern Natal (Fig. 12), whereas populations
having a high proportion of open umbilici
(score 1.0-1.7) were found more fre-
quently in the southern and western parts
of the sampling area.

Costulation

Intra-sample variation was less, ac-
cording to our system of scoring, than
in the columella or umbilicus; only 9
samples included examples of all 4 cat-

BULINUS NATALENSIS/TROPICUS COMPLEX I 159

Transvaal

PRETORIA.
bs E ee м / ro
= y sn ;
‚ ES
Orange Free State 0 Fe

LESOTHO

| |
= O

‚Eastern Cape

HIG. 12.

% PORT SHEPSTONE

Bulinus natalensis/tropicus complex.

‘MOZAMBIQUE
%
>
O me

>

UMBILICUS

SAMPLE MEAN SCORE
O 26-35
O 18-25
О 10-1:7

100 Km

Distribution of samples, showing the variation

in the size of the umbilicus. Key to scoring system: 1, open; 2, semi-open; 3, rimate; 4, closed.

egories of costulation and 3 categories
were represented in 44 samples (Fig. 11).
Periostracal lamellae were present in
75 samples, in some of which only the
small shells or the upper whorls of larg-
er specimens were lamellate; in other
Samples lamellae were present on shells
of all sizes. Variation in the develop-

ment of the lamellae on different parts
of the shell of Bulinus tropicus led Stig-
lingh (1966) to consider the possibility
that the formation of lamellae might be
directly influenced by environmental
conditions. However, variation could
also be due to the wearing away of la-
mellae in nature or during the prepar-

160 BROWN, OBERHOLZER AND VAN EEDEN
Transvaal \
1
|
1
|
| A i
ö E =
Lino conve Be
e a
PRETORIA 57, 5 oe
AG N ER,
ri \
| y i
H |
® o / 2
о sn it
E р Lie
| ;
ES a
| Orange Free State $
e
o; ©
. e.»
= va q.
be a Fe e @ ©
\ ann
> N
A > e. DER
|.” ME Oo __
LESOTHO г e \
A De
| A
4 RS &
2 E - я Фо a e
р 2%. COSTULATION
À г ee. SAMPLE MEAN SCORE
et @ 1.00-1.89
©
/ PORT SHEPSTONE O 1.90-2.79
Eastern Cape e 2.80-3.79
500m
UMTATA *
FIG. 13. Bulinus natalensis/tropicus complex. Distribution of samples, showing the variation

in shell ornamentation.

ation of shells for examination, and it is
noteworthy that lamellae are often de-
tectable near the suture on large shells
having the rest of the surface smooth.
Sample scores (Table 1) varied be-
tween 1.0 in 20 shells from Nottingham
road, Natal (85) that all have well devel-
oped lamellae, and 3.5 in 15 more or

Key to scoring system:
ribs; 2, moderate lamellae; 3, no lamellae; 4, nearly smooth.

1, well developed lamellae over transverse

less smooth shells from Lake Sibayi, |
The frequency distribution of |

Natal (8).
sample scores (Fig. 9) is continuous

and skewed towards the upper limit of |
the range, i.e., a high proportion of

samples contained many shells having
poorly developed lamellae.
Lamellae were lacking from all shells

BULINUS NATALENSIS/TROPICUS COMPLEX I 161

COLUMELLA
3-0 e
ео о 14
2.5 o. . .
eo. e...0p o
De о ecco%e © с

+ UMBILICUS : hi
4 г 7 eee
ion, a
2.5 . .
| 3 Se. De
2-01 . Ber: Sa u >
aee
5 y de 5
С E? ® e
1-1 1-6
L:AL

3.5 COSTULATION

UNAS 16
3-01 о
2 e 2 rae e с
2) о о ere . 7 .
2 я г 5
1:5. . ee a
SÍ == = И oe an
1-1 1:2 123 1-4 1-5 1-6
L: AL
3.0, COLUMELLA e
> de 17
ze! à eo ee =
e в * eDe e
. > ees e s e
te el
2-0 : . Arto. e
20 Se
1.5) sd à
№5 2.0 2-5 3:0 3.5
UMBILICUS

FIGS. 14-17. Bulinus natalensis/tropicus complex. Correlated variation in pairs of shell fea-
tures. Each point represents a sample; sample mean values for the ratio between shell length
and aperture length (L:AL) plotted against sample mean scores for the other features.
А, В, С: samples from the district of the type locality of В. natalensis (localities 36, 37, 77).
D: mean value for 9 samples from Lake Sibayi (localities 6-14) representing B. zuluensis.

E: Bulinus truncatus from Egypt (locality 79).

in 10 samples, all from localities situ-
ated near the coast of northern Natal:
Lake Sibayi (6, 8-10, 12-14), Lake Um-
pangazi (15), Mozi Pan (17), Lake Cubu
(29). Although lamellate shells were
present in a few samples from this re-
gion (Fig. 13), strongly lamellate popu-
lations (Sample mean score 1.00-1.89)
were found more commonly at higher
altititudes.

Correlations between shell characters

The sample mean values (Table 1)
for each of the 6 possible pairs of char-
acters were plotted on graphs; a single
mean value calculated for each charac-
ter represented all 9 samplesfrom Lake

Sibayi (6-14). The data have the ap-
pearance of an elliptical cloud, suggest-
ing a relation between the 2 variables,
in the case of 3 pairs of characters;
L:AL and columella, L:AL and umbilicus,
columella and umbilicus (Figs. 14, 15,
17). For the other 3 pairs of characters
the wider scatter of the data suggest
that the variables are unrelated (Fig.
16). Correlation coefficients were cal-
culated and confirmed the relation be-
tween L:AL, columella and umbilicus
(Table 2), increase in L:AL being cor-
related with decreases in the scores
for columella and umbilicus. Accord-
ingly, populations with long spires (re-
sembling Bulinus tropicus) tend to have

162 BROWN, OBERHOLZER AND VAN EEDEN

TABLE 2. Correlated variations in pairs of shell characters

of the B. natalensis/tropicus complex.

Data for

shell characters are means calculated for each of
78 population samples (a single mean value was used
for the 9 samples from Lake Sibayi, Natal).

ee

Correlation
coefficient (r)

Probability

———— ee ———

L/AL: columella
L/AL: umbilicus
L/AL: costulation
columella: umbilicus
columella: costulation

0. 423 0. 001
0.437 0.001
0. 080 0.100
0. 500 0.001
0.027 0.100
0.

256 0. 05-0. 02

umbilicus: costulation

a concave columella and an open umbil-
icus, while populations having a de-
pressed shell (resembling B. natalensis
or B. zuluensis) generally have atwisted
columella and a closed umbilicus. Vari-
ation in surface ornamentation showed
no significant correlation with any other
shell feature, although all the samples
without lamellae had depressed shells.

MANTLE

Each mantle was awarded a score of
1, 2, or 3 points according to whether
the pigmentation was dark, moderately
dark, or pale. Pigmentation comprised
superficial dark spots, varying in inten-
sity and sometimes absent, and an under-
lying background colour of grey, or
rarely brown. All 86 samples for which
animals were available contained exam-
ples of dark mantles, and some pale
ones were present in 59 samples. Mean
sample scores (Table 1) varied between
1.0 (i.e., all dark) for 100 animals from
Malelane, Transvaal (64), and 2.5 (i.e.,
a high proportion pale) for 100 animals
from Lake Sibayi (7). In the frequency
distribution of sample mean scores (Fig.
9), 3 darkly pigmented samples (64, 81,
84) have low values isolated from the
main body of the range, but these sam-
ples share no other distinguishing char-
acters. There appears to be no signifi-
cant pattern in the geographical varia-
tion, apart from the occurrence in Lakes

Sibayi and Umpangazi (15) of a high
proportion of lightly pigmented snails
having the living body more red in col-
our than is usual.

COPULATORY ORGAN

Each snail was awarded a score of 1,
2, or 3 points according to whether the
copulatory organ was normal, abnormal,
or absent (i.e., the animal was aphallic).
The absence of the copulatory organ
(“aphallie”) in some populations of Buli-
nus was first reported by De Laram-
bergue (1939). Some of our snails con-
tained immature stages of one or pos-
sibly more species of trematode and
were examined with particular care, as
it was observed that in some heavily
parasitised snails the copulatory organ
did not develop beyond an inconspicuous
rudiment. A demarcation between the
preputium and the penis sheath could
usually be detected in these rudimentary
organs and the vas deferens was present;
such snails were classified as normal.
Individuals regarded as abnormal (95
out of 5,740 examined) had the vas defe-
rens ending in the body wall without any
connection to the copulatory organ, which
was reduced to a blindly ending sac of
variable size lacking any subdivision
into preputium and penis sheath; in such
animals the prostate gland was unu-
sually small. This condition, which
apparently is not induced by infection

BULINUS NATALENSIS/TROPICUS COMPLEX I 163

with parasites, was described by De
Larambergue (1939: Fig. 22) as “aphal-
lie partielle”. Hamilton-Atwell (1966)
reported comparable abnormalities of
the genital system in a few individuals
from apopulationofB. “depressus Haas”
containing 96% aphallic animals.

One or more aphallic snails (totalling
47) were present in 14 samples, some of
them also containing abnormal animals.
One or more abnormal copulatory or-
gans were found in 22 other samples
(Table 1). Highest incidences observed
were 24% aphallic and 6% abnormal in
a sample of 100 animals from Nyalazi,
Natal (20), and 6% aphallic and 16% ab-
normal in a sample of 100 snails from
Lake Sibayi (9). Another sample of 100
snails from Lake Sibayi (7) contained
only 1 aphallic animal. The majority
of samples included few, if any aphallic
or abnormal individuals (Fig. 9); the
outstandingly high frequencies in 2sam-
ples (9, 20) do not seem to be taxonom-
ically significant, for sample 9 is from
Lake Sibayi, from where other samples
had low frequencies.

Aphallic snails were found only in
samples from eastern Natal and Mo-
zambique (Fig. 18), apart from the oc-
curence of a Single individual in the
Bergville district (75) near the western
border of the province. The majority
of the samples from the western and
southern parts of the area sampled con-
tained only normal animals.

CHROMOSOME NUMBER

Chromosomes were examined in dia-
kinesis figures in squashes of ovotestis
tissue and also, for some localities, in
mitotic metaphase in squashed embryos.
Eighteen bivalents or 36 chromosomes
(n = 18) were observed for all 17 local-
ities sampled (indicated in Table 1).

DISCUSSION

In some populations belonging to the
Bulinus natalensis/tropicus complex the
Spire is relatively longer in large shells
than in small ones, i.e., the ratio L:AL
|
|

increases with L, as in some other spe-
cies of Bulinus (Wright & Brown, 1962;
Stiglingh et al., 1962; Brown, 1966).
This may reflect the manner of growth
in individual shells, but it is conceivable
that natural selection might play a part
in populations with highly variable young
snails (Fig 5; locality 77, 6-7 mm) by
eliminating juveniles having depressed
Spires. Although the depressed shell
may have no disadvantage in itself, it
might be correlated with other proper-
ties, unfavourable under certain condi-
tions. In other circumstances the de-
pressed shell seems to have a selective
advantage, for lacustrine species of
Bulinus generally have a short spire
possibly adapted to present small re-
sistance to water movement in littoral
situations (see Brown et al., 1971, Dis-
cussion). It might be that the significant
differences in mean L:AL demonstrated
among samples of B. natalensis from
different stations on the shore of Lake
Sibayi are due to local variation in se-
lection pressure. Snails were collected
from stems of Juncus and Phragmites
spp. growing on sandy substrata exposed
to wave action; colonies were separa-
ted by stretches of unsuitable shore,
such as beaches lacking vegetation or
stagnant marsh, where no B. natalensis
were found. Perhaps isolation between
some colonies has allowed independent
adaptation to different degrees of wave
action. Supporting evidence for effec-
tive isolation between some colonies of
B. natalensis in Lake Sibayi is provided
by the considerable differences in fre-
quencies of aphallic animals between
collecting stations (e.g., localities 7 and
9).

Two samples collected at an interval
of 3 years from Tongaat in Natal showed
considerable morphological differences.
The first (53) was obtained from a
stream that was subsequently dammed
to form a small lake from which the
second sample (35) was taken. The
spire in the lake sample (L:AL = 1.27)
is significantly shorter than inthe stream
sample (L:AL = 1.36). The angular type
of mesocone was predominant on the

164 BROWN, OBERHOLZER AND VAN EEDEN

first lateral radular teeth of the lake
Sample, whereas the non-angular type
of mesocone was most frequent in the
stream sample (Oberholzer et al., 1970).
These differences between the samples
were possibly due to some change in the
environmental conditions that led to the
replacement of the earlier population
(identified as Bulinus tropicus by Brown
et al., 1967) by one that resembled B.
natalensis more closely.

The small but significant differences in
spire length between samples of the Bu-
linus natalensis/tropicus complex dis-
cussed above serve to demonstrate the
fact that intra-population variation is
often small in comparison with variation
within the whole taxon. Low intra-
population variation in shell features is
usual in Lymnaea peregra (Müller)”, a
snail in which variation has received
particular attention (Hubendick, 1951;
Okland, 1964). Hubendick calculated
Sample mean values for the ratio be-
tween aperture length and total length
(AL:L, in our terminology); standard
deviations were given as percentages of
sample means (s X 100:X), i.e., the co-
efficient of variation (V) used inthe pre-
sent work. In L. peregra Hubendick ob-
tained an average value for V of 1.22
(highest 2.13), while inthe B. natalensis/
tropicus complex our mean value was
4.86 (highest 7.83) indicating consider-
ably greater intra-population variation.
However, all our values for V lie within
the range commonly met within data
from taxonomically homogeneous biolo-
gical material (Simpson et al., 1960).

Variation in the spire, columella, um-
bilicus and costulationis apparently con-
tinuous both within and between our sam-
ples, which consequently might be re-

garded as representing a single variable
species. The distribution in Figs. 14-17
of samples representative of Bulinus
tropicus, natalensis, zuluensis and trun-
catus suggests that none is clearly dis-
tinguishable by means of shell features.
The one sample of B. truncatus lies
among those having the least twisted
columella (Fig. 14) and the most open
umbilicus (Fig. 15), but the values are
not outstanding. In our samples of the
natalensis/tropicus complex, variation
in the spire, columella and umbilicus is
related and a geographical pattern is
apparent to the extent that the depressed
spire and the closed umbilicus showed
some association with eastern Natal
(Figs. 10, 12). Turning to anatomical
features, aphallic individuals were ob-
tained most frequently in populations
from near the Natal coast (Fig. 18), and
in the same area there is a particularly
high frequency of the angular type of
mesocone on the first lateral radular
tooth (Oberholzer et al., 1970). Possible
causes underlying these geographical
patterns of variation are discussed, to-
gether with taxonomical questions, by
Brown et al. (1971).

Our observations on the columella,
umbilicus and costulation provide the
first quantitative data for these features
in the genus Bulinus and serve to dem-
onstrate their limitations as taxonomic
characters. Numerical scoring pro-
vided a convenient means for recording
data, but variation was continuous and
so extensive within populations that, for
each feature, 60% or more samples
contained examples of 3 or all of the 4
character categories recognised. In
the case of umbilicus and costulation,
some intra-sample variation was related

5Some authors have followed Kennard & Woodward (1926) in using pereger on the grounds that
there is no Latin adjective pereger -ra -rum and that form should, therefore, not be used.
However, peregra has continued to be employed by many authors and is acceptable in view of
Article 32 (a) (ii) of the International Code of Zoological Nomenclature (1961), which states that
incorrect latinisation should not be considered as an inadvertant error of the kind that would
justify the changing of the original spelling of a name.

BULINUS NATALENSIS/TROPICUS COMPLEX I 165

Transvaal

PRETORIA |;
Sr

O

i Eastern Cape

1590 m
O

UMTATA °

FIG. 18. Bulinus natalensis/tropicus complex.

PORT
SHEPSTONE

w
sean

@ SOME ABNORMAL COPULATORY ORGANS
@ SOME APHALLIC ANIMALS

@ APHALLIC AND ABNORMAL

O NORMAL

Geographical distribution of snails having an

abnormal copulatory organ, or no copulatory organ (aphallic).

to shell size. Costulation showed least
intra-sample variation, according toour
system of scoring. However, the taxo-
nomic value of periostracal lamellae is
reduced by the ease which they may be
rubbed away.

The majority of our samples contained
some animals having intense black spots

in the superficial tissues of the mantle,
apparently like those which De Laram-
bergue (1939: 162) found to be inherited
as a genetically dominant character in
Bulinus contortus. Many of our samples
included examples of the darkest and
palest types of mantles and various
intermediates; consequently it seems

166 BROWN, OBERHOLZER AND VAN EEDEN

that any dominance of dark pigment in
these populations is incomplete.

Among irregularities in the genital
system of Bulinus contortus, De Laram-
bergue (1939; 11) found the condition
of “aphallie partielle” (in our terminol-
ogy an “abnormal” copulatory organ) in
only 11 individuals (0.35%) out of 3,101
that he examined from natural popula-
tions. He further observed that the fre-
quency of such “abnormal” individuals
in laboratory-bred strains of predom-
inantly aphallic snails was not signifi-
cantly greater than in strains of pre-
dominantly normal snails. In the B.
natalensis/tropicus complex we obtained
the considerably higher frequency of
95 abnormal individuals (about 1.7%)
out of 5,740 examined. Half of the ab-
normal individuals occurred in samples
that contained no aphallic snails, yet the
majority of aphallic snails (44 out of 47)
and abnormal individuals (78 out of 95)
were obtained in southern Mozambique
or near the Natal coast. This geograph-
ical association between the aphallic
and abnormal conditions may indicate
some genetic linkage between them.

ACKNOWLEDGEMENTS

We are grateful to Dr. Almeido Franco
and Dr. Lidia De Medeiros (Instituto
Investigacao Medica, Lourenzo Marques)
for facilities during fieldwork in Mo-
zambique. Thanks are due to Mr. P. G.
Geldenhuys and Mr. L. Le Hanie (South
African State Health Department) for
their diligence in collecting a number of
samples describedhere. We are indebted
to Dr. G. Mandahl-Barth for the sample
of Bulinus truncatus from Egypt, Dr.
C. A. Wright (British Museum, Natural
History) for providing facilities for cyto-
logical study, Mr. D. Claugher for making
cytological preparations and Mr. V. Ham-
ilton-Atwell for preparing some dia-
grams. We thank Mrs. A. Gismann for
her careful editing. The first author is
greatful to Professor J. A. Van Eeden
for accommodation in the Institute for
Zoological Research, University of Pot-

chefstroom from 1966 to 1968. We wish
to express our appreciation for the fi-
nancial support given us by the South
African Council for Scientific and In-
dustrial Research, the Department of
Agricultural Technical Services of the
Republic of South Africa, and the Med-
ical Research Council of the United
Kingdom.

REFERENCES

AZEVEDO, J. F. DE, MEDEIROS, L.
FARO, M., GANDARA, A. & MORAIS,
T. DE, 1961, Os moluscos de agua
doce do Ultramar Portugues. 3. Mo-
luscos de Mocambique. Est. Ens. Doc.
Junta Invest. Ultramar, 31: 1-116.

BROWN, D. S., 1966, On certain mor-
phological features of Bulinus africa-
nus and B. globosus (Mollusca: Pul-
monata) and the distribution of these
species in south eastern Africa. Ann.
Natal Mus., 18(2): 401-415.

BROWN, D. S., SCHUTTE, С. Hoe
BURCH, J. B. & NATARAJAN, R.,
1967, Chromosome numbers in rela-
tion to other morphological charac-
ters of some southern African Bu-
linus (Basommatophora: Planorbidae).
Malacologia, 6(1-2): 175-188.

BROWN, D. S., OBERHOLZER, G. &
VAN EEDEN, J. A., 1971, The Bulinus
natalensis/tropicus complex (Basom-
matophora: Planorbidae) in south-
eastern Africa: 2. Taxonomy and gen-
eral discussion. Malacologia, 11
171-198,

CONNOLLY, M., 1939, A monographic
survey of the South African non-
marine Mollusca. Ann. 5. Afr. Mus.,
33: 1-660.

HAMILTON-ATWELL, V. L., 1966, The
shell, radula, pallial organs and gen-
ital system of Bulinus (Bulinus) de-
pressus Haas (Mollusca: Basommato-
phora). Unpublished Thesis, Univer-
sity of Potchefstroom. [In Afrikaans].

HUBENDICK, B., 1951, Recent Lymnae-
idae. Kungl. svenska veten. Handlin-
gay, 3(1): 1-222.

INTERNATIONAL CODE OF ZOOLOGI-

BULINUS NATALENSIS/TROPICUS COMPLEX I 167

CAL NOMENCLATURE, 1961, xvii +
176 p. London.

KENNARD, A. S. & WOODWARD, B. B.,
1926, Synonymy of the British non-
marine Mollusca. xxiv + 447 p. Brit-
ish Museum (Natural History), London.

KRAUSS, F., 1848, Die Stidafrikanischen
Mollusken. Ebner & Seubert, Stutt-
gart. 140 p.

LARAMBERGUE, M. DE, 1939, Etude de
l’autofécondation chez les Gastéro-
podes Pulmonés. Recherches sur 1’
aphallie et la fecondation chez Bulinus
(Isidora) contortus Michaud. Bull.
biol., 73: 19-231.

MANDAHL-BARTH, G., 1957, Interme-
diate hosts of Schistosoma. African
Biomphalaria and Bulinus: 2. Bulinus.
Bull. Ша НИЙ Org., 17: 1-65.

MANDAHL-BARTH, G., 1965, The spe-
cies of the genus Bulinus, interme-
diate hosts of Schistosoma. Bull.
Wld Hlth Org., 33: 33-44.

OBERHOLZER, G., BROWN, D.S., &
VAN EEDEN, J. A., 1970, Taxonomic
characters of the radula inthe Bulinus
natalensis/tropicus complex (Basom-
matophora: Planorbidae) in south-
eastern Africa. Wetenskaplike Byd-

vaes Potchefstroom Univ. В, 10: 1-58.

OKLAND, J., 1964, The eutrophic lake
Borrevan (Norway) - an ecological
study on shore and bottom fauna with
special reference to gastropods, in-
cluding a hydrographic survey. Folia
limnol. Scand., 13: 1-337.

SIMPSON, G. G., ROE, A. LEWONTIN,
В. C., 1960, Quantitative Zoology. Re-
vised ed., vii + 440 p. Harcourt Brace,
New York.

STIGLINGH, I., 1966, Further contribu-
tions to the study of Bulinus tropicus
(Krauss). Unpublished Thesis, Uni-
versity of Potchefstroom.

STIGLINGH, I, VAN EEDEN, J. A. €
RYKE, P. A., 1962, Contributions to
the morphology of Bulinus tropicus
(Gastropoda: Basommatophora: Plan-
orbidae). Malacologia, 1(1): 73-114.

VAN EEDEN, J. A. 1958, Two useful
techniques in freshwater malacology.
Proc. malac. Soc. Lond., 33: 64-66.

WRIGHT, С. A. € BROWN, D. S., 1962,
On a collection of freshwater gastro-
pod molluscs from the Ethiopian high-
lands. Bull. Brit. Mus. (natur. Hist.)
Zool., 8(6): 285-312.

ZUSAMMENFASSUNG

DER KOMPLEX BULINUS NATALENSIS/TROPICUS
(BASOMMATOPHORA: PLANORBIDAE) IN SUDOSTAFRIKA:
I. SCHALE, MANTEL, GESCHLECTSORGAN UND CHROMOSOMENZAHL

D. S. Brown, G. Oberholzer und J. A. Van Eeden

Bulinus natalensis (Küster) von Stidafrika ist in den verschiedenen neueren Ver-
éffentlichungen entweder als Synonym von В. tropicus (Krauss) oder als getrennte
Art betrachtet worden; einige Populationen sind als intermediär angesehen worden.
B. natalensis ist in die Artengruppe des B. truncatus (Audoin) gestellt worden, der
ein Überträger der Schistosomiasis des Menschen in Nordafrika ist. Deshalb ist es
wichtig, die taxonomische Stellung und Identifizierung des B. natalensis zu klären.

Die vorliegende Arbeit schildert Untersuchungen der Schale, des Mantels und des
Geschlechtsorganes von 86 Proben aus Populationen, die zum Bulinus-natalensis/
tropicus-Komplex gehören und zumeist in Natal, Südafrika, gesammelt worden sind,
und von einer Probe des B. truncatus aus Ägypten. Quantitative Daten werden für
4 Schalenmerkmale gegeben (Gewindehöhe, Beschaffenheit der Spindel und des Nabels,
Vorhandensein von Lamellen auf dem Periostracum) und für 2 anatomische Merkmale
(Mantelpigmentierung und Geschlechtsorgan), die bei fast 6000 Schnecken untersucht

worden sind.

Die Gewindehöhe wurde als relativer Wert dargestellt, und andere

Merkmale wurden in 3-4 Klassen unterteilt, die mit 1-4 Punkten bewertet wurden.
Diese zahlenmässige Klassifizierung eignete sich zum Festhalten der Daten und Be-

rechnen der Variation.

168

BROWN, OBERHOLZER AND VAN EEDEN

Viele Proben hatten ihre Eigentilmlichkeiten; es gab statistisch erfassbare Unter-
schiede in der Gewindehthe zwischen Proben, die anverschiedenen Orten des gleichen
Seeufers gesammelt worden waren, und zwischen Proben, die zu verschiedenen Zeiten
an einer Stelle entnommen worden waren, die eine tiefgreifende Skologische Ver-
änderung durgemacht hatte. Jedenfalls sind die Variationen sowohl innerhalb einer
Probe als auch zwischen den Proben kontinuierlich.

Die haploide Chromosomenzahl betrug 18 ftir 17 besammelte Fundstellen, dies
stimmt überein mit früheren cytologischen Untersuchungen Uber den Komplex Bulinus
natalensis/tropicus.

Anscheinend bestehen keine scharfen Unterschiede zwischen den Arten Bulinus
natalensis, В. tropicus und B. zuluensis, doch für gewisse Merkmale ist die Variation
korreliert und geographisch bedingt. Schalen, die wie B. natalensis und B. zuluensis
aussehen, wurden am häufigsten in der Küstengebiet von Natal gefunden; diese Popu-
lationen zeichnen sich im allgemeinen durch ein gedrilcktes Gewinde aus, eine gedrehte
Spindel, engen Nabel, schwach entwickelte Oberhaut-Lamellen, und durch das Vor-
kommen von teilweise oder ganz aphallischen Individuen.

НА.

RESUME

LE COMPLEXE BULINUS NATALENSIS/TROPICUS
(BASOMMATOPHORA: PLANORBIDAE) DANS L’EST SUD-AFRICAIN:
I. COQUILLE, MANTEAU, ORGANE COPULATEUR ET NOMBRE DE CHROMOSOMES

D. S. Brown, G. Oberholzer et J. A. Van Eeden

Bulinus natalensis (Küster) et B. tropicus (Krauss) d’Afrique du Sud, ont été con-
sidérés comme distincts ou comme synonymes dans différentes publications récentes;
quelques populations ont été classées comme intermédiaires, В. natalensis a été
inclus dans le groupe spécifique B. truncatus (Audouin), qui est en relation avec la
transmission de la bilharziose en Afrique du Nord. En conséquence, la clarification
du statut taxonomique et l’identification de B. natalensis sont importants.

La présente étude decrit des observations sur la coquille, le manteau et l’organe
copulateur dans 86 échantillons de populations appartenant au complexe Bulinus
natalensis/tropicus, récoltés surtout au Natal, Afrique du Sud, et pour un échantillon
de B. truncatus, en Egypte. Des données quantitatives ont été fournies pour 4 carac-
téres de coquille (longueur de la spire, type de columelle et d’ombilic, présence de
lamelles périostracales) et 2 traits anatomiques distinctifs (pigment palléal et organe
copulateur) étudiés sur environ 6,000 individus. La longueur de spire a été exprimée
comme un rapport tandis que les autres caractéres ont été classés en 3-4 catégories,
auxquelles on attribue 1, 2, 3 ou 4 points, Cette échelle numérique a fourni un sys-
tème commode pour enregistrer les données et évaluer les variations.

De nombreux échantillons ont des caractères distinctifs; il y a des differences
statistiquement significatives dans la longueur de la spire entre des échantillons
obtenus de différentes stations d’un méme rivage lacustre, ainsi qu’a des moments
différents dans une localité ayant subi de profonds changements écologiques. Cepen-
dant, las variation intra et inter-échantillons est apparemment continue.

Une nombre de base haploide de 18 chromosomes a été constaté pour 17 localités,
en conformité avec de précédentes observations cytologiques sur le complexe Bulinus
natalensis /tropicus.

П n’y a pas apparemment de differences nettes entre les espèces Bulinus natalensis,
B. tropicus et B. zuluensis, si ce n’est que certains caractères sont en corrélation et
montrent un modelage géographique. Les coquilles se rapportant a B. natalensis et
B. zuluensis ont été le plus souvent obtenues dans la région cotiére du Natal; ces
populations étaient généralement caractérisées par une spire déprimée, une columelle
tordue, un ombilic étroit, des lamelles périostracales faiblement développées et la
présence de quelques individus partiellement ou entierement aphalliques.

AIR

BULINUS NATALENSIS/TROPICUS COMPLEX I

RESUMEN

EL COMPLEJO BULINUS NATALENSIS/TROPICUS
(BASOMMATOPHORA: PLANORBIDAE) EN EL SUDESTE DE AFRICA:
1. CONCHA, MANTO, ORGANO COPULADOR Y NUMERO CROMOSOMATICO

D. S. Brown, G. Oberholzer y J. A. Van Eeden

En varias publicaciones recientes, el Bulinus natalensis (Küster) de Africa del Sur,
ha sido considerado ya diferente o ya sinónimo del B. tropicus (Krauss); algunas pob-
laciones han sido clasificadas como intermedias. B. natalensis ha sido incluído en el
grupo de especies del B. truncatus (Audouin), el cual está asociado con la trasmisión
de esquistosomiasis humana en Africa del norte. Por lo tanto una aclaración de la
posición taxonómica e identificación del B. natalensis es de importancia.

El presente trabajo describe observaciones hechas sobre la concha, manto y organo
copulador en 86 muestras de poblaciones pertenecientes al complejo B. natalensis,
tropicus, la mayoría colectadas en la provincia de Natal, Africa del Sur, y en una
muestra de B. truncatus de Egipto. Se dan los datos cuantitativos de 4 caracteres
conchológicos (longitud de espira, tipo de columela y ombligo, presencia de lamelas
periostricales) y 2 aspectos anatómicos (pigmento del manto y Organo copulador),
estudiados en una cantidad cercana а 6000 caracoles. La longitud de la espira fué
expresada como una relación, y otros aspectos fueron clasificados en 3 o 5 categorías
concediendo a cada una valores de 1, 2, 3, o 4 puntos. Esta cuenta por puntos provee
un sistema conveniente para registrar los datos y valorizar la variación.

Muchas muestras tienen caracteres distintivos; mostraron diferencias estatisti-
camente significantes en la longitud de la espira entre muestras obtenidas en diferen-
tes estaciones de una misma orilla lacustre, y entre muestras colectadas en diversas
oportunidades en una localidad que sufrió un cambio ecológico drástico. Sin embargo
las variaciones dentro o entre las muestras aparentemente son contínuas.

El número haploido básico de 18 cromosomas fué observado en muestras de 17
localidades, en conformidad con observaciones citológicas previas del Bulinus
natalensis/tropicus.

Pareceria no existir diferencias entre las especies Bulinus natalensis, B. tropicus,
у В. zuluensis; sin embargo para ciertos aspectos la variación esta correlacionada
y muestra un patrön geografico. Conchas semejando B. natalensis y B. zuluensis se
obtuvieron con mayor frecuencia en la region costera de Natal; estas poblaciones se
caracterizan generalmente por la espira deprimida, columela torcida, ombligo
estrecho, lamelas periostricales muy pobremente desarrolladas, y la presencia de
algunos individuos parcial o totalmente afálicos.

Voda D.

ABCTPAKT

КОМПЛЕКС (BASOMMATOPHORA, PLANORBIDAE) BULINUS NATALENSIS/TROPICUS
ИЗ ЮГО-ВОСТОЧНОЙ АФРИКИ

1. РАКОВИНА, МАНТИЯ, КОПУЛЯТИВНЫЕ ОРГАНЫ И ЧИСЛО ХРОМОСОМ
Д.БРОУН, Г.ОБЕРХОЛЦЕР И ДЖ.ВАН ИДЕН

Различные современные авторы рассматривают Bulinus natalensis (Kuster) из
южной Африки или как вид, отличный от В. tropicus (Krauss), или как его синоним.
Некоторые из популяции считались промежуточными. В. natalensis был отнесён
к группе В. truncatus (Audouin), которые связаны с трансмиссией человеческого
шистозомиазиса в Северной Африке. Позтому очень важно было выяснить
таксономическое положением и точное определение В. natalensis.

В настоящей работе рассматриваются денные по морфологии раковины,
мантии и копулятивного органа из 86 проб, полученных из популяций,
относящихся к комплексу "Вийти$ natalensis/tropicus", собранных, главным
образом, в провнции Наталь, Ю.Африка. 1 проба В. truncatus была получена

169

170

BROWN, OBERHOLZER AND VAN EEDEN

из Египта. Приводятся данные измерений 4 признаков раковины (длина
завитка, тип колюмеллы и пупка, наличие слоёв периостракума) и 2
анатомических (пигментация мантии и копулятивный орган). Было

исследовано около 6000 экземпяров моллюсков. Длина завитка выражалась в
соотношении, другие признаки были разделены на 4 категории, каждая из
которых подразделялась на 1, 2, Зи 4 степени. Такая количественная
решетка признаков являлась удобной системой для классификации моллюсков и
для оценки их изменчивости.

Многие пробы моллюсков были вполне различимы по свсим признакам. Они
имели статистически значительные различия в высоте завитка между теми,
которые были собраны на разных станциях на одном и том же берегу озера и
теми, которые собирались в различное время в местах сильно-отличающихся
по своим условиям. Однако, изменчивость моллюсков и внутри отдельных
проб и между разными пробами являлась видимо непрерывной.

Основное число в 18 гаплоидных хромосом наблюдалось в 17 местах сбора
проб, что подтвердило прежние цитологические наблюдения в комплексе
"Bulinus natalensis /tropicus".

Видимо, нет ясных различий между видами Bulinus natalensis, В. tropicus и
В. zuluensis, хотя изменчивость некоторых признаков коррелируется и имеет
географический характер. Раковины, похожие Ha В. natalensis и В. zuluensis
встречались чаще в прибрежном районе Наталя; эти популяции обычно
характеризуются низким завитком, изогнутой колюмеллой, узким пупком,
слабой пластинчатостью периостракума и наличем частично или полностью
афалических индивидуумов.

2. А. Е.

MALACOLOGIA, 1971, 11(1): 171-198

THE BULINUS NATALENSIS/TROPICUS COMPLEX
(BASOMMATOPHORA: PLANORBIDAE) IN SOUTH-EASTERN AFRICA:
II. SOME BIOLOGICAL OBSERVATIONS, TAXONOMY AND GENERAL DISCUSSION

О. в. Brown!, G. Oberholzer ” and J. A. Van Eeden ?
ABSTRACT

The South African Bulinus natalensis (Küster) and B. tropicus (Krauss) have
been regardedeither as distinct species or as synonyms in different publications,
and some populations have recently been classified as intermediate. B. natal-
ensis has been included in the B. truncatus (Audouin) species group, which, in
northern Africa and south-western Asia, is associated with the transmission of
human schistosomiasis. For this reason it is important to elucidate the taxo-
nomic status and identification of B. natalensis.

Eighty-six samples of snails belonging to the Bulinus natalensis/tropicus com-
plex were studied. The sampling area in south-eastern Africa, described in the
present paper, includes the type localities of B. natalensis and B. zuluensis
(Melvill & Ponsonby). Observations on the shell, genital anatomy and radula,
described in detail elsewhere, are summarised. The haploid chromosome num-
ber n=18 is apparently uniform in the B. natalensis/tropicus complex, apart
from additional chromosomes in some populations. Egg proteins from popula-
tions representing В. natalensis and tropicus showed no significant differences
when analysed by electrophoresis. Experimental infections attempted with 3
species of Schistosoma were unsuccessful, even in the case of snails from popu-
lations having certain anatomical characters of the B. truncatus group.

The nominal species Bulinus natalensis, B. tropicus and B. zuluensis were
represented in our material, though no satisfactory taxa could be defined be-
cause of continuous variation. However, a geographical pattern was evident in
the variation of certain morphological characters. Populations having depressed
shells, angular mesocones on the first lateral teeth of the radula, and including
some aphallic animals (B. natalensis) were found almost exclusively in the trop-
ical or sub-tropical regions of South Africa. Populations with comparatively
long-spired shells, non-angular mesocones and a normal copulatory organ (B.
tropicus) were found to predominate in the temperate climatic region.

The study of snails from the type district of Bulinus natalensis indicated that a
high frequency of angular mesocones might be regarded as characteristic of that
species. The majority of the present samples were classified according to the
predominant type of mesocone as В. natalensis ( = 50% angular) ог В. tropicus
(= 50% non-angular). The type locality of В. natalensis lies near the southern
limit of that form, and the wide variation in morphology observed in this area
was perhaps due to interbreeding with B. tropicus: human activities may have
resulted in the breakdown of any ecological isolating factors.

Climate is the factor most likely to determine the ranges of Bulinus natalensis
and B. tropicus in South Africa. The role of natural selection is considered in

Е. : .
British Medical Research Council, c/o Experimental Taxonomy Section, Zoology Department,
British Museum (Natural History), London, S.W. 7.

2 Potchefstroom Division of the Bilharzia Research Group of the South African Council for Scien-
tific and Industrial Research, Potchefstroom University, Transvaal, Republic of South Africa.

(171)

172

BROWN, OBERHOLZER AND VAN EEDEN

maintaining these forms distinct despite interbreeding. B. zuluensis is a local
form characterised by an extremely depressed spire and a high frequency of
angular mesocones; possibly it originated through the adaptation of B. natalensis
to lacustrine conditions on the coastal plain of northern Natal, and later colonised
a variety of habitats, retaining the depressed shell form.

Bulinus natalensis has certain morphological characters in common with the
B. truncatus group, but, to judge from its chromosome number, egg-proteins
and immunological reactions, it is more closely related to B. tropicus. Because
B. natalensis and B. tropicus, with 18 pairs of chromosomes, and B. truncatus
group populations, with 36 pairs, apparently occur together in some areas of
tropical Africa, their correct identification could be of practical importance, as
the latter are probable potential hosts of Schistosoma haematobium, while B.
natalensis from only 1 locality have been experimentally infected and B. tropicus
is considered refractory. In the absence of clear diagnostic characters in the
shell or radula, the evidence of chromosome number, biochemical and immuno-
logical data will be valuable for the identification of snails belonging to the B.
truncatus group. It remains to be seen whether further study of morphological
and other features will facilitate differentiation between B. natalensis and B.

tropicus.
INTRODUCTION

The freshwater planorbid genus Bu-
linus inhabits the African continent and
islands in the Indian Ocean (Wright,
1971), and the Mediterranean region,
extending eastwards in south-western
Asia to Iran. Some taxa serve as inter-
mediate hosts to species of Schistosoma
that cause schistosomiasis (bilharziasis)
in man, cattle and other animals. Many
taxa of Bulinus have not yet been satis-
factorily defined, and little information
has been published about variation with-
in particular populations or over geo-
graphical areas of significant size.

Mandahl-Barth (1957, 1960, 1965) rec-
ognised 4 groups of species within Bu-
linus. The members of the B. africanus
(Krauss) and. В. forskalii (Ehrenberg)
groups present in our area (Fig. 1) are
recognisable by a combination of con-
chological and anatomical characters
(Van Eeden & Oberholzer, 1965; Brown,
1966; Oberholzer € Van Eeden, 1967)
and do not concern us here. The other
2 species groups established by Man-
dahl-Barth were typified by the northern
B. truncatus (Audouin) and the southern
В. tropicus (Krauss), distinguished pri-
marily, as regards morphology, by the
presence on the 1st lateral radular tooth

of arrow-head shaped mesocones and
triangular mesocones respectively. A-
phalic animals (lacking the copulatory
organ) are common in some populations
of the B. truncatus group, but occur very
rarely in the B. tropicus group.

The species Bulinus natalensis and B.
tropicus (Küster) have been regarded in
different publications either as synonyms
(Mandahl-Barth, 1957; De Azevedo, Me-
deiros, Da Costa Faro et al., 1961) or
as distinct species (Connolly, 1939, Man-
dahl-Barth, 1965). Some populations
have been classified as intermediate
(Brown, Schutte, Burch & Natarajan,
1967). It is important to elucidate the
taxonomic status and identification of
B. natalensis because this species was
placed by Mandahl-Barth (1965), ac-
cording to the radula and the frequent
absence of the copulatory organ, in the
B. truncatus group, members of which

|
|

are generally regarded as potential ш- |

termediate hosts of Schistosoma haema-
tobium. There is no evidence that B.
natalensis transmits schistosomiasis
under natural conditions, though Pitch-
ford (1965) reported that a South African
snail “of the truncatus group” served as

|}

|
|

host to several species of Schistosoma |

in the laboratory. Lo, Burch & Schutte
(1970) obtained a low degree of in-

BULINUS NATALENSIS/TROPICUS COMPLEX II

1000km

FIG. 1. Africa, showing the area sampled
(rectangle) and the range of Bulinus natalensis
(broken line) according to Mandahl-Barth
(1965) and the present observations. B.
natalensis may extend further northwards to
Ethiopia, indicated by a query mark.

fection in B. natalensis from Lake Si-
bayi, Natal exposed to S. haematobium
from Iran. B. tropicus is not known to
be susceptible to infection with this para-
site, under natural or experimental con-
ditions.

The southernmost localities given by
Mandahl-Barth (1965) for the Bulinus
truncatus group are situated in northern
South West Africa and in the Transvaal,
Republic of South Africa. But many
more populations had been identified,
Since 1959, according to the shape ofthe
mesocone and the frequent absence of
the copulatory organ, from the Trans-
vaal (Van Eeden, Allanson & De Kock,
1964; Van Eeden, Brown & Oberholzer,
1965; Schutte, 1966) and Natal (Van
Eeden et al., 1965; Brown et al., 1967).

Brown et al. (1967) found that all snails

ties, whether they had anatomical char-

|
‘es, whe cytologically from 87 locali-

|
|
|

acters of В. tropicus or В. truncatus,
had a basic haploid chromosome number

173

of n=18, a character of В. tropicus
group (Burch, 1964). A new assemblage
was proposed, the B. natalensis group,
to accommodate snails with anatomical
characters similar to B. truncatus, but
having the chromosome number n = 18
instead of n = 36 found by Burch (1964)
in B. truncatus and related species.

The present study is based on 86 pop-
ulation samples from southern Africa
comprising nearly 6,000 snails, belong-
ing to what will be referred to as the
Bulinus natalensis /tropicus complex, and
1 sample of B. truncatus from Egypt.
Samples were collected from restricted
loci of apparently uniform ecology. Par-
ticular attention was devoted to districts
in Natal that included the type localities
of B. natalensis and B. zuluensis (Mel-
vill & Ponsonby); both these species and
also B. tropicus are identifiable in our
material. The coastal plain of north-
eastern Natal contains many freshwater
lakes that have been scarcely influenced
by human activities, whereas further
south and inland many habitats are small
dams constructed by european farmers.

Data on the shell, mantle, copulatory
organ and chromosome number are giv-
en in detail by Brown, Oberholzer & Van
Eeden (1971) and the radula was de-
scribed by Oberholzer, Brown & Van
Eeden (1970). These observations are
briefly summarised inthe present paper,
which further gives results obtained
from electrophoretic analyses of egg-
proteins and attempted experimental in-
fections of snails with Schistosoma spp.

We chose to study a limited number
of features, all of them referred to pre-
viously in the literature on Bulinus, and
did not attempt to discover new taxo-
nomic characters. Davis & Lindsay
(1967) were rightly concerned that char-
acters observable with difficulty, and
perhaps of great potential value should
not be neglected, but so far the taxo-
nomic value of no character, whether
morphological, cytological or biophysi-
cal has been analysed on a sufficiently
large scale in the genus Bulinus. At
present, therefore, it seems justifiable

174 BROWN, OBERHOLZER AND VAN EEDEN

to concentrate attention on easily ob-
served features. It is also of practical
importance that the shell and radula may
be studied in dry or poorly preserved
material.

TOPOGRAPHY, CLIMATE AND
AQUATIC HABITATS

Our material was collectedfrom east-
ern South Africa mainly in Natal pro-
vince, and from southern Mozambique
(Figs. 1, 2). Zululand is the northern
part of Natal bounded by the Tugela
river to the south and the Mozambique
border towards the north. The coastal
plain of north-eastern Zululand is known
as Tongaland.

The major topographical feature is
the Eastern Escarpment, which extends
from the Eastern Cape to the Zambesi
river and is crowned by the Drakens-
berg mountains that reach a maximum
altitude of 3229 m (10,822 feet) in west-
ern Natal. The course of the escarp-
ment is indicated by the 1,500 m con-
tour in Fig. 2. The greater part of the
inland plateau lying to the west of the
Eastern Excarpment is over 900 m
(3,000 ft.) with an innermost area of
about 1,200 m (4,000 ft.), which is called
Highveld and occupies most of the Cape
Province, the Orange Free State and the
Transvaal. The major rivers flowing
eastward from the escarpment into the
Indian Ocean are, proceeding from north
to south: the Limpopo, Crocodile/Ko-
mati, Pongola/Maputo and Tugela. The
elevation of southern Africa in the Ter-
tiary period has resulted in erosion
producing deeply-incised river gorges
in the foothills of the escarpment. The
coastal plain is negligible in southern
Natal, though it increases northwards
from the Tugela river and merges into
the broad tropical plain of Mozambique.

The varied topography contributes to
diversity in climate. Rain falls mainly
on the coastal plain and on the eastern
slopes of the mountains and is concen-
trated in the austral summer months.
Some rain usually falls in every month
in Natal, though in the comparatively

arid eastern Transvaal and southern
Mozambique there may be hardly any
precipitation between April and October.
According to the system of climato-
ecological regions defined by Van Zin-
deren Bakker (1962), the semi-arid tro-
pical region includes southern Mozam-
bique and north-eastern Natal, while our
remaining collecting stations lie either
within the semi-arid warm temperate
region or the cool temperate region.

A tropical climate may be defined
(Köppen, 1931) as one in which the cold-
est month has a mean temperature of
over 18°C. In southern Africa July is
the coldest month and the 18°isotherm
extends southwards to include the coast-
al plain of north-eastern Natal (Fig. 2).
Isotherms run approximately parallel to
the escarpment (Niddrie, 1951) butthere
are variations (for example, in relation
to the Tugela river basin) indicatingthat
cool conditions extend eastwards on sa-
lients from the escarpment while warm-
er conditions penetrate inland up the
river valleys.

Because of seasonal rainfall and vio-
lent precipitation, the rivers fluctuate
greatly in volume and carry heavy loads
of silt. The smaller lotic habitats tend
to be ephemeral because of high insola-
tion and evaporation. Populations be-
longing to the Bulinus natalensis/tropi-
cus complex occur in a variety of habi-
tats which may be described in 4 groups:

(1) Margins of rivers and streams
where the rate of flow is slow enough to
permit the deposition of mud and suffi-
ciently constant to allow the growth of
aquatic vegetation. These conditions
are most frequent where watercourses
meander in mature valleys or through
the coastal plain.

(2) Marshy hollows, known as vleis,
that may contain water only seasonally;
these are common in the foothills of the
escarpment and on the inland plateau.

(3) Lakes and pans that are most nu-
merous on the coastal plain of Mozam-
bique and northern Zululand, where the
largest is Lake Sibayi.

(4) Artificial habitats including large
reservoirs, small farm dams, quarry

BULINUS NATALENSIS/TROPICUS COMPLEX II 175

PT maw de ao ue ann da ec au

` À !: MOZAMBIQUE
Ps)
TRANSVAAL x EN, |
fet Wy q]
yoy, al y 2 |
N и
сгамеп! *, N Er >
à \ 7 ° |
O, eng eal tet eS
E ur \ 2 | yO
‘27 CROCODILE'R. 5 26
= 2 м
PRETORIA, '°°°” \ a o Г
eee oy д ARNES PR /
¿__-- © comptus A BS e 2. 4 el
= = |
fc SERS !
N m
о = yy I S
(SWAZILAND =.
i \r. — -—L
I 4 =
| il
|

E O o <P
Met > Е. SIBAYI
ORANGE FREE STATE io ^^ ee de cr
HARRISMITH = NATAL \®
o® ¡09 es
Le. = E ee L.ST. LUCIA
WEN : “0 096 N las
=: a
uluensis e
ARA
“о, 4
% %
>

natalensis
«« diaphanus

DURBAN

INDIAN OCEAN

angular 250% (natalensis)

PORT intermediate

SHEPSTONE :
non - angular .. (tropicus)

woo” EASTERN CAPE

06e

no type

UMTATA
100 km

FIG. 2. Distribution within the area enclosed by a rectangle in Fig. 1 of sampling.stations for
the Bulinus natalensis/tropicus complex. The symbols indicate either the type of mesocone
dominant (50% or more) among those examined from each populations, or that no one type reached
| 50% (sample frequencies according to Oberholzer et al. , 1970). The types of mesocone were:
angular (sides angulate resulting in an “arrowhead” shape); non-angular (sides straight resulting
in a “triangular” shape, or curved); intermediate (sides strongly curved, or the 2 sides of dif-
ferent types). A single mean value is shown for 8 samples from Lake Sibayi, Natal. The Drak-
ensberg escarpment is indicated by the 1,500 m contour. The 18°C July (coldest month) iso-
therm (after Poynton, 1964) may be regarded as the southern limit of the tropical climatic re-

gion. The type localities of the species В. comptus, В. craveni, В. diaphanus, В. natalensis
and B. zuluensis are indicated.

176 BROWN, OBERHOLZER AND VAN EEDEN

pits and irrigation channels. Snails are
not abundant in large reservoirs when
the water level fluctuates widely and fre-
quently, apparently because of the highly
unstable conditions in the littoral zone.
However, the small farm dams used by
livestock are very favourable for the
B. natalensis/tropicus complex, even
though the water may not be permanent.
The construction of farm dams andirri-
gation systems, particularly in rela-
tively arid regions such as the Croco-
dile river valley in the Eastern Trans-
vaal (Fig. 2), has probably led to sub-
stantial increases in the number of dis-
crete populations and the overall abun-
dance of these snails.

Although snails are usually most abun-
dant amongst aquatic vegetation growing
on a muddy substratum, we observed
the greatest densities in 2 artificial
habitats almost devoid of higher plants;
a concrete-lined channel drainingfroma
sugar-mill and polluted with domestic
rubbish, and a farm dam containing rot-
ted sugar cane (Brown et al., 1971; lo-
calities 5, 52). In these localities the
moderate organic pollution may have
contributed to the exceptional abundance
of the snails by enriching the food re-
sources.

River waters derived from different
geological formations in Natal have char-
acteristic chemical compositions (Kemp,
1963), but no corresponding differences
in the aquatic faunas have been recorded.
Schutte & Frank (1964) examined 155
aquatic habitats in the south-eastern
Transvaal and concluded that none of the
chemical compositions encountered were
outside the tolerance limits of fresh-
water snails. The unusually high con-
centrations of chloride ions (135 ppm)
in Lake Sibayi (Allanson et al., 1966)
apparently has no adverse effect on the
molluscan fauna. There are no reports
for south-eastern Africa of streams

comparable to those with unusually high.

acidity that support a characteristic
fauna in the Western Cape (Harrison &
Agnew, 1962). On consideration of our

present knowledge of water chemistry
in south-eastern Africait seems unlikely
that chemical factors are decisive in
determining the distribution of B. natal-
ensis/tropicus complex as a whole, or
the ranges of local forms. On the other
hand, zonal and altitudinal variations in
the climatic temperature do appear tobe
correlated with geographical variation in
the snails (see Discussion, p 188).

OBSERVATIONS
Method of sampling

Eighty-six random samples of snails
were collected from restricted loci of
apparently uniform ecology; many farm
dams were so small and shallow that
all parts could be reached with a hand-
net. In Lake Sibayi and other large
bodies of water the collecting stations
were restricted to a few square metres
of the shore. Locality numbers given in
the present paper are those used by
Brown etal. (1971) and Oberholzer et
al. (1970).

Shell and anatomy

The species Bulinus natalensis, B.
tropicus and B. zuluensis, identified ac-
cording to the shell, were represented
in our material (Brown et al., 1971).
But, although many populatons had dis-
tinctive characters, both intro-and inter-
population variation are apparently con-
tinuous. However, variation in certain
shell features is interrelated and a geo-
graphical pattern is discernable in which
populations with a depressed spire, a
twisted columella and a nearly closed
umbilicus are particularly common in
the tropical and sub-tropical regions of
eastern Natal.

Variation in the shape of the mesocone
on the first lateral radular tooth is con-
tinuous also (Oberholzer et al., 1970),
though populations having high frequen-
cies of angular (i.e., arrow-head shaped)
mesocones are concentrated in eastern
Natal (Fig. 2.). The majority of samples
containing aphallic animals were ob-

BULINUS NATALENSIS/TROPICUS COMPLEX II 177
100 SOME ABNORMAL COPULATORY ORGANS ©
o SOME APHALLIC ANIMALS e
APHALLIC AND ABNORMAL ®
90 NORMAL O
O
80 e
0 >
©
70
р à
О ©
W e
> 50 O
E OWES
= 40 of
9 O
oO
* 30 O al
a O O
O
O
20 O OS O
8 o
O >
2 Q ое O
e 0 — 1.4 15 1-6

SAMPLE MEAN LAL

FIG. 3. Bulinus natalensis/tropicus complex in south-eastern Africa. Correlation diagram for
the mean ratio shell length:aperture length (L:AL), frequency of the angular mesocone, and the
condition of the copulatory organ, for samples from 84 localities. Data from Brown et al. (1971)
and Oberholzer et al. (1970); a single mean value is included for 8 samples from Lake Sibayi,

Natal (Nos. 7-14).

tained in eastern Natal (Brown et al.,
1971). However, despite similarities in
geographical pattern, variation in spire
length, mesocone shape and copulatory
organ is not closely interrelated (Fig. 3);
the level of probability for the correla-
tion coefficient (r) for sample mean L:
AL? and frequency of angular mesocone,
calculated for the entire series of sam-
ples, is insignificant (r = 0.007, P>0.01).
When samples from Natal only are con-
sidered, the correlation between this
pair of characters is moderately signif-
icant (r = 0.28, P approximately 0.03),

3 Total shell length (L): aperture length (AL).

partly at least because of the higher
proportion of samples resembling Bu-
linus zuluensis, in which the depressed
spire is associated with ahighfrequency
of angular mesocones.

The 1 sample of Bulinus truncatus
studied was not clearly distinguishable
from the B. natalensis/tropicus complex
in respect of the shell features, the size
of the 1st lateral radular tooth, or the
shape of its mesocone.

On inspection our data do not suggest
any significant intra-sample heteroge-
neity. Numerical analysis might reveal

A measure of exsertion of the spire.

178

minor discontinuities in variation, but
these would not necessarily correspond
to acceptable taxa. Minor discontinui-
ties within populations could be due, for
example, to the existence of self-ferti-
lising strains or to the presence of suc-
cessive overlapping generations that ex-
perienced different environmental con-
ditions for part of their development.

Chromosome number

The haploid chromosome number n =
18, with between 1 and 3 additional
chromosomes in a few populations, has
been reported for snails belonging to
the Bulinus natalensis/tropicus complex
from 105 localities south of the Zambesi
river (Burch, 1964; Natarajan, Burch &
Gismann, 1965; Brownet al., 1967, 1971).
Snails with additional chromosomes were
obtained from 4 localities situated ei-
ther in Rhodesia or near the Natal coast,
and resembled В. natalensis to a greater
or lesser extent.

Egg-proteins

In a study of egg-proteins by electro-
phoresis (Wright & Ross, 1965), a sam-
ple from South Africa (Umhlatuzani riv-
er, Durban) was identified as Bulinus
tropicus. Radulae from the same local-
ity were later classified as “interme-
diate” by Brown et al. (1967), andfurther
specimens had 39% angular mesocones
(Oberholzer et al., 1970), so that this
population was perhaps more closely
related to B. natalensis. Dra EXA
Wright has now made electrophoretic
analyses of egg-protein from 4 of our
sampled populations (Table 1) and the
patterns obtained were all of the same
type and similar to that previously de-

BROWN, OBERHOLZER AND VAN EEDEN

scribed for snails from the Umhlatuzani
river. The populations studied included
examples of B. natalensis and B. trop-
icus (frequency of angular mesocone
0%-95%; L:AL = 1.26-1.53) and conse-
quently it seems improbable that there
is taxonomically significant variation in
egg-protein within this complex.

Susceptibility to infection with Schisto-
soma

Experimental infections were attempt-
ed by Dr. R. J. Pitchford in 1967 at the
Bilharzia Research Unit, Nelspruit,
Eastern Transvaal. Snails from 3 local-
ities in the Crocodile river valley (Buf-
felspruit, Kaapmuiden, Komatipoort) and
from Lake Sibayi (localities 7, 62-64)
were exposed to miracidia of Schisto-
soma haematobium, S. bovis and S. mat-
theei but no cercariae were shed, Snails
from the same collecting station in Lake
Sibayi gave a sample frequency of 95%
angular mesocones, while frequencies
for the other localities varied between
7% and 43%.

TAXONOMY

Seven nominaltaxa belonging to the Bu-
linus natalensis/tropicus complex have
been recorded from our area.* The
geographical distribution of records is
given in Table 2.

1841 Physa natalensis Küster.

geni valley, Durban, Natal.°

1848 Physa diaphana Krauss. Umgeni

valley, Durban, Natal.

1848 Physa tropica Krauss, Lepenula

river, Transvaal.

1886 Physa craveni Ancey (new name

for P. lirata Craven, 1880). Mooi

Um-

+The type localities of Physa verreauxii and P. cyrtonota, both described by Bourguignat (1856),

are given by Mandahl-Barth (1957) as the Olifants river, Transvaal.

However, Bourguignat

stated that the type localities lay in the Cape of Good Hope, and they may be situated in the
Olifants river near Knysna, which is outside our collecting area.

According to Küster, “In Bächen des Umgani-Valley, an der Natal-ktiste”. Krauss (1848) gave

the locality simply as “In stagnis natalensibus”.

BULINUS NATALENSIS/TROPICUS COMPLEX II 179

TABLE 1. Populations belonging to the Bulinus natalensis/tropicus complex from which egg-

proteins were investigated by electrophoresis on cellulose acetate. All populations

gave patterns similar to that illustrated by Wright & Ross (1965, Fig. 12). Localities
numbered according to Brown et al. (1971, Table 1).

Mean ratio shell length:
aperture length
(L/AL)

Frequency of

Identification
angular mesocone*

Locality

5, Xinovane (Mozambique intermediate 30% 1953
7, Lake Sibayi (Natal) “natalensis” 95% Е. 26
39, Eston (Natal) intermediate 32% 1. 28

83, Potchefstroom (Transvaal) “tropicus”

*A mesocone with angular sides is characteristic of the Bulinus truncatus group according to

Mandahl-Barth (1957).
(50% + ) are here identified as В. natalensis.

TABLE 2. Bulinus natalensis/tropicus complex.

Populations with high frequencies for this type (angular) of mesocone

Nominal species recorded from Natal, the

Eastern Transvaal and southern Mozambique.

Natal

Eastern Transvaal

Southern Mozambique

В. natalensis B. natalensis B. natalensis

B. diaphanus
B. tropicus
B. corneus
B. zuluensis
B. depressus

B. tropicus
B. craveni
B. comptus
B. depressus

B. tropicus
B. corneus

Data from Connolly (1939), De Azevedo et al. (1957), Schutte & Frank (1964), Van Eeden et al.

(1965), Oberholzer & Van Eeden (1967).

river, Transvaal.®

1889 Physa cornea Morelet. Port
Elizabeth, Eastern Cape Prov-
ince.

1903 Isidora compta Melvill & Pon-
sonby. Boksburg, Transvaal
(near Johannesburg).

1903 Physa zuluensis Melvill & Pon-
sonby. East Zululand, Natal.

1936 Bulinus hemprichii depressus
Haas. Lake Bangweolo, North-
ern Rhodesia.

Snails from some localities in the
Eastern Transvaal and 1 in Natal were
identified as Bulinus depressus, accord-
ing to the very short spire, by Van
Eeden (Van Eeden et al., 1965). These
identifications were apparently incor-
rect as the South African snails had ana-
tomical characters of the B. truncatus
group (angular mesocones, aphallic indi-
viduals), whereas Mandahl-Barth (1968)
examining material from the ‘region of
the type locality of B. depressus clas-

6 probably in the Lydenberg district, Eastern Transvaal, because all of the other material from
the Transvaal described by Craven was from that district.

180 BROWN, OBERHOLZER AND VAN EEDEN

sified it as a subspecies of B. tropicus
on the basis of its non-angular meso-
cones. Other South African snails, from
the Northern Transvaal, identified as
B. depressus by Schutte (1965, 1966) and
Hamilton-Atwell (1966) also had ana-
tomical characters of the B. truncatus
group. The South African populations
of B. “depressus” are apparently closely
related to B. natalensis, but the fre-
quency of aphallic individuals is greater,
at least in the Northern Transvaal (Ham-
ilton-Atwell found that almost all of 120
snails from one locality were aphallic),
than in B. natalensis in Natal.

The original descriptions of all these
species are limited to shells; Bulinus
natalensis, B. tropicus and B. zuluensis
are clearly recognisable in our mate-
rial and are discussed below. B. dia-
phanus was described from a shell of
4 ‘> whorls at 6.5 mm length, whereas
according to Krauss (1848) shells of B.
natalensis complete 4 whorls only at
12 mm length, and the largest shell ob-
tained by us from the Umgeni valley
consists of less than 4 whorls at9.4 mm
length. It is possible, as suggested by
Connolly (1939) that B. diaphanus is a
dwarf form derived from B. tropicus,
although in view of its type locality it
could equally well be related toB. natal-
ensis. В. сотпеи$ has been recorded
from only 1 locality in Natal (Mooi river;
Connolly, 1939) and several places in
southern Mozambique (De Azevedo, Me-
deiros € Da Costa Faro, 1957), and it is
distinguishable from B. tropicus appar-
ently only by its smaller size. В. craveni,
and B. comptus seem to show no signif-
icant differences from B. tropicus and
were placed in the synonymy of that
species by Connolly (1939) and Mandahl-
Barth (1957). Transverse lamellae of
periostracum provide the main charac-
ter of В. craveni, but occur on some
shells in the majority of our samples.

Therefore, this feature seems to be un-
suitable for a taxonomic diagnosis.

Bulinus natalensis

The original shells were collected by
Krauss from streams in the Umgeni
valley, near Port Natal (Durban) on the
Natal coast. Ktister (1841) described an
indistinct fold on the columella and
Krauss (1848) mentioned the somewhat
bent columella as one of the most im-
portant characters distinguishing Bu-
linus natalensis from B. diaphanus and
В. tropicus. According to Connolly
(1939), B. natalensis is “mainly recog-
nisable by the thin columella with dis-
tinct twist on its inner margin”, ' Each
of these authors illustrated a different
shell from the original series (Fig. 4,
a-c), all with the columella of the shape
classified as straight or twisted by
Brown etal. (1971). | Mandahl-Barth
(1957), followed by De Azevedo et al.
(1961), placed B. natalensis in the syn-
onymy of B. tropicus, but later, having
studied material from central Africa,
Mandahl-Barth (1965) recognised B. na-
talensis as a distinct species belonging
to the group of B. truncatus.

The lower Umgeni valley has been
affected greatly by human settlement
and we did not obtain any snails to the
south of the river near the city of Dur-
ban in the area where Krauss probably
collected. However, we have examined
abundant material from 3 localities sit-
uated in the northern part of the lower
Umgeni basin (localities 36, 37, 77).
Many shells from the Mhlangana river
at Avoca (locality 37) resemble B. natal-
ensis as illustrated by Küster and Krauss
(compare Pl. 1, Figs. 1, 2 with Fig. 4a,
b). In this sample the ratio L:AL varied
between 1.12 and 1.43 (Pl. 1, Figs. 3, 4);
the variation in columella shape included
concave and twisted types (Pl. 1, Figs.
5, 6); the umbilicus was rimate or mod-

TMandahl- Barth (1957, 1965) also described the columella of Bulinus natalensis as “twisted” and
this term has been used in subsequent descriptions by Brown et al. (1967, 1971).

BULINUS NATALENSIS/TROPICUS COMPLEX II 181

OY &

OS

f
Te

m

FIG. 4. Type or paratype shells copied from original illustrations.

a-c, Bulinus natalensis. a, type (Küster, 1841) cf. Pl. 1, Fig. 2. b, paratype (Krauss, 1848)
cf. Pl. 1, Fig. 1. c, paratype (Connolly, 1939).

d,e, B. tropicus. d, type (Krauss, 1848) cf. Pl. 1, Fig. 11. e, paratype (Connolly, 1939).

fi; B. zuluensis, Type (Melvill & Ponsonby, 1903) cf. Pl. 1, Fig. 9.

erately open, and some shells had la-
mellae of periostracum. Every examined
radula had either the angular or inter-
mediate types (see legend Fig. 2) of
mesocone predominant, with a sample
frequency of 68% for the angular type.
Snails from 2 other localities in the
Umgeni valley are considerably different
from those found at Avoca. A sample
from a farm dam about 2 miles north-
wards (locality 36) gave a comparable
frequency of angular mesocones (72%),
_ but the shells generally had longer spires
_ and L:AL reached 1.54 (Pl.1, Fig. 11).
_ Although the snails with longer spires
resembled Bulinus tropicus (Fig. 4d),
| about half their mesocones were angular.

|

Snails from a quarry pool at Kwa Mashu
(locality 77), 5 miles west of Avoca,
had even longer spires with L:AL vary-
ing between 1.30 and 1.74 (Pl. 1, Figs.
7, 8); non-angular or intermediate meso-
cones were predominant and the angular
type had a sample frequency of only 25%.

Variation in the spire of shells from
the lower Umgeni valley closely ap-
proached the range found in our entire
series of samples (Pl. 1, Figs. 3, 8, 12),
and the frequency of angular mesocones
in individual snails varied between 0
and 10 (10 mesocones examined in each
of 59 snails). Variation in both features
is apparently continuous (Fig. 5), and
there is a significant correlation be-

182

BROWN, OBERHOLZER AND VAN EEDEN

PLATE 1

The scale line represents 6 mm in the case of Figs. 1-14, and 4 mm in the case of
Figs. 15, 16.

FIGS. 1-12, 14-16. Bulinus natalensis/tropicus complex. Shells from eastern
South Africa. Locality numbers in parentheses refer to those listed in Table
1 of Brown et al. (1971, this issue of Malacologia).

1-6, Mhlangana river at Avoca near Durban, Natal (37): 1, resembling B.
natalensis as illustrated by Krauss (1848); 2, resembling B. natalensis as
illustrated by Küster (1841); 3, 4, extreme examples of variation in spire;
5, 6, extreme examples of variation in columella (5, concave; 6, twisted.

7, 8, pool in quarry at Kwa Mashu near Durban (77): extreme examples of
variation in spire. Fig. 8 has the most exserted spire in the entire series
of shells.

9, 10, Lake Umpangazi, Natal (15): 9, resembling B. zuluensis as illus-
trated by Melvill & Ponsonby (1903); 10, shell with more strongly twisted
and reflected columella.

11, farm dam 2 miles north of Avoca near Durban (36): shell having a long
spire and resembling B. tropicus as illustrated by Krauss (1848).

12, farm dam at Gingindlovu, Natal (31): the most depressed shell in the
entire series of shells.

14, Ngwetispruit (stream), Komatipoort, Eastern Transvaal (62): example
resembling B. reticulatus in the pronounced shouldering of the whorls.

15, 16, farm dam at Ermelo, Eastern Transvaal (60): 15, shell with open
umbilicus; 16, shell with well developed lamellae of periostracum.

FIG. 13. Bulinus globosus from Lake Umpangazi, Natal (15). The shell is narrow
in comparison to most shells of the B. natalensis/tropicus complex and the
twist on the columella is nearer to the base.

BULINUS NATALENSIS/TROPICUS COMPLEX II

184 BROWN, OBERHOLZER AND VAN EEDEN

e
1.6
P
o
.
e ir a
> o
1-5
Г e
Е
AL .
e : D
1-4 | . 4 o
e a =
e e a
e e a о A À A
A A
e ao a a
1-3, e À
oo A
4 о a о о
о
о
je} о a
a
1-2 |
о
D
À 4 4 À —— 1 4 —

о 1 2 3 4 5 6 7
ME SOCONE
FIG. 5. Ratio shell length:aperture length
(L:AL) plotted against the frequency of the
angular type of mesocone on the first lateral
tooth (10 mesocones examined in each radula)
for individual snails from the lower Umgeni
river valley, Natal (the type district of Bu-
linus natalensis). Three populations are re-
presented: No. 36, 2 miles north of Avoca
(triangles); No. 37, Mhlangana river at Avoca
(squares); No. 77, Kwa Mashu (solid circles).
Sample No. 37 contained a high proportion of
shells resembling the original description of
B. natalensis.

tween individual values for L:AL and
frequency of the angular mesocone (cor-
relation coefficient = 0.88; P = 0.001)
confirming the impression that a de-
pressed spire tends to be associated
with the angular type of mesocone. The
general resemblance of shells from the
Mhlangana river, Avoca (locality 37) to
B. natalensis encourages us to regard a
moderate to high frequency of angular
mesocones as a character of this spe-
cies. Further, this population lives in
a comparatively natural habitat that is
perhaps similar to the one originally
sampled by Krauss.

Bulinus tropicus

According to Krauss (1848) the type
locality of Bulinus tropicus in the Le-
penula river lies between latitudes 25°
and 26° South, i.e., in the zone of Pre-

toria in the Transvaal and not in Natal
as claimed by Bourguignat (1856: 236).
Despite efforts to trace the locality it is
unknown today (Stiglingh, Van Eeden &
Ryke, 1962: 75). Krauss differentiated
B. tropicus from B. natalensis by refer-
ence to its less rapidly increasing whorl,
distinct umbilicus, and the lack of a
twist in the columella; the type of B.
tropicus, and also a paratype illustrated
by Connolly (1939), show comparatively
long spires (Fig. 4d, e). The mesocone
of a list lateral radular tooth from a
paratype has nearly straight sides (Con-
nolly, 1939: Fig.43) and Mandahl-Barth
(1957) regarded a “triangular” (i.e.,
straight-sided, non-angular) mesocone
as characteristic of his B. tropicus spe-
cies group. Subsequent authors (Stig-
lingh et al., 1962; Schutte, 1965) have
drawn attention to considerable varia-
bility in the ınesocone of B. tropicus
and Brown et al. (1967) found continuous
variation between the non-angular (tri-
angle like) and angular (arrow-head like)
shapes.

Bulinus zuluensis

This species was described by Melvill
& Ponsonby from a depressed shell
(Fig. 4f) having aninflated ultimate whorl
and a twisted columella; the precise
locality in Zululand is not known. We
collected similar shells from Lake Si-
bayi and other localities in north-east-
ern Natal, some specimens having the
columella reflected at the base (Pl. 1,
Figs. 9, 10). These samples have high
frequencies (up to 95%) of angular meso-
cones. Connolly (1939) placed Bulinus
zuluensis in the synonymy of B. natal-
ensis and support for his opinion is pro-
vided not only by the continuous varia-
tion of spire length in our material
(Brown etal., 1971), but also by the
finding of some unusually depressed
snails (Pl. 1, Fig. 3) in the lower Um-
geni valley, the type district of B. natal-
ensis.

Identification

The nominal species Bulinus tropicus,
B. natalensis and B. zuluensis constitute

BULINUS NATALENSIS/TROPICUS COMPLEX II 185

a series in which the length of the spire
decreases and the frequency of angular
mesocones increases. Continuity in the
variation of these and other features
studied prevents the satisfactory defini-
tion of taxa, yet the geographical pattern
in the variation of certain shell features
and especially in the mesocone (Fig. 2)
should be recognised. We have chosen
to identify as B. natalensis those sam-
ples giving frequencies of 50% or more
angular mesocones, simply because few
of the sample frequencies lie near this
arbitrary borderline (Fig. 3). A fre-
quency of at least 50% non-angular
mesocones is regarded as diagnostic
of В. tropicus in our area. Even so,
variation is such that in 24 of the sam-
ples 50% of the mesocones are interme-
diate in shape, or no 1 type of mesocone
reaches this frequency. If the rules of
nomenclature were tobe strictly applied,
B. tropicus might be regarded as a syn-
onym or infra-specific form of B. natal-
ensis, and as pointed out by Mandahl-
Barth (1957: 20) this would cause con-
siderable confusion. It is perhaps pre-
ferable to treat these forms as species
in the knowledge that they are closely
related.

Depression of the spire and high fre-
quencies of angular mesocones were
associated in Bulinus natalensis in Natal,
and the most depressed shells and high-
est frequencies of angular mesocones
were found in populations resembling
B. zuluensis. However, this correlation
between spire length and mesocone shape
is apparently not maintained inthe East-
ern Transvaal or in southern Mozam-

bique, where long-spired populations
With moderately high frequencies of
‚ angular mesocones were found. В. zulu-
| ensis may thus be a local form peculiar
to the coastal region of north-eastern
Natal.

‚ The identification of the sample from
_Ngwetispruit, Eastern Transvaal (local-
ity 62) presents a peculiar difficulty.
‚In our other material depression of the
Spire is associated with increased shoul-
‘dering of the body whorl (Pl. 1; Figs. 6,
10, 12), and shells with elongated spires
|

usually have evenly rounded body whorls
(Pl. 1, Figs. 2, 8, 11). However, some
shells from Ngwetispruit have elongated
spires and shouldered whorls (Pl. 1,
Fig. 14) and resemble specimens de-
scribed by Oberholzer & Van Eeden
(1967: Figs. 9, 10) from the southern
part of the nearby Kruger National Park.
In general appearance these shells are
similar to Bulinus reticulatus Mandahl-
Barth, though spiral sculpture is not
well developed. But the sample from
Ngwetispruit includes also some shells
Similar to B. tropicus and variation is
apparently continuous. The unusual
characters of this population, included
provisionally in the B. natalensis/trop-
¿cus complex, could possibly be due to
interbreeding with B. reticulatus, un-
doubted populations of which occur in
the Kruger National Park (Oberholzer €
Van Eeden, 1967) and in southern Mo-
zambique (Brown € Oberholzer, 1966).

DISCUSSION
Variation and adaptation

Variation in freshwater snails is fre-
quently described but little understood.
The best known species is probably
Lymnaea peregra (Miller), which is
comparable to the Bulinus natalensis/
tropicus complex in abundance and ha-
bitat range. In both taxa many popula-
tions have distinctive characters and
may vary little in comparison to their
taxon considered as a whole. The nar-
rowness of intra-population variation led
Hubendick (1951: 31) to conclude that
the majority of populations of L. peregra
are genetically homogeneous as the re-
sult of frequent self-fertilisation; this
conclusion implies that differences be-
tween populations are largely dependent
on the genetic constitutions of founder
individuals. The operation ofthe “found-
er effect” would be favoured by the short
historical life of many of the small
bodies of water inhabited by the B. natal-
ensis/tropicus complex. Fluctuations
in annual rainfall have marked effects
on the surface water in semi-arid areas
and the extermination of a snail popula-

186 BROWN, OBERHOLZER AND VAN EEDEN

tion is probably not an infrequent event.
Colonisation of newly available habitats
would be most likely from lakes or
rivers, or other comparatively perma-
nent waters, and consequently there
could arise groups of populations de-
rived from particular centres of disper-
sal and recognisable by distinct char-
acters. However, it may be that some
differences between populations are the
result of selection pressures that we
do not understand. Many taxonomic
characters of freshwater snails have no
obvious functions, but they are probably
influenced by pleiotropic genes that may
also control features subjected to intense
selection.

Genetic inheritance has been demon-
strated in the genus Bulinus for mantle
pigmentation and the aphallic condition
of the genital system (De Larambergue,
1939). Conceivably, mantle pigmentation
could be adapted to give protection from
solar radiation or against predators
hunting by sight, and there may be some
adaptive significance in the unusually
light pigmentation that is characteristic
of some populations in lakes, e.g., Si-
bayi (B. natalensis; Brown et al., 1971),
Malawi (B. nyassanus; Wright, Klein &
Eccles, 1967) and Awasa (Bulinus sp.;
Brown, 1965).

The aphallic condition, if it were
associated with an increased capacity
to produce offspring through self-fer-
tilisation, could be advantageous in in-
creasing the chance of culonies being
founded by single snails, However,
normal individuals are known to repro-
duce satisfactorily in isolation (De Lar-
ambergue, 1939), and it seems that
aphallic Bulinus natalensis have no se-
lective advantage in eastern Natal, judged
from their rarity in our samples.

Berrie (1959) concluded that much of
the variation in the radular teeth of
Lymnaea peregra is not adaptive and
this seems to be the case also in the
Bulinus natalensis /tropicus complex, as
populations having high frequencies of
angular mesocones occurred in a wide

variety of water-bodies (Table 3). How-
ever Wright et al. (1967) suggested that
the broadly angular mesocones of B.
succinoides (Smith) of Lake Malawi might
be adapted to gathering epiphytic algae
from Vallisneria plants and itis possible
that similar adaptation has taken place
in the populations of В. natalensis living
on Juncus stems in certain lakes in
north-eastern Natal (e.g., Lake Sibayi).
Van Eeden et al. (1962), having exam-
ined Bulinus tropicus from 9 localities,
suggested that a depressed shell form
was characteristic of dams, while a
longer spire was typical of populations
inhabiting flowing waters. According to
our present observations on B. tropicus
(26 population samples giving a frequency
of 50% or more for the non-angular
type of mesocone), not only depressed
but also long spired populations live in
dams and other standing waters (Table
4,) while the samples obtained from
flowing waters had spires well within
the range of variation found in standing
waters. Depressed populations of B.
natalensis were found in a variety of
habitats (Table 3) including lakes, dams
and slowly flowing rivers, but all samples
examined from larger lakes were of the
depressed type (localities 6-16, 22-25).
Some of these populations lived on ex-
posed shores (Table 3, group A) and it
seems possible that the short spire was
to some extent an adaptation to reduce
the effects of wave-action in dislodging
the snail from the substratum. De-
pressed shells are characteristic of
several species of Bulinus inhabiting
lakes; В. succinoides and В. nyassanus
(Smith), Lake Malawi; B. transversalis
(Martens) and B. truncatus trigonus
(Martens), Lake Victoria; Bulinus sp.,
Lake Awasa, Ethiopia. Certain species
of Lymnaea living in some European
lakes produce depressed shell forms in
littoral situations exposed to wave-
action; it was found by Piaget (1929) for
Lymnaea stagnalis (Lin.) and Boycott
(1938) for L. peregra, that some lacus-
trine forms remained constant in lab-

TABLE 3.

A. Lakes with sandy littoral substratum exposed to
considerable wave-action.

6-14
15
22,23
27

B. Lakes or pans with muddy substratum and
denser aquatic vegetation than in A.

16
117
18
24
25
26

C. Dams.

20

21
30

31

BULINUS NATALENSIS/TROPICUS COMPLEX U

Some ecological features of 17 localities for the Bulinus natalensis /trop-
icus complex in north-eastern Natal. Populations having very depressed
shells (L/AL<1. 20) were present in all categories of habitat. All samples
except number 16 are identified as B. natalensis according to the high
frequencies of the angular type of mesocone. Localities numbered ac-
cording to Brown et al. (1971, Table 1).

angular
mesocones

(%)*

Locality (No. and name) TJA

Lake Sibayi 89 15222
Lake Umpangazi 95 1.16
Lake Bangazi 67 1-20
Lake Umzingazi 73 1228

Ujengu pan 10 1.10
Mozi pan 70 1.23
Sekunti pan 56 1.33
Lake Futululu 57 125
Lake Teza И TAO
Pool near Umfolozi river, Mtubatuba. 80 1232

Very shallow and heavily trampled by cattle.

Nyalazi. Pool formed by dam in stream. 95 1027
Dense aquatic weed.

Mtubatuba. Similar to No. 20. 61 1. 23
Eshowe. Small lake formed by dam in 69 thes 21
Mlalazi river. Peaty margins.

Gingindlovu. Dam in sugar-canefield. 51 125119

Dense aquatic weed.

D. Slow-flowing rivers.

19

28

32

with emergent grass.

Mzinene river near Hluhluwe. Muddy pool 122
with water-lilies.

Enseleni river. Emergent grass and 3 LS
rotting sugar-cane.

Inyezane river, Gingindlovu. Muddy trickle Laila)

*Ten first lateral teeth were examined in each of between 4 and 26 radulae per local-
ity; the percentage of angular mesocones is given for the total number of mesocones
examined (40-260).

187

188 BROWN, OBERHOLZER AND VAN EEDEN

TABLE 4. Variation in the spire length of Bulinus tropicus from standing and from flowing waters.

Spire length increasing from left to right

Sample mean
L:AL*

Standing waters
(pond, dam, isolated
pool in stream-bed) 2 5

Flowing waters
(streams, irrigation
channel)

*L:AL = shell length:aperture length

oratory-bred colonies and presumably
were determined genetically. In these
species of Lymnaea the most depressed
forms are restrictedtolakes; in L. stag-
nalis they occur in exposed littoral situa-
tions only and different forms with longer
spires are found in the sub-littoral re-
gion. In contrast, some depressed popu-
lations of B. natalensis occurred innon-
lacustrine habitats (Table 3), and B.
nyassanus and B. succinoides of Lake
Malawi live in the zone below about 5 feet
(Wright et al., 1967) where agitation of the
water should be slight. It may be con-
cluded that adaptation to water movement
is only 1 possible factor determining the
occurrence of depressed forms belonging
to the B. natalensis/tropicus complex.

The distribution of Bulinus natalensis in
south-eastern Africa

The distribution in our area of Bulinus
natalensis, and other populations in which
the angular and intermediate types of
mesocone were common (Fig. 2), cor-
responds closely to the incidence of warm
climatic conditions. This distribution
pattern is highly significant when con-
sidered in relation to the many animals
that are known to have tropical ranges
with southward extensions in the coastal
region of south-eastern Africa, e.g.,
Amphibia (Poynton, 1964), freshwater
Mollusca (Brown, 1967), landsnails (Van

Bruggen, 1969). Experimental investi-
gations of freshwater snails (Shiff, 1964;
Sturrock, 1966; Prinsloo, 1966) have
demonstrated that temperature has a
profound effect upon the fecundity of
Bulinus globosus (Morelet), Biompha-
laria pfeifferi (Krauss), B. tropicus and
Lymnaea natalensis Krauss, and it seems
likely that variation in climatic tem-
perature with latitude and altitude is an
important factor indeterminingthe range
of B. natalensis.

Having suggested that Bulinus natal-
ensis and B.tropicus are genetically
adapted respectively to warm and cool
conditions, it is necessary to consider
how the differences between them are
maintained, since morphological inter-
gradation indicates that interbreeding
might occur. Moreover, gene-flow is
apparently favoured by the existence in
South Africa of many farm dams sup-
porting populations of snails and large
numbers of water-birds, which are
thought to play an important part in dis-
persal (Kew, 1893; Boycott, 1936). Re-
cent studies in ecological genetics have
established that natural selection pres-
sures may be far more powerful than
was generally believed, even leading in
the case of the English Meadow Brown
butterfly Maniola jurtina to the subdivi-
sion of a single interbreeding and con-
tinuous population into distinct local

BULINUS NATALENSIS/TROPICUS COMPLEX II

forms (Ford, 1964: 68). It seems likely
that populations of Bulinus are subjected
to powerful selection pressures, atleast
during some stages of their development.
Shiff (1964) calculated the reproductive
potential of a single B. globosus to be
729 descendents in 20 weeks at 25°C,
while Stiglingh (1966) recorded 478 eggs
from a single B. tropicus in 10 weeks;
if similar numbers of eggs are laid
under natural conditions many individ-
uals must be eliminated during periods
of stable population density andrigorous
selection may take place. Even if a
propagule of B. natalensis transported
into the southern temperate region were
to succeed in breeding, the potential
colony would fail if fecundity and the
rate of survival of the offspring were too
low. Conversely, the reproductive ca-
pacity of B. tropicus is probably dimin-
ished in the tropical region; in the lab-
oratory Prinsloo (1966) observed that
out of a total of 69 viable eggs kept at
30°C only 19 hatched, though a far greater
proportion did so atlower temperatures.
Nonetheless, populations of B. natalensis
and B.tropicus probably can exist, at
least temporarily, outside their main
areas of distribution, and examples may
be the populations of B. natalensis at
Pietermaritzburg (Brown etal., 1967;
locality 4) and “B. tropicus” with angu-
lar mesocones collected near Grahams-
town, Eastern Cape Province (Stiglingh
et al., 1962). The introgressive hybrid-
isation of a B. natalensis population with
nearby В. tropicus populations might
produce a group of populations in which
the frequencies of the angular andinter-
mediate types of mesocone were un-
usually high for the area; an instance of
this perhaps is seen in the Harrismith
district (Fig. 2).

If the distributions of Bulinus natal-

| ensis and В. tropicus are related to

| climatic temperature, it might be ex-
| pected that
|

intermediate populations
would be particularly common in areas
experiencing a climate transitional be-
tween tropical and temperate conditions.
In more than half of the samples ob-

| tained to the south of Durban neither

189

the angular nor the non-angular types of
mesocone were dominant (Fig. 2); pos-
Sibly this area forms part of an “inter-
mediate zone” that might extend into
the unsampled parts of central and
northern Natal, and Swaziland, The
intermediate zone should be narrow on
steep escarpments where transitions in
climate are accelerated, and broad near
the coast where climatic change is re-
lated mainly to latitude andis moderated
by the warm Indian Ocean,

It is possible that human influence has
encouraged interbreeding between Вий-
nus natalensis and B. tropicus, through
the breakdown of any ecological isolating
factors. In the Umgeni valley, where a
high degree of variation was observed
(see page 181), the original forest vege-
tation has been cleared almost entirely
and marshes have been drained. Such
changes may have rendered this area
more suitable for B. tropicus than was
previously the case. The presence of
long-spired snails resembling this spe-
cies in a dam anda quarry pool (local-
ities 36 and 77) could be significant, as
such artificial habitats would perhaps
be more easily colonised than natural
waters already inhabited by B. natalen-
sis,

The origin of Bulinus zuluensis

Although a more or less depressed
shell is characteristic of Bulinus natal-
ensis in Natal, the spire is comparatively
long in the single sample from Mozam-
bique having over 50% angular mesocones
and also in the samples from Mosam-
bique and the Eastern Transvaal having
moderate frequencies of angular meso-
cones (localities 1, 4, 62, 64). Clearly
the depressed shell is not necessarily
correlated with the angular type of meso-
cone or with adaptation to warm condi-
tions. The prevalence of the extremely
depressed B. zuluensis type of shell in
eastern Natal is due apparently to local
factors. It is possible that the B. zulu-
ensis form developed fromB. natalensis
in Lake Sibayi or other lakes on the
coastal plain of northern Natal as the
result of adaptation to lacustrine con-

190 BROWN, OBERHOLZER AND VAN EEDEN

ditions. The process might have been
aided by the temporary isolation of the
lakes during a period of lowered rainfall
when smaller bodies of water may have
dried up. It is conceivable that the
lacustrine form later colonised a vari-
ety of nearby habitats, probably with
genetic modification but retaining amore
or less depressed shell. The adaptation
of the lacustrine genotype to different
conditions may have been accomplished
because competition from other natal-
ensis genotypes was reduced by the
restriction of gene-flow in the narrow
coastal strip of distribution.

The wider distribution of Bulinus natal-
ensis

According to the synonymy and local-
ities given by Mandahl-Barth (1965), the
range of Bulinus natalensis includes
southern Angola, south-eastern Congo,
Rhodesia, Zambia and southern Tangan-
yika (Fig. 1). B. natalensis has been
recorded also from Ethiopia by several
authors (cited by Brown, 1965); shells
from the crater lake Hora Harsadi (= lake
Biete Mengest) were so identified by
Connolly (1928), and as snails from this
lake have angular mesocones (Brown,
1965) and 18 pairs of chromosomes
(Brown & Burch, 1967), the population
conforms to our present concept of B.
natalensis. Accordingly, B. natalensis
or closely related forms may be widely
distributed in central and eastern Africa,
where various subspecies of B. tropicus
occur (Mandahl-Barth, 1957, 1960). Fur-
ther studies are required to investigate
the possibility that these species have
in general as in southern Africa different
distribution patterns that can be related
to climate. Probably a number of more
or less distinct forms, all related to
B. natalensis, will be recognisable, but
because of morphological intergradation
between B. natalensis and B. tropicus it
is perhaps not satisfactory to regard
these species as representatives of dif-
ferent species groups as did Brown et
al. (1967).

The identification of Bulinus natalensis
is rendered difficult not only by mor-

phological intergradation with B. trop-
icus, but also by the presence in some
areas of snails with 36 pairs of chromo-
somes belonging to the B. truncatus
group. The examination of snails from
over 100 localities indicates that popu-
lations having 36 pairs do not occur in
southern Africa. However, Burch(1964)
reported this number of chromosomes
for specimens of B. coulboisi (Bour-
guignat) from Tanganyika, where B.
natalensis also occurs (Mandahl-Barth,
1965). Both species were placed in the
same sub-group ofthe B. truncatus group
by Mandahl-Barth (1965), and as there
is apparently no clear morphological
difference between them the evidence
of chromosome number and biochemical
data may be indispensable for their
separation. Correct identification could
be important in relation to epidemiol-
ogical studies, for at least some forms
of B. coulboisi are susceptible to infec-
tion with S. haematobium (Mandahl-
Barth, 1965; Lo, 1969), while B. natal-
ensis from only 1 locality has been
experimentally infected and B. tropicus
is considered to be refractory.

The range of Bulinus natalensis may
also overlapthatofB. truncatus trigonus
in East Africa and even that of B. trun-
catus truncatus, which extends south-
wards to Uganda (Mandahl-Barth, 1965).
Mandahl-Barth (1965) placed these sub-
species in an “eastern” group having the
first lateral radular teeth about 25 y long,
whereas B. natalensis was included in
another group having lateral teeth less
than 20 u. Schutte (1965) compared the
size of the mesocone in Egyptian speci-
mens of B. truncatus truncatus with
South African snails identified as B.
depressus (probably to be regarded as
B. natalensis, see page 180); the mean
dimensions were greatest in the Egypt-
ian snails, though the ranges overlapped
extensively with those for South African
specimens. Oberholzer etal. (1970)
found extensive overlap in the length of
the 1st lateral tooth between В. natal-
ensis and B. truncatus from 1 locality
in Egypt. In respect of shell features
also, this sample of B. truncatus lay

BULINUS NATALENSIS/TROPICUS COMPLEX II 191

within the range of variation observed
in the B. natalensis/tropicus complex.
Clearly, a single sample of B. truncatus
has a limited value for purposes of com-
parison. However, it seems that mor-
phological characters may not provide
a satisfactory means for distinguishing
this species from B. natalensis; cyto-
logical, biochemical and immunological
data will probably play an important
part in establishing their distributions.

The Bulinus truncatus and B. tropicus
species groups

The morphological definitions by Man-
dahl-Barth (1957, 1965) of species groups
have contributed greatly to our under-
standing of the genus Bulinus, but the
distinction of the B. truncatus and B.
tropicus groups is unsatisfactory be-
cause the shape of the radular mesocone
is highly variable within populations, and
because there is continuous variation
between the angular and non-angular
shapes (Stiglingh et al., 1962; Schutte,
1965; Brown etal., 1967; Oberholzer
et al., 1970). There are apparently no
clear morphological differences between
В. tropicus and В. natalensis, nor be-
tween В. natalensis and В. truncatus.
The close relationship between the 1st
pair of species is confirmed by cyto-
logical and biochemical data. However,
B. truncatus differs from the other 2
Species in its higher chromosome num-
ber (Burch, 1964) and the electrophoretic
pattern given by egg-proteins (Wright
& Ross, 1965). The results of immuno-
logical studies by Burch & Lindsay
(1970) using foot muscle proteins also
Support these findings: they concluded
that B. natalensis from Lake Sibayi,
Natal was closely related to populations
identified as B.tropicus from South
Africa and Rhodesia (all n = 18), where-
as non-identity reactions were observed
with B. coulboisi (n = 36)from Tanzania.

So far as known, those species in the
complex under discussion that transmit
human schistosomiasis belong within
the Bulinus truncatus group as defined
_ by the possession of 36 pairs of chromo-
| somes (Burch, 1964). Neither B. natal-

ensis nor B. tropicus,both having 18
pairs of chromosomes, are known to
serve as intermediate hosts under nat-
ural conditions. However, B. natalensis
may not be entirely resistant to infection;
Pitchford (1965) found South African
snails “of the truncatus group”, possibly
B. natalensis, to be hosts of several
species of Schistosoma and Lo etal.
(1970) obtained a low degree of infec-
tion (3% of 108 snails) in B. natalensis
from Lake Sibayi, Natal, using $. haema-
tobium from Iran.

ACKNOWLEDGEMENTS

We are grateful to Dr. Almeido Franco
and Dr. Lidia de Medeiros for facilities
at the Instituto Investigacao Medica,
Lourenzo Marques and assistance during
field work in Mozambique, and to Dr.
R. J. Pitchford and Dr. C. A. Wright for
permission to refer to their unpublished
observations. We thank Dr. G. Mandahl-
Barth for providing a sample of Bulinus
truncatus from Egypt, Mr. P. G. Gelden-
huys and Mr. L. Le Hanie who collected
several South African snail samples,
and Mr. K. De Kock for photographing
shells. The first author is indebted to
Professor J. A. Van Eeden for accom-
modation in the Institute for Zoological
Research, Potchefstroom University
from 1966-1968, and toDr. C. A. Wright
for comments on this paper and accom-
modation in the Experimental Taxonomy
Section of the Zoology Department, Brit-
ish Museum (Natural History), We
wish to express our appreciation for the
financial support given us by the South
African Council for Scientific and Indus-
trial Research, the Department of Agri-
cultural Technical Services of the Re-
public of South Africa, and the Medical
Research Council of the United Kingdom.

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BULINUS NATALENSIS/TROPICUS COMPLEX II

ZUSAMMENFASSUNG

DER KOMPLEX BULINUS NATALENSIS/TROPIC US
(BASOMMATOPHORA: PLANORBIDAE) IN SUDOSTAFRIKA:
II. EINIGE BIOLOGISCHE BEOBACHTUNGEN, TAXONOMIE UND DISKUSSION

D. S. Brown, G. Oberholzer und J. A. Van Eeden

Der südafrikanische Bulinus natalensis (Küster) und B. tropicus (Krauss) sind in
verschiedenen Publikationen entweder als verschiedene Arten oder als Synonyme
betrachtet worden, und einige Populationen sind neuerdings als intermediär angesehen
worden. В. natalensis ist in die Artengruppe des В. truncatus (Audouin) gestellt
worden, der in Nordafrika und Südwestasien ein Uberträger der Schistosomiasis des
Menschen ist. Darum ist es wichtig, die taxonomische Stellung und Identifikation
des B. natalensis zu klären,

Sechsundachtzig Proben von Schnecken, die zum Komplex B. natalensis/tropicus
gehören, wurden untersucht. Das Sammelgebiet in SE-Afrika, das in dieser Arbeit
beschrieben wird, schliesst die Originalfundorte von B. natalensis und B. zuluensis
(Melvill & Ponsonby) ein. Untersuchungen Über dieSchale, Anatomie der Geschlechts-
organe und Radula, die an anderer Stelle ausführlich besprochen wurden, sind hier
zusammengefasst. Die haploide Chromosomenzahl n=18 ist augenscheinlich einheit-
lich im Komplex B. natalensis/tropicus, abgesehen von zusätzlichen Chromosomen in
einigen Populationen. Die Proteine der Eier von B. natalensis und tropicus zeigten
keine wesentlichen Unterschiede bei Untersuchung mittels Elektrophor. Künstliche
Infection wurde mit 3 Arten von Schistosoma vergeblich versucht, selbst bei Schnecken
von Populationen, die gewisse anatomische Charaktere der B.-truncatus-Gruppe
hatten.

Die Arten Bulinus natalensis, B. tropicus undB. zuluensis warenin unserem Material
vertreten, aber wegen continuierlichen Übergängen konnte keine zufriedenstellende
Abgrenzung vorgenommen verden. Aufalle Fälle war eine geographische Verteilung
gewisser morphologischer Charaktere offensichtlich. Populationen mit gedrückten
Schalen, winklingen Mesoconen an den ersten Radula-Seitenzähnen, bei denen auch
aphallische Individuen vorkamen (B. natalensis), wurden fast ausschliesslich in den
tropischen oder subtropischen Gebieten Südafrikas gefunden. Populationen mit relativ
hochgewundenen Schalen, nicht winkligen Mesoconen und einem normalen Geschlechts-
organ (В. tropicus) wurden als in der Zone gemässigten Klimas vorherrschend fest-
gestellt.

Die Untersuchung der Schnecken aus dem Original-Fundgebiet von Bulinus natalen-
sis zeigte, dass die Häufigkeit winkliger Mesoconen als Charakteristikum dieser Art
betrachtet werden könnte. Die Mehrzahl der vorliegenden Proben wurde nach dem
vorherrschenden Mesoconus-Typ entweder als B.natalensis (= 50% winklig) oder
В. tropicus (> 50% nicht winklig) klassifiziert. Die Original-Fundstelle von В. natal-
ensis liegt nahe der Stidgrenze dieser Form, und die grosse Variabilität der Morphologie,
die hier beobachtet werden konnte, war vielleicht durch Bastardierung mit B. tropicus
verursacht; Kulturmassnahmen können die ökologischen Schranken gestört haben.

Höchstwahrscheinlich ist das Klima der Hauptfaktor für die Verbreitung von
Bulinus natalensis und B. tropicus in Südafrika. Die Aufrechterhaltung der beiden
verschiedenen Formen trotz Kreuzung wird als Ergebnis natürlicher Zuchtwahl
angesehen. B. zuluensis ist eine Lokalform mit besonders gedrücktem Gewinde und
grosser Häufigkeit winkliger Mesoconen; möglicherweise entstand sie durch die
Anpassung des B.natalensis an lacustrine Bedingungen in der Küstenebene von
Nord-Natal und verbreitete sich später Uber verschiedene Biotope, wobei sie die
gedrückte Schalenform beibehielt.

Bulinus natalensis hat gewisse morphologische Charaktere mit der Gruppe des
B. truncatus gemeinsam, aber, nach der Chromosomenzahl, den Ei-Proteinen und
dem immunologischen Verhalten zu urteilen, ist er näher verwandt mit B. tropicus.
Weil B. natalensis und B. tropicus mit 18 Chromosomenpaaren und die Populationen
der B.-truncatus-Gruppe mit 36 Paaren, augenscheinlich in manchen Gebieten des
tropischen Afrika zusammen vorkommen, könnte ihre korrekte Bestimmung von
praktischer Bedeutung sein, da die letztere wahrscheinlich gelegentlich Zwischenwirt
von Schistosoma haematobium ist während B. natalensis nur von einer Fundstelle
experimentell infiziert werden konnte und B. tropicus als abweisend angesehen wird,
In Ermanglung klarer diagnostischer Merkmale der Schale oder Radula werden die
Chromosomenzahl, die biochemischen und immunologischen Befunde wichtig für die
Erkennung von Schnecken der B.-truncatus-Gruppe sein. Es ist abzuwarten, ob weit-
ere Untersuchung morphologischer und anderer Merkmale die Abgrenzung zwischen
B. natalensis und B. tropicus erleichtern werden.

H. 2.

195

196

BROWN, OBERHOLZER AND VAN EEDEN

RESUME

LE COMPLEXE BULINUS NATALENSIS/TROPICUS
(BASOMMATOPHORA: PLANORBIDAE) DANS L’EST SUD-AFRICAIN:
П OBSERVATIONS BIOLOGIQUES, TAXONOMIE ET DISCUSSION GENERALE

D. S. Brown, G. Oberholzer et J. A. Van Eeden

Bulinus natalensis (Küster) et B. tropicus (Krauss) d’Afrique du Sud, ont été con-
sidérés comme distincts ou comme synonymes dans différentes publications et quel-
ques populations ont recemment été classées comme intermédiaires. B. natalensis
a été inclus dans le groupe spécifique B. truncatus (Audouin), qui, en Afrique du Nord
et le Sud-Ouest asiatique, est en relation avec la transmission de la bilharziose.
Pour cette raison, il est important d’élucider le statut taxonomique et l’identification
de B. natalensis.

Quatre-vingt-six échantillons de populations appartenant au complexe Bulinus
natalensis/tropicus ont été étudiés. L’aire d’échantillonnage dans l’Est Sud-africain,
décrite dans le présent article, comprend les localités-type de B. natalensis et B.
zuluensis (Melvill et Ponsonby). Des observations sur la coquille, l’anatomie génitale
et la radula, décrites en detail ailleurs, sont resumées. Le nombre chromosomique
haploide n=18 est apparemment uniforme dans le complexe B. natalensis/tropicus,
sauf chromosomes additionnels dans certaines populations. Les protéihes des oeufs
provenant des populations représentant B. natalensis et tropicus n’ont montré aucune
différence significative aprés analyse par électrophorése. Des infections expérimen-
tales tentées avec 3 espèces de Schistosoma ont été négatives, même dans les cas
où les individus appartenaient à des populations ayant certains caractères anatomiques
du groupe B. truncatus.

Les espéces nominales Bulinus natalensis, B. tropicus et B. zuluensis sont repré-
sentées dans notre matériel, bien qu’aucun taxon satisfaisant n’ait pu @tre défini par
suite d’une variation continue. Cependant, un modelage géographique est évident
pour certains caractéres morphologiques. Les populations ayant des coquilles
déprimées, des mésocônes anguleux sur la premiere dent laterale de la radula et
comportant des animaux aphalliques (B. natalensis) ont été trouvés presqu’exclusive-
ment dans les régions tropicales et sub-tropicales d’Afrique du Sud. Les populations
à coquilles à longues spires, à mésocônes non anguleux et à organe copulateur normal
(B. tropicus) ont été trouvées prédominantes en zone tempérée.

L'étude d’individus du district type de Bulinus natalensis montre qu’une haute
fréquence de mésocónes anguleux pourrait être considérée comme une caracté-
ristique de cette espèce. La majorité des échantillons ont été classés selon le type
de mésocône prédominant soit comme B. natalensis (250% d’anguleux) ou B. tropicus
(250% de non-anguleux). La localité-type de B. natalensis se trouve à la limite sud
de l’aire de cette forme et l’importante variation morphologique observée dans cette
aire est peut-être due à des croisements avec B. tropicus: les activités humaines ont
pu perturber certains facteurs écologiques d’isolement.

Le climat est le facteur le plus probable pour déterminer les domaines de Bulinus
natalensis et B. tropicus en Afrique du Sud. On considère que le rôle de la sélection
naturelle est de maintenir ces formes distinctes en dépit des croisements. B. zulu-
ensis est une forme locale caractérisée par une spire extrêmement déprimée et une
haute fréquence de mésocónes anguleux; elle pourrait tirer son origine d’une forme
adaptative de B. natalensis aux conditions lacustres existant dans la plaine côtière du
Nord du Natal et qui, plus tard, aurait colonisé une variété d’habitats en conservant la
forme déprimée de la coquille.

Bulinus natalensis a certains caractères morphologiques en commun avec le groupe
В. truncatus, mais, si Гоп en juge d’après le nombre de chromosomes, les proteihes
des oeufs et les réactions immunologiques, il est plus proche de B. tropicus. Comme
B. natalensis et B. tropicus, avec 18 paires de chromosomes, et le groupe B. truncatus
avec 36 paires, se rencontrent apparemment ensemble dans certaines aires d'Afrique
tropicale, leur identification correcte serait d’importance pratique. En effet, B.
truncatus est un hôte probable de Schistosoma haematobium, tandis que B. natalensis
n’a été infecté expérimentalement que d’une localité et que B. tropicus est considéré
comme réfractaire. En l’absence d’un diagnostic clair pour les caractères de la
coquille et de la radula, ce sont le nombre de chromosomes et les données biochi-
miques et immunologiques qui sont valables pour l'identification des mollusques du
groupe В. truncatus. Il reste à savoir si des études ultérieures portant sur la mor-
phologie ou d’autres critères, rendront plus facile la différenciation entre В. natalensis

et B. tropicus.
и А. Г.

BULINUS NATALENSIS/TROPICUS COMPLEX II

RESUMEN

EL COMPLEJO BULINUS NATALENSIS/TROPIC US
(BASOMMATOPHORA: PLANORBIDAE) EN EL SUDESTE DE AFRICA:
II. OBSERVACIONES BIOLOGICAS, TAXONOMIA Y DISCUSION GENERAL

D. S. Brown, G. Oberholzer y J. A. Van Eeden

Bulinus natalensis (Küster) y В. tropicus (Krauss), ambos sudafricanos, han sido
considerados como especies distintas o como sinónimos en diferentes publiciones han
sido recientemente clasificadas como intermedias. B. natalensis ha sido incluído en
el B. truncatus (Audouin) -grupo especifico- el cual en el Africa del norte y sudeste
Asia está asociado con la trasmisión de la esquiatosomiasis humana. Por tal razón
es importante dilucidar la condición taxonómica e identificación de B. natalensis.

Se estudiaron 86 muestras de caracoles del complejo В. natalensis/tropicus. El
área geográfica donde se obtuvieron las muestras descriptas en este trabajo, incluye
las localidades típicas de B. natalensis y B. zuluensis (Melvill & Ponsonby). Obser-
vaciones sobre la concha, anatomía genital y rádula, detalladas en otro trabajo, se
sumarizan aquí. El número cromosomático haploido n = 18 es, aparentemente, uni-
forme en el В. natalensis/tropicus, aparte de algunos cromosomas adicionales en
ciertas poblaciones. Proteinas del huevo en B. natalensis/tropicus, cuando se anali-
zaron por electroforesis, no indicaron diferencias. Experimentos de infección con 3
especies de Schistosoma, fracasaron aún en los casos de caracoles de poblaciones
que tenian ciertos caracteres anatómicos del grupo de B. truncatus.

Nominalmente, las especies B. natalensis, B. tropicus y B. zuluensis estaban re-
presentadas en nuestro material, aunque satisfactoriamente los taxa no puieron
definirse a causa de la continua variación. Sin embargo, un patrón geográfico fué
evidente en la variación de ciertos caracteres morfológicos. Poblaciones teniendo
conchas deprimidas, mesoconos angulares en los primeros dientes laterales de la
rádula, e incluyendo algunos individuos afálicos (B. natalensis), se encontraron casi
exclusivamente en las regiones tropicales o subtropicales del Africa del Sur. Pobla-
ciones con, comparativamente, conchas de larga espira, mesoconos no angulares y
órgano copulador normal (В. tropicus) predominaron en la región templada.

El estudio de caracoles, del distrito del tipo de B. natalensis, indicó que una alta
frecuencia de mesoconos angulares podría ser considerada como una caracteristica
de esa especie. La mayoría de las muestras fueron clasificadas de acuerdo al tipo
de mesocono predominante como B. natalensis (=50% angular) o B. tropicus (250% no
angular). La localidad típica de B. natalensis está cerca del limite de distribución
de aquella forma, y la gran variación observada en la morfología en tal area, quizá
se deba al cruzamiento con tropicus: actividades humanas puede haber resultado en
el trastorno de los factores ecológicos de aislamiento.

Clima es el factor que parece determinar la distribución de B. natalensis y B.
tropicus en Africa del Sur, El rol de la selección natural es considerado en la man-
tención de esas formas como distintas a pesar del cruzamiento. B. zuluensis es una
forma local caracterizada por una espira extremadamente deprimida y alta frecuencia
de mesoconos angulares; posiblemente se originó a traves de la adaptación de B.
natalensis a condiciones lacustres sobre la llanura costera del norte de Natal, y
despues colonizó una variedad de habitats, conservando la espira deprimida.

B. natalensis tiene ciertos caracteres morfológicos comunes con el grupo de B.
truncatus pero, a juzgar por el número de sus cromosomas, proteína del huevo y
reacciones inmunológicas, esta más cercanamente relacionado a tropicus. Debido a
que los grupos de B. natalensis/tropicus -con 18 pares de cromosomas- y el de B.
truncatus -con 36 pares- se encuentran, aparentemente, juntos en algunas áreas del
Africa tropical, su correcta identificación puede ser de importancia práctica, ya que
el último es probable huesped potencial de Schistosoma haematobium, mientras que
B. natalensis la infección hecha experimentalmente resultó positiva solo en caracoles
de una localidad única, y B. tropicus es considerado refractivo. En la ausencia de
caracteres diagnosticos claros en la concha o rádula, la evidencia del número cromo-
somático y los datos bioquímicos y inmunológicos, son de valor para la identificación
de los caracoles del grupo de B. truncatus. Queda por ver, si futuros estudios de la
morfología y otros a spectos podran facilitar la diferenciación entre B. natalensis y

B. tropicus.
J. J. P.

197

198

BROWN, OBERHOLZER AND VAN EEDEN

КОМПЛЕКС ‘*BULINUS NATALENSIS/TROPICUS’’ (BASOMMATOPHORA, PLANORBIDAE)
ИЗ ЮГО-ВОСТОЧНОЙ АФРИКИ
Il. Некоторые биологические наблкления, систематика и общие рассужения

N.SpoyH, Г.Оберхольцер и Пж.ВанИлен

Кжно-африканские Bulinus natalensis (Kuster) и B. tropicus (Krauss)
рассматривались авторами или как отлельные випы,‘или как синонимы, и
некоторые популяции в ч cun TCA перехотными. B. natalensis

a

B. truncatus (Audouin), которые в Северной Африке и
3 вязаны с трасмиссией человеческого wucTos0MmMa3zuca.
Поэтому очень в осветить таксономическое положение и лать возможность
точного опретеленияВ. natalensis. SHIM изучены 82 npo3 из комплекса
“*Bulinus a 7. Район сбора материала в юго-восточной Африке,
описанный в настоящей оаботе, вклкчает и места нахсжления типовых форм
В. natalensis и В. zuluensis (Melvill a. Ponsonby).

Были cEelekbl ECO AMERACCA танные по строению _DAKCEHb, рапулы и
AHATOMAM половой системы. Гаплоидное число хромосом (18), BUTUMO,
одинаково Y всех NpelcTası Й комплекса “В. natalensis/tropicus””, кроме TOTO,
= некотосых погуля циях им очные хромосомы. Протеин яиц особей
из популяции В. natalensis и В. tropicus He тал различий после анализа метолом

i

были включены в группу
р A

югозапатной A

электрофореза Зкспериментальное эаражение моллюсков тремя вилами
Schistosoma не пали положительных резульатов, пеаже в том случае, когпа
моллюски были из популяций, имеюсих анатсмические признаки группы

В . truncatus.

T

В матесиале автором были препст вилы Bulinus natalensis, В. tropicus
и В. zuluensis, хотя нельзя было удовлетворительно определить таксоны,
благодаря непрерывной изменчивости Однако, опрепеленная географичность
наблюдалась в характере изменчивости их морфологии. Популяции, имевшие
низкую раковину, угловатый мезокон nepsoro бокового зуба рапулы и,
включая некоторые афаллические особи (В. natalensis), были найлены почти
исключительно в тропических или субтропических районах Ю. Африки. Популяции

со сравнительно дли завитком, не угловатыми мезоконами и нормальными
копулятивными органами (В. tropicus) преобладали в умеренной клима-
тической зоне.

Изучение улиток из типового мес:ообитания Bulinus natalensis показало,

что большая частота встречаемости форм с оугловатым мезоконом может
рассматриваться. как характернае пля этого вида. 5сльшая часть имеющихся
проб сыла определена по преоблалактему типу строения мезокона, как
В. natalensis (=50% угловатых) или В. tropicus (=50% не-угловатых).

Типичное местообитание В. natalensis лежит близ южной границы
распространения этой формы, и наблюлаящаяся здесь большая их
морфологическая изменчивость вероятно происхдит благоларя интерэрилингу
этой формы с В. tropicus: человеческая леятельность может влиять Ha
нарушение некоторых изолируюгих экслогических факторов. Скорее всего
климат представляет собой фактор, определяющий распространение В. natalensis
и В. tropicus в Кжной Африке. Роль естественного отбора сказывается в
сохранении этих видов, несмотря на интербрилинг. В. zuluensis является
локальной Формой, харэктеризуютейся исключительно низким завитком и
большой, частотой встречаемости угловатого мезокона; BO3MOXHO, OH
происходит, благопаря адаптации В. natalensis к озрным условиям на прибрежной
равнине северного Наталя, и позже заселил различные местообитания,
сохранив низкую форму раковины.

Bulinus natalensis имеет некоторые морфологическим признаки, общие с
группой В. truncatus, но суля по числу хромосом, составу протеина их яици
иммунологическим реакциям, они более близки и родственны к В. tropicus.

Поскольку В. natalensis и В. tropicus с 18 парами хромосом и популяции из
группы В. truncatus с 36 парами хромосом, видимо встречаются в некоторых
местах тропической Африки вместе, их правильное определение может иметь
практическое значение, поскольку последние возможно являктся потенцальными
хозяевами Schistosoma haematobium, вто время как В. natalensis лишь из 1 места
пробовали искусственно заражаль. а В. tropicus был признан невосприимчивым.
Без ясных диагностических признаков строения раковины или радулы, число
хромосом, биохимический и иммунологческий анализы будут очень ценны
для определения моллюсков, принадлежащих к группе В. truncatus. Остается
убедиться сможет ли дальнейшее изучение морфолгических и других признаков
облегчить установление различий В. natalensis и В. tropicus.

2.А. Е.

MALACOLOGIA, 1971, 11(1): 199-215

NOTES ON THE BIOLOGY OF ANGUISPIRA ALTERNATA
(STYLOMMATOPHORA: ENDODONTIDAE)!

Adela Skipton Elwell? and Martin J. Ulmer?
ABSTRACT

Anguispiva alternata, the intermediate host of the trematode Postharmosto-
mum helicis, was studied in Iowa in nature and was reared in the laboratory
for a period of over 4 years.

The snail exhibits a habitat preference for deciduous woodlands, mesic mois-
ture conditions, decomposing wood, adequate leaf litter, and low light intensi-
ties. When the snails are not generally active, the best collecting sites are
leaf-clogged spillways. Throughout late spring and summer they can be found
on or in the soil (2-3 cm deep) and on or under the bark of decaying trees. The
most satisfactory laboratory colonies were established in round plastic con-
tainers (26 cm x 9.5 cm) with a perforated cover, containing, from the bottom
up, 0.5-0.8 cm of limestone gravel, 1.2-1.5 cm of sand, 1-2 cm of friable
soil, and topmost leaves, sticks, bark and stones. Food (dried maple leaves,
fresh lettuce, calcium carbonate powder, oatmeal or other cereal) was provided
on unbleached paper towels so as to facilitate weekly removal of old food and
accumulated fecal material. Best results were obtained with containers pre-
pared in advance, with 5-10 snails each, at a relative humidity of 96-100% and
with weekly maintenance.

Laboratory observations indicate that A. alternata does not produce sperm
until its greatest diameter is at least 9 mm and does not oviposit until it is at
least 13 mm. Copulation was observed only once. Colonies maintained at room
temperatures over long periods tended to cease egg production; however, ovi-
position could be initiated by refrigeration at about 10°C for 4 or more weeks
and then keeping them at 20-25°C for 2-4 weeks. Washing formerly refriger-
ated snails and freshening containers also helped stimulate oviposition; a suit-
able substrate was important. The eggs (2-3 mm in diameter) were deposited
at soil depths of 1.5-2.5 cm in masses of 2-40 eggs. Time elapsed between
laying of 2 successive eggs, usually around 15 minutes, varied from 3 minutes
to over an hour. Eggs kept at 20-25°C in plaster of Paris containers hatched
after 28-32 days, those buried in the soil usually after 30-35 days. Snails kept
at 10°C and 30°C did not oviposit. Newly hatched snails (2-3 mm in diameter)
kept at 22°C grew about 0.7 mm during the 1st week and 0.5 mm in the 2nd
week, reaching sizes of about 4, 5, and 6-7 mm by the end of the 13%, 2nd, and
3rd months respectively. By extrapolation of laboratory data, itis estimated
that these snails may attain sizes of 5-8 mm during their 1st summer and 11-
16 mm in their 2nd summer in the wild. Growth is curtailed at 10 C; at 30° it
approximates that at 22°C, although mortality is increased at the higher tem-
perature.

A. alternata avoids high light intensities and is killed by temperatures of 44-
45°C. It can withstand freezing temperatures provided that it has adequate

1
This study was supported in part by National Science Foundation Grants GB-2384 and GB-5465X.
2
| Biology Department, Bemidji State College, Bemidji, Minnesota, 56601.
3
Department of Zoology & Entomology, Iowa State University, Ames, Iowa 50010.

(199)

200

ELWELL AND ULMER

opportunity to become desiccated. Snails taken from frozen ground become
active in 1 hour to 1 day at 22°C. Even very young snails withstand desiccation
for several weeks; large snails estivate for months. Epiphragms can be pro-
duced in 5 minutes when conditions become unfavorable and the snails can be-
come active in minutes when moist conditions return. Tree climbing appears
to be associated with excess soil moisture, and once oriented in an upwards
direction on trees snails rarely turn around and come down of their own voli-
tion. Feeding experiments show that the snail feeds willingly upon the foods
listed above, but consistently avoids dead and decaying animal tissue, mam-
malian feces and dry materials.

The main cause of mortality in the study areas appeared to be predation by
small mammals (mice, chipmunks). Unfavorable environmental conditions may
have contributed. The umbilicus of A. alternata harbored a variety of small
creatures, including nematodes, mites, insects, small earthworms, rotifers,
protozoans, and minute snails. The mantle cavity sometimes contained nema-
todes and protozoans. Metacercariae and sporocysts of Postharmostomum
were frequently found in the pericardial chamber and hepatopancreas respectively.

INTRODUCTION

A relatively common and attractive
snail, Anguispira alternata (Say 1816)
(Fig. 1) has received major taxonomic
attention from Macmillan (1940) andfrom
Pilsbry (1948) and has been the subject
of a number of scattered studies con-
cerning some aspects of its morphology,
behavior, and paleontology (see Baker
1902, 1904; Douglas 1963; Gugler 1963;
Hubricht 1952; Ingram 1941, 1944, 1946;
Jones 1932, 1935a, 1935b; Muchmore
1959). А. alternata has also appeared
in numerous checklists and has been
cited as an intermediate host in the life
cycles of certain helminth parasites.
Older writers, with few exceptions, were
content with descriptions of the shell
and certain anatomical features, but
avoided significant mention of the snail’s
habitat and behavior. Observations con-
cerning the biology of A. alternata in-
cluded herein were made during a study
of the interrelationships between the
snail and the digenetic trematode Post-
harmostomum helicis (Leidy, 1847) Rob-
inson 1949, which utilizes A. alternata
as a first and second intermediate host.

MATERIALS AND METHODS
Snails used in this project were col-

lected in Iowa in Story, Emmet, Boone,
Dickinson, and Hancock Counties. Snails

were placed in cans, jars, or plastic
bags as they were collected and were
provided with sticks and leaves taken
from the sites of collection. Most were
allowed to estivate or were refrigerated
in collecting containers until they were
used, but some were placed in rearing
chambers to establish laboratory colo-
nies. In terraria and plastic containers
used as rearing chambers, a 0.5-0.8 cm
layer of small gravel (usually limestone
fragments) on the bottom of the container
was covered with a layer of sand to a
combined depth no greater than 2 cm,
then 1-2 cm of friable soil was spread
on the sand. An overall depth of 3 cm
or less was found to be most desirable
for observations concerning oviposition
and hatching. Leaves, sticks, bark, and
stones were used in the chambers, and
dried maple leaves, fresh lettuce, cal-
cium carbonate powder, and oatmeal or
Pettijohns (a wheat cereal) were pro-
vided periodically, generally as needed.
The most satisfactory chambers for
long-term maintenance were covered
round plastic containers measuring 26
cm in diameter and 9.5 cm in height,
although smaller plastic boxes measur-
ing 21.6 x 5 6.4 cm were satisfactory
for some shorter experiments. A hot
dissecting needle was used to melt 4-6
holes in the rather tightly fitting covers.
In preliminary observations only 5 snails
were placed in each chamber, but later

BIOLOGY OF ANGUISPIRA

it was found that 10 snails could be
maintained successfully in either the
large or small plastic boxes so long as
adequate amounts of food materials were
provided and the containers were fresh-
ened at regular intervals. Optimal
moisture conditions were most difficult
to maintain, especially in colonies kept
at different temperature levels; close
observation was essential to adjust this
factor. Best results were obtained when
the containers were prepared a week or
more in advance and the conditions were
partially adjusted before introducing the
snails. Relative humidity values of 96-
100% with moist, but not muddy, soil
appeared to favor snail activity. An un-
bleached paper towel was placed over
the soil in each container and food ma-
terials were provided onthe towel, which
facilitated the removal of old food mate-
rials and much excreta. Snails fed ex-
tensively on the towels, even in the pre-
sence of other food materials. Once
established, moisture conditions were
relatively easy to maintain by spraying
the towels briefly with distilled water
when fresh foods and towels were pro-
vided, usually on a weekly, biweekly, or
monthly basis, depending on the number
of snails in the containers and the degree
of snail activity desired. Weekly main-
tenance was most effective in keeping
10 snails actively moving about and
feeding in the round containers described
above.

Eggs laid in the snail rearing con-
tainers were sometimes allowedto hatch
where they were laid, but in most cases
they were carefully removed (by using
a #1 size brush and section lifter) and
placed on small pieces of paper towel
in plaster of Paris containers having a
small amount of dirt in them. These
containers were patterned after those
used by one of us (Ulmer) in rearing
terrestrial snails from eggs, and were
molded at a thickness of 1-2 cminround
pint or half-pint cardboard cartons.
These were covered with glass or plas-

| tic and placed in larger pans or dishes

containing approximately 1-2 cm of wa-

201

ter, just adequate to keep internal sur-
faces moist without introducing standing
water. Newly hatched snails were often
maintained in the hatching chambers for
a month or more by providing food in
small quantities.

A. alternata found under natural con-
ditions are almost invariably “clean”
in appearance, rarely having mudor dirt
encrusted shells even when they have
been burrowing. In contrast, the shells
of laboratory specimens kept in overly
crowded, dirty or moist containers fre-
quently become contaminated with var-
ious growths that cause dirt to adhere.
Shells of laboratory snails kept under
proper conditions generally resemble
those observed in nature. The presence
of earthworms, Collembola (“springtail”
insects), and other invertebrates in lab-
oratory colonies never appeared re-
strictive for the snails, and may actually
have been advantageous in that they
maintained soil aeration and facilitated
burrowing by the snails.

Measurements on eggs and small
shells were made under a dissecting
microscope and recorded to the nearest
tenth of a millimeter. The greatest dia-
meter of snail shells was the measure-
ment employed throughout this study.
The greatest diameters of larger shells
were estimated to the nearest 1/10 mm.

During this study, many shells were
marked with Testor’s model paints, a
highly satisfactory procedure, provided
the shells were adequately prepared be-
fore marking and that the paints were
not too thick when applied. Snails were
first cleaned thoroughly with water and
wiped dry, then the dorsum of each shell
was again cleaned with a water-soaked
cotton swab. Prior to application of
paint with a #0 or #1 size brush, the
shell was again cleaned with 70 or 80%
ethanol on a cotton swab and allowed to
dry. Animals were kept from crawling
on each other. White and yellow paints
were most satisfactory, especially in
locating buried or burrowing snails, but
red, blue, black, and silver were also
useful, In many cases the major por-

202 ELWELL AND ULMER

2 3!
lud!

FIG. 1. Shells of Anguispira alternata A. Apical view B. Umbilical view C. Chewed shell
found near chipmunk burrow. Note white area, probably representing feeding activities of
other snails. D. Remains of A. alternata eaten by laboratory chipmunk.

FIG. 2. Apparatus employedin determining food preferences of Anguispira alternata. Each of
the 8 sides measures 21.6 ст. The central compartment, approximately 10 cm in diameter,

|

BIOLOGY ОЕ ANGUISPIRA

tion of the shell surface was covered
with white or yellow and other colors
were used on top of this paint. When
snails were properly prepared, markings
remained identifiable, even though it
was necessary in a few cases to repaint
numbers that were being wornoff. Those
retained in outdoor cages kept their
markings better than did some kept in
the laboratory, perhaps due to excessive
moisture or activity in captivity. There
was never any indication that the paint
interfered with snail growth or activi-
ties other than avoidance of painted
areas when snails in low-calcium con-
tainers fed on each others’ shells.

In experiments dealing with snail
growth and behavior, some snails were
maintained at temperatures averaging
approximately 22°C (+3°) whiles others
were kept in a refrigerator at approxi-
mately 10°C (+2°) and in a warming
oven at approximately 30°C (+1°). For
a limited time light-temperature cham-
bers were available, but for most of
the study there were no accurate light
controls in use. Refrigerated snails
were exposed to light only when the re-
frigerator door was opened, probably
an average of only twice daily for 20
seconds to afew minutes. Snails in the
warming oven were exposed to only a
little more light than were the refriger-
ated ones. Snails in the laboratory and
animal room were frequently exposed
to long periods of light of moderate
intensities and short periods of darkness.

Soil and air temperatures were mea-
sured with common laboratory centi-
grade thermometers, the soil tempera-
tures being taken at the surface and at
2.5 cm depths. In order to make obser-
vations on feeding preferences, an oc-
tagonal-shaped wooden chamber (21.6

203

cm on a side) was constructed. It con-
sisted of 8 trapezoidal compartments,
all of which opened into a central round
area approximately 10 cm in diameter.
This apparatus is shown in Figure 2.
Each of the eight compartments was
provided with a container of water,
usually with a strip of paper toweling
extended from the water to increase
humidity. Different food materials were
offered singly or in combination in each
compartment. Marked snails were placed
in a small, uncovered jar or dish in the
center of the apparatus. The whole ap-
paratus was then covered with a piece
of glass and the movements of the snails
were periodically checked to determine
food preferences.

Some attempts were made to utilize
Snail attractants in woodlands to facil-
itate collecting. Although Douglas (1963)
found A. alternata to be attracted to var-
ious materials such as peanut butter,
oatmeal, and fruits used as bait for
other animals, such materials were not
effective in the habitats studied. During
this study the most effective attractants
proved to be empty portland cement
bags and other large pieces of heavy
paper or cardboard. Calcium may have
been an added attraction in the cement
bags. Over an extended period of time,
materials that retained moisture or pre-
vent the soil from drying out were effec-
tive in concentrating A. alternata, but
they were of no significant value in aid-
ing the collection of snails over a peri-
od of only a few days.

Dissection was done under a dissecting
microscope after washing the snail care-
fully and opening its shell from the ven-
tral surface by pressing 2 sturdy dis-
secting needles against inside surfaces
of the umbilicus. Sufficient force was

contains an aluminum dish within which marked snails can be seen; in each trapezoidal com-
partment is an aluminum water dish. Foods of various types in combination with decaying wood

| were offered in all but one compartment in the set-up shown here.

The floor of the apparatus

was covered with aluminum foil to facilitate cleaning and to negate the effects of past experi-

ments, and the top was covered with clear or dark glass, depending on the experiment.

vations were made at intervals.

Obser-

204 ELWELL AND ULMER

exerted to fracture the shell, but not so
much that underlying tissues were torn.
Shell fragments were then picked away,
leaving the snail essentially intact. It
was often difficult to separate the api-
cal portion of the hepatopancreas from
the columella and in many dissections
this tissue was inadvertently damaged
or separated. Hermaphroditic duct,
uterus, spermatheca, spermathecal duct,
and the penis sac were examined for
sperm by making aqueous mounts of
portions of the structures and examin-
ing them with a compound microscope.
Pericardial cavity, kidney, and hepato-
pancreas were routinely examined for
parasites.

OBSERVATIONS
Habitat

Anguispira alternata was found pre-
dominantly in weli-established decidu-
ous forests with mesic soil conditions
and generally low light intensities dur-
ing the summer. They were most nu-
merous on north-facing slopes where
there were downed trees in various
stages of decomposition and abundant
leaf litter in fall, winter and spring.
Limited observations made in this study
tend to support the opinions of Burch
(1955) and Atkins (1966) that the snails
prefer areas in which soil has a high
calcium content. Best collecting sites
in fall andearly spring were leaf-clogged
spillways, perhaps because of greater
water retention. In at least one collec-
ting area there was a conspicuous size
differential between snails found on and
in the soil and those found under bark
on decaying trees. Larger snails (8-19
mm) were found on the soil surface or
at depths of approximately 2-3 cm; smal-
ler ones (3-7 mm) were found under
bark on decaying trees.

Reproductive Maturity

All ovipositing snails observed during
this study were 13mm or more in
greatest diameter. No sperm were found
in the reproductive tracts of snails

smaller than 9 mm indiameter, although
some snails larger than 9 mm and smal-
ler than 12 mm did not contain sperm.
There was a considerable variation in
the degree of reproductive organ devel-
opment among snails of the same size.
In specimens less than 9 mm, repro-
ductive systems appeared very imma-
ture and underdeveloped in comparison
with other structures, and inmany cases
tubules were so small and transparent
that they were easily overlooked in a
quick dissection. Scheltema (1964) also
found a relationship between shell size
and reproductive maturity in the mud
snail Nassarius obsoletus. Because of
the role of environmental factors in
determining feeding and other activities
of A. alternata, it is difficult to assess
age of the snails on the basis of their
size. On the basis of projected growth
curves, it would appear thatA. alternata
may possibly lay eggs in the spring or
early summer approximately 2 years
after hatching. Kingston (1966), how-
ever, reports that laboratory reared A.
alternata laid eggs for the first time at
4 years of age.

In spite of repeated attempts to pro-
cure data on courtship and copulation,
only one mating was observed. One of
the 2 snails engaged in the incident laid
13 eggs the next day.

Egg-laying could be initiated by re-
frigeration at 10°C for 4 or more weeks
followed by a 2-4 week period of expo-
sure to 20°-25°C temperatures. Clean-
ing the snails and freshening the con-
tainers also seemed to aid in initiation
of oviposition by formerly refrigerated
snails. Snails maintained in the labora-
tory at room temperatures over a long
period of time tended to cease laying
eggs, even though they were well cared
for. Although newly collected snails
occasionally laid a few eggs in tempo-
rary containers devoid of earth sub-
strate, snails maintained in the labora-
tory for more than 2 days did not ovi-
posit in the absence of a substrate suit-
able for burrowing. Soil, fine gravel
(used by Kingston, 1966), or decaying

|

BIOLOGY OF ANGUISPIRA

wood served well. Burrowing and ex-
tensive defecation preceded oviposition
and most eggs were deposited at soil
depths between 1.5-2.5 cm. Some factor
or complex of factors related to sub-
strate may trigger oviposition in A.
alternata, for fecal material released
prior to egg-laying containedlarge quan-
tities of soil in contrast to fecal mate-
rial released at other times. In many
cases 2 snails burrowed together, and
it was frequently difficult or impossible
to ascertain which snail had laid a given
egg clutch. The number of eggs known
to have been laid by individual snails
varied from 2 to 25, but some masses
were found that contained 40 or more
eggs. Larger masses appeared to con-
tain more than one clutch when they
were carefully separated, indicating that
Oviposition sites were shared by 2 or
more snails.

Although observations of egg-laying
are made with difficulty it was found
that 15 minutes or less usually elapsed
between the laying of 2 eggs, although
sometimes an hour or more passed.
One snail laid 14 eggs within 45 minutes.
No oviposition occurred among snails
while they were being maintained at
temperatures approximating 10°C or
30°C.

Hatching of Eggs

A. alternata’s nearly spherical eggs
are generally between 2 and 3 mm in
greatest diameter and have sparkling
white calcareous shells covered with a
thin, almost membranous layer of mucus.
There was considerable variation in in-
cubation periods among eggs of the same
clutch. Of 309 eggs hatched in plaster
of Paris containers kept at 20°-25°C
during 1965 and 1966, most hatched
after incubation periods of between 28-
32 days. Three snails removed from
their eggshells on the 36th day and 4
removed on the 41st day survived, but 6
others died. Several 46 day old eggs
contained living snails too immature to
Survive. A few young hatching after 35-

205

40 days’ incubation were observed to be
abnormally quiescent and did not grow
as rapidly as most of the other snails.
The percentage of eggs hatching in indi-
vidual clutches varied from 40-100%,
although in most clutches hatching suc-
cess was between 90-100%. Eggs left
where they were laid in sufficiently
moist, uncrowded containers well sup-
plied with food usually hatched in 30-35
days and very few failed to hatch. Some
buried clutches required 35-42 days of
incubation. Although adult snails laid
eggs in crowded containers, their bur-
rowing frequently disrupted the egg mas-
ses and a few snails were observed
feeding on unhatched eggs.

Kingston (1966) presented data on
clutch and egg size comparable to our
findings and found that A. alternata eggs
maintained at 16°-19°C required from
46-54 days of incubation. He reported
incubation periods ranging from 20-72
days, extremes that were not encoun-
tered during this study.

Greatest diameters of newly hatched
A. alteynata were almost identical to
that of their eggshells (2-3 mm). It was
sometimes difficult to ascertain accu-
rately the time of hatching, for the young
eroded the eggshell away from inside
and often moved about with a large por-
tion of eggshell still covering most of
the shell. Ashatchingbecame imminent,
the eggshell became darker and incres-
ingly translucent, and the young snail
could be seen moving about inside. After
hatching, the young often fed on their
own cast eggshells, and occasionally on
unhatched eggs in the same clutch.
Young snails hatched in the plaster of
Paris containers generally moved about
freely, but those hatched in burrows in
terraria sometimes remained clustered
for as long as 2 months before moving
to the surface of the container. Such
observations tend to support findings in
nature, for clusters of very small snails,
or young snails appearing to be of the
same age, are frequently found in rotting
wood or in the soft soil under logs or

206 ELWELL AND ULMER

leaf litter.

Some Aspects of Anguispira alternata
Behavior

1. Responses to Moisture

A.alternata of all sizes have a re-
markable ability to withstand desiccation
by withdrawing into their shells and se-
creting epiphragms in the manner of
other terrestrial pulmonates described
by Binney (1885: 10-11). In this study,
even very young snails (2-3 mm) were
able to withstand dry conditions for pe-
riods of several weeks, and large snails
estivated for months at a time with no
apparent ill effects. Epiphragms were
often produced in as little as 5 minutes
and served to hold snails to trees, logs
or other substrates when conditions be-
come unfavorable for activity. During
periods of estivation, no externally mea-
surable growth occurred. The snails
responded quickly to rapidly-changing
environmental moisture conditions, se-
creting epiphragms as the environment
dried out and oftenbecoming active with-
in minutes in response to moisture fol-
lowing periods of dryness. Response
to moisture appeared to be delayed at
low temperatures. Snails removedfrom
frozen ground during the winter took
from 1 hour to 1 day to become active
when placed in moist containers at tem-
peratures near 22°C.

Whenever possible, A. alternata extri-
cated itself rapidly from immersal in
water. Tree-climbing by large numbers
of snails was commonly observed fol-
lowing rains or heavy dew which re-
sulted in saturated surface soils. Of
approximately 23 snails whose shells
and positions on live trees were marked,
none appeared to move downward, but
simply estivated as conditions became
dry, only to proceed upwards when the
tree surface became wet again. Several
snails were observed to follow branches
out to the tips of twigs, where they esti-
vated for days before disappearing.
Blinn (1961) reported similar findings
in his work with Allogona profunda and

Mesodon thyroidus. Inthe present study,
all types of deciduous trees in the areas
investigated were utilized by climbing
snails. Although the greatest height at
which snails were seen was 7-8 m from
the ground, trees were not routinely
examined at this height and it is possi-
ble that snails move considerably higher.

2. Responses to Light and Heat

A. alternata was repeatedly observed
to be negatively phototropic under nor-
mal conditions. Although light does not
influence activity to the same extent as
does moisture or temperature, it appears
to be a factor in limiting activity during
the daylight hours in normal habitats.
When exposed to light intensities of 2153-
2259 lumens/m?, active snails turned
away toward lower intensities of 215-
269 lumens/m?. Snails living in con-
tainers constantly subjected to lights of
moderate room intensities seemed to
acclimate themselves to continuous light
and were frequently observed moving
about. Snails observed in nature were
much more active at night and on dark,
cloudy days than they were during pe-
riods of bright sunlight, even when tem-
perature and moisture conditions were
favorable for activity. When active
Snails in dim light were suddenly sub-
jected to bright light, they responded by
secreting themselves under available
cover. A few individuals were more
refractory to the effect of light than
others.

The responses of A. alternata to high
light intensities and solar heat were ob-
served on a hot, humid day in July. In
one instance, 4 adult snails were placed
in a plastic container and shade was
provided an inch away from them, in
the direction toward the sun. The ani-
mals were positioned in such a way that
their apertures were directed toward
the sun. Three of the 4 moved into the
shade, but the fourth, observed in pre-
vious experiments to be strongly nega-
tively phototropic, turned away from the
sun and moved toward the far end of the
container, in which no shade was avail-

BIOLOGY OF ANGUISPIRA 207

able. In another instance, 5 adult snails
were placed on hot concrete (surface
temperature 45.3°C), with their aper-
tures directed toward the sun. In 5
minutes, one snail moved 7-8 cm north
away from the direction of the sun, then
stopped. Reactions of the second snail
indicated confusion: it extended its foot,
moved briefly southward toward the
sun, then turned sideways and clumsily
worked its way around the side of a
wooden block (a distance of about 2 cm)
but seemed unable to completely shade
itself before becoming inactive. The
remaining 3 snails remained completely
retracted. Activity in heat stress was
disorganized and ineffective waves of
muscle contraction were often seen mov-
ing along the foot. Movement of snails
on hot surfaces was different from nor-
mal movement in that the shell dragged
alongside and was not held up over the
foot. Furthermore, some snails held
the posterior end of the foot up in a
most peculiar fashion.
Six adult snails placed in a plastic
container exposed to noon sunlight of
53820 lumens/m2 and a temperature of
44.4°C. were observed toturnaway from
the sun within 5 minutes and move to-
ward the north end of the container,
even though they had been placed near a
shaded compartment at the south end.
Upon reaching the north end they ap-
peared confused; several climbed the
sun-drenched walls and fumbled about,
while the others eventually moved back
toward the shaded compartment at the
south end. Within 30 minutes from the
beginning of the trial 2 snails succeeded
in entering the shaded chamber, but the
others retracted into their shells. An
hour and 25 minutes after the beginning
| of the experiment, the 4 exposed snails
_ were dead, but the 2 shaded ones quickly
recovered when removed to more mod-
erate temperatures. During this period
| light intensity varied from 21528-53820
| lumens/m?, dipping briefly to 10764 as
| afew scattered clouds moved across the
sky. A similar experiment in which the
Shaded block house was positioned in

the north end of the container ended
essentially the same way, with 2 snails
entering the safety of the shade, 2 others
fumbling about in a disorganized fashion
until they retracted, and the remaining
2 starting definitely in a northward di-
rection, but retracting before reaching
the shade. Some snails exposed to in-
tense noon sunlight died within 10 min-
utes.

In limited observations (see Elwell,
1967) it was found that alternating light
and dark was most favorable for growth
and that continuous darkness was disad-
vantageous.

3. Effects of Low Temperatures

Repeated observations of A. alternata
exposed to sub-freezing temperatures
determined that, provided the snails
have been reasonably well-fed and then
allowed to desiccate, they were able to
withstand freezing conditions very well
for months at a time. However, when
recently active snails were subjected to
sudden freezing, they did not recover.

Feeding Preferences

A number of experiments were con-
ducted in an attempt to determine some
feeding preferences of A. alternata.
Snails in these experiments repeatedly
avoided fresh and rotting meat, dead
snail tissue (removed from shell), and
mammalian fecal material, and demon-
strated a preference for plant materials.
In addition to animal tissues and excre-
ta, other materials offered singly and in
combination were: calcium carbonate,
lettuce, decaying and new wood, dried
and fresh deciduous leaves, oatmeal,
Pettijohn cereal (uncooked), galactose
and sucrose sugars, soiled wood shav-
ings from a mouse cage, sphagnum
moss, and paper towels. Feeding con-
tainers were kept moist to encourage
optimal activity. Lettuce and oatmeal
were much fed upon, especially early in
feeding experiments, although after in-
gestion of these materials, the snails
usually moved to either paper towels or
soft, decaying wood.

208 ELWELL AND ULMER

FIG. 3. Actively moving Anguispira alter-
nata. Note extended tentacles.
FIG. 4. Typical position of Anguispira alter-

nata while feeding. Note withdrawn tentacles.

In one experiment a round plastic con-
tainer, set up in the same manner as
other rearing chambers with a paper
towel over the soil surface, was used to
offer lettuce, oak leaves, soiled shav-
ings, mouse feces, a dead snail, oatmeal
and calcium carbonate. Thirty marked,
previously starved snails were placedin
the center of the container at 2330hours
and kept in darkness except for spot
checks to ascertain activity. After half
an hour, 9 snails were feeding on lettuce,
6 on oatmeal, and most of the others

were just in the process of moving away
from the center. Snails bound toward
food materials (Fig. 3) extended their
tentacles outwards more than quiescent
snails, and feeding snails (Fig. 4) were
observed to have short tentacles, ap-
proximately '/ the length of the “quest-
ing” snails. Snails feeding on one food
appeared to extend their tentacles im-
mediately before proceding to another
food. About 1/2hours after the begin-
ning of the experiment, 9 snails were
feeding on lettuce and 9 on oatmeal. By
this time some of the original lettuce
and oatmeal feeders had moved off in
other directions, and some were climb-
ing on the top and sides of the container.
By 0400 hours most of the snails were
inactive and during the following day the
animals gradually gathered on andunder
the portion of the paper towel nearest
the oatmeal. During the following 2
days there was little movement, 20 or
more snails remaining under the paper
towel at all times. On the 4thday snails
were observed on the shavings for the
first time, though they did not appear
to be feeding. The dead snail and the
fecal material were consistently avoided
and the calcium carbonate was visited
by only a few individuals.

Other experiments utilizing the octag-
onal wooden apparatus previously de-
scribed also demonstrated the prefer-
ences of the snails for mixtures of oat-
meal, lettuce, leaves, moist, decaying
wood, paper, and calcium carbonate. As
the apparatus was allowed to dry out it
was obvious that the snails sought re-
maining pockets of moisture. Slime
trails seemed to attract snails, perhaps
due to the water-retaining property of
the mucus. Fungal growth did not deter
the feeding of normal, healthy snails.
Sphagnum moss, clean, boiled wood, and
fecal materials were not fed upon. Food
materials presented in small plastic
bowls did not attract animals as much
as did foods presented on pieces of
aluminum foil on the floor of the con-
tainer.

BIOLOGY OF ANGUISPIRA

(in mm)

Diameter of shell

1 2 3 4 5 6
Age

FIG. 5.
tions at temperatures averaging 22°C.

Growth, Development and Activity

Because the growth of A. alternata
depends so much on the snails’ activity,
which is determined by environmental
factors, it is virtually impossible to
determine the age of an individual on
the basis of its size. Measurements
made onnewly-hatched snails maintained
under favorable moisture, food andtem-
perature conditions indicate that young
snails may increase approximately 0.1

mm in greatest diameter per day for

|
|
|

|

the first week.
_ curves for 2 snails kept at approximately

Fig. 5 shows growth

22°C for 3 4/2 months after hatching.

| Newly hatched snails approximately 2
| mm in greatest diameter may grow as
much as 0.7 mm in their first week,

0.5 mm their second week, and may be
about 4 mm in diameter by the end of

209

8 9 KOS a 12 EE

(in weeks)

Growth of 2 Anguispira alternata maintained under favorable food and moisture condi-

their first month. By the end of the
second month they may be over 5 mm
and by the end of the third month they
may be 6-7 mm. If one assumes that
conditions favorable for activity and
growth would exist in some localities in
lowa for perhaps 3 or 4 months of the
year, it is reasonable that young snails
may attain a size of 5-8 mm by the end
of their first summer, assuming that
hatching occurred before the middle of
June. Snails hatching later may be 3-5
mm by the end of the summer.

During the second summer, 5-8 mm
individuals may reach 11-15 mm in
greatest diameter, and it is possible
that some robust individuals living in
optimal habitats may attain sizes of 16
mm or more. It appears that most
snails produce sperm during their sec-
ond summer and perhaps some attain

210 ELWELL AND ULMER

reproductive maturity, manifested by
oviposition. On the basis of growth
curves presented in Figs. 5 and 6 and
dissection data obtained from 106 A.
alternata, we estimate that most A.
alteynata in favorable habitats in Iowa
begin oviposition 2-3 years from their
hatching, probably during the 3rd sum-
mer. Since snails are so dependent on
moisture and temperature, it is to be
expected that average growth rates vary
considerably depending upon habitat and
environmental fluctuations. Growthdur-
ing a cool or dry summer, for instance,
may be retarded by comparison with
growth during a mild summer with fre-
quent gentle rains.

Projection of growth curves for free-
living snails using laboratory-obtained
data is frought with pitfalls. Dry con-
ditions initiate estivation, yet excessive
soil moisture may drive the snails up
trees, where again, estivation may occur.
Snails living in micro-habitats near
woodland springs with moderate amounts
of water constantly available may be
far more active and grow much faster
than snails living under logs or dry
litter elsewhere in the same forest. It
appears that responses of A. alternata
to moisture, light, wind and foods gen-
erally keep the animals in optimal habi-
tats and facilitate return to such habi-
tats following excursions initiated by
generally favorable conditions. How-
ever, the ability of the animals to esti-
vate, thus allowing for survival during
some unfavorable conditions, tends to
provide for species dispersal and colo-
nization of new areas.

Growth of snails kept at temperatures
near 10°C is severely curtailed, as can
be seen in Fig. 6. Although snails re-
tained at 30°C grow at nearly the same
rate as those kept at 22°C, they were
not as healthy as those at 22°C or 10°C,
and there was a higher mortality rate
among snails kept at the high tempera-
ture. Most snails at 10°C remainhealthy
and are sometimes observed moving
about and feeding, although they are
obviously not as active, nor do they feed

as much, as snails kept at the higher
temperatures. It is possible that growth
of the 10°C snails was significantly in-
fluenced by their weekly removal from
the refrigerator for maintenence and
examination. Herzberg & Herzberg
(1960) found that cold severely inhib-
ited growth of Helix aspersa maintained
at 5° C.

Mortality

During this investigation, chewed A.
alteynata shells (Fig. 1) were found in
all study areas. Several times, hun-
dreds of chewed shells were found scat-
tered around logs where chipmunks had
been observed in the process of feeding.
When snails were offered to laboratory
chipmunks (Tamias striatus) and white-
footed deer mice (Peromyscus manicu-
latus and P. leucopus) they were rapidly
consumed, the shells being chewedinthe
same fashion as those found in nature.
In the study areas the fact that more
chewed than unchewed discarded shells
were found indicates that predation was
the leading cause of mortality. Ingram
(1942) reported that short-tailed shrews
(Blarina brevicauda talpoides) stocked
a “culture” with various Slugs and snails,
including A. alternata. Inour study areas
shrews were not trapped, though Mus,
Tamias, and Peromyscus were; no at-
tempt was made to trap larger mam-
mals, such as raccoons and opossums,
who may also feed on the snails.

When collections of estivating snails
were made, there were usually some
individuals that did not recover from
estivation, which suggests that these
animals may not have been adequately
prepared to endure the rigors of unfa-
vorable environmental conditions. It is
probable that some snail mortality fol-
lows lengthy spring thaws (during which
snails become active) that are termi-
nated by freezing temperatures.

Mortality attributable to insects was
not observed, although on one occasion
a 3mm dipteran larva was found in the
mantle cavity of one individual. As will
be shown in another paper, mortality

BIOLOGY OF ANGUISPIRA 211

(IN MILLIMETERS)

DIAMETER OF SHELL

4 8 12 16 4
A. 22°C (AVERAGE )

B. 30° C(AVERAGE

O =REPLACEMENT

C. 10°C (AVERAGE)

TIME (IN WEEKS)

FIG. 6.

was far greater among snails parasi-
tized with the trematode Postharmosto-
mum helicis when the snails were kept
at 30°C; presumably parasitism, in com-
bination with other stresses, contributes
to mortality. Bacterial or viral infec-
tions may cause some deaths as sug-
gested by the sluggish behavior and ab-
normal mucus secretion of some snails
preceding their demise. The mucus of
these animals was cloudy, contained
clumps of white material and was laden
with bacteria. Overly moist containers
with decaying lettuce and an unsuitable
substrate contributed to this condition.
It did not appear that fungus encountered
was a Significant cause of mortality
among otherwise healthy snails, though
it may have contributed to the death of

Growth of Anguispira alternata maintained at different average temperatures

individuals weakened or disadvantaged
by environmental factors or other infec-
tions.

Animal Associates of Anguispira
alternata

The umbilicus of А. alternata was
found to harbor a variety of small crea-
tures, including nematodes, mites, in-
sects (especially Collembola) and insect
larvae, smallearthworms, rotifers, pro-
tozoans, and minute snails. The mantle
cavity of many A. alternata contained
nematodes and protozoans. As previ-
ously noted, a 3 mm dipteran larva was
found in the mantle cavity of a 16.2 mm
snail. Metacercariae of the trematode
Postharmostomum helicis were fre-
quently found in the pericardial cavity

212 ELWELL AND ULMER

of the snails, and occasionally sporo-
cyst infections were found in the hepa-
topancreas. Protozoans found occasion-
ally in the mantle cavity, kidney, peri-
cardial cavity, and reproductive sys-
tems appeared to by the ciliate Myxo-
phyllum steenstrupi, reported from pul-
monate snails (including A. alternata) in
Iowa by Penn (1958). Unidentified nema-
todes were sometimes found in the re-
productive ducts and uterus of the snails
in relatively large numbers. A mite
(order Astigmata, suborder Acaridei)
was once found in the stomach of a
5.3 mm A. alternata

LITERATURE CITED

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the structure and distribution of ter-
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BAKER, F.C., 1902, Mollusca of the
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Bull. of Natur. Hist. Surv., No. 3, Part
2.

BAKER, F. C., 1904, Spire variation in
Pyramidula alternata. Amer. Natur.,
38: 661-668.

BINNEY, У. G., 1885, A manual of North
American land shells. U.S. Nat. Mus.,
Bull. 28.

BLINN, W. C., 1961, Aspects of ecology,
behavior, and physiology of land snails,
particularly of Mesodon thyroidus
(Say) and Allogona profunda (Say).
Dissertation Abstracts, 22: 2915.

BURCH, J. B., 1955, The land snails of
Hanover, Henrico, and Chesterfield
Counties, Virginia. Virginia J. Sci.,
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DOUGLAS, C. L., 1963, Population anal-
yses, variation and behavior of Angui-
spira alternata. Trans. Kansas Acad.
Sci., 66(2): 186-194. _

ELWELL, А. S., 1967, Biology of An-
guispiva alternata (Gastropoda: Endo-
dontidae) with special reference to
the digenetic trematode Postharmos-
tomum helicis. Dissertation Abstracts
28(4): 1725-26B.

GUGLER, C. W., 1963, The eggs and
egg-laying habits of some midwestern
land snails. Trans. Kansas Acad. Sci.,

66(2): 195-201.

HERZBERG, F. & HERZBERG, A., 1960,
The effect of cold on the growth of
Helix aspersa. J. Exp. Zool., 145(3):
191-196.

HUBRICHT, L., 1952, The land snails
of Pittsylvania County, Virginia. Nau-
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INGRAM, W. M., 1941, Habits of land
Mollusca at Rensselaerville, Albany
County, New York. Amer. Midl.
Natur., 25(3): 644-651.

INGRAM, W. M., 1942, Snail associates
of Blarina brevicauda talpoides (Say).
J. Mammalogy, 23(3): 255-258.

INGRAM, W. M., 1944, Notes on winter
habits of land mollusks at Ithaca,
New York. Nautilus, 58(1): 25-27.

INGRAM, W. M., 1946, Land Mollusca
of the Edmund Niles Huyck Preserve,
Rensselaerville, New York. Nautilus,
59(3): 87-93.

JONES, D. T., 1932 (1933), Some ana-
tomical features of the tiger snail,
Anguispiva alternata (Say). Proc.
Indiana Acad. Sci., 42: 243-250.

JONES, D. T., 1935a, Burrowing of
snails. Nautilus, 48(4): 140-142.

JONES, D. T., 1935b, The formation of
shell in the tiger snail. J. Morphology,
57(2): 547-568.

KINGSTON, N., 1966, Observations on
the laboratory rearing of terrestrial
molluscs. Amer. Midl. Natur., 76(2):
528-532.

MacMILLAN, G. K., 1940, A mono-
graphic study of the snails of the
genera Anguispira and Discus of North
America, exclusive of Mexico. Ann.
Carnegie Inst., 27: 371-426.

MUCHMORE, У. B., 1959, Land snails
of E. N. Huyck Preserve, New York.
Nautilus, 72(3): 85-89.

PENN, J. H., 1958, Studies on ciliates
from mollusks of Iowa. Proc. Iowa
Acad. Sci., 65: 517-534.

PILSBRY, H. A., 1948, Land Mollusca
of North America (North of Mexico).
Volume 2, Part 2. Acad. Natur. Sci.
Philad., Monograph No. 3.

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sarius obsoletus. Chesapeake Sci.,
5(4): 161-166.

BIOLOGY OF ANGUISPIRA

ZUSAMMENFASSUNG

ZUR BIOLOGIE VON ANGUISPIRA ALTERNATA
(STYLOMMATOPHORA, ENDODONTIDAE)

A. S. Elwell und M. J. Ulmer

Anguispira alternata, der Zwischenwirt des Trematoden Postharmostomum helicis,
wurde in Iowa in Freiheit untersucht undim Laboratorium ther 4 Jahre lang geztichtet.

Die Schnecke zeigt Vorliebe für sommergrüne Laubwälder, mässige Feuchtigkeit,
modriges Holz und Laub sowie schwaches Licht. Wenn die Tiere nicht aktiv sind,
findet man sie am Sichersten in von Laub erfüllten Wasserrinnen. Im späten Frühling
und Sommer können sie auf dem Boden oder 2-3 cm tief darin gefunden werden und
auf oder unter der Rinde modriger Bäume. Die erfolgreichsten Laboratoriumszuchten
wurden in runden Plastbüchsen (26 x 9,6 cm) angesetzt, mit durchlöchertem Deckel,
in die zuunterest 0,5-0,8 cm Kalkbrocken, darauf 1,2-1,5 cm Sand, 1-2 cm bröcklige
Erde und obenauf Laub, Aststückchen, Rinde und Steine getan worden waren. Futter
(getrocknete Ahornblätter, frischer Salat, Kalkpulver, Hafermehl oder andere Getreide-
erzeugnisse) wurde auf Stückchen ungebleichten Papiers gegeben, um den wöchent-
lichen Wechsel des Futters und die Entfernung der Fäces zu erleichtern. Die besten
Resultate wurden mit Büchsen erreicht, die für einerelative Feuchtigkeit von 96-100%
vorbereitet, mit 5-10 Schnecken besetzt und wöchentlich nachgesehen wurden.

Beobachtungen im Laboratorium zeigen, dass A. alternata kein Sperma pro-
duziert, ehe ihr grösster Durchmesser mindestens 9 mm beträgt, und keine Eier
legt, ehe sie mindestens 13 cm gross ist. Корша wurde nur einmal beobachtet.
Kolonien, die bei Zimmertemperatur gehalten wurden, legten lange Zeit keine
Eier. Aber Eiablage konnte dadurch veranlasst werden, dass man sie 4 Wochen
oder länger bei 10°C hielt und dann 2-4 Wochen bei 2032550: Ktihlgehaltene
Schnecken zu waschen oder Abkühlen der Büchsen half ebenfalls, die Eiablage herbei-
zuführen. Ein günstiges Substrat war wichtig. Die Eier (2-3 mm im Durchmesser)
wurden 1,5-2,5 cm tief in den Boden gelegt und zwar zu 2-40 Stück. Zwischen der
Ablage zweier aufeinanderfolgender Eier vergingen 3 Minuten bis Über eine Stunde,
im Durchschnitt 15 Minuten. Eier, die bei 20-25° in Gipsbehältern lagen, schlüpften
nach 28-32 Tagen, die im Boden vergrabenen gewöhnlich nach 30-35 Tagen. Schnecken,
die bei 10° oder 30° gehalten wurden, legtenkeine Eier. Frisch geschlüpfte Schnecken
(2-3 mm in Durchmesser), die bei 22° gehalten wurden, wuchsen während der ersten
Woche etwa 0,7 mm, in der zweiten 0,5 mm und massen am Ende des ersten Monats
4 mm, im zweiten 5 und im dritten 6-7 mm. Danach ist anzunehmen, dass diese
Schnecken während des ersten Sommers Grossen von 5-8 mm und im zweiten Sommer
11-16 mm erreichen können. Bei 10° lässt das Wachstum nach, bei 30° ist es Ähnlich
dem bei 22°, aber die Sterblichkeit ist bei höheren Temperaturen grösser.

A. alternata vermeidet helles Licht und stirbt bei Temperaturen von 44-45°. Sie
kann Frost Überstehen, vorausgesetzt, dass sie vorher trockengehalten war. Schnecken,
die aus frostigem Boden genommen werden, werdenbei 22° in einer Stunde, spätestens
nach einem Tag aktiv. Selbst ganz junge Schnecken können Trockenheit von mehreren
Wochen überstehen. Grosse Schnecken halten einen monatelangen Trockenschlaf.
Ein Epiphragma kann innerhalb 5 Minuten gebildet werden, wenn die Bedingungen
ungünstig werden, und die Schnecken können in Minuten wieder aktiv werden, wenn
Feuchtigkeit vorhanden ist. Auf Bäume klettern sienur bei starker Bodenfeuchtigkeit,
und wenn sie einmal aufwärts steigen, kehren sie selten freiwillig um. Fütterungs-
versuche zeigen, dass sie das oben genannte Futter gern fressen, aber sie vermeiden
konsequent totes und faulendes tierisches Gewebe, Säugetier-Fäces und trockene
Materialien.

Die hauptsächlichste Todesursache im Untersuchungsgebiet schien das Gefressen-
werden durch kleine Säuger (Mäuse, Spitzmäuse). Ungünstige Umweltbedingungen
können dazu beigetragen haben. Der Nabel von A. alternata beherbergt verschiedene
kleine Tiere wie Nematoden, Milben, Insekten, kleine Regenwürmer, Rädertierchen,
Protozoen und winzige Schnecken. Die Mantelhöhle enthielt manchmal Nematoden
und Protozoen. Metacercarien und Sporocysten von Postharmostomum worden oft
im Herzbeutel oder im Hepatopancreas gefunden,

H. 2.

213

214

ELWELL AND ULMER

RESUMEN

NOTAS SOBRE LA BIOLOGIA DE ANGUISPIRA ALTERNATA
(STYLOMMA TOPHORA: ENDODONTIDAE)

A. S. Elwell y M. J. Ulmer

Anguispira alternata, huésped intermediario del trematodo Postharmostomum
helicis, fue estudiado en su ambiente natural en lowa, y criado en el laboratorio por
un periodo de 4 años.

El caracol habita con preferencia en bosques de hoja caduca y mediana humedad,
maderas en descomposición y hojarasca, y lugares de iluminación pobre. Cuando no
estan an actividad, los mejores lugares para colectarlos es donde hay resaca de
arrastre atestado de hojas. Al final de la primavera y en el verano pueden encon-
trarse sobre, o en el suelo (enterrados a 2-3 cm) y sobre o bajo la corteza de troncos
caídos. Las más satisfactorias colonias de laboratorio se formaron en recipientes
plásticos, redondos, (26 cm x 9,5 cm) con una cubierta perforada, y conteniendo en el
fondo, de abajo a arriba, 0,5-0,8 cm de piedras caliza, 1,2-1,5 cm de arena, 1-2 cm
de suelo desmenuzado, y una cubierta de hojas, palitos, corteza de arbol y piedritas,
Alimento (hojas secas de arce, lechuga fresca, polvo de carbonato de calcio, y avena
u otro cereal) se proveyó en toallitas de papel sin blanquear para facilitar su retiro
semanal con los desechos. Los mejores se obtuvieron en recipientes preparados por
adelantado, con 5 a 10 caracoles en cada uno, humedad relativa de 96-100% y mante-
nimiento semanal,

Observaciones de laboratorio indican que A. alternata no produce esperma hasta
que su diámetro es al menos de 9mm y no ovoposita hasta que alcanza 13 mm.
Cópula se observó una sola vez. Colonias mantenidas a temperaturas de habitación
corriente por un largo periodo, tienen la tendencia de cesar en la ovoposiciôn; sin
embargo esta puede iniciarse por refrigeraciön alrededor de los 10°C por 40 mas
semanas y después manteniéndolos a 20-25 De por 2-4 semanas. Lavando los cara-
coles que se habian refrigerado, asi como los recipientes, estimula la ovopisiciön; un
adecuado substrato es importante. Los huevos (2-3 mm en diametro) fueron deposi-
tads a 1,5-2,5 cm debajo la superficie del substrato en grupos de 2 a 40. El tiempo
de puesta entre uno y otro huevo fu& de 15 minutos generalmente, pero variando de
3 minutos a una hora. Huevos conservados en receptäculos de yeso a 20-25 C
hicieron eclosiön después de 28-32 dias, y aquellos enterrados después de 30-25 dias.
Los individuos mantenidosa 10°C y 30°C no pusieron huevos, Caracoles recién nacidos,
(2-3 mm en diámetro) conservados a 22° С crecieron alrededor de 0,7 mm durante la
primera semana and 0,5mm en la 2. alcanzando tamafios de 4, 5 y 6-7 mm al
terminar el primer, segundo y tercer mes respectivamente. Por inferencia de los
datos de laboratorio se estima que estos caracoles pueden llegar a medir 5-8 mm
durante el primer verano y 11-16 mm en el segundo, en condición silvestre. El
crecimiento se reduce a 10°C; a 30°C es cercano al de 22 er aunque la mortalidad
aumenta a altas temperaturas.

A. alternata evita la luz intensa, y las temperaturas de 44° a 45°C los mata.
Puede soportar temperaturas frígidas si tiene oportunidad desecarse. Caracoles
tomados de suelos helados comienzan a ser activos entre 1 hora y 1 dia a 22 С. Aún
los más jovenes soportan desecación por varias semanas; los adultos estivan por
meses. Pueden producir epifragmas en 5 minutos cuando las condiciones tornan des-
favorables, y pueden reactivarse en minutos cuando las condiciones humedas son
restablecidas. Escalamiento arbóreo parece estar asociado con el exceso de humedad
en el suelo, y una vez orientados hacia arriba raramente retornan o bajan a voluntad.
Experimentos mostraron que el caracol acepta los alimentos mencionados anterior-
mente, pero, con consistencia, evitan tejido animal muerto o descompuesto, estiercol
o materias secas,

La principal causa de mortalidad en las áreas estudiadas parece ser por pequeños
mamiferos predatores (ratones, ardillitas). También pueden contribuir las condi-
ciones de ambiente desfavorable. El ombligo del caracol A. alternata alberga una
serie de pequeños organismos, incluyendo nematodes, ácaros, gorgojos, diminutas
lombrices, rotíferos, protozoos y hasta otros caracoles pequeños. La cavidad paleal
algunas veces contiene nematodes y protozoos. Metacercarias y esporocistos de
Postharmostomum se encontraron con frecuencia en la cámara pericardial y hepato-

páncreas respectivamente.
A We 32}

BIOLOGY OF ANGUISPIRA

ABCTPAKT

ЗАМЕТКИ ПО БИОЛОГИИ ANGUISPIRA ALTERNATA (STYLOMMATOPHORA,
ENDODONTIDAE)

А.Илвелл и М.Улмер

Изучался моллюск Anguispira alternata, промежуточный хозяин трематоды
Postharmostomum helicis; объект исследовался как в приролных условиях (штат
Иова), так и в лабораторных, гле культивировался втечение 4-х лет.

Моллюск предпочитает жить в опавшей листве лесных массивов, в умеренно-

влажных условиях, в гниющей лревесине, в затенённых местах. Korma
моллюски нахолятся в неактивном состоянии, TO лучшие места их сбора -
гниющая опавшая листва. Поздней весной и летом их можно находить на или
в почве (2-3 см глубины), на или пол корой гниющих перевьев. Самые

хорошие колонии в лаборатории развивались в круглых пластиковых
контейнерах (26 x 9.5 см) с перфорированной крышкой, содержащих на лне
слой 0.5-0.8 см известкового гравия, слой 1.2-1.5 см песка, 1-2 см рыхлой
почвы, и сверху - листья, кусочки дерева, камешки. Пища (сухие кленовые
листья, свежий салат-латук, порошок карбоната кальция, овёс или другие
хлебные злаки), разложенная на чистом бумажном полотенце, обле гчает
ежедневное удаление старой пищи и фекалий. Наилучшие результаты были
получены в заранее подготовленных контейнерах на 5-10 моллюсков каждый,
при 96-100% относительной влажности.

Лабораторные наблюдения показали, что А. alternata не производит спермы,
пока не достигает своего наибольшего диаметра по крайней мере 9 мм и не
откладывает яиц, пока не достигнет, по крайней мере 13 мм. Копуляция
наблюдалась лишь один раз. Колонии содержались при комнатной температуре
втечение долгого времени, пока не прекращалась продукция яиц; однако, от-
кладка яиц могла снова начаться после охлаждения на 10°С втечение 4 или
больше недель, с последующим содержанием при температуре 20-250 BN SEIS
2-4 недель; промывка моллюсков после охлаждения и освежения KOHTENHEDOB
также стимулировали кладку яиц; важен также подходящий субстрат. Яйца (2-
3 мм диаметром) откладывались в почву на глубину 1.5-2.5 см, комочками по
2-40 яиц. Время между откладками 2 яиц было около 15 минут, изменяясь OT 3
минут до 1 часа и более. Яйца, содержавшиеся в пластиковых контейнерах,
выводились через 28-32 дня, а Te. которые были в почве - обычно через 30 -
35 дней. Моллюски, жившие при температуре 10 и 30°С не откладывали яиц.
Молодь моллюсков (2-3 мм в лиаметре) при 22°C имели прирост 0. 7мм в первую
нелелю и 0.5 мм во вторую, лостигая размера 4.5 -5-7 мм в конце 1-го,
2-го и 3-го месяцев, соотственно. Путём экстраполяции лабораторныхданных,
данных, было подсчитано, что моллюски могут достигать в приросте размера
5-8 мм за первое лето их жизни и 11-16 мм - за второе. При 10°C прирост
сокращается, а при 30°C примерно равнялся тому. который наблюдался при
22°C, хотя при Sonee высокой температуре их смертность увеличивается.

A. alternata избегает сильной освешаности, а при температуре 44-45'C
отмирает. Она может выдерживать замерзание и, вилимо. также относится и
к высыханию. Моллюски, взятые из замерзшего грунта, становятся активными
через промежуток от 1 часа до 1 пня при 22°C. Jlaxe очень молодые моллюски
вылерживают высыхание втечение нескольких нелель, а крупные особи -
втечение летних месяцев могут нахопиться в состоянии покоя. Эпифрагма
может образовываться при неблагопритяных условиях втчение 5 минут; при
возобновлении необхолимых условий влажности, моллюски через несколько
минут могут вновь стать активными. Вползание их Ha перевья вилимо
связано с избытком влажности в почве; однажды ориентировавшись на
дереве в лвижении вверх моллюски сами по себе релко илут в обратном
напрпалени, вниз. Эксперименты по питанию показали, что они охотнее
всего питаются пищей, указанной выше. избегая тканей мёртвых или
разлагающихся животных, фекалий млекопитающих и высохших вешеств.

Главной причной смертности моллюсков в изучаемых местах видимо служило
напаение на них мелких млекопитающих (мышей, бурунпуков), а также
неблагоприятные условия обитания. В пупке A. alternata могут поселяться
различные мелких организмы, включая нематод, клещей, насекомых, мелких
земляных червей, коловраток, простейших и мелких моллюсков. В мантийной
полости иногла также встречаются нематоды и простейшие. В перикардлиальной
камере и в печени часто находится метацеркарии и спороцисты Postharmostomum.

я. А. Е.

215

MALACOLOGIA, 1971, 11(1): 217-224

THE CHROMOSOMES OF SOME AUSTRALASIAN PARYPHANTIDAE
Helene M. Laws

South Australian Museum
Adelaide, South Australia

ABSTRACT

Six Australasian members of the family Paryphantidae were studied cytologi-
cally, the observed chromosome numbers (n) being as follows: Paryphanta
busbyi (Gray), 32; Victaphanta atramentaria (Shuttleworth), 29; Rhytida dunniae
(Gray), 32; Strangesta gawleri (Brazier), 30; Strangesta tumidula Iredale, 30;
Schizoglossa novoseelandica (Pfeiffer), ca. 32. The mitotic chromosome com-
plement of Victaphanta atramentaria showed 17 metacentric pairs, including the
2 largest of the complement, and 12 submetacentric pairs. The proportion of
metacentric chrornosomes in V. atramentaria is similar to that previously ob-
served inHelix pomatia but different chromosomes of the complement are meta-
centric. Both differ from succineid snails in which nearly all chromosome
pairs are metacentric and from known basommatophorans in which submetacen-

trics predominate.

INTRODUCTION

Despite increasing interest in the
chromosomes of stylommatophoran
snails there are many families, partic-
cularly those of southern distribution,
which areas yet unsampled cytologically.
The Paryphantidae are among these and
this report gives, to my knowledge, the
first observations of chromosome num-
bers for the family. Among the other
families of the Streptaxacea (as defined
by Wenz & Zilch, 1960), chromosome
numbers are known for only 2 species
of the North American Haplotrematidae;
Haplotrema sportella has n = 29 (Ford,
1962 in Burch 1965) and H. vancouver-
ense п = 30 (Burch, 1965).

The family Paryphantidae is centered
in the Indo-Pacific region where mem-
bers are found in eastern Australia,
New Zealand, Indonesia and Melanesia;
2 genera are found in South Africa south
of latitute 25° South.

MATERIALS AND METHODS

Species of paryphantid snails which
were used in this study are listed in
Table 1.

Gonad samples, taken after removal

of the protoconch and apical whorls,
were either fixed and stained directly in
aceto-orcein or Stained in aceto-orcein
after fixation in acetic-alcohol ( 1:3
v:v) and storage in 70% ethyl alcohol.
After being examined, slides were made
permanent by mounting in Euparal after
alcohol dehydration. After excision of
gonad samples, snails were relaxed and
fixed and permanent preparations of the
radulae and reproductive systems were
made. These will form part of an ana-
tomical study of Australasian paryphan-
tids; they have been placed in the col-
lections of the South Australian Museum
and, along with the shells, are kept as
vouchers for the cytological observa-
tions,

RESULTS

Victaphanta atramentaria showed 29
bivalents at late prophase of the 1st
meiotic division of spermatogenesis
(Fig. 3). In 1 individual a number of
mitotic figures confirmed the meiotic
chromosome counts and also gave in-
formation concerning the morphology of
the chromosomes. Fig. 2 shows the mi-
totic chromosomes and in Fig. 3 they
have been arranged accordingto sizeand

(217)

218 H. M. LAWS

TABLE 1. Australasian Species of Paryphantidae used for Chromosome Studies

Species Locality S.A. M. * Reg. No.
Paryphanta busbyi (Gray) Mangamuka Gorge, North Auckland, N.Z. D. 14939
Victaphanta atramentaria Labertouche, Victoria, Aust. D. 14898

(Shuttleworth)
Rhytida dunniae (Gray) Near Kaitaia, North Auckland, N.Z. D. 14938
Strangesta gawleri (Brazier) Rapid Bay, South Aust. D. 14972
Strangesta tumidula Iredale Section 501, Hundred of Kongorong, D. 14971
South Aust.
Schizoglossa novoseelandica Inglewood, Taranaki, N.Z. D. 14970

(Pfeiffer)
*South Australian Museum, Adelaide

centromere position.

There has been variation in the use
by various authors of terms to describe
centromere position. I use metacentric
to describe medianly constricted chro-
mosomes which appear V-shaped, in-
cluding chromosomes in which the con-
striction is so close to the centre that
a decision cannot be clearly made as to
whether the element is V- or J-shaped.
Obviously J-shaped chromosomeslIterm
submetacentric, using “submedianly
constricted” and “subterminally con-
stricted” to distinguish respectively be-
tween elements with the constriction
nearer the mid-point of the chromosome
and those with it nearer the end. Chro-
mosomes in which the small arm is
beyond the resolution of the light micro-
scope are acrocentric.

It is clear that among the 10 largest
chromosome pairs, 5 have a median
constriction and 5 are submetacentric.
Nine of the next 13 pairs are metacen-
tric and among the 6 smallest chromo-
some pairs there are probably 3 with
median constrictions; with decreasing
chromosome size it becomes increas-

FIG. 1, 2. Spermatogonial mitosis in Victaphanta atramentaria.

ingly difficult to be certain of centromere
position. The 2 largest chromosome
pairs are both metacentric.

In both Strangesta gawleri and S. tu-
midula the chromosome number, asseen
in meiotic figures, is n = 30 (Fig. 4-6).
There is also a range of chromosome
size but no suitable mitotic material
was available for study of the chromo-
some morphology.

Meiotic divisions in both Paryphanta
busbyi and Rhytida dunniae show achro-
mosome number of п = 32 (Fig. 7, 8).
Similarly, the meiotic number for Schiz-
oglossa novoseelandica is probably n =
32; for this species material was very
limited and the counts should be re-
garded as tentative.

DISC USSION

The results of karyotype analysis by
other workers, and the observations
described in this paper for Victaphanta,
are summarized in Table 2. In the het-
erurethran succineids metacentric or
submetacentric chromosomes predomi-

Fig. 1, Mitotic prometa-

phase, 2n =58. Fig. 2, Chromosomes of Fig. 1 arranged according to size in 2 series, meta-
centric pairs on the left and submetacentric on the right. The 10 largest chromosome pairs

have been numbered in order of decreasing size.

AUSTRALASIAN PARYPHANTIDAE CHROMOSOMES

221: ци
CC 10 00 ВО ts вы
6 ny to «8

sa ha ce ce
80 ae vn ma we

D oc =$ uw «+ +

220 H. M. LAWS

2 Er
Ya > >
cept à >

3

FIG. 3-6.
atramentaria, 29 bivalents.
tumidula, 30 bivalents.

nate and the largest chromosome pair
may fall in either category; in the 2
helicids and Victaphanta metacentrics
make up a greater proportion of the
chromosome complement andthe largest
pair is metacentric. Superficially, Helix

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6

Diakinensis of spermatogenesis in 3 species of Paryphantidae. Fig. 3, Victaphanta
Fig. 4, Strangesta gawleri, 30 bivalents. Fig. 5, 6, Strangesta

resembles Victaphanta in that the pro-
portions of metacentric to submetacen-
tric chromosomes are very Similar.
However, the distribution of the 2 chro-
mosome forms is distinct; among the
first 10 chromosome pairs (arranged

AUSTRALASIAN PARYPHANTIDAE CHROMOSOMES 221

FIG. 7, 8. Diakinensis of spermatogenesis in Paryphanta busbyi and Rhytida dunniae. Fig. 7,
Paryphanta busbyi, 32 bivalents. Fig. 8, Rhytida dunniae, 32 bivalents.

according to decreasing length) of Vic-
taphanta the 3rd to 5th and the 8th and
10th are submedianly constricted, while
in Helix pomatia the 5th, 9th and 10th
are submetacentric. In contrast to the
3 sigmurethran species and to the suc-
cineids which show a wide variety of
karyotype, the basommatophorans Me-
lampus bidentatus lineatus (Ellobiidae),
Acroloxus lacustris (Acroloxidae) and
Laevapex fuscus (Ancylidae) have chro-
mosome complements in which sub-
metacentrics predominate (Natarajan &
Burch, 1966; Burch, 1962).

The recent development of gonadal
tissue culture techniques facilitates kar-
yotype analysis of land snails (Burch,
1968) and mitotic chromosome morphol-
ogy should in the future provide a useful
tool for comparative studies.

The chromosome numbers n = 29, 30
and 32 which are described above for
members of the Paryphantidae arecom-
parable to those already found in 2
species of Haplotrema (Haplotremati-
dae), n= 29 and п = 30 (Burch, 1965);
these 2 families have been grouped
together, along with the Streptaxidae
and Chlamydephoridae as the Streptaxa-

cea. As yet, no other members of the
group are known cytologically.

The presence of 3 different chromo-
some numbers among 6 members of the
Paryphantidae offers promising possi-
bilities for the use of chromosome
numbers inassessing relationships with-
in the family. Such relationships have
in the past been determined mainly on
conchological evidence (Solem, 1959)
although Powell (1930) has shown the
usefulness of radular structure in de-
limiting the New Zealand genera. The
few studies of the reproductive system
show that it also affords a number of
useful taxonomic characters and it is
to be hoped that a combined anatomical
and cytological approach will help to
clarify paryphantid intrafamily relation-
ships.

ACKNOWLEDGEMENTS

I wish to acknowledge assistance from
a Nuffield Foundation grant to Dr. A.
W. B. Powell and to express my grateful
thanks to him for help in collecting
Paryphanta busbyi and Rhytida dunniae;
I am also grateful to Dr. B. J. Smith

H. M. LAWS

222

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AUSTRALASIAN PARYPHANTIDAE CHROMOSOMES 223

of the National Museum of Victoria and
Mrs. J. Aslin of Mt. Gambier, South
Australia for sending specimens of Vic-
taphanta and Strangesta tumidula, and
to Mrs. Sue McGrath for typing assis-
tance.

REFERENCES

BURCH, J. B., 1962, Cytotaxonomic stu-
ies of freshwater limpets (Gastropoda:
Basommatophora). I. The European
Lake Limpet, Acroloxus lacustris.
Malacologia, 1: 55-72.

BURCH, J. B., 1964, Chromosomes of
the succineid snail Catinella rotundata.
Occ. Paps. Mus. Zool. Univ. Mich.,
638: 1-8.

BURCH, J. B., 1965, Chromosome num-
bers and systematics in éuthyneuran
snails. Proc. first Europ. malacol.
Congr., p 215-241.

BURCH, J. B., 1968, A tissue culture
technique for caryotype analyses of
pulmonate land snails. Venus, Jap.
J. Malacol., 27: 20-27.

BURCH, J. B., PATTERSON, C. M. &
NATARAJAN, R., 1966, Chromosomes
of four species of North American
Succineidae. Venus, Jap. J. Malacol.,
24: 342-353,

BUTOT, J. J. М. € KIAUTA, B., 1967,
The chromosomes of Catinella are-
naria (Bouchard-Chantereaux, 1837)
with a review of the cytological con-

ditions within the genus Catinella and
considerations of the phylogenetic po-
sition of the Succineoidea ord. nov.
(Gastropoda: Euthyneura). Beaufortia,
14: 157-164.

NATARAJAN, R. & BURCH, J. B., 1966,
Chromosomes of some archaeopulmo-
nata (Mollusca: Basommatophora).
Cytologia, 31: 109-116.

NATARAJAN, R.; HUBRICHT, L. &
BURCH, J. B., 1966, Chromosomes of
eight species of Succineidae (Gastro-
poda, Stylommatophora) from the
southern United States. Acta Biol.
Hung., 17: 105-120.

PATTERSON, С. М. € BURCH, J. В.,
1966, The chromosome cycle in the
land snail Catinella vermeta (Stylom-
matophora: Succineidae). Malacolo-
gia, 3: 309-325.

POWELL, А. У. B., 1930, The Pary-
phantidae of New Zealand: their
hypothetical ancestry, with descrip-
tions of new species and a new genus,
Rec. Auckl. Inst. Mus., 1: 17-56.

RAINER, J., 1967, Chromosomenunter -
suchungen an gastropoden (Stylomma-
tophora). Malacologia, 5: 341-373.

SOLEM, A., 1959, Systematics of the
land and freshwater mollusca of the
New Hebrides, Fieldiana: Zoology,
43: 1-238.

WENZ, W. & ZILCH, A. 1959-1960. In
Handbuch der Paläozoologie. Band 6
(II) Borntraeger, Berlin. xii + 834 p.

ZUSAMMENFASSUNG

DIE CHROMOSOMEN EINIGER AUSTRALASIATISCHER PARYPHANTIDEN

H. M. Laws

Sechs australasiatische Arten der Familie Paryphantiden wurden cytologisch
undersucht, folgende Chromosomenzahlen (n) wurden festgestellt: Paryphanta busbyi
(Gray) 32; Victaphanta atramentaria (Shuttleworth) 29; Rhytida dunniae (Gray) 32;
Strangesta gawleri (Brazier) 30; Strangesta tumidula Iredale 30; Schizoglossa novo-

seelandica (Pfeiffer) ca. 32.

Der diploide Chromosomensatz von Victaphanta atra-

mentaria bei der Mitose zeigte 17 metazentrische Paare einschliesslich dier 2
grössten im Satz und12 submetacentrische Paare. Das Verhältnis der metazentrischen
Chromosome der V. atramentaria ähnelt dem früher untersuchten der Helix pomatia,
aber andere Chromosome des Satzes sind metazentrisch. Beide unterscheiden sich
von den Succineiden, bei denen fast alle Chromosomensaare metazentrisch sind, und
von den bekannten Basommatophoren, bei denen die submetazentrischen vorherrschen.

H. Z.

224 H. M. LAWS
RESUME
LES CHROMOSOMES DE QUELQUES PARYPHANTIDAE D’AUSTRALASIE
H.M. Laws

Six représentants, en Australasie, de la famille des Paryphantidae ont été étudiés
cytologiquement, les nombres chromosomiques observés (n) étant les suivants:
Paryphanta busbyi (Gray), 32; Victophanta atrementaria (Shuttleworth), 29: Rhytida
dunniae (Gray), 32; Strangesta gawleri (Brazier), 30; Strangesta tumidula Iredale, 30;
Schizoglossa novoseelandica (Pfeiffer), ca. 32. La garniture chromosomique de
mitose de Victaphanta atramentaria montre 17 paires métacentriques, y compris les
2 plus grandes de la garniture, et 12 paires submétacentriques. La proportion de
chromosomes métacentriques chez V. atramentaria est semblable a celle précédem-
ment observée chez Helix pomatia mais où ce sont des chromosomes différents de
la garniture qui sont métacentriques. Les 2 espéces différent des Succinées, chez
lesquelles presque toutes les paires de chromosomes sont métacentriques et des
Basommatophores connus chez lesquels les submétacentriques dominent.

A. Г.
RESUMEN

LOS CROMOSOMAS DE ALGUNOS PARYPHANTIDAE DE AUSTRALASIA
H. M. Laws

Se estudiaron citologicamente seis miembros de la familia Paryphantidae de Aus-
tralasia, siendo sus números de cromosomas (n) observados, como sigue: Paryphanta
busbyi (Gray), 32; Victaphanta atramentaria (Shuttleworth), 39; Rhythida dunniae
(Gray), 32; Strangesta gawleri (Brazier), 30; Strangesta tumidula Iredale, 30; Schizo-
glossa novoseelandica (Pfeiffer), ca. 32, El complemento mitötico cromosomätico de
Victaphanta atramentaria moströ 17 pares metacentricos, incluyendo los dos mas
grandes del complemento, y 12 pares submetacentricos. La proporciön de cromo-
somas metacéntricos in V. atramentaria es similar a la que se observö previamente
en Helix pomatia pero diferentes cromosomas de el complemento son metacéntricos.
Ambos difieren de los caracoles succineidos en los cuales casi todos los cromosomas
pares son metacéntricos, y de otros basommatoforos en los que se conoce predomi-
nancia de metacéntricos.

91.35
АБСТРАКТ
ХРОМОСОМЫ НЕКОТОРЫХ АВСТРАЛО-АЗИАТСКИХ PARYPHANTIDAE
ЭЛЕН М. JIOYC
Исследовались цитологически 6 австрало-азиатских представителей
семейства Paryphantidae; оказалось, что число хромосом (п) у них было
следующее: Paryphanta busbyi (Gray) - 32; Victaphanta atramentaria (Shuttleworth) - 29;
Rhytida dunniae (Gray) - 32; Strangesta gawleri (Brazier) - 30; Str. tumidula
Iredale - 30; Schizoglossa novoseelandica (Pfeiffer) - около 32. Митотический

,
набор хромосом у V. atramentaria состоит из 17 метацентрических nap,
самые крупные пары набора и 12 субметацентрических пар.
метацентрических хромосом у ТУ. atramentaria сходно с тем,
Wu A

Соотношение

которое ранее наблюдалось у Helix pomatia, отличаясь тем, что различные
хромосомы набора являются метацентрическими. 0ба они отличаются от
Succineidae, где почти все пары хромосом-метацентрические, и OT

Basommatophora, y которых преобладают субметацентрические пары.
Z.A.F.

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Карты должны быть достаточно крупными, чтобы выдержать уменьшение

наполовину или на 113% Это слеует иметь виду особенно В
отношении обозначений. Буквы и цифры после уменьшения не должны быть
менее 1 мм высоты, желательно крупнее. Ряд рисунков и фотографий

желательно сгруппировать вместе наиболее удобным образом, B
соответствии со страницей TeKCTa.

Библиография: CM. любой номер МАЛАКОЛОГИИ, чтобы иметь
представление о желательной форме цитирования литератры. Следует
отметить, что журнал употребляет знак € для “and” (по-русски "и");
“etal.” ("и другие") можно употреблять в тексте, но не в списке
литературы (в конце статьи); кроме номера тома в списке литературы
приводятся номера страниц цЦитированной статьи или книги; для книг
необходимо также указывать издателя и город, где книга напечатана.

оттиски. Автор получает 50 оттисков своей статьи. бесплатно;
дополнительные копии могут быть получены за плату, если они

заказывались во время - т.е. не позже времени возвращения корректуры в
редакцию; позже этого заказы на дополнительные оттиски выполнены быть
не могут.

Корреспонденция. Все рукописи и рисунки, как и заказы на подписку на
журнал, оплата и справки должны направляться на имя помощника редактора,
- Д-ра Ч.Дж.Бейна по адресу - Музей Зоологии, Мичиганский Университет,
Энн Арбор, Мичиган, 48104, США [S.-K. Wu, Museum of Zoology, The University of

Michigan, Ann Arbor, Michigan 48104, U.S.A.].

j~ MAB 2

vo Tp 1 1 NO. 2 MUS. COMP. ZOOL, M A Y 19 72
| LIBRARY

| JUN 23 1972

| HARVARD

UNIVERSITY

MALACOLOGIA

a

|

‚м
4
р a

International Journal of Malacology

р Revista Internacional de Malacologia
~ Journal International de Malacologie
| 4 \

Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

MALACOLOGIA

General Editors
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MOL. 11 NO. 2 MAY 1972

MALACOLOGIA

International Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie

Международный Журнал Малакологии

Internationale Malakologische Zeitschrift

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MALACOLOGIA, 1972, 11(2): 225-280

COMPATIBILITY AND HOST-PARASITE RELATIONSHIPS BETWEEN SPECIES
OF THE GENUS BULINUS (BASOMMATOPHORA: PLANORBIDAE) AND AN
EGYPTIAN STRAIN OF SCHISTOSOMA HAEMATOBIUM (TREMATODA: DIGENEA) ”

Chin-Tsong Lo?

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

ABSTRACT

The ability of various bulinine snails to act as intermediate hosts of an Egyp-
tian strain of the blood fluke Schistosoma haematobium was investigated, to-
gether with factors affecting snail susceptibility and the effect of the parasite on
infected snails.

Twenty-eight laboratory bred populations, representing about a dozen species
and subspecies of Bulinus from various parts of Africa and adjacent regions
were exposed to Schistosoma haematobium under standardized conditions. Snail
size varied from 2-4 mm high; temperature ranged from 24° to 26°C; individual
exposure from 10 to 20 miracidia; 2 ml of water were provided per snail. Pur-
chased spring water was routinely applied for all purposes. Cercariae emerged
in the truncatus group from Bulinus truncatus truncatus, B.t. rohlfsi, В. seri-
cinus (W. Aden), B. coulboisi, B. guernei (all with the haploid chromosome
number n=36) and from Bulinus sp. (n=72); and, in the africanus group from B.
globosus. None were obtained from B. tropicus and several populations of Bu-
linus sp. belonging to the tropicus species group (with n=18) and from B. for-
skalii and B. scalaris (both in the forskalii species group), although in the latter
species mother sporocysts grew and persisted for about 2 months without liber-
ating daughter sporocysts. Although South African B. globosus showed the high-
est infection rate (76%), B. guernei from Gambia (35% infected) was found to be
the most suitable host for the maintenance of the parasite as regards ease of
breeding, survival, infectivity and cercarial output. The order of suitability
for establishing the life cycle among the receptive snails in the truncatus group
was: good - В. guernei (Gambia), В. sericinus (W. Aden) and В. t. truncatus
(Iran); fair - В. t. rohlfsi (Mauritania), В. t. truncatus (Corsica), В. ЕЁ. trun-
catus (Sudan), В. t. rohlfsi (Ghana) and В. coulboisi (Tanzania); poor - B. t.
truncatus (Egypt) and B. sp. (n=72, Ethiopia). That our laboratory strain of B.
truncatus from Egypt (3% infected) was less susceptible than practically any
other receptive snail (except for B. globosus from Mozambique with 2%) demon-
strates that local snail-parasite specificity need not necessarily develop.

A species of ameba, Hartmannella biparia, was found infecting some speci-
mens of Bulinus globosus; it possibly reduces the schistosome infection in these
snails.

lAdapted from a dissertation submitted in partial fulfillment of the requirements for the degree
of Doctor of Philosophy at the University of Michigan, April, 1968.

2This investigation was supported, in part, by a U.S. Public Health Service Training Grant
(5-T1-AI-41) from the National Institute of Allergy and Infectious Diseases and, in part, by a
grant (DA-49-193-MD-265) from the U.S. Army Medical Research and Development Command.

3Present address: Department of Parasitology, College of Medicine, National Taiwan Univer-
sity, Taipei, Taiwan, China.

(225)

226

C. T. LO

To determine the best success of the parasite, several factors affectiug the
susceptibility of snails were studied in Bulinus guernei under a standard set of
conditions, varying only the factor under investigation. Generally higher infec-
tions were obtained under the following conditions: high alkalinity (optimum
results: 49% at pH 9.6); high temperature (67% at 30°C, but less at yet higher
temperatures, and negative below 10°C); large miracidial dose (70% at 60+ per
snail); in young snails (maximum of 67% in surviving 3-day old snails; however,
because of high mortality, snails 1-2 weeks old yielded the maximum of infected
specimens); in snails fixed in position (54%), when the extended snail body ex-
poses a maximum area, and when anesthetized (81%), presumably because of
lesser mucus secretion coupled with extension and immobility.

Infection did not retard growth of snails. Mortality of infected snails over 3
days old, before the onset of cercarial emergence, was not higher than in un-
infected snails. No infected snail survived beyond 32 weeks. Infected snails
produced from 7 to 100 times (av. 15 times) fewer eggs than uninfected ones and
abnormalities were 17 times as frequent. The spawn showed several types of
abnormality, singly or in combination, such as lack of eggs in the gelatinous
matrix, small size of ovum, lack of embryo, location of embryo outside the egg
membrane, polyembryony, presence of cercariae in egg-mass or egg.

Cercarial incubation periods were shorter and more uniform when snails were
kept at high temperatures (23 days at 30°C; 35-49 days at 24°C). The peak of
cercarial emergence was reached 1-2 weeks after the first shedding and the
numbers shed daily fluctuated greatly thereafter, depending on temperature (op-
timal at 35°C, suppressed at 40°C) and light, as well as on the intensity of in-
fection, health of snail and aquatic conditions. The infection was partially
“cured” when infected snails were kept at 35-37°C for a week, as evidenced by
decreased cercarial output and increased oviposition. Estimated maximum
daily and total shed from a snail was about 2,500 and 20,000 cercariae respec-
tively. Infected snails of a larger size survived longer, laid more eggs and
produced more cercariae than smaller snails.

More snails produced male cercariae than they did female cercariae, the fe-
male:male ratio being 1:2.6. Only when a snail was heavily exposed to miracidia
did bisexual infections appear, at a frequency of 7% (10 miracidia) and 9% (20
miracidia).

CONTENTS

page

INTRODUCTION 222 cits tate ate feeds sous AR
MATERIALS AND METHODS.... .227
RESULTS AND DISCUSSIONS .... .233

i

Susceptibility of Bulinus spp. to
Schistosoma haematobium
Infection ss oho tame wer col ee soe

NOR SEA GYOUD ta ee ene 233

2. tropicus and truncatus Groups.240

3 GURZCAUUS (GT OUD . 0 22.4 CAO

4. Chromosome Number and
BUSCEDEIDILY 2270 0 0. 1241

5. Local Snail-Parasite Com-
A ве A a 2A2

6. Infectivity of Miracidia... .242

7. Efficiency of various Snails as
Hosts in the Laboratory ... .243

8. Barriers to successful

Infection “to. а

II. Some Factors affecting Infection

in Bulinus guernet ". 2.2. ..2AA
1. Hydrogen Ion Concentration. .244
2. Temperature ..... «sa eee
3. Number of Miracidia..... .247
4. Age of Snails.... „zer ЛИ
5. Fixing of Snail Position... .247
6. Anesthetization. ........ .248

Ш. Host-Parasite Relationships

between Bulinus and Schisto-

soma haematobium .......250
1. Effect of Infection on the

Growth of Bulinus spp..... .250
2. Effect of Infection on the

Survival of Bulinus spp... . .252
3. Effect of Infection on the

Fecundity of Bulinus spp... .254
4. Production of Cercariae. . . .262
5. Sex Ratios in Schistosoma

haematobium „. - co... 22277208

BULINUS AND SCHISTOSOMA HAEMATOBIUM 227

INTRODUCTION

Much information has accumulated
regarding host-parasite compatibility
between bulinine snails and Schistosoma
haematobium since 1950, but our know-
ledge of this problem is still far from
complete. Experimental data (summar-
ized in Table 4) often are fragmentary
and conditions differ from laboratory to
laboratory. Thus, as pointed out by
Gismann (1954), one has to be careful
when comparing the data.

In addition to these uncertainties, the
taxonomy of Bulinus has been in confusion
for many years, and many questions re-
garding the intermediate snail hosts and
the parasites remain unanswered, In
recent years, considerable attention has
been paid to these snails because of their
importance in public health and also on
account of their basic biological interest.
Mandahl-Barth (1958) consolidated the
Originally over 100 nominal species and
Subspecies in the genus Bulinus to about
20, grouping them into species groups,
partly to replace earlier subgeneric di-
visions. In his later publications, how-
ever, some species have been added and
others deleted or regrouped (e.g., Man-
dahl-Barth, 1965). As regards schis-
tosomes of the haematobium group, all
having terminal-spined eggs, several
human and animal species have been
distinguished, mainly, S. haematobium
(causing human vesical schistosomia-
sis), S. capense (as a separate southern
form of the species), S. intercalatum (a
form with large egges causing human
intestinal infection), S. mattheei (prin-
cipally a schistosome of ungulates in
southern Africa) and S. bovis (infecting
ungulates in the north). It has been
proposed to classify all forms as sub-
Species of $. haematobium (Amberson &
Schwarz, 1953), but it is apparent that
more information is needed regarding
Snail-parasite compatibility and defini-
tive host-parasite relations before valid
conclusions can be made. Crossing ex-
periments among the nominal species
of Schistosoma in this group so as to
Study the possibility of interbreeding
and the fate of hybrids would seem of

value,

The present studies were initiated in
order to compare the ability of different
strains of S. haematobium to infect vari-
ous Species, Subspecies and strains of
bulinine snails. Although several strains
of S. haematobium have been tested, the
present report deals only with that ori-
ginating from Egypt. One of the most
susceptible snails was then selected
for testing the effect of some factors
which influence the infection in snails.
Finally, effects of schistosome infection
on the biology of Bulinus were investi-
gated, The snail hosts used in the study
by no means cover the complete range
of Bulinus, but major representatives
have been included,

MATERIALS AND METHODS
1. Parasite and Snails

The Schistosoma haematobium used in
this study was of an Egyptian stock,
established by Dr. E. G. Berry in 1956
at the National Institutes of Health, Be-
thesda, and brought to the University of
Michigan in 1965. The golden hamster
(Cricetus auratus) and several species
of Bulinus (Bulininae, Planorbidae) have
been used for maintaining the life cycle.

In all, 28 populations of Bulinus from
the 4 species groups and representing
at least 10 species, were tested (Table
1, Fig. 1); only laboratory bred speci-
mens were used. Most of these snail
colonies were established through the
efforts of Drs. H. van der Schalie and
J. В. Burch, but an additional number of
colonies was contributed by Dr. E. G.
Berry.

Since the age of a snail is one of the
important factors affecting its suscep-
tibility (Archibald & Marshall, 1932;
Moore et al., 1953), an effort was made
to delimit this variable. To this end,
a growth curve was obtained for B.
guernei, and from this curve the approx-
imate ages of snails were determined
(Fig. 2). The curve couldalso be applied
without great error to the various mem-
bers of the tropicus and truncatus groups,
particularly in the young stages. Imma-
ture specimens from 2-4 mm high (ave-

228

TABLE 1.

Species

tropicus group:

B. tropicus
(Krauss)
B. tropicus
B. tropicus
B. tropicus
B. tropicus

B. tropicus

B. tropicus

B. tropicus

B. tropicus

Be sp:

B. Sp.

B. Sp.
truncatus group:

В. Е. truncatus
(Audouin)

В. t. truncatus

В. t. truncatus
B. t. truncatus
В. t. rohlfsi

(Clessin)

B. t. rohlfsi

Haploid
chromo-

some No.

(n=)

18

18

18

18

18

18

18

18

18

18

18

18

36

36
36

36

36

36

C+T-LO

Origin Year
Mwe Tabari, Kenya 1960
De Villiers reservoir, Malelane,| 1961
Transvaal, South Africa
near Salisbury, Rhodesia 1961
Crocodile Creek, Lake 1965
Melllwaine, Rhodesia
Fisherman's Bend, Lake 1965
Mclllwaine, Rhodesia
head of False Creek, Lake 1965
Mclllwaine, Rhodesia
Little England Farm, tributary |1965
of Gwebi River, near Salisbury,
Rhodesia
a pond on Sinoia Rd. , about 5 mid 1965
N. of Gwebi Agr. College, near
Salisbury, Rhodesia
a pond at Marlborough, near 1965
Salisbury, Rhodesia
rock quarry, 10 km N.W. of 1965
Asmara, Ethiopa
near Debra Birhan, Ethiopia 1965
Lake Bishoftu, Ethiopia 1967
an irrigation canal near 1959
Khartoum, Sudan
Corsica 1963
WHO experimental project 1964
area, near Alexandria, Egypt
Dezful, Iran 1966
vicinity of Kumasi (Ashanti) 1961
Tagant Plateau, Mauritania 1963

Species and populations of Bulinus used in the study

Collector

E.G. Berry

С.

=

un

RENE

H. J. Schutte

de V. Clarke and

. J. Shiff

B. Burch and
Bosch

B. Burch and
Bosch

B. Burch and
Bosch

B. Burch and
D. Harrison

B. Burch

B. Burch

. B. Burch

B. Burch and

. S. Brown

Gemetchu

A. Malek

Grètillat

E. Kuntz
Massoud and
N. (Chu

Wickremasinghe

Gretillat

BULINUS AND SCHISTOSOMA HAEMATOBIUM

Table 1 (cont. )

Species

B. coulboisi
(Bourguignat)

Mwanza, Tanzania

229

Collector

McClelland

В. guernet Gambia C. A. Wright
(Dautzenberg
В. sericinus* Western Aden C. A. Wright
(Jickeli)
B. sp. a small stream 16 mi. N. of J. B. Burch
Addis Ababa, on the Debra
Marcos Rd., Ethiopia
forskalii group:
B. forskalii Gambia C. A. Wright

(Ehrenberg)

B. scalaris

(Dunker) Rhodesia
africanus group:

B. globosus
(Morelet)

B. globosus
B. globosus

B. globosus

7 mi. S. of Salisbury,

Adeiso, Ghana

Lourengo Marques, Mozambique

near Salisbury, Rhodesia

Transvaal, South Africa

L. Husting and
A. Garnett

E. G. Berry

E. G. Berry

L. Husting and
A. Garnett

C. A. Wright

*This species is probably a subspecies of Bulinus truncatus, and was reported as such in the
abstract of this study (Lo, C. T., 1969, Malacol. Rev. 2: 135-136).

rage age 7-19 days) were used for the
study of susceptibility, but some larger
Specimens of 5-6 mm were also included
for some species which did not reproduce
satisfactorily, i.e., B. globosus, B. for-
skalii, B. scalaris and B. sp. from Lake
Bishoftu, Ethiopia.

2. Water

Spring water bought from Arbor
Springs Water Company in Ann Arbor
was used in 95% ofthecases. This water

was very suitable for the mass cultur-
ing of snails, in part because of its high
calcium content. The chemical compo-
sition of this water is shown in Table 2,

3. Maintenance of Snails

Most snails were bred and maintained
in 15-liter aquaria, each provided witha
charcoal filter connected to a compressed
air outlet. Snails were fed with fresh
lettuce 2-3 times a week; occasionally
Cerophyl* was given. This method was

4Dehydrated cereal grass leaves manufactured by Cerophyl Laboratories, Inc., Kansas City,

Mo., U.S.A. Production is no longer continued.

230

FIG. 1. Shells of some of the laboratory-bred bulinine snails used in the study. A, B. tropicus;
Kenya. В, В. tropicus; South Africa. С, В. tropicus; Fisherman’s Bend, Lake Mclllwaine,
Rhodesia. D, B. sp.; 10km Northwest of Asmara, Ethiopia. E, B. sp.; near Debra Birhan,
Ethiopia. F, B. sp.; Lake Bishoftu, Ethiopia. G, B. t. truncatus; Sudan. H, B. t. truncatus;

Egypt. I, В. t. truncatus; Corsica. J, В. t. truncatus; Iran. К, В. t. rohlfsi; Ghana. Г, В. |

t. rohlfsi; Mauritania. М, В. coulboisi; Tanzania. N, В. guernei; Gambia. O, В. sericinus;

Western Aden. P, В. sp. (n=72); Ethiopia. ©, В. forskalii; Gambia. В, В. scalaris; Rhodesia. |

$, В. globosus; Ghana. T,B. globosus; Mozambique. U, В. globosus; Rhodesia. У, В. globosus;
South Africa.

BULINUS AND SCHISTOSOMA HAEMATOBIUM 231

TABLE 2. Chemical composition of the water
used*

Substance ppm
Total solids (Residue on evapcration) | 481.0
Calcium 110.0
Magnesium 2942
Alkalinity in terms of CaCO3

Normal carbonate 11.7

Bicarbonate 289. 2
Hardness in terms of CaCO3 394. 8
Chlorides 40. 0
Sulphates 90. 9
Iron 0. 06
Sodium 26. 2
pH (7.95)

A theoretically possible combination of the
salts present is as follows :*

salt ppm

Sodium chloride 65.9
Sodium sulphate 0.9

Magnesium sulphate 50. 1
Calcium sulphate 70.8
Magnesium carbonate 66. 2
Calcium carbonate PANT

*The data were supplied by Arbor Springs Wa-
ter Company.

satisfactory for all Bulinus snails except
those in the africanus and forskalii
groups. These were raised in plastic
trays (25 x 22 x 6 cm), with water about
4 cm deep and without active aeration;
they were fed with fresh lettuce, algae
and occasionally boiled lettuce. The
algae were collected from Petri dish
cultures prepared for raising Oncome-
lania snails (van der Schalie & Davis,
1965).

Snails exposed to miracidia were
maintained in the same manner except
that a dried snail food was added to the
diet. This food was made by mixing
10 g of cerophyl, 10 g of commercial
fish food (minimum 40% crude protein),
and 1 g of sodium alginate in a blender
with 300-400 ml of hot tap water. The
mixture was spread evenly over filter
paper to dry. The paper, coated with
food on one side, was then cut into small
pieces approximately 1 x 1 cmand either

HEIGHT OF SHELL IN MM

4 1 — 1 4 =! 1 1

1 L
10 20 30 40 50 60 70 80 90 100 110 120 130

DAYS AFTER HATCHING

FIG. 2. Growth curve of Bulinus guernei ob-
tained from 50 snails. Arrow indicates the
onset of oviposition. Solid lines: range.
Broken line: average.

used at once or stored, Not more than
50 exposed snails were maintained in
each aquarium; in plastic trays, the
number varied from 20-40. It was usu-
ally not necessary to change water dur-
ing the prepatent period.

4. Hatching the Eggs of Schistosoma
haematobium

The large intestine of infected ham-
sters was the source of S. haematobium
eggs. To hatch the eggs, the portion of
intestine having masses of egg nodules
was severed and the feces were rinsed
out with tap water. It was then cut into
pieces about 1 cm long and homogenized
for 10-20 seconds with 20-30 ml of cold
water (15-20°C) at a low speed in a
Waring blender. The homogenate was
strained through a nylon screen (300 u
mesh) into a 300 ml beaker. Particles
trapped on the screen were again homo-
genized and strained; the procedure was
repeated 2 or 3 times, each time at a
higher speed than before, full speed
being applied inthe final homogenization.
The beaker was then filled with cold
water and eggs were allowed to settle
for 15 minutes, after which the water
was drawn out with an aspirator until
about 5 ml of sediment remained. The
sediment was diluted with about 150 ml
of water (25°C), and placed in a water
bath (30°C) for hatching the eggs. Five

232 Car. то

to 10 minutes later the miracidia were
ready for use. Only vigorously swim-
ming miracidia less than 2 hours old
were used.

5. Snail Exposure and Control of Factors

Glass vials 18 mm diameter and 15
mm high were used for individual ex-
posure. To each vial were added: 2 ml
of water, a Snail and a specified number
of miracidia. The exposure lasted for
at least 5 hours under a 30-watt day-
light lamp placed about 50 cm above.
An occasional check was made to insure
that all snails stayed in the water. In
mass infection, 10-50 snails were ex-
posed together in a container, allowing
2-5 ml of water and 20-50 miracidia
per snail.

During the whole study period, snails
were routinely exposed individually or
en masse at roomtemperature (23-27°C )
for maintenance of the cycle. However,
for comparison of susceptibility snails
were exposed individually to 10-20 mira-
cidia at 24-26°C. For testing the effects
of temperature on Snail infection, a
refrigerator was used for obtaining 5
and 10°C; to get 15 and 20°C hot and
cold tap water were properly mixed;
and a water bath was applied for 25°C
or above.

The hydrogen ion concentration was
adjusted by adding 0.1 М HCl or 0.1 М
NaOH and measured with a Beckman pH
meter type 96. Precipitation occurred
at pH 10-12. It was removed by filtra-
tion prior to use, though neither its
effects on susceptibility were deter-
mined, nor what quantity of ions were
removed from the water.

To fix the snails in position during
exposure, a Small amount of fingernail
polish was applied to the body whorl of
the shell opposite its aperture, making
it adhere to the bottom of vial. Aftera
few minutes of drying, water and mira-
cidia were added.

The effect of anesthetization on sus-
ceptibility was studied with Nembutal.
Snails were placed in 1% Nembutal Solu-
tion, i.e., 0.05% sodium pentobarbital,

for 1 hour, rinsed twice, and exposed.
6. Determination of positive infection

One week after miracidial penetration,
mother sporocysts could be seen in the
head-foot region under a dissecting mi-
croscope at 10 x magnification, Mother
sporocysts measured from 100 to 150 u
at that time, and 300-600 u at 2 weeks,
when extended. They formed swellings
and appeared as translucent white spots |
when located near the surface, but those
located deep in the snail tissue appeared |
as slightly dark shadows, often difficult |
to diagnose. At 3 weeks, most of them

had attained their maximum size which |

made detection easier. At that time,
daughter sporocysts could also be seen ©
in the pseudobranch in many instances.
Daughter sporocysts present in the liver
region became more visible at 4 weeks |
and infection could be verified by the |
emergence of cercariae at 5 weeks. It
was expedient to examine snails narco- |
tized with Nembutal.

To evaluate how accurately infection |
could be detected in snails by the pre-
sence of sporocysts before the emission |
of cercariae, 54 positive В. guernel, |
maintained at 24°C, were observed at |
weekly intervals after infection. After
1 week mother sporocysts were found |
in 46%; after 2 weeks, in 94%; after 3 |
weeks, in 98%; and after 4 weeks, in
100%.

At times, exposed snails were exam- |
ined for sporocysts after removing the ©
shell. A dip into Bouin’s solution for
10-30 seconds facilitated the detection of
daughter sporocysts, since they appeared |
solid white against the yellow snail |
tissue,

7. Observation of infected Snails

Infected snails (5 or 10) were kept in
either 500 ml or 1000 ml graduated
beakers after they had started to shed |
cercariae (i.e., with 100 ml of water
for each snail), Water and food were |
replaced every other day.

At that time, ‘/o of the water was |
transferred to a 150 ml beaker aftera

BULINUS AND SCHISTOSOMA HAEMATOBIUM 233

thorough mixing. A small amount of
formalin was added to the beaker to
kill and fix the cercariae. After set-
tling, Supernatant water was removed
to a depth of 1-2 cm by Suction, and the
number of cercariae counted.

Once or twice a week mortality, growth
and fecundity were recorded for both
infected snails and uninfected controls.
Snails in control groups were taken as
much as possible from the very group
of snail which had been exposed to
miracidia, but then turned out to be
negative.

8. Determination of Sex of Cercariae

White mice of the Webster strain
were used for determining the sex of
cercariae produced by individual snails.
The mice were infected with cercariae
either by tail immersion or intraperi-
toneal injection. The latter method was
faster and had a higher worm recovery
(16%) than the former (11%). The num-
ber of cercariae given to each mouse
varied from 50 to 300. Mice were
examined for schistosomes 3-4 months
after infection.

RESULTS AND DISCUSSIONS

I, SUSCEPTIBILITY OF BULINUS SPP.
TO SCHISTOSOMA HAEMATOBIUM IN-
FECTION

A total of 4,338 snails was exposed to
miracidia for comparison of suscepti-
bility. For each snail population, ex-
posure experiments were conductedfrom
one (B. sp. from Lake Bishoftu, Ethi-
opia) to more than 10 times (B. t. trun-
catus, Sudan; and B. guernei, Gambia),
but 3-6 times was most common, Each
time 1-2 heavily infected hamsters were
used. Results of these experiments are
summarized in Table 3. Forthe purpose
of discussion, experimental results ob-
tained by other workersare summarized
bin Table 4, which also contains some
data obtained by the author from other
strains of S. haematobium thanthe Egyp-
tian.

Miracidia increased their swimming

speed and tried to penetrate the snail
tissue when placed together with any
one species of Bulinus; yet not all spe-
cies became infected, This miracidial
behavior was expected in view of pre-
vious reports that miracidia of Schisto-
soma mansoni reacted even to empty
Shells and fine gravel as they did to
living snails (Abdel-Malek, 1950). It is
known that other schistosomatid mira-
cidia, such asS. mansoni, Trichobilhar-
zia elvae, T. physellae and Schistoso-
matium douthitti can penetrate unsuit-
able snail hosts although they rapidly
die before any appreciable development
(Newton, 1952; Sudds, 1960).

1. forskalii Group

Bulinus forskalii has been incrimi-
nated as the transmitter of Schistosoma
haematobium on the island of Mauritius
and also in West Africa, and has occa-
sionally been reported to harbor schis-
tosome cercariae in various parts of
Africa. However, incorrect snail iden-
tification within the forskaki group has
caused some confusion in the literature.
The role of B. forskalii as a vector has
been reviewed and discussed by Cowper
(1953) and Wright (1956a). It now ap-
pears that, although designatingthe snail
as B. forskalii, LeRoux (1954) and Mc-
Cullough & Duke (1954) in Gambia were
dealing with either В. forskalä, or В.
senegalensis Müller, or with a mixture
of both. The B. forskalii reported from
Mauritius by Adams (1934) and Cowper
(1953) has now been shown to be B.
cernicus (Morelet) (Wright, 1956a). The
positive experimental results with un-
disputed B. forskalii are those by Berry
(pers. comm.) in Nigeria, Malek (1958)
in the Sudan, and Smithers (1956) in
Gambia, not counting the single infection
among 1,500 snails reported by Kuntz
(1955) from Egypt. Negative results
were obtained by Cowper (1953) with the
Egyptian parasite, McCullough (1955a,b)
with the parasite from Ghana, Cridland
(1955) with the parasite from Uganda,
Wright (1963) with the parasite from
Aden, and Capron et al. (1965) with the

234

TABLE 3. Experimental infection of Bulinus spp.

haematobium.

Haploid
Species
B. tropicus 18
B. tropicus 18
B. tropicus 18
B. truncatus truncatu 36
В. t. truncatus 36
B. t. truncatus 36
B. t. truncatus 36
В. t. rohlfsi 36
B. t. rohlfsi 36
B. coulboisi 36
В. guernei 36
B. sp. 18
B. sp. 18
B. sericinus 36
B. sp. 18
B. sp. 72
В. forskalii 18
B. scalaris 18
B. globosus 18
B. globosus 18
B. globosus 18
B. globosus 18

C. T. LO

Origin
of
snail

Kenya

S. Africa
S. Rhodesia?
Egypt
Sudan
Corsica
Tran
Ghana
Mauritania
Tanzania
Gambia

Debra Birhan,
Ethiopia

Asmara, Ethiopia
W. Aden

L. Bishoftu,
Ethiopia

Ethiopia
Gambia

S. Rhodesia
Ghana
Mozambique
S. Rhodesia
S. Africa

No.
exposed

197
112
239
313
710
136
311
120
108
300
566
118

100
85
50

204
80
82

130

182
60

135

Surviving
160 81

59

with an Egyptian strain of Schistosoma

Positive!

9

1Expressed as the % of surviving snails that shed cercariae or contained various developmental

stages of cercariae on crushing.

2Combined results of 7 populations.

3Mother sporocysts were present in the foot in 14 snails (20%), up to 65 days, but there was no

shedding of cercariae.

BULINUS AND SCHISTOSOMA HAEMATOBIUM 235

TABLE 4. Experimental infection of Bulinus spp. with different strains of Schistosoma haemato-
bium from the literature and from this reportt1,

Results2

Origin Species Origin
of of of Reference?
parasite Bulinus snail

Egypt B. truncatus Egypt Moore et al., 1953

B. truncatus Israel 2 ? ? 30 | + | Witenberg € Saliter-
nik, 1957
B. coulboisi Congo р te ? ? + LeRoux, 1954
В. globosus* | S. Africa ? % E 70 | + | Gismann, 1954
Br globosus* Nigeria ? % 0 0| - | Gismann, 1954 (Berry)
В. forskaliió | Gambia ? ? ? ? | + | LeRoux, 1954
B. forskalii Egypt % ? 0 0 | - | Cowper, 1953 (Barlow)
B. forskalii | Egypt 700 ? 0 о | -6 | Kuntz, 1955
B. forskalii Egypt 1500 ? 1 | .07 + | Kuntz, 1955 (Wells)
Sudan B. truncatus Sudan 775 559 190 34 | + | Malek, 1958
B. truncatus Sudan ? ? ¡0 ? + | Archibald & Marshall,
1932
B. globosus® Sudan 2 % 0 0 | - | Archibald & Marshall,
1932
Bj africanus* Sudan ? ? 0 0 | - | Archibald € Marshall,
1932
B. abyssini- Sudan % % 0 0 | - | Archibald € Marshall,
cus?» ++ 1932
B. ugandae** | Sudan 735 372 6 2 | + | Malek, 1958
B. forskalii Sudan 1070 642 23 4 | + | Malek, 1958
Algeria | B. truncatus Corsica 3401 | 1522 817 53 | + | Capron et al., 1965
B. truncatus Egypt 130 115 20 17 | + | Capron et al., 1965
В. t. rohlfsi Chad 516 276 127 46 | + | Capron et al. , 1965
B. tropicus ? 40 38 0 0 | - | Capron et al., 1965
B. forskalii Y 67 28 0 0 | - | Capron et al. , 1965
Senegal | B. truncatus Iran 76 74 1 1 + [This report
B. guernei Gambia 98 88 i! 1 | + | This report
В. truncatus Corsica 40 36 0 0 | - | Capron et al. , 1965
В. Е. rohlfsi Chad 20 9 4 44 | + | Capron ef al. , 1965

TFor footnotes 1-18, *,+,++, see p 239.

236

Table 4 (cont. )

Origin Species
of of
parasite Bulinus

Gambia | B. forskalii
В. forskalii®

Sierra B
Leone

globosus

=

globosus

Ghana Bente rohlfsil 0

В. guerneill

В. globosust?

B. globosus
B. globosus12

B. forksalüi

truncatus

Е. rohlfsi

Nigeria | B

=

B. globosus
B. globosus

B. forksalii

Western
Africal3 В. truncatus

Uganda | B. trigonust?*
B. tropicus
B. coulboisi
В. nasutus*t

B. africanus

ovoideus**

B. globosus
Be ugandae!>
B. forskalii

С. TEO

Gambia 22
Gambia %

Sierra 9

Leone

Sierra L. 262
Ghana 60
Gambia ?

Ghana 20
Ghana 76
Ghana 106
Ghana 95
Egypt 22
Nigeria 6
Nigeria ?

Nigeria 200
Nigeria ?

Egypt ?

Uganda 645
Uganda 300
Uganda 30
Uganda 500
Uganda 170
Uganda 250
Uganda 210
Uganda 313

? 11
12 2
9 3
16241 118
60 | 59
2 ?
20 | 18
25 | 14
? ?
83 0
? 0
? ?
? 0
? 5
? ?
? 0
? 0
? 0
? 0
454 | 163
? 0
2 | 109
? 0
? 0

33

98

90
56

Reference

Smithers, 1956

Blacklock & Thompson, |
1924

Blacklock & Thompson !
1924

Gorden et al., 1934

McCullough, 1955b,
1956

McCullough & Duke,
1954

McCullough, 1955b
Ingram, 1924

Edwards € McCullough |
1954

McCullough, 1955a,
1955b

Cowper, 1947
Cowper, 1959
Cowper, 1959

Cowper, 1959
(Onabamiro)

Berry (pers. comm. )

Standen, 1949
Cridland, 1955
Cridland, 1957
Cridland, 1957

Cridland, 1955
Cridland, 1955

Cridland, 1955

=

Cridland, 1955 |
Cridland, 1955 |

m ~~ ———

BULINUS AND SCHISTOSOMA HAEMATOBIUM 237

Table 4 (cont. )

Origin
of
parasite

South
Africa

Southern
Rhodesia

Species
of

Bulinus

B. scalaris Uganda 50
В. sp. (n=18)16 $. Africa 2
B. depressus | S. Africa ?
(n=18)16

B. tropicus S. Africa ?
B. tropicus S. Africa 2
B. tropicus W. Came- ?

roon

В. truncatus Israel 2
B. truncatus Egypt te
B. coulboisi ? %
B. africanus S. Africa ?
B. africanus S. Africa 7

B. globosus
B. globosus
B. globosus
B. globosus
BE ugandae**
B. senegalen-
sist
B. forskalii

В. reticulatus*

B. globosus
B. globosus
B. guernei

S. Africa 178

Rhodesia %
Kenya ?
Ghana 2
Tanzania ?
Gambia 2
N.Rhodesia %
W. Aden ?

S.Rhodesia 47
S. Africa 66
Gambia 110

151

105

53

12
60

35

71:
98

Reference

Cridland, 1955
Schutte, 1966
Schutte, 1966

Porter, 1938
DeMeillon, 1948

Wright & Bennett,
1967a

LeRoux, 1958
LeRoux, 1958
LeRoux, 1958
Cawston, 1922

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

Wright & Bennett,
1967a

This report
This report
This report

238

Table 4 (cont. )

Origin
of
parasite

Western
Aden

Yemen

Iran

Iraq

Mauritius

Mauri-
tania

Morocco

B
B.
B
B

.

B.
B.

Species
of
Bulinus

truncatus
truncatus
truncatus
truncatus
sericinus*

forskalii

B. forskalii

beccarii*

reticulatus*

cernicust

mariei

truncatus

Origin
of
snail

Egypt
Sudan
Iraq
Iran

W. Aden
Angola
Kenya

Gambia

W. Aden
W. Aden

Mauritius

Madagascar

Israel

sp. (n=18)16|S. Africa

truncatus
truncatus
truncatus

truncatus

cernicus
truncatus
truncatus

Е. rohlfsi

truncatus

t. rohlfsi

truncatus

18+

Iran
Iran
Iraq

Israel

Mauritius

Egypt

Ca T:. LO

Oo. 49-9. 40: ESS Sm

>= .o" 2 ©) “Oo > E

Reference

Wright, 1963
Wright, 1963
Wright, 1963
Wright, 1963
Wright, 1963
Wright, 1963
Wright, 1963
Wright, 1963

Wright, 1963
Wright, 1963

Wright & Bennett,
1967b

Wright & Bennett,
1967b

Witenberg & Saliter-
nik, 1957

Schutte, 1966
Chu et al., 1966a
This report17
Mills et al. , 1936

Witenberg & Saliter-
nik, 1957

Adams, 1934
Cowper, 1953
Capron et al., 1965
Capron et al., 1965
Capron et al., 1965
Capron et al,, 1965

Witenberg & Saliter-
nik, 1957

BULINUS AND SCHISTOSOMA HAEMATOBIUM 239

Algerian parasite (Table 4). In the
present study, using В. forskalii from
Gambia not a Single infected snail was
obtained.

Testing for the susceptibility of Bu-
linus scalaris in Uganda, Cridland(1955)
obtained negative results. In the pre-
sent study successful penetration of
miracidia occurred in many of the ex-
posed В. scalaris from Southern Rho-
desia. Out of 70 surviving snails, 14
(20%) had developing mother sporo-
cysts in their foot when examined 2-4
weeks after exposure, Further obser-
vations were made for up to 65 days,

but no daughter sporocysts were seen
either in the liver or in other regions.
These snails did not shed cercariae in
Spite of the fact that other species of
Bulinus exposed at the same time and
positive for mother sporocysts, all shed
cercariae within this period. Three
specimens of B. scalaris having mother
sporocysts in their foot were killed at
intervals. Serial sections were made.
These showed that some mother sporo-
cysts had developed and did live up to
65 days after penetration and perhaps
longer, but that many of them had
started to degenerate after about a

Footnotes to Table 4.

lFor schistosome strains other than the Egyptian already quoted in Table 3.

2Question marks in the columns under this head indicate that exact numbers were not given.
3Parentheses refer to the person who provided the original data quoted by authors.

4Quoted as Physopsis without specific designation in the original.

°Identity questionable, probably a mixture of В. senegalensis and В. forskalii(see Smithers, 1956).

6Six specimens (0.9%) had small poorly developed sporocysts when crushed 8 to 15 days after
exposure.

TExpressed as the percentage of number of snails exposed.

SIncludes the result obtained with B. didieri, a synonym of B. globosus, but considered a distinct
species in the original.

9Listed as В. eximia, but now considered a synonym of B. abyssinicus.
10] isted as В. sp. in the original.
llIdentified as В. truncatus, but later considered to be В. guernei (see Smithers, 1956).
12] jsted аз В. africanus, but now considered to be B. globosus.
13Country of parasite’s origin not indicated.

14Results were combined from 3 subspecies of B. trigonus, which is itself now considered to be
merely a subspecies of B. truncatus.

15Listed as В. globosus ugandae which is now considered to be B, ugandae.

16schutte, on morphological grounds, considered these snails to belong to the truncatus group,
but chromosome numbers determined later and immunological studies show that they belong to
the tropicus group (Lo, Burch € Schutte, 1970).

17Data were provided by Mrs. N. Giles of our laboratory.
18Reported as B. forskalii, but later shown to be B. cernicus (see Wright, 1956a).

* = truncatus group
+ = forskalii group
++ = africanus group

240

month (Fig. 3). The process of degene-
ration could be seen in living snails by
the change of size and color of sporo-
cysts. No daughter sporocysts were
found in the sections. If any had been
liberated, their number must have been
very small.

2. tropicus and truncatus Groups

As expected, Bulinus tropicus, long
known to be insusceptible on epidemio-
logical and experimental evidence, was
also refractory to infection in our labo-
ratory. More than 500 snails from 3
African regions were exposed, but none
of them shed cercariae or harbored any
larval stages. Histologic observations
of 3 specimens of B. tropicus from Ken-
ya, each exposed to more than 100 mira-
cidia for 5 hours and then killed, were
all negative for mother sporocysts. The
absence of larval forms suggests that
the process of penetration inthis species
may be difficult, if not impossible. Por-
ter (1938) reported one experimentally
infected specimen of B. tropicus inSouth
Africa, but subsequently Success in this
species was not attained with any of
various strains of Schistosoma haemato-
bium (DeMeillon, 1948; Cridland, 1957;
Capron et al., 1965; Wright & Bennett,
1967a). Thus, from the bulk of available
experimental evidence, B. tropicus from
various parts of Africa al! appear re-
fractory to various strains ci S. haema-
tobium (Table 4). However, it has
lately come to light that some South
African forms of the B. tropicus com-
plex are capable of carrying schisto-
somes (see p 241).

All 5 species or subspecies of snails
in the truncatus group here tested:
Bulinus truncatus truncatus, В. Е. rohlfsi,
B. sericinus, B. coulboisi and B. guer-
nei were susceptible to infection. Among
B. t. truncatus, the population from Iran
proved to be most susceptible; the snails
from the Sudan and Corsica came next;
and the snails from Egypt were least
susceptible. From the 2 populations
of В. Е. rohlfsi, the Mauritanian snails
showed a higher infection rate than those

C. T. LO

from Ghana. B. coulboisi from Tanzania
were a better host than the Egyptian B.t.
truncatus. Highest infections were ob-
tained with B. guernei from Gambia and
B. sericinus from Western Aden, es-
pecially with the former. About 2,000
specimens of B. guernei were exposedto
from 1-50+ miracidia in more than 10
separate trials during this study with
high infections; 100% positive infection
was obtained in 50 snails mass-exposed
to 50+ miracidia per snail.

Bulinus from Ethiopia are of par-
ticular interest with regard to their
taxonomy and susceptibility. Brown
(1965) listed 2 species in the truncatus
group, i.e., В. Е. sericinus andsBasp:
and none in the tropicus group. However,
studies of chromosome numbers by
Burch (1964, 1967a, 1967b) revealed that
the situation is much more complex,
He showed that, from the view point of
chromosome numbers at least, 4 separ-
ate taxa were recognizable, having hap-
loid chromosome numbers n=18, 36, 54
and 72 respectively; Brown & Burch

(1967) surmised that the populations.

with n=36 (i.e., those like B. truncatus)
would probably prove to be the most
important in the eventual transmission
of Schistosoma haematobium.

Three populations of snails from Ethi-
Opia having n=18 were available for
study, and they were all refractory.
Shell characters, chromosome numbers
and refractiveness to the infection indi-
cate that they probably belong to the
tropicus group. Snails with n=72 were
susceptible, although the cercarial incu-
bation period appeared to be slightly
longer, and the cercarial production was
poor. Unfortunately snails having n=36
and n=54 were not available.

3. africanus Group

All of the 4 populations of Bulinus
globosus were susceptible, and among
them the South African snails had the
highest infection of 76% The low sus-
ceptibility of the snails from Ghana and
Mozambique might ensue from their
inherent properties, but another infecting

BULINUS AND SCHISTOSOMA HAEMATOBIUM 241

FIG. 3. Two degenerating mother sporocysts
in the foot of Bulinus scalaris 65 days after

infection. Cells in one of them (upper left)
have disintegrated (X 140).

FIG. 4. Bulinus globosus infected by a pro-
tozoon Hartmannella biparia. A. Nodules at
low magnification (X 135); a: a granuloma
composed of snail amoebocytes and the para-
sites, b: epithelium of intestine, c: mantle,
4: hepatic lobule. В. High magnification
(X 340; a: Hartmannella biparia inside host
cell, b: snail amoebocytes.

agent present in these snails might also
have contributed. Two to 4 weeks after
exposure to miracidia, 40-80% of the

snails from these 2 populations were
noticed to have small nodules around
the intestine in the liver region. The
number of nodules in a snail varied
from a few to as many as 50. The size
of each nodule ranged from less than
100 y to 600 u. When aggregated and
fused, they formed a white patch with an
uneven surface somewhat resembling
the daughter sporocysts of Schistosoma
haematobium. Nodules were also seen
in the mantle collar, the foot and on the
kidney surface. Each nodule was made
up of a great number of snail amoebo-
cytes and many round bodies, measuring
from 7 to 20 y in diameter, which con-
sisted of snail cells infected by a pro-
tozoan Hartmannella biparia (Fig. 4A).
This protozoan has been reported from
the same stock of snails, i.e., B. globo-
sus from Mozambique, as new (Richards,
1968). Snails harboring Hartmannella
grew more slowly than normal ones,
In addition, all Schistosoma-infected
Snails, except one, were those which
did not have these protozoans, and con-
sequently were the larger specimens.
It is possible that the presence of H.
biparia prevented S. haematobium in-
fection either by competing for food or
by increasing snail amoebocyte activity.

4, Chromosome Number and Suscepti-
bility in the tropicus-truncatus Groups

As expected, the present study con-
firmed that the snails in the tropicus
group (n=18) were refractory, while
those examined in the polyploid trun-
catus group (n=36 and n=72) were all
susceptible. Bulinus from Western Aden
with n=72 have previously been found
infected with schistosome cercariae by
Wright (Burch, 1964). These observa-
tions agree with the view expressed in
various publications (Burch, 1964, 1967b;
Burch & Natarajan, 1966; Natarajan et
al., 1965; Brown & Burch, 1967) to the
effect that polyploidy has apparently
occured only in the northern susceptible
forms.

However, the long held belief that all
“southern” Bulinus of the tropicus group,

242 ST.LO

now known to have a haploid chromo-
some number of 18, are non-susceptible
has lately been shaken, Pitchford (1965)
observed infection in a southern Bulinus
population, which he therefore believed
to belong in the truncatus group. Schut-
te (1966) noted the presence, in South
Africa, of 2 forms of Bulinus, one un-
named, and the other assigned to B.
depressus (Haas), that he also both
referred to the truncatus group, as a
proportion of the mesocones on their
lateral radular teeth were truncatus-
like, and as aphallic individuals (a trun-
catus character) had been found to occur
in them. The unnamed form was shown
to be susceptible to Schistosoma haema-
tobium, S. bovis and S. mattheei while
results for B. depressus were negative.
Brown etal. (1967) erected a special
natalensis group for these intermediate
forms, The separation of the natalensis
from the tropicus group, however, large-
ly based on lateral tooth morphology was
not supported by immunological findings
(Burch & Lindsay, 1966, 1970), while
Brown, Oberholzer & van Eeden (1971),
on morphological grounds, also came to
the conclusion that the “natalensis -tropi-
cus complex” did not allow a clearcut
separation. Subsequently Lo, Burch &
Schutte (1970) have confirmed that 2
populations of Bulinus originating from
Nelspruit and Lake Sibaya that were
cytologically and immunologically in-
distinguishable from B. tropicus, were
susceptible to schistosome infection.

5. Local Snail-Parasite Compatability

The data presented in Table 3 illus-
trate the unpredictability of the degree
of susceptibility among various snails.
Surprisingly, our laboratory strain of
Schistosoma haematobium from Egypt
showed great ability to infect a variety
of snails in both the truncatus and
africanus groups. Not only this, but
Bulinus globosus from South Africa, B.
gueynei from Gambia, В. truncatus from
Iran and B. sericinus from Western
Aden, all very distant from Egypt, proved
to be much better hosts than В. truncatus

from Egypt, or at least thanour particu-
lar laboratory strain. The role of
bulinine snails as vectors of S. haema-
tobium has been discussed and results
have been summarized by various wor-
kers (Gismann, 1954; Kuntz, 1955; World
Health Organization, 1957; Malek, 1961a;
Wright, 1966). A review of the litera-
ture on snail susceptibility to schisto-
some infection reveals that in some
cases a high degree of local snail-
parasite specificity does exist (Cowper,
1947; Files & Cram, 1949; McCullough,
1957), but contradictory results are
also on record (Files & Cram, 1949;
Chiu, 1967).

McCullough (1957), in Ghana, found 2
strains of Schistosoma haematobium,
one using Bulinus truncatus rohlfsi asthe
intermediate host and the other B. glo-
bosus. It first appeared as though these
hosts were not interchangeable, but he
later showed that by giving a large
number of miracidia (100+) B. globosus
could be infected with the parasite adap-
ted to В. t. rohlfsi, and vice versa. In
contrast, the Egyptian parasite here used
could infect, though to a variable extent,
all the snails tested in the truncatus
and africanus groups (Table 3), whereas
the Rhodesian parasite could only infect
В. globosus and none of the 6 species
or subspecies of snails in the truncatus
group (Table 4, and unpublished).

6. Infectivity of Miracidia

A comparison of the infection rates
obtained by Chu etal. (1966a) using
Iranian strains of Bulinus truncatus and
Schistosoma haematobium and those ob-
tained in the present study withthe same
stocks of snail and parasite (both were
obtained from the authors), shows a
striking difference (Table 4). These
authors attained 40-80% (av. 69%) posi-
tive infections in snails individually ex-
posed to 2 miracidia, while we obtained
only 9% despite the fact that 5 miraci-
dia were given. Although other factors
such as water chemistry should also be
taken into consideration, the difference
in our results is mainly attributed to

BULINUS AND SCHISTOSOMA HAEMATOBIUM 243

the higher infectivity of miracidia from
human patients, than of those from the
ground intestine of hamsters,

The duration and the degree of in-

portant role in the infectivity of the
miracidia. It was apparent that the
thousands of miracidia obtained from a
sacrificed hamster were not uniformly

viable. A gradient of viability was
noticeable even immediately after hat-
ching, as judged from the mode and speed
of swimming. It was also noticed that
as early as 3 '/3 months after infection,
dead eggs were present in the intestine
of the hamster. Best hatching of eggs
was obtained from hamsters killed be-
tween 5 and 8 months after infection,
and having a heavy worm load, i.e.,
20 pairs or more of adult worms in
copula. Less satisfactory results were
observed with hamsters infected for 12
Or more months. It is possible that
host tissue reaction may modify the
viability of miracidia.

fection in hamsters might play an im-

TABLE 5.

System of classifying the suita-
bility of Bulinus spp. as hosts of
Schistosoma haematobium in the
laboratory.

rapid
medium
slow

Criteria Points alotted

a. Population
growth of un-
infected snails

20% or more
10-19%
1-9%

very high
high
medium
low

b. Infection rate

c. Total No.
of cercariae
produced

7. Efficiency of various Snails as Hosts
in the Laboratory

SND бо ME © = № ©

In order to analyze the efficiency ог
ease of maintaining the schistosome

TABLE 6. Suitability of 10 populations of Bulinus for maintaining the cycles of Egyptian

Schistosoma haematobium,

à Е *
Points received

Origin
of
snail

Snail

Cates ony, species

Total

Gambia

W. Aden

guernet

Good

sericinus

t. truncatus | Iran

. t. rohlfsi
t

Mauritania

. truncatus | Corsica

Fair ‚ t. truncatus | Sudan

. E. rohlfsi

Ghana

a a D OO =

coulboisi Tanzania

t. truncatus

Egypt

sp. (n=72) Ethiopia

*Even where points given are the same, the order of listing does reflect grading in des-
cending order, but at a level not expressible with the relatively rough point system.

244 CARLO

cycle, snails were gradedfromthe view-
point of 3 major criteria. For each
of these, points were given to each of
the snail species considered, so as to
allow comparison (Table 5).

Based on these criteria, 10 popula-
tions of snails in the truncatus group
were placed in 3 categories, i.e., good,
fair and poor (Table 6).

Bulinus globosus from South Africa
was not included in the comparison
because of its high mortality, inspite of
the fact that it was highly susceptible
and emitted large numbers of cercariae.
It was difficult to rear B. globosus in
sufficient numbers, and the author was
therefore reluctant to use it in his ex-
perimental series, but with improved
culture methods, this South African snail
should make an excellent carrier of
laboratory life cycles.

8. Barriers to successful Infection

Factors affecting susceptibility have
been discussed by Wright (1956b) and
Malek (1961a,b). They can be classified
in various ways, such as biological and
non-biological, physical and physiologi-
cal, etc. Malek (1961b) distinguished 3
categories: parasite, snail, and environ-
mental factors. But, as pointed out by
Wright (1956b), although factors may be
itemized for convenience, susceptibility
is acomposite result of numerous factors
acting together. From the viewpoint of
processes of infection, we can conceive
of 2 barriers which obstruct success of
the parasite: (1) a penetration barrier
and (2) a developmental barrier, Suc-
cessful penetration certainly depends on
factors connected with the parasite, the
snail, and the aquatic medium, while
development depends on the biochemical
environment of the snail’s body. Pene-
tration occurs in a number of snails,
though subsequent development does not
take place in all of them.

With Bulinus scalaris, miracidia had
penetrated and mother sporocysts had
grown quite well for some time, but
eventually all of them died without libe-
rating daughter sporocysts. In В. tro-

picus, as in all other non-susceptible
snails, barriers were probably so great
that none of the snails became infected.
Among the receptive snails reported
here, the degree of susceptibility pro-
bably reflects the effect of the pene-
tration barrier in each population. This
is true of at least B. guernei since in
this snail, the miracidia that succeeded
in penetration all eventually matured
into cercariae. Because of the less
specific nature of the penetration pro-
cess, it is possible to increase snail
infection by lowering the penetration
barrier, which can be attained by modi-
fying conditions during snail exposure,
as will be shown below.

II. SOME FACTORS AFFECTING IN-
FECTION IN BULINUS GUERNEI

Several easily measurable factors
were tested for their influence on snail
infection. Except for the factor under
investigation, the other experimental
conditions were standardized as follows:
miracidia less than 2 hours old, 30°C,
pH 8.0, individual exposure to 10 mira-
cidia in 2 ml of water, and snails 3-5
mm high. Only Bulinus guernei was
used for this study because it had been
shown to be the most suitable host
available.

1. Hydrogen Ion Concentration

Results of snail exposure at different
pH values are shown in Table 7. The
data are not critical because pH values
did not remain static during exposure,

Observations were also made on the
survival of groups of 20 miracidia each
under different pH conditions for com-
parison with the snail data. A mira-
cidium was considered dead when cili-
ary movement completely stopped in all
parts of its body. At pH 3, miracidia
were active for 5-10 seconds, then ra-
pidly became sluggish; most of them
stopped ciliary movement in 2 minutes,
some only persisting up to 4 minutes, |
At pH 4, they were active for 10-30 |
seconds, then gradually became sluggish;
normal swimming was discontinued in 1

|

BULINUS AND SCHISTOSOMA HAEMATOBIUM

TABLE 7.
various pH values.

Initial
pH

SZENEN Be

10
ial
12

minute although ciliary movement per-
sisted up to 6 minutes. At pH 5, they
swam normally for about 1 minute;
within 3 minutes the majority of them
stopped swimming or showed abnormal
Swimming patterns. Death occurred in
5-22 minutes, At pH 12, the miracidia
ruptured almost immediately, disinte-
grated, and became unrecognizable in
30 seconds. It thus seems impossible
for miracidia to penetrate into the snail
at pH values of 3, 4, 5 and 12, because
of their short survival time. That posi-
tive results were obtained at initial pH
values of 4 and 5 is due to the fact that
the snails were placed into the water
before introducing the miracidia, the
presence of the snail probably changing
the pH to near 6 or above in a very
Short time. In all other cases, viz.,
from pH 6 to 11, normal-looking mira-
cidia were present up to 10 hours. For
the analysis of data, therefore, it seems
more appropriate to consider the pH
values obtained at the end of exposure,
1.е., after 5 hours, rather than the ini-
tial pH.

Positive results were obtained in
snails exposed at final pH values ran-

Snails

245

Exposure of Bulinus guernei to miracidia of Schistosoma haematobium at

pH values at 5 hours

D. 3.0
6. 4.1
6. 5.2
Te 6.4
8. 7.7
8. 8.6
8. 9. 0
0» 9.4
9. 10.4

i 11.8

ging from 6,1 to 9.6. Differences in the
infection rates were Significant at the
1% level of probability (P<0.01). Fur-
thermore, pH levels could be grouped
according to percentages of infection
which were Significantly different from
each other: (1) at pH 6.1, the infection
was low (11%); (2) at pH levels from 6.9
to 8.6, infection increased to 23-28%;
and (3) at pH readings from 9.4 to 9.6,
the highest infections, 33% and 49%
respectively, were obtained, It was
clear that miracidia could tolerate a
wide range of hydrogen ion concentra-
tions, at least from pH 6.1 to 9.6, in
terms of successful infection. The
lowest limit of pH at which infection
could be established was somewhere
between 5 and 6.1; the highest limit
was between 9.6 and 11.8.

Table 7 also shows that Bulinus guer-
nei could tolerate an initial pH ranging
from 3 to 11. At pH 3, the snails im-
mediately became inactive upon contact
with the water, many of them turned the
aperture side up, but recovered gradu-
ally when returned to a maintaining
aquarium. At pH 12, all snails were
dead within 5 hours. Statistically, the

246 €. E. LO

snails’ ability to survive for 5 hours
between initial pH values of 3 and 11
was not significantly different (P>0.3),
pH 10 excluded, A high mortality in
the pH 10 group was caused by unhealthy
conditions in that particular aquarium.

Thus present results indicate that
while at an initial pH of 3-5 the snails
can survive, the miracidia’s survival is
limited to such a short period that a
successful penetration seems unlikely.
At an initial pH of 12, not only the snails
but all miracidia also died in a short
time and infection was, therefore, im-
possible. Optimal results were obtained
at initial pH 10 and 11, resulting in pH
9.4 and 9.6 after 5 hours. It has been
demonstrated for Schistosoma mansoni
that miracidia survived longer at pH
8-9 than at pH 7-8 or 5-6 (Maldonado
et al., 1950). The higher percentage of
infection observed in more alkaline me-
dia might be brought about either by a
prolonged miracidial life, or by changes
in the Snail mucus or epithelium.

2. Temperature

The results of snail infection at tem-
peratures between 5° and 35°C, at 5°
intervals, are shown in Table 8. Dif-
ferences in infection rates among groups
were highly significant (P<0.001). The
highest infection was obtained at 30°C
(67%), and the peak is probably some-
where between 30°C and 35°C. Results
at 20°C and 25°C were not significantly
different (P>0.05).

At 5°C the miracidia were so sluggish
that there was little swimming activity;
most of them crawled on the bottom of
the container. At 10°C the movement
was slowed down considerably from nor-
mal, but normal swimming patterns were
still retained. Above 10°C, the swimming
activity was proportionally more vigor-
ous with increase in temperature, re-
sulting in a higher infectivity. However,
the highest infection which occurred at
30°C, did not coincide with the most
vigorous swimming activity at 35°C.
At 35°C, miracidia were more active,
but they exhausted themselves so rapidly

TABLE 8. Exposure of Bulinus guernei to
miracidia of Schistosoma haemato-

bium at various temperatures.

Positive
snails

Surviving
snails

No. of
snails
exposed

that many of them probably did not have
sufficient time to complete penetration,
Moreover, the snails had not been given
time to adjust to this temperature prior
to the exposure, and this caused many
of them to withdraw into their shells.
Contracted muscle, decreased area of
exposure, and increased mucus secre-
tion from these snails under such un-
comfortable conditions, perhaps contri-
buted to the decreased infection, At
30°C, both the snails and the miracidia
were active; the head-foot region of the
Snails was fully extended and provided a
greater area for penetration.

Mortality of snails among the various
groups was not significantly different
(P>0.1) if the group exposed at 35°C is
excluded. In that group 48% of the
snails had died during the cercarial
incubation period, most of the deaths
taking place the day after exposure.

Results obtained in this study slightly
differ from those of Chu et al. (1966b),
who tested several groups of Bulinus
truncatus at temperatures ranging from
10°C to 38°C with the Iranian strain of
Schistosoma haematobium. They ob- |
tained positive results inall cases, while ©
in the present study we obtained a nega-
tive result at 10°C, as did DeWitt (1955)

AS

|

BULINUS AND SCHISTOSOMA HAEMATOBIUM

with $. mansoni.
3. Number of Miracidia

As shown in Table 9, the infection
rate in this comparative series in-
creased with the number of miracidia
given to each snail. With only a single
miracidium, 6% of surviving snails be-
came infected; with 60+ miracidia the
infection was 70% The differences
among all groups were highly significant
(P<0.001). The relationship between
the infection rate and the number of
miracidia was not linear, i.e., the rela-
tive rate of increase became progres-
sively smaller as more miracidia were
supplied, for which reason a 100% in-
fection was hard to attain (Fig. 5B).
However, as stated earlier (p 240), a
group of 50 snails (non standard; sizes
not measured, etc.) mass exposed to
50+ miracidia became all positive. In
this study, when the snails were exposed
to one miracidium each, an average of
16 miracidia were expended in order to
produce one infected specimen; at 50
miracidia per snail, the number expended
was 79 (Table 9). Thus it is clear that
for the propagation of the parasite a
Single miracidium per snail appears to
be the most efficient ratio. Data on the
relation between miracidial dose and
percentage of infection are also avail-
able from other studies for the Iranian
strain of Schistosoma haematobium(Fig.
5A) and the Puerto Rican strain of S.
mansoni (Fig. 5C, D) (Chu et al., 1966d;
Schreiber & Schubert, 1949b; Stirewalt,
1951).

4. Age of Snails

Archibald & Marshall (1932) using
Sudanese material and Moore et al.

` (1953) with Egyptian material showed

that young Bulinus truncatus were more
Susceptible than adults to Schistosoma
haematobium infection. This was also

‚ found to be true for В. guernei (Table

10). Differences in infection rates were
highly significant for certain age groups
(P<0.001). Analysis revealed that in-
fection rates among the 3 groups com-

247

prising 3, 7, and 12-day old snails, and
also between the 2 groups with 20 and
28-day old specimens, were not different
(P>0.25 and P>0.5 respectively). But
infection rates between the 2 pooled
Samples of these groups, i.e., those
from 3, 7, 12 days olds (measuring
1-3.5 mm) and from 20, 28 days olds(4-
5.5 mm), were very different (P<0.001):
at a miracidal dose of 10 per snail, the
former showed infections from 40-67%
(av. 47%), while the latter were 18-22%
(av. 20%) positive. The group having a
shell height of 7.2-8.2 mm (55 days old)
was negative. However, whena larger
dose (50+) of miracidia was applied,
positive infection was obtained in even
larger specimens (8-9 mm, 60 days old).

Since age and size are interrelated it
is difficult to assess whether the low
infection among the larger snails is due
to age or size (Newton, 1953). Experi-
ments using snails which are old but
stunted in growth should give ananswer,
Archibald & Marshall (1932) attributed
the higher susceptibility in young snails
to their softer tissue. The present
study indicates that the difficulty with
Old specimens lies in penetration and
not in the development within the snail’s
body. More abundant mucus secretion
in the larger, hence the older snails,
no doubt hinders miracidial penetration.

Snails about 3 days old (1-1.5 mm)
had the lowest survival rate of 24%,
while in other groups it ranged from
74% to 98% (Table 10). Later study of
snail mortality (p 252) and daily hand-
ling of snails seemed to indicate that
environmental factors played a much
greater role than did the parasite in
causing snail death, except for the very
young snails (3-day old group). With
the combined effect of mortality and
susceptibility in mind, it is apparent
that snails from 2 to 4mm, or an
average age of 7-18 days, are the best
choice for obtaining the maximum num-
ber of infected specimens.

9. Fixing of Snail Position

By keeping snails immobilized during

248

exposure, the percentage of infection
was increased 6-fold. In an unrestrained
group, among 46 survivors of 50 snails
(5-6 mm high when exposed), 4 (9%)
became infected; in a corresponding
fixed-position group, 14 (54%) out of 26
Survivors became positive. The dif-
ference was highly significant (P< 0.001).

In an effort to free itself from a fixed
position, a snail would maximally extend
its head-foot region beyond the shell,
thereby greatly increasing its chances
of infection because of the much larger
area offered for penetration. In addi-
tion, the chances of dislodging a pene-
trating miracidium by jerks or evasive
movement are probably greatly de-
creased. But, since the procedure of
affixing the snails was time consuming,
and since almost one half of the snails
(22 out of 50) became free during ex-
posure (these were discarded), the me-
thod is not practical in a large scale
operation,

6. Anesthetization

When snails were narcotized with
Nembutal, 38 (81%) of the 47 survivors
(exposed to 10 miracidia each) became
infected (Table 11, group a); in the con-
trol group(b), only 17 (37%) of 46 sur-
vivors became positive. The difference
was highly significant (P<0.001). When,
however, the miracidial dose was in-
creased to 30-40 per snail (group c),
the infection increased to 75% (54 out of
72) even without anesthesia. Observa-
tion further showed that each anesthe-
tized snail harbored on the average 1.7
sporocysts (group a); the corresponding
number without anesthesia was 1.2(group
b), though with 30-40 miracidia, also
without anesthetization (group c), it rose
to 1.6. Miracidial efficiency similarly
increased greatly with narcotization,
i.e., from 27 to only 12 miracidia per
infected snail, being even better than
the optimal efficiency of 16 attained
with single miracidia (Table 9).

The frequency distribution of the num-
ber of sporocysts showed that with
anesthesia (group a), about half (53%) of

C. T. LO

100 A
90
80
70
B
60
50
N S. haematobium
30
20
Z 10
O
—
oO
Eg
fa
2
je
©
BS
S. mansoni
19225 5 7 10 12 20
NO. OF MIRACIDIA/SNAIL
FIG. 5. Relation between miracidial dose

and percentage ofsnail infection with Schisto-
soma haematobium and S. mansoni. A. from
Chu et al. (1966b); B. present study; C. from
Schreiber & Schubert (1949b); D. from Stire-
walt (1951).

the infected snails had one sporocyst,
and the rest from 2 to 4 sporocysts.
In contrast, without anesthesia(groupb),
88% of the infected snails had but one
sporocyst, while only 12% had 2 or 3
sporocysts and none had more, The
results in group c, with a high mira-
cidial dose, approximate those of group

BULINUS AND SCHISTOSOMA HAEMATOBIUM 249

TABLE 9. Exposure of Bulinus guernei to varying numbers of Schistosoma haematobium mira-
cidia.

No. of
miracidia Miracidial efficiency!
per snail No. exposed

pa <

i
lExpressed as the number of miracidia expended to produce one infected snail regardless of the

number of miracidia which penetrated. Obtained by dividing the total number of miracidia
used on surviving snails by the total number of positive snails.

2The snails were mass-exposed 3 times in 3 days; each time 20+ miracidia per snail were pro-
vided.

TABLE 10. Exposure of Bulinus guernei of various age groups to 10 mira-
cidia each of Schistosoma haematobium.

Estimated
average age
(days)

Snail size at
exposure!
(mm)

10-185
2. 0-2. 5
3. 0-3. 5
4. 0-4. 5
5. 0-5. 5
7. 2-8. 2
8. 0-9. 02

ISnails falling in the gaps between size classes were excluded.

250+ miracidia per snail.

a; one snail, however, had 6 sporocysts. came 100% positive (p 240), a majority
In another experiment where 50 Bulinus of the snails harbored from 4 to 6
gueynei were mass exposed to an even sporocysts and some had as many as 8,
higher dose of miracidia (50+) and be- The increase in the infection rate

250 C. T. LO

under anesthesia was probably brought
about by the decrease in the snails’ sen-
sitivity to miracidial irritation, by de-
creased mucus secretion and by the
relaxation and extension of the snail
body. However, Nembutal itself may
perhaps adversely affect miracidia; it
was observed at any rate that miracidia
were not attracted to snails narcotized
with a 5% Nembutal solution (as against
1% employed here) for 1 hour.

III. HOST-PARASITE RELATIONSHIPS
BETWEEN BULINUS AND SCHISTO-
SOMA HAEMATOBIUM

1. Effect of Infection on the Growth of
Bulinus spp.

a. During prepatent Period

The height of snails which had been
exposed to miracidia 5 weeks earlier
was measured in order to see if there
were any significant differences between
positive and negative specimens. Influ-
ence of environmental factors was negli-
gible since they had been reared in the
same aquaria. A total of 7 populations
of Bulinus was available for such com-
parison and results are shown in Table
12. Analyses of variance homogeneity
and mean homogeneity indicated that in
all cases, the differences were not sig-
nificant.

Bulinus guernei was investigated in
greater detail. The snails used were
those already reported on in the age-
susceptibility study (Table 10). At 4
weeks after exposure none of the 5 size
classes studied showed significant dif-
ferences in shell height between infected
and uninfected snails (Table 13). When
the mean heights of negative snails (Y)
were subtracted from those of positive
snails (X) in each group, an interesting
trend became apparent, i.e., the differ-
ences became progressively smaller as
the initial size was larger. The first 4
size classes, comprising specimens from
1.0 mm to 4.5 mm, consistently showed
slightly larger mean values in unin-
fected snails, while the largest class,
5.0-5.5 mm, positive snails attained

uninfected
infected----

B. truncatus;
Iran

a

HEIGHT OF SHELL IN MM
.
o

©

6 8 10 12 14 16
WEEKS AFTER EXPOSURE

FIG. 6. Average growth curves of uninfected
(solid line) and infected (broken line) Bulinus
from 6 to 16 weeks after exposure. The
initial number of snails and size range (ver-
ticall lines) are indicated above the starting |
point (6 weeks).

a larger size than negative snails.
Table 13 further shows that snails which
were initially larger did not always re-
main so (e.g., the 3 mm and 5 mm |
classes), indicating that conditions in |
each aquarium, nearly identical at the
beginning, had changed; more favorable
conditions being reflected by larger

BULINUS AND SCHISTOSOMA HAEMATOBIUM

251

TABLE 11. Effect of anesthetization on the penetration of Schistosoma haematobium miracidia
into Bulinus guernei and frequency distribution of mother sporocysts.

Experimental Av
ote Pata No. (and %)| No. (and %) of snails having end Miracidial
of positive | following No. of sporocysts: E er
(and No. of snails ‘ sporocysts | efficiency
e survivors | 1 2 3 4 5 6 .
surviving) per snail

Anesthetized (47); 20

10 miracidia.

b. Not anestnetized (46); 15

10 miracidia.

28
(52)

c. Not anesthetized (72);
30-40 miracidia;
mass infection.

12
(53) (32)

1
(88) (6)

23
(42)

4 2 12
10) (5)
1 27
(6)
1 40-53

(2) (2)

TABLE 12. Size of infected and uninfected Bulinus spp. 5 weeks after exposure to 10-20 mira-
cidia of Schistosoma haematobium,

Origin
Species of Bulinus of
snail

B. t. truncatus Egypt

В. t. truncatus Sudan

В. t. truncatus Iran
В. t. rohlfsi Ghana

B. coulboisi Tanzania

B. sericinus W. Aden

B. globosus S. Africa

Snail size. The results also suggest
that the effect of the aquatic environ-
ment on the growth of these snails was
much more profound than that caused by
the parasites.

b. After the Onset of cercarial Emer-
gence

Growth curves were obtained for 3
species of Bulinus from positive and
| negative snails measured between the
| 6th and 16th week after exposure, With-
| in each species, snails were divided into
2-3 size classes (Fig. 6). None of the 8

Mean shell height (mm)
and standard deviation

Mean difference
in growth (mm)
Negative X-Y

(Y +S.D.)

Positive
(X+S.D.)

6292002 6‘ 0

Е И 2509 -0.1

6.8 +1.4 ‚015 -0.2

6.9 +0.8 7641056 +0. 3

6.7 1..0

7
tf
6

8.8 20.2 8.6 +0.2 +0. 2
6.8,505.7 -0.1
5

5.8 21.3 OEM +0. 2

size groups studied showed at any time
a significant difference in mean shell
height between the infected and uninfected
snails at the 1% level of probability.
Comparison of curves, however, shows
that in the smallest size class of B.
truncatus and B. guernei, uninfected
snails grew faster than infected ones.
In the larger size groups the situation
was reversed; in most cases the infected
snails grew faster than the uninfected
ones. In B. sericinus, uninfected speci-
mens grew more than infected snails
with a minor deviation after the 13th

252

TABLE 13.

Number of snails

Snail size at
exposure (mm)

4 weeks after exposure

Mean shell height and
standard deviation (mm)

Positive

(X+S. D.)

EAT. LO

Size of Bulinus guernei exposed to 10 miracidia of Schistosoma haematobium.

Mean dif-
ference

in growth

(Y)

Negative
(Y+S.D. )

1.0-1.5 4,90 + 0.68 | 5.42 + 0. 54

2. 0-2. 5 5.88 + 0.80 | 6.04 + 0.60 >0. 4
3. 0-3. 5 5. 26 + 0.73 | 5.37 + 0. 56 70.5
4. 0-4. 5 7.01 + 0.20 | 7.05 + 0.49 70.5
5. 0-5. 5 6.96 + 0.30 | 6.90 + 0.45 >0.5

TABLE 14.

Mortality in Bulinus guernei of various size groups, exposed and not exposed to
miracidia of Schistosoma haematobium during 4 weeks of prepatent period.

Snail size
at
exposure
(mm)

surviving

1.0-1.5 50 12
2. 0-2.5 50 43
3. 0-3. 5 50 40
4. 0-4. 5 50 49
5. 0-5. 5 50 46

week in the small size group.

2. Effect of Infection on the Survival of
Bulinus spp.

a. During prepatent Period

Data on the survival of exposed snails
were derived from the same groups of
Bulinus guernei already quotedin Tables
10 and 13. Control groups were also
set up for comparison (Table 14), The
mortality among the size classes within
the exposed group differed significantly
(P<0,001) because many snails had died
in the smallest size class, The same
trend was also evident in the controls.

| Exposed to 10 miracidia | to 10 miracidia

No. %
RM Led me surviving | surviving

Bee

When comparison is made between ex-
posed and unexposed groups of the same
class, mortality is seen to be signifi-
cantly different in the 1.0-1.5 mm class
only (P<0.001).
concluded that in exposed snailslessthan
1.5 mm high, the high mortality during
the 4 weeks after exposure was caused
by both infection and improper environ-
mental conditions whereas in snails
larger than 2 mm death was caused

Therefore, it may be

mainly by factors other than the para=

site,

Although Bulinus guernei survived well
during the cercarial incubation period,
it was not so in B. globosus, where in-

BULINUS AND SCHISTOSOMA HAEMATOBIUM 253

fected specimens began to die from 3
to 4 weeks after infection. Moreover,
this species was less tolerant of inten-
sified light and increased temperature,
which were employed to stimulate cer-
carial emergence, and some of the small
snails died after one or after afewdays.

Except for the snails less than 1.5
mm, the number of miracidia provided
for a snail had little bearing on mor-
tality in Bulinus guernei, at least up to
50 miracidia. In a previous experiment
(p 240), in which 50 B. guernez were
exposed en masse to 50+ miracidia per
snail, all survived the cercarial incuba-
tion period.

b. After the 6th Week

After the onset of cercarial emergence
snail mortality rapidly increased. Lon-
gevity was recorded for 10 populations
(Table 15). The maximum survival
after exposure ranged from 8 weeks
(Bulinus truncatus truncatus, Egypt) to
32 weeks (B. guernei), and the average
survival time ranged from 8 to 16.7
weeks. The specimen of B. guernei that
had survived for 32 weeks was killed
for histological study, since it had been
less active for several days and would
probably soon have died.

The extent of mortality causedby infec-
tion in Bulinus truncatus truncatus (Iran),
В. t. truncatus (Sudan), В. sericinus and
В. gueynei is shown by their survivor-
ship curves together with those of their
controls (Fig. 7). All of the infected
Specimens died more quickly than the
controls. Among the infected snails,
curves for both populations of В. t.
truncatus (Sudan and Iran) declined
Sharply from the beginning, while in B.
sericinus and B. guernei the decline was
much slower. Among the control groups,
the Sudanese В. Е. truncatus all died
within 21 weeks, when 40-80% of the
other 3 populations were still alive. It
is clear that prevailing laboratory con-
ditions were less suitable for the Suda-
nese snails than for the other 3 popula-
tions.

Attention was also focused on snail

о =B. sericinus

O =B. truncatus;
Sudan

— uninfected

--- infected

=)
<
>
>
rs
>
u
E
©
100}
wo N = =B. guernei
\ »
901
à eo =B. truncatus;
80F * I
\ ran
\
TOP :
h
Ge
e
50+ os
\
\
40 à
\
\
30+ R
« »
20- e .
LA =
\
10 e 0
X VA
QA 1 1 ми fi 1 1 y Ey HEEE
DO AAA EN AAA A 32
WEEKS AFTER EXPOSURE
FIG. 7. Survivorship curves for uninfected

Bulinus spp. (solid line) and infected Bulinus
spp. (broken line) from the 6th week after
exposure onwards. Initial numbers of posi-
tive and negative specimens were, respec-
tively, 21, 21 for B. sericinus; 51, 20 for B.
t. truncatus from the Sudan; 30, 30 for B.
t. truncatus from Iran; and 60, 35 for B.
guernei.

254

size in connection with mortality. Re-
sults from 4 populations (Table 16)
consistently showed that smaller speci-
mens survived for shorter periods than
larger ones,

Infected specimens of Bulinus guernei
and В. sericinus survived for a long
time. They seldom appeared sick, and
feeding seemed normal. On the other
hand, B. truncatus truncatus and B. glo-
bosus appeared to be more sensitive to
infection. Infected snails of B. sp.,
(n=72) were very inactive throughout
their lives, and cercarial production
was low. Sincethese snails proved hard
to raise even without infection, it is
difficult to say whether they actually
are as sensitive to schistosome infec-
tion as our limited observation would
suggest.

The survival times reported by various
authors for Bulinus truncatus after the
first shedding of cercariae vary greatly
and undoubtedly reflect the prevailing
laboratory conditions. Infected speci-
mens were short-lived, most dying in
10-21 days, in the experiments of Moore
et al. (1953) or in about 2 weeks(Capron
et al., 1965). Archibald (1933) reported
that experimentally infected B. truncatus
were capable of shedding cercariae for
75 days, while naturally infected snails
(Sudan) survived for 4 !/› months in the
laboratory. Probably the longest sur-
vival time on record is that fora positive
snail from Iran surviving for 329 days
(Chu et al., 1966a). The latter authors
further found, in contrast to my results,
that snails exposed to fewer miracidia
survived longer. In the present study
the most revealing indicator of ultimate
Survival of infected snails was the size
they attained during the incubation peri-
od.

For Bulinus globosus, Wright & Ben-
nett (1967a) reported that the majority
of infected snails died within 3 weeks
after the first shedding. In the present
study 41% of 70 snails were still alive 3
weeks after the first shedding, the last
snail surviving for 9 weeks, 1.е., 14
weeks after exposure.

Ст. то

3. Effect of Infection on the Fecundity of
Bulinus spp.

The egg-laying capacity after cercar-
ial emergence was recorded in 5 popu-
lations of Bulinus spp. (Table 17). Though
generally, the suppression of egg laying
was noticed from the 3rd week after
infection, observation started between
the 6th and the 8th week after infection,
and continued for 4-12 weeks, when 13-
100% of infected snails were still alive.

a. Fecundity in infected and uninfected
Snails

Table 17 shows that the control group
of any size class or any Species hada
much higher fecundity than the infected
group. The average numbers of eggs
per snail per week ranged from 0 to 8.3
in the infected groups, and in 8 out of
12 groups, it was less than 1.0. In the
controls, 9 groups out of 12 had more
than 10 eggs/snail/week. A comparison
between positive and negative snails
within the same size class reveals that
the smallest difference occurred in the
8.4 mm group of Bulinus truncatus trun-
catus from the Sudan, in which the in-
fected snails had 8.3 eggs as compared
to 55.4 in the control, i.e., 7 times less,
The largest difference (100-fold) was
seen in B. coulboisi, despite their large
size (7.4 mm). The infected group laid
0.1 eggs/snail/week as comparedto 10.1
in the control.
10 to 59 times as great in the remaining
groups, except for the smallest size B.
sericinus, where infected specimens did
not produce a single egg.

Differences were from

The total

average number of eggs/snail/week re-

gardless of species and size was 1.2,

for the infected and 17.6 for the unin-

fected snails, i.e. the latter were 15

times as productive.

The number of clutches/snail/week
was consistently higher in the controls,
ranging from 0.9 to 6.6 (av. 3.1), while
in the infected groups it ranged from

0.04 to 3.3 (av. 0.5), the uninfected |

group laying 6 times as many clutches,
As for the average number of eggs per

BULINUS AND SCHISTOSOMA HAEMATOBIUM 255

TABLE 15. Survival of Bulinus spp. infected with Schistosoma haematobium (10-20 miracidia)
irrespective of snail size.

No. of
snails

Survival after
exposure (weeks)

Species
of Bulinus

Origin
of snail

В. t. truncatus Egypt 50) 8
В. t. truncatus Sudan 10.9 19
B. t. truncatus Corsica 1145 12
B. t. truncatus Tran 9.6 14
В. t. rohlfsi Ghana 15.0 18
B. sericinus W. Aden 14.8 22
B. coulboisi Tanzania 10. 2 13
B. guernei Gambia 16.7 32
B. sp. (n=72) Ethiopia 995 11
B. globosus S. Africa 2 14

TABLE 16. Survival of various size groups of Bulinus spp. infected with Schistosoma haematobium.

: : Size (mm) 6 weeks | Average survival Maximum
Snail species No. of 3
ale nas after exposure after exposure survival
(X +S. О.) (weeks) (weeks)
B. truncatus truncatus 9 14
Iran 13 14
8 10
B. sericinus 10 22
W. Aden 8 22
3 17
В. guernet 10 32
Gambia 24 27
26 24
B. globosus 13 14
S. Africa 16 14
21 12
20 12

256 Corks LO
TABLE 17. Fecundity of cercaria-shedding and uninfected Bulinus spp.
Size (in
Snail zur) No. of пе % of
г when bani egg- normal
Species started clutches eggs
(X +S. D.)
198 8.3 Sata PASS) 97.0
FR
lo lan! 119 100
123 22 ileal 2.9 92.7
ite 13 1.0 0.8 21289538
mee me 0.1 0.04 | 2.0 | 100
т 4. 3 0.9 4.8 100
0.1 0.2 Or 50.0
17 0.2 0.2 1.1 88. 2
Ba 63 0.9 0.5 1.8 82.5
a 0 0 0.3 0 0
0.6 0.3 2.13 88.5
В. 61 0.9 0.3 32 82. 0
27 0.6 0.2 Ч 84.6
Total 305 se 0.5 Pep il 91.0
Lin 2133 wee 17 3.1 5.8 | 98.7

*Abortive clutches, consisting of gelatinous matrix only

clutch, it ranged from 3.6 to 8.6 eggs
(av. 5.8) in the controls, and from 0 to
3.2 (av. 2.1) in the infected snails, the
former having about 3 times as many
eggs. In other words the size of the
clutch was less affected in the infected
snails than the frequency of oviposition.
This tendency agrees with the results
reported by Chu etal. (1966d), but
differs from those of Natarajan (1961).

In addition to decreased egg produc-

tion, infected snails had an increased
tendency to lay abnormal eggs: whereas
98.7% of 12,285 eggs were normal in
the uninfected group, only 91% of the
643 eggs laid by infected snails were
normal,

b. Fecundity in Snails of different
Size (Tables 17, 18)

While uninfected Bulinus truncatus
truncatus (Sudan and Iran) and B. seri-

257

BULINUS AND SCHISTOSOMA HAEMATOBIUM

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258

cinus of larger size produced more
eggs than smaller ones, the situation
was reversed in B. guernei, where the
smallest size class produced more eggs/
Snail/week. These smallest snails ap-
peared to be at their peak of reproduction
for reasons unknown.

The tendency in infected snails was
similar to that in uninfected snails. Egg
production was about 6 times greater in
the 8.4mm group than in the 6.0 mm
group of Bulinus truncatus truncatus
from Sudan, and 22 times greater in the
8.6 mm group than in the 4.8 mm group
of B. t. truncatus from Iran. The smal-
lest group of B. sericinus (4.6 mm) de-
posited 6 abortive “clutches”, that were
composed of only the gelatinous masses
and contained no eggs. Differences
among the 3 size groups of B. guernei
(8.7, 7.2 and 6.2 mm), however, were
slight, the number of eggs/snail/week
ranging from 0.6 to 0.9.

c. Weekly Egg Production

Average weekly egg production for
infected and uninfected snails of 5 popu-
lations (4 species) of Bulinus is shown
in Table 18. Generally, there is nocon-
sistent pattern as to the number of eggs
produced from week to week. Some of
the more salient features among the
infected specimens are as follows: Egg
production was low or entirely lacking
in Bulinus coulboisi during the whole
period. Large and medium classes of
B. t. truncatus from Iran continued to
lay eggs until the 13th week after ex-
posure, then ceased; in the smallest
size class, egg laying occurred only
in the 8th week. Large and medium
classes of B. sericinus started egg lay-
ing, possibly after a period of suppres-
sion, in the 11th and 12th week respec-
tively. In the smallest class of B.
guernei there was a complete suppres-
sion of egg laying after the 10th week.

d. Abnormal Eggs

Anomalies, as observed and analyzed
as to category in 5 populations of Bulinus,
were more frequent in the infected than

EITIEO

in the uninfected snails. In the former,

46% of egg-clutches and 16.9% of eggs |

were abnormal; the corresponding fig-

ures for the latter were 3.5% and 1.1% !

(Table 19). In uninfected snails, abnor-
malities seemed to increase with age.
Frequently, anomaly in an egg was not
limited to one feature, but was a combi-
nation of several. Abnormalities can be
classified into 7 categories, as follows:

(i) Absence ofovaingelatinous matrix.
The condition was observed in all of
the species studied, The frequency of
such abortive spawn in infected snails
varied from 3.3% in Bulinus truncatus
rohlfsi to 41.4% in В. sericinus. In the
uninfected groups, it ranged from 0% in
B.t. truncatus from the Sudan and in В.
sericinus, to 0.7% in B. t. truncatus
from Iran and in B. t. rohlfsi. These
gelatinous masses were smaller than
normal clutches, appeared cloudier, and
contained an irregularly shaped, con-
densed portion.

(ii) Egg larger than normal. Only one
Such egg was found out of a total of
25,903 eggs examined. Although this
egg was laid by an infected Bulinus
guernei, there is no reason to attribute
the irregularity to the infection,

(iii) Egg smaller than normal (Fig.
8A, C, J). Small eggs were 10 times
more frequent in the infected groups:
4.22%, against 0.41% in the uninfected
groups.

(iv) Absence of embryo in the egg
(Fig. 8J). This feature was also more
frequently seen in the infected groups:
3.52% as opposed to 0.29%. It was not
encountered in infected Bulinus trun-
catus from Sudan, perhaps because of
the small numbers examined.

(v) Embryo located outside the egg
membrane and associated irregularities
(Figs. 8G, H). A total of 107 such eggs
was observed, Of these, 105 were found
in the uninfected group of Bulinus trun-
catus truncatus from Iran, but none in
the corresponding infected group. They
appeared more frequently at a later
period in life, suggesting that senescence
might have been the major cause, Em-

|
|
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259

BULINUS AND SCHISTOSOMA HAEMATOBIUM

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FIG. 8. Abnormal eggs deposited by infected and uninfected Bulinus (not to scale; diameter of a
normal egg is about 0.8 mm). A. Two eggs within an egg-clutch of infected В. guernei. They
are about 1/2 to 1/3 of the size of normal eggs. One of them contains 2 embryos. Part of a
normal egg is seen on lower left. B. Egg of uninfected B. t. rohlfsi with 3 embryos. C. Eggs of
infected В. guernei. Note one small abnormal egg with 4 embryos. D. Egg of uninfected В.
guernei With 5 embryos. E. Egg of uninfected В. guernei with 6 embryos, one of which is dis-
integrating. F. Egg of uninfected B. guernei with 11 embryos (from Lo, 1967). G. Eggs of
uninfected B. t. truncatus from Iran. Some eggs are collapsed. H. Eggs of uninfected B. t.
truncatus from Iran. They are smaller than normal, and in one case the embryo is located out-
side the egg. I. Two eggs from infected B. guernei. One is abnormal with cloudy albumen. J.
Egg from infected B. guernei. Two are smaller and without embryos; one of the 2 normal eggs
contains cercariae. A portion of gelatinous mass is condensed and appears irregular. K. Three
eggs of infected B. guernei, each with 3 to 6 cercariae (not all the cercariae are visible on the
photograph). L. A cercaria inside the egg of B. guernei, showing the abnormal shape of its
everted anterior region.

BULINUS AND SCHISTOSOMA HAEMATOBIUM

TABLE 20.
and uninfected Bulinus spp.

Infection

Snail species Sn

and origin

schistosome

2u ES

B. t. truncatus;
Sudan

B. t. truncatus;
Tran

В. Е. rohlfsi;
Ghana

B. sericinus;
W. Aden

В. guernei;
Gambia

CO № BE ed

o SES,
Ropa
—

©

00

co

w

= —

D

be
m
for)

Total

No. of embryos:

261

Frequency distribution of polyembryonic and cercaria-containing eggs in infected

Number of eggs* with the following

No. of cercariae:
aa > Dir ee.

©
[ep]

AMIS ONG |. *

oo на

[— ©) SS)
o

iw)

D

o

o

o

S

pa
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o
o
o
o
o
o
o

COMICS [E SS)

2 651772

ey | Asp (Gy a

> © EUX) SIESH eres) DIS SS)
[© |) lee SS oo (К >

+For other data relative to these eggs see the appropriate columns of Table 18.

*Includes all eggs which contained either 1 tail, 1 head, 2 heads or 2 tails.

**Includes 4 eggs which had an extra tail or head in addition to one complete cercaria.

bryos in the gelatinous mass could de-
velop only to a very limited degree and
never progressed far enough to hatch.

Often connected with this condition
were collapsed eggs that were usually
small (Fig. 8G). About half of them
had embryos either inside or outside
the egg membrane, while others had no
embryos at all. The close proximity of
collapsed eggs and embryos suggests
dislocation of embryos by rupture of
the egg membrane, presumably intra-
uterine, because the firm elastic struc-
ture of the gelatinous envelope makes
rupture after deposition unlikely.

(vi) Polyembryony. Polyembryonic
eggs are well known from lymnaeids and
other pulmonate snails. Recently Etges
& Gresso (1965), for instance, showed
an egg of Biomphalaria glabrata which
contained 4 embryos, all of which devel-
oped and hatched normally. The author
has reported some observations on poly-
embryony in 7 species and subspecies
of uninfected Bulinus earlier (Lo, 1967).

Additional information has been assem-
bled since then and some of the combined
results on 5 populations are recorded
here (Figs. 8A-F).

Infected groups consistently showed a
higher proportion of polyembryony than
uninfected groups (0.51 vs. 0.15%). The
number of embryos per egg varied from
2 to 6. From a total of 44 polyembry-
onic eggs 34 (77%) had 2 embryos. The
number of eggs with 3, 4, 5 and
6 embryos occurred at a frequency
of 2, 3, 4 and 1 respectively (Table
20). Lo (1967) indicated that eggs
with up to 5 embryos could hatch
viable young, although their size at
hatching became smaller in proportion
to the number of embryos. The egg
with 6 embryos, shown in Fig. 8E, did
not hatch. One of the embryos died at
an early stage; the other 5 developed
further, but eventually all died inside
the egg.

(vii) Presence of cercariae in egg
(Figs. 8J-L) or in gelatinous mass.

262

Cercariae in the egg of Biomphalaria
glabrata infected with Schistosoma man-
soni have been previously reported by
Brumpt (1941) and Etges & Gresso(1965).
These latter authors observed that the
cercariae were alive in the egg for a
period of 24 hours. In the present
study such eggs were more frequently
encountered than all of the other ab-
normalities combined, their frequency
ranging from 8.75% (Bulinus sericinus)
to 15.37% (В. guernei) and averaging
11.45%. В. truncatus truncatus from
Iran is an exception Since no cercariae
were found in 241 eggs examined (Table
19). The occurrence of such eggs was
related to the number of cercariae pre-
sent in the snails, i.e., was more fre-
quent when the shedding was heavy.
Cursory observation of B. guernei
showed that more such eggs were ob-
tained from the 10th to 15th week after
infection, even though they were also
found as early as 7 and as late as 20
weeks, The number of cercariae in an
egg varied from '/› (head or tail) to 6
(Figs. 8J-L), although the majority, 123
eggs (69%), had only one cercaria(Table
20).

Inside the egg cercariae were less
active because of the viscosity of the
albumen, They were motile, but never
able to swim freely. Most of them died
within half a day after egg deposition.
The maximum survival time was about
30 hours, a life span considerably short-
er than that in clean water, where they
can survive for 2 or 3days. In one case,
a cercaria was seen with its anterior
portion everted (Fig. 8L) which canper-
haps be taken as an indication of un-
favorable conditions in the egg. The
presence of cercariae did not affect nor-
mal development of the embryo. Among
the 122 abnormal egg-clutches of Bulinus
guernei, one had a cercaria which was
embedded in the gelatinous mass out-
side the eggs. The cercaria was immo-
bile and appeared dead.

In addition to the above abnormalities,
the albumen of one egg was found to be
whitish and cloudy instead of transparent

COTE

and yellowish. The embryo was present
but died at a very early stage (Fig. 81).
4. Production of Cercariae

a. Incubation Period

It has been shown that temperature
affects the cercarial incubation period

of Schistosoma haematobium (Gordon et |

al., 1934; Chu etal., 1966c). In the
present study, incubation periods at var-
ious temperatures have been recorded
for 10 populations of Bulinus (Table 21).

At 30°C all 7 Bulinus guernei shed
cercariae on the 23rd day after infection.
However, they had been kept at 24°C
for 3 days during the prepatent period
and the incubation period would probably
have been shorter had they been kept
at 30°C throughout.

At temperatures between 26 and 28°C,
all of the 96 infected B. guernei shed
between the 25th and 30th day.

At 24-26°C the earliest shedding (a-
mong 9 populations of Bulinus spp.) oc-

curred on the 32nd day in B.guernei. Al- —

though more than 90% of B. guernei had
liberated cercariae by the 40th day, re-
lease could obviously be much delayed, as

shown by a specimen dissected and found ~
positive on the 63rd day. Four positive

snails of B. sp. (n=72) from Ethiopia

started shedding quite late, between the

50th and 56th day. Evenbefore emission,
these snails appeared sick, and it seemed
likely that the prolonged incubation peri-
od was due to poor health rather than
to a species difference. An analogous
condition was also observed in some
individuals of other species. Such spe-
cimens not only had a longer incubation

period, but also a low cercarial output, |

and died earlier. Greater resistance
of some snails or lesser vitality of
some miracidia may also account for
a prolonged incubation period. The one
specimen of B. guernei mentionedabove
had sporocysts but had not released
cercariae until it was dissected on the
63rd day. Number of daughter sporo-
cysts and cercariae were both small,
and in addition there was an intense

Snail tissue reaction around the para- |

BULINUS AND SCHISTOSOMA HAEMATOBIUM 263

TABLE 21. Frequency distribution of positive Bulinus spp. with respect to cercarial incubation
period at various maintenance temperatures.

Temp.

(°C) 24-26° 24°

| co
o
o

Snail
Sp.

Incu.
period
(day)

23
24
25 27

26 15

27 42

28 6

29 3

30 3

31

32 2

33 13 1

34 24 4

35 18 1

36 9 21 il
37 2 1 1
38 25 12

39 5 13

40 36 4 3
41 1

42 1

43 2

44

45

46

47

48

49

50

51

52

53

54

55

56

57

58

59

60

61

62

63

1**
| Total snails - 138 57 3 2 A4 il 4 5 75
shedding:

*Checked for the first time; some of these snails presumably started shedding a little earlier.
**Killed and found to be cercaria positive.

S. Rhodesia
9 Africa

a
+

a

©
—
a

+

E

Corsica

. t. truncatus
Sudan

BRESP:

[72]
>
+
S
o
S
>
>
+
+
9

В. Е. truncatus

В. guernei

В. guernel

В. t. truncatus
B. coulboisi
B. sericinus
ıB. globosus
В. guernei

B. globosus

1

|B. guernei

o
pa
coo

bo
©
*

20*

NODE ws SENDE SESEZSHST Or
Fa
w
m >.

=
L(Y a Yo a) (ee)
MSP ate QO > (SO Sa hoe ONE

NAO LS Oo to =
N © © RH hH © © © MH wa no YY FE

264

sites.

From 8 positive Bulinus guernei kept
at 24°C, the first shedding was seen on
the 35th day, and the last one onthe 49th
day. In 75 specimens of B. globosus
from South Africa, 80% of the snails
shed between the 36th and the 44th day,
although the last specimens did not do
so until the 60th day.

It is thus clear that at a higher
temperature, the incubation time ina
group was more uniform, Considering
Bulinus guernei alone, at 30°C, all snails
began to shed on the same day; at 26-
28°C, the difference between the first
and the last shedding was 6 days; at 24-
26°C, it was 12 days; and at 24°C, it
was 15 days. These results agree with
those of Chu et al. (1966c) for Schisto-
soma haematobium and S. bovis in Iran,
but differ from those obtained by Foster
(1964) in Tanganyika for Biomphalaria
pfeifferi infected with Schistosoma man-
soni. He found that between 22.85 and
31.75°C, the maximum incubation time
was generally 3-4 days longer than the
minimum regardless of temperature.

Shedding Bulinus of large and small
size which had been infected with Schisto-
soma haematobium when they were about
the same size shed cercariae at the
same time, indicating that retarded
growth in the snails did not affect the
incubation period, An increase of tem-
perature or light so as to stimulate
emission of cercariae shortened the
incubation by 1-2 days.

Gordon etal. (1934) with the Sierra
Leone parasite and Bulinus globosus,
showed that at 34-35°C the majority of
the snails shed on the 27th and the 28th
day; the minimum incubation time was
22 days at 32-33°C, 35 days at 26-28°C,
and 66 days at 20-22°C. Chu et al.
(1966c) in Iran and for Schistosoma hae-
matobium recorded as many as 154days
of incubation in B. truncatus during the
cold months.

b. Shedding Pattern

The number of cercariae emerged
was recorded for 69 Bulinus guernei

C. T. LO

which started to shed between 25-27th
day. The minimum number of cercariae
emerging from a snail on the first day
was one, the maximum 218 (Table 22).
For the first 2 days the minimum num-
ber of cercariae was not related to
snail size, but the maximum number did

increase with the increase of size. It !

was not determined how long this trend
would continue. On the whole large
specimens shed more than did smaller
ones, except for the largest group (8.4
mm), in which cercarial output was
lower than in the second largest group
(7.3 mm). This trend held true also in
long-term observation (Table 24),

The peak of cercarial production was
reached 1-2 weeks after the onset of
shedding. Individual variation was great.

Size of snails as well as health condi- |
tion, intensity of infection and aquarium |

conditions all contributed substantially
to the output of cercariae, After reach-
ing its peak, the numbers emitted daily
varied greatly; and there were parallel
shedding patterns regardless of species,
time of infection, or size, reflecting
daily changes in light and temperature.
Fig. 9 illustrates the shedding pattern
for Bulinus guernei.

even 10 days. During this period the

production of cercariae was low, usually

between 10-50 a day.

Before dying, the ©
snail became inactive for 2-3 days or |

c. Number of Mother Sporocysts and |

cercarial Output

From a group of about 100 positive
Bulinus guernei which had been exposed
to 10-20 miracidia at the same time,
34 snails of similar size were separated
before shedding. They were divided
into 3 groups, each containing a different
number of mother sporocysts in the

head-foot region, namely: A, 12 snails |

with 1 sporocyst; B, 12 snails with 2
sporocysts; and C, 10 snails with 3 (7
snails) or 4(3 snails) sporocysts. All
cercariae produced by these snails were
collected for 8 consecutive days from
the first shedding and also several times
later (Table 23).

BULINUS AND SCHISTOSOMA HAEMATOBIUM 265

Comparison of the number of cercariae
shed on the same day showed that up to
the 8th day, differences between the 3
groups were Slight; but for the 22nd,
30th and 37th day, groups A and B pro-
duced considerably more cercariae than
group C. These snails were checked
several times later and group C con-
sistently showed a lower cercarial out-
put than the other 2 groups. The
originally similar snail sizes had al-
ready notably diverged by the 30th day
amounting to 8.3 + 0.8 mm for groups
A and B, and 8.1 + 0.8 mm for Group C.
Since the cercarial output after the 22nd
day appears to be almost inversely
proportional to the number of mother
sporocysts, while it concords well with
the size of the snail, size (i.e., the
amount of food available to the para-
sites) is thought to be the most likely
direct causative factor. As for the
Smaller size of group C, it was prob-
ably due to a greater number of daughter
sporocysts, which slightly but progres-
Sively suppressed the growth of the
snails. Therefore, other than possible
stunting, the number of mother sporo-
cysts seems to have little direct influ-
ence on the production of cercariae.
This view is supported by the observa-
tion that the area in the liver region
occupied by daughter sporocysts was
not related to the number of mother
sporocysts. It is also supported by the
findings of Pan (1965) who reported
that exhausted daughter sporocysts of
Schistosoma mansoni in .Biomphalaria
glabrata could regenerate to produce
more cercariae, that some migrating
daughter sporocysts had started to de-
generate, and that all mother sporocysts
were degenerating 35 days after in-
fection.

The results for Bulinus guernei are
Similar to those of Vogel (1948) and
Pesigan et al. (1958), who observed that
Oncomelania snails exposed to 1 mira-
cidium of Schistosoma japonicum shed
no less cercariae than those exposed
to more than one; but differ from the
report by Chu etal. (1966d), that B.

truncatus exposed to 2 or more mira-
cidia of S. haematobium shed more than
did those exposed to 1 miracidium. It
must be pointed out that in these reports
the size of snails was not considered.

d. Snail Size and cercarial Output

After reaching the peak of shedding,
the number of cercariae produced by 9
populations of Bulinus was recorded
for 6-70 days. It is evident from Table
24 that larger snails produced more
cercariae/snail/day than the smaller
ones. The only exception was again
found in the largest group of Bulinus
guernei which had a smaller daily out-
put than the next smaller group, as
already reported above (Table 22). Nev-
ertheless, the largest specimens of B.
guernei, though they had a lesser daily
shed, liberated the largest total number
of cercariae because of their longer
survival,

Although an accurate comparison
among various species could not be
made, Bulinus guernei, B. sericinus and
B. truncatus truncatus (Iran) were the 3
best snails for getting a large quantity
of cercariae. However, the highest
number of cercariae seen in any one
snail in a day, was about 2500, in a
Sudanese B. t. truncatus. Maximal daily
output of Schistosoma haematobium cer-
cariae, reported in the literature, is
950 from a South African specimen of
B. globosus (Wright & Bennett, 1967a),
and 1,180 from an Iranian B. truncatus
(Chu et al., 1966d); but since the latter
figure was an average for 10 days, the
maximum must have been even higher,
The largest daily sheds recorded for
Biomphalaria glabrata infected with S.
mansoni, were 4,158 and 7,500 cercariae
(Schreiber & Schubert, 1949a; Faust &
Hoffman, 1934).

In this study the highest total number
of Schistosoma haematobium cercariae
produced by one snail (Bulinus guernei)
was estimated at 20,000. Chu et al.
(1966d), in contrast, reported about
40,000 for Iranian B. truncatus. As
regards S. mansoni, Faust & Hoffman

266

300

200

100

OF CERCARIAE/SNAIL/DAY

NO.

50 60 70

CT LO

80 90 100 110

DAYS AFTER INFECTION

FIG. 9:

Emergence of Schistosoma haematobium cercariae from Bulinus guernei, examined

every other day. Solid line: specimens of 8 mm and larger. Broken line: specimens ranging

from 6 to 7.9 mm.

(1934) recovered 210,000 cercariaefrom
one Biomphalaria glabrata infected with
1 miracidium, and the snail was still
alive and shedding when the observation
was discontinued,

e. Effect of Temperature on cercarial
Output

Forty positive Bulinus guernei which
had been exposed to 10 miracidia each

were selected 8 weeks after infection
and divided into 8 groups, each containing
5 snails with a mean shell height of 7.1
mm, Each group was then exposed for
1 hour to 1 of 8 different temperatures
ranging from 5 to 40°C, and the cer-
cariae emerging during this period were
counted. The emergence of cercariae
was completely suppressed at 5°C and
10°C. The numbers liberated at 15°C

BULINUS AND SCHISTOSOMA HAEMATOBIUM 267

TABLE 22. Production of Schistosoma haematobium cercariae by Bulinus guernei during the
first week of shedding.

No. of cercariae per snail*

Size class aa
in i oy 5th om 7th phd
(X +S. D.)

Rac he
2-

14

26 11-198
41 106-365
82 1-490
61 3-540

4.5 +0.3

5.5 20.2
6.5 +0.3 241
7.3 80.3 270
8.4 +0.2 230

*Snails were placed under a 75 watt lamp for 4 hours.

TABLE 23. Relationship between the number of mother sporocysts and the output of cercariae
by Bulinus guernei infected with Schistosoma haematobium.

A: 1 sporocyst B: 2 sporocysts

No. of No. of
snails snails

C: 3-4 sporocysts

cer./snail
/day

No. of
snails

cer./snail
/day

cer./snail
/day

11 days average

lLight intensity was increased by placing a 75 watt lamp 30 cm above the snails.

23, 2 and 3 individuals for groups A, Band C respectively, started shedding on this day.

3Placed under a 275 watt sun lamp for 2 hours; cercariae emerged during this period and for 2
hours afterwards were collected.

268 C. T. LO

TABLE 24.
haematobium.

Size
in mm
(K +S. D.)

No. of
snails

Species of Bulinus

B. sericinus

B. guernei

В. Е. truncatus;
Iran

В. t. truncatus;
Sudan

B. t. rohlfsi;
Ghana

B. sp. (n=72)

Estimated cercarial production by some Bulinus spp.

Study
period
(days)

infected with Schistosoma

Total cerc.
per snail

Survival after 1st
shedding (days)

8625 | 16240
8778 | 14896
4158 7623
182 13038 | 19292
147 9760 | 17934
126 5140 | 12222

56 4257 7224
56 2943 6104

28 403 868
91 3975 6825
91 1219 2093

po oa

B. coulboisi

B. globosus;
S. Rhodesia

56***

Е : i Ñ ;

2940 | 10976

*Obtained by multiplying average cercariae/snail/day by average survival.

**Obtained by multiplying average cercariae/snail/day by maximum survival.

***Based on the data shown in Table 15; note that survival data for S. Rhodesian B. globosus
were not available, and that consequently those for B. globosus from S. Africa have been

substituted.

and 20°C were low: 44 and 50 per snail
respectively. At 25°C, the maintenance
temperature, 266 cercariae per snail
were counted, The number of cercariae
increased greatly at 30°C and 35°C,
amounting to 716 and 796 respectively.
However, at 40°C, it droppeddrastically
to 45 per snail.

In order to assess the long term
situation, 3 groups of 4 Bulinus guernei
were maintained at 25, 30 and 35°C

respectively, and the total number of
cercariae produced in 2 weeks was re-
corded. There was no significant dif-
ference in the average daily output per
snail between the 25°C and 30°C groups
(223 against 207 cercariae; P>0.01);
but at 35°C, the number (86 cercariae)
was significantly lower than in the other
2 groups (Р<0.001).

The inhibitory effects of high temper-
atures on cercarial emergence undoubt-

BULINUS AND SCHSISTOSOMA HAEMATOBIUM

35-37°C

© na
CNO
Sy Ke)

©
©

N ©
©
©

NO. OF CERCARIAE/SNAIL/DAY
S 5 5
© ©

FIG. 10.

Eggs:

269

24-269С

Jp_ — >> E EEE E-A3>— A,

0,10,3,8,4,7,054,0,0,0,

15 20 25 30

DAYS

Effect of exposure to 1 week of high temperature on the production of cercariae and on

egg-laying by 2 Bulinus guernei infected with Schistosoma haematobium.

edly applied to snails as well as para-
sites: Immersion of Bulinus guernei in
water at 40°C for 1 */2 hours usually
killed them within a day, and it is well
documented that high temperatures have
a deleterious effect on the survival of
various schistosome cercariae (Khalil,
1924; Krakower, 1940; Jones & Brady,

1947). Porter (1938) reported that Schis-

|

|

tosoma haematobium cercariae survived
for 12 hours at 40°C, while the survival

time was greatly increased at lower

temperatures, The present results are
in line with those of Gumble etal.
(1957), who demonstrated a complete
Suppression of shedding in Oncomelania
nosophora at 6-10°C, and a partial

| suppression at temperatures above 30°C.

Because of the suppressive effect of
heat on cercarial production it was
thought that exposure to higher temper-
atures might cure the schistosome in-
fection in the snails. Subsequently, 6
infected Bulinus guernei were main-

tained at 35-37°C for 7 days, then
returned to an ambiance of 24-26°C.
The mortality was high: 3 snails sur-
vived the study period of 32 days (Fig.
10). After a heavy shed on the first
day of heat treatment, the number of
cercariae emitted decreased sharply.
Although the snails were returned to
temperatures of 24-26°C after the 7
days of high temperature, cercarial
output continued to be low up to the 25th
day, after which it gradually increased.
On the 22nd day, or about 2 weeks after
transfer from high temperature, both
Snails started to lay eggs, but ceased
again as cercarial output increased.
Thus, the immersion of 7 days at tem-
peratures of 35-37°C temporarily re-
duced the infection, but did not eliminate
it.

5. Sex Ratios in Schistosoma haema-
tobium

For determining the sex of cercariae,

270 ESTILO

TABLE 25. Sex of Schistosoma haematobium recovered from mice infected with cercariae

emerged from single Bulinus spp.

No. of mice harboring:

No. of miracidia
per snail

2 worms only

gd worms only

Sex ratio*

($ : 5)

$ and © worms

*Bisexual infection was included and reckoned as 1 Gand 1 ©.

mice were exposed to cercariae derived
from single snails. A total of 122 snails
from 8 populations were successfully
used, i.e., the cercariae they shed grew to
sexually differentiated worms in mice.
These snails were: Bulinus truncatus
truncatus (Egypt), 1; В. Е. truncatus (Cor-
sica), ; В. t. truncatus (Iran), 11; B. t.
truncatus (Sudan), 19; B. t. rohlfsi(Gha-
na), 3; B. coulboisi, 5; B. sericinus, 9;
and B. guernei, 72. All species were
combined for analysis of data(Table 25).

Female:male ratios remained very
constant with materials from snails
exposed to multiple miracidial doses,
ranging from 1:2.4 to 1:2.5. With cer-
cariae deriving from single miracidia,
no females were obtained which resulted
in a total average of 1:2.6. Bisexual
infection appeared only when 10-20 mira-
cidia were given and in not more than
10% of cases. This lowfrequency seems
to agree with the distribution of mother
sporocysts previously discussed (com-
pare Table 11).

Experimental evidence from this re-
port and from others shows that in the
majority of cases and for all 3 human
schistosomes, a greater number of snails
produce male cercariae.. The reported
female:male ratios are, for Schisto-
soma mansoni; 1:1.3 (Stirewalt, 1951);
for 5. japonicum: 1:2.8 (Pesigan et al.,
1958), 1:1.9 (Kikuchi, 1962) and 1:1
(Vogel, 1941). Among naturally infected

snails, male infection also usually pre-
dominates over female infection in all
of the 3 species (Faust, 1927; Maldonado
& Velez-Herrera, 1949; Paperna, 1965).
However, a ratio close to 1:1 in S.
japonicum is cited by Ikeda & Makino
(1936).

Similarly, in the bisexual infections,
there were more male worms than fe-
male worms, since the vast majority
of unpaired parasites were males. Mal-
donado & Vélez-Herrera (1949) obtained
about twice as many males asthe females
using Biomphalaria glabrata which were
naturally infected with both sexes of
Schistosoma mansoni.

Male predominance in human schisto-
some has been well noted in the litera-
ture. Assuming that male and female
zygotes are produced in equal numbers
by adult worms, one must postulate a
greater failure of female parasites,
which might occur at various larval
stages. Vogel (1948) suggested that
male and female miracidia might be
affected to different degrees by climatic
conditions before penetration. Faust
(1927) suggested that male parasites
might have a greater resistance while
in the snail. In the present study tests
with 1 miracidium per snail indicated
that a greater number of male mira-
cidia penetrated into the snail and devel-
oped in it. The protandric condition,
reported for Schistosoma mansoni

BULINUS AND SCHISTOSOMA HAEMATOBIUM 271

(Evans & Stirewalt, 1952) and S. haema-
tobium (Wright & Bennett, 1967a, b),
might partly contribute to the male pre-
dominance. Evans & Stirewalt further
proved that male cercariae were more
infective than female cercariae. In
addition, it could also be that male
sporocysts can produce more cercariae
than female sporocysts; it may be pos-
sible too that, when male and female
sporocysts are present together in one
snail, the number of cercariae produced
by each sex could be modified by inter-
actions between the sexes.

ACKNOWLEDGEMENTS

I wish to express my Sincere grati-
tude to Dr. E. G. Berry for his assist-
ance and suggestions at various times
during this study, and Drs. H. van der
Schalie and J. B. Burch for their sup-
port and encouragement. Special ac-
knowledgement is extended to Mrs. Anne
Gismann who critically reviewed the
manuscript and added many improve-
ments. I am also indebted to Dr. R.
Natarajan for determining snail chromo-
some numbers, and to Dr. V. Collaro
for maintaining the snail colonies.

LITERATURE CITED

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syi to infection with certain strains of
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ADAMS, А. В. D., 1934, Studies on Bil-
harzia in Mauritius. I. The experi-
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with Schistosoma haematobium. Ann.
trop. Med. Parasitol., 28: 195-204.

AMBERSON, J. M. & SCHWARZ, E.,
1953, On African schistosomiasis.
Trans. Roy. Soc. trop. Med. Hyg., 47:
451-502.

ARCHIBALD, R. G., 1933, The endemi-

Same author as MALEK, Е.А. (ED.)

ology and epidemiology of schisto-
somiasis in the Sudan. J. trop. Med.
Hyg., 36: 345.

ARCHIBALD, R. G. & MARSHALL, A.,
1932, A descriptive study of the cer-
cariae of Schistosoma haematobium
in the Sudan. J. trop. Med. Hyg., 35:
225-228.

BLACKLOCK, D. B. & THOMPSON, M.
G., 1924, Human schistosomiasis due
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Leone. Ann. trop. Med. Parasitol., 18:
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BROWN, D. S., 1965, Freshwater gastro-
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BROWN, D.S. & BURCH, J. B., 1967,
Distribution of cytologically different
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sommatophora: Planorbidae) in Ethi-
opia. Malacologia, 6: 189-198.

BROWN. БОВ, SCHUTTE, С. Hiiid.,
BURCH, J. B. € NATARAJAN, R.,
1967, Chromosome numbers in rela-
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of some southern African Bulinus (Ba-
sommatophora: Planorbidae). Mala-
cologia, 6: 175-188.

BROWN, D. S., OBERHOLZER, G. €
VAN EEDEN, J. A., 1971, The Bulinus
natalensis/tropicus complex (Basom-
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Eastern Africa: I. Taxonomy and bio-
geography; Idem II: Shell, mantle,
copulatory organ and chromosome
number. Malacologia, 11: 141-170;
171-198.

BRUMPT, E., 1941, Observations bio-
logiques diverses concernant Planor-
bis (Australorbia) glabratus, höte in-
termediaire de Schistosoma mansoni.
Ann. Parasitol., 18: 9-45.

BURCH, J. B., 1964, Cytological studies
of Planorbidae (Gastropoda: Basom-
matophora). I. The African subgenus
Bulinus s.s. Malacologia, 1: 387-400.

BURCH, J. B., 1967a, Chromosomes of
intermediate hosts of human bilharzi-
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BURCH, J. B., 1967b, Some species of
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intermediate hosts of schistosomiasis

272

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BULINUS AND SCHISTOSOMA HAEMATOBIUM 273

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BULINUS AND SCHISTOSOMA HAEMATOBIUM 275

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276

CUT be

ZUSAMMENFASSUNG

DIE BEZIEHUNGEN ZWISCHEN ARTEN DER GATTUNG BULINUS
(BASOMMATOPHORA: PLANORBIDAE) ALS WIRT UND EINEM AGYPTISCHEN
STAMM VON SCHISTOSOMA HAEMATOBIUM (TREMATODA: DIGENEA) ALS PARASIT

@.-T. Lo

Die Fähigkeit verschiedener Bulinus -Schneckenarten, als Zwischenwirt des ägypti-
schen Stammes von Schistosoma haematobium zu dienen, wurde untersucht, ausser-
dem die Faktoren, die die Empfänglichkeit der Schnecken beeinflussen, und die Wir-
kung des Parasiten auf infizierte Schnecken.

Achtundzwanzig im Labor gezogene Populationen, die etwa ein Dutzend Bulinus-
Arten und -Unterarten von verschiedenen Teilen Afrikas und angrenzenden Gebieten
umfassten, wurden der Infektion mit Schistosoma haematobium unter gleichen Be-
dingungen. ausgesetzt. Die Schnecken waren 2-4 mm hoch; die Temperatur betrug
24-26°C; jedem Tier wurden 10-20 Mirazidien beigegeben; 2 ml Wasser wurden zu
jeder Schnecke gegeben. Gewöhliches Quellwasser wurde in allen Fällen verwendet.
Zerkarien kamen aus folgenden Arten der truncatus-Gruppe: Bulinus truncatus trun-
catus, В. Ё. rohlfsi, В. sericinus (W. Aden), В. coulboisi, В. guernei (alle mit der
haploiden Chromosomenzahl n=36) und aus Bulinus Sp. (n=72); auchaus B. globosus von
der africanus-Gruppe. Zerkarien wurden weder bei B. tropicus festgestellt noch bei
mehreren Populationen von Bulinus sp., die zu der tropicus-Artengruppe gehören
(n=18) noch bei B. forskalii und B. scalaris (beide aus der forskalii-Artengruppe),
wenn auch in der letztgenannten Art Mutter-Sporokysten heranwuchsen und etwa 2
Monate lang am Leben blieben, ohne Tochter-Sporokysten zu entlassen, Obgleich der
südafrikanische В. globosus den höchsten Prozentsatz an Infektionen hatte (76%), wurde
B. guernei aus Gambia (zu 35% infiziert) als der günstigste Wirt für die Haltung des
Parasiten befunden, in bezug auf die Leichtigkeit der Züchtung, Überleben, Empfäng-
lichkeit und der gelieferten Menge von Zerkarien. Am besten geeignet, den Lebens-
Zyklus aufrecht zu erhalten, waren von den empfänglichen Schnecken B. guernei
(Gambia), B. sericinus (W. Aden) und B. t. truncatus (Iran); weniger geeignet waren
B.t. rohlfsi (Mauritania), B. t. truncatus (Korsika), B. t. truncatus (Sudan), B. t. rohlfsi
(Ghana) und B. coulboisi (Tansania); schlecht waren B. t. truncatus (Ägypten) und B.
sp. (n-72, Äthiopien. Dass unser Zuchtstamm von В. truncatus aus Ägypten (3%
infiziert) weniger empfänglich war als alle anderen untersuchten Arten (ausgenommen
В. globosus aus Mozambique mit 2%) zeigt, dass eine lokale Wirt-Parasit-Spezilität
nicht entwickelt zu sein braucht.

Eine Amöbenart, Hartmannella biparia, wurde in einigen Exemplaren von B. globo-
sus gefunden; diese vermindert möglicherweise die Empfänglichkeit für Schistosoma
bei diesen Schnecken,

Um die günstigsten Verhältnisse für den Parasiten festzustellen, wurden ver-
schiedene Faktoren, die Einfluss auf die Empfänglichkeit der Schnecken haben können,
bei Bulinus guernei untersucht, unter gleichbleibenden Bedingungen, wobei nur der
untersuchte Einzelfaktor variiert wurde. Allgemein wurde stärkere Infektion unter
folgenden Umständen erzielt: Hohe Alkalität (beste Ergebnisse waren 49% bei pH 9,6);
hohe Temperature 67%bei 30°C, aber weniger bei noch höheren Temperaturen und nega-
tiv unter 10°C); grosse Mirazidien-Dosis (70% bei 60+ jeSchnecke); bei jungen Schnec-
ken (maximum von 67% bei Überlebenden, 3 Tagen alten, Schnecken; wegen deren hoher
Sterblichkeit lieferten jedoch 1-2 Wochen alte Schnecken die meisten infizierten Tiere);
bei an der Schale festgeklebten Schnecken (54%), wobei der ausgestreckte Schnecken-
körper eine grosse Angriffsfläche bietet, und bei betäubtenSchnecken (81%) vermutlich
wegen der geringeren Schleimsekretion verbunden mit Streckung und Unbeweglichkeit.

Die Infektion verzögerte das Wachstum der Schnecken nicht. Bei infizierten
Schnecken, die älter als 3 Tage waren ehe die Zerkarien austraten, war die Sterblich-
keit nicht höher als bei nicht infizierten Schnecken. Keine infizierte Schnecke lebte
länger als 32 Wochen. Infizierte Schnecken lieferten 7-100 x ($ 15x) weniger Eier
als gesunde, und Abnormitäten waren 17x so häufig. Der Laich zeigte verschiedene
Arten von Abnormität, einzeln oder kombiniert, wie Fehlender Eier in der gelatinösen
Grundmasse, geringe Grösse des Eies, Fehlen des Embryos, Lage des Embryos
ausserhalb der Ei-Membran, Anwesenheit mehrerer Embryonen in einem Ei, oder
von Zerkarien in der Grundmasse oder dem Ei.

Die Dauer der Zerkarienentwicklung war kürzer und einheitlicher, wenn die
Schnecken bei hoher Temperatur gehalten wurden (23 Tage bei 30 °C; 35-49 Tage bei

BULINUS AND SCHISTOSOMA HAEMATOBIUM

24°C). Der Gipfel des Zerkarien-Ausstosses wurde 1-2 Wochen nach dem ersten
Ausstoss beobachtet; und danach schwankte die Zahl der taglich entlassenen Zerkarien
beträchtlich, was von der Temperatur (optimal bei 35°C, bei 40°C fast unterdruckt)
und dem Licht abhing, ebenso auch von der Intensitat der Infektion, Gesundheit der
Schnecke und der Beschaffenheit des Wassers. Die Infektion wurde teilweise “geheilt”,
wenn infizierte Schnecken eine Woche lang bei 35-37 °C gehalten wurden, das zeigte sich
durch verminderten Austritt von Zerkarien und erhöhte Eiproduktion. Schätzungsweise
war das Maximum an Zerkarien von einer Schnecke 2500 Stück an einem Tage und
20.000 insgesamt. Grössere infizierte Schnecken lebten länger, legten mehr Eier und
gaben mehr Zercarien als kleinere Schnecken.

Mehr Schnecken lieferten männliche Zerkarien als weibliche. Das Verhältnis
zwischen weiblich und männlich war 1:2,6. Nur wenn eine Schnecke sehr stark in-
fiziert war, stiess sie Zerkarien beider Geschlechter aus. Dies geschah in einer
Häufigkeit von 7% (10 Mirazidien) und 9% (20 Mirazidien).

RESUME

COMPATIBILITE ET RELATIONS HÖTE-PARASITE ENTRE DESESPECES
DU GENRE BULINUS (BASOMMATOPHORA: PLANORBIDAE) ET UNE FORME
EGYPTIENNE DE SCHISTOSOMA HAEMATOBIUM (TREMA TODA: DIGENEA)

CATHO

Les études portent sur la possibilité qu’ont divers bulins d’agir comme hôtes
intermédiaires d'une forme égyptienne de la bilharzie Schistosoma haematobium.
Elles concernent a la fois les facteurs affectant le mollusque et les effets du parasite
sur les mollusques infectés.

Vingt-huit populations élevées au laboratoire, représentant environ une douzaine
d'espèces ou sous-espèces de Bulinus provenant de différentes parties de l’Afrique
et de régions adjacentes, ont été exposées à Schistosoma haematobium sous conditions
standard. La taille du mollusque variait de 2-4 mm de haut; la température de 24°C
à 26°C; l’exposition individuelle de 10 à 20 larves miracidium; chaque mollusque
recevait 2 ml d’eau Pour tous les usages on a régulièrement utilisé de l’eau de
source du commerce, Les cercaires ont été obtenues dans le groupe truncatus: de
Bulinus truncatus truncatus, В. t. rohlfsi, В. sericinus (Ouest-Aden), В. coulboisi, В.
guernei (tous avec le nombre haploide de chromosomes n=36) et de Bulinus sp. (n=72);
et dans le groupe africanus, de B. globosus. Aucune cercaire n’a été obtenue de B.
tropicus (avec n=18), ni de В. forskalii et В. scalaris (tous deux du groupe forskalii),
bien que dans cette derniere espece des sporocystes meres aient grandi et se soient
maintenus environ 2 mois sans libérer de sporocystes filles. Bien que l’espece
sud-africaine B. globosus ait montré le taux d’infection le plus élevé (76%), on estime
que c’est B. guernei de Gambie (35% d’infection) qui est le plus apte a propager le
parasite en égard à sa capacité de reproduction, de survie, d’infection et de libération
de cercaires. L’ordre de convenance pour établir le cycle biologique parmi les
mollusques réceptifs du groupe truncatus a été: bon - B. guernei (Gambie), B.
sericinus (Ouest-Aden) et В. t. truncatus (Iran); passable - В. t. rohlfsi (Mauritanie),
В. t. truncatus (Corse), В. Е. truncatus (Soudan), В. t. rohlfsi (Ghana) et В. coulboisi
(Tanzanie); médiocre - B. t. truncatus (Egypte) et B. sp. (n=72, Ethiopie). Que notre
forme de laboratoire dé B. truncatus provenant d'Égypte (3% d'infection) soit moins
susceptible d’infection que presque tous les autres mollusques réceptifs (exception
pour B. globosus du Mozambique avec 2% d’infection), démontre que le besoin local
d’une spécificité mollusque - parasite, ne se développe pas nécessairement.

Une espèce d’amibe, Hartmanella biparia, a ete trouvée infectant certains exem-
plaires de Bulinus globosus; il est possible que cela réduise la bilharziose chez
ces mollusques.

Pour déterminer le meilleur succès du parasite, plusieurs facteurs, affectant la
susceptibilité des mollusques, ont été étudiés chez Bulinus guernei sous conditions
standard où ne variait que le facteur teste. En général, le taux d’infection le plus
élevé a été obtenu dans les conditions suivantes: forte alcalinité (résultats optimum:
49% au pH 9,6); température élevée (67% à 30°C, mais moins à plus haute température
et négatif au-dessous de 10°C); forte dose de larves miracidium (70% pour 60+larves

277

278

GT. LO

par mollusque); dans les mollusques jeunes (maximum de 67% sur des individus äges
de 3 jours; cependant ä cause d’une forte mortalite, les mollusques de 1-2 semaines
comptaient le maximum d’individus infectés); dans les mollusques en position fixe
(54%), quand leur corps en extension presentait le maximum de surface et quand ils
étaient anesthésiés (81%), sans doute à cause d’une sécrétion plus faible de mucus
combinée à l’extension et l’immobilité.

L’infection n’a pas retardé la croissance du mollusque. La mortalité des individus
de plus de 3 jours, avant l’assaut des cercaires émergentes, n’a pas été plus élevée
que celle des non-infectés. Aucun mollusque infecté n’a vécu plus de 32 semaines.
Les mollusques infectés ont produit de 7 à 100 fois (moyenne 15 fois) moins d’oeufs
que les non-infectés et les anormalités y ont eté 17 fois plus fréquentes. La ponte a
montré plusieurs types anormaux, seuls ou combinés, tels que: absence d’oeufs dans
la matrice gélatineuse, petite taille des oeufs, absence d’embryons, embryons localisés
hors de la membrane de l’oeuf, polyembryonie, présence de cercaires dans les oeufs
ou dans la ponte.

Les périodes d’incubation des cercaires ont été plus courtes et plus uniformes
quand les mollusques étaient maintenus à températures élevées (23 jours à 30° С;
35-49 jours à 24°C). Le maximum d’emergences de cercaires était atteint 1 à 2
semaines après la première émission et le nombre de cercaires émises journellement
a beaucoup varié par la suite, selon la température (optimum à à 35° C, suppression à

40°C) et la lumière, tout comme l'intensité d’infection, la santé des mollusques et les
conditions de milieu, Les infections furent partiellement “sueries” en maintenant
les individus infectés à 35-37°C pendant une semaine, ceci étant mis en évidence par
la diminution de cercaires produites et l’augmentation des oeufs pondus. Les esti-
mations maximales journalières et totales sont respectivement de 2500 et 20000
cercaires libérées. Les mollusques infectés de grandetaille survivent plus longtemps,
pondent davantage et libèrent davantage de cercaires que les mollusques de petite
taille.

Ilya plus de mollusques à produire des cercaires mâles que des cercaires femelles,
le taux de féminité étant 1:2,6. Ce n’est que lorsqu'un mollusque a été fortement
exposé à des larves miracidium qu’apparaft l’infection bisexuelle, a une fréquence

de 7% (10 larves) et 9% (20 larves). Fo

RESUMEN

RELACIONES DE COMPATIBILIDAD ENTRE HUESPEDES Y PARASITOS EN ESPECIES
DEL GENERO BULINUS (BASOMMATOPHORA: PLANORBIIDAE) DE UNA RAZA
EGIPCIA DE SCHISTOSOMA HAEMATOBIUM (TREMATODA: DIGENEA)

C.-T. Lo

Se investigó la habilidad de varios caracoles bulininos para actuar como huéspedes
de una cepa egipcia de Schistosoma haematobium, el helminto chato de la sangre,
junto con factores que afectan la susceptibilidad del caracol y el efecto del parásito en
los moluscos infectados.

Veintiocho poblaciones criadas en laboratorio representando una docena de especies
y subespecies de Bulinus de varias partes de Africa y regiones adyacentes, fueron
expuestas al parásito bajo condiciones regularizadas. Los caracoles eran de tamafios
entre 2 y 4 mm; la temperatura se conservö entre 24° y 26°C; los individuos fueron
expuestos a 10-20 miracidios; y por cada caracol se proveyó 2 ml de agua. En forma
rutinaria se compró agua surgente para todos los experimentos. Las cercarias emer-
gieron, en el grupo de truncatus, de Bulinus truncatus truncatus, B. t. rohlfsi, B
sericinus (West Aden), B. coulboisi, B. guernei (todos con cromosoma haploide n=36),
y de un Bulinus sp. (n=72); en el grupo africanus de B. globosus. Ninguna cercaria se
obtuvo de В. tropicus ni de poblaciones de Bulinus sp. que pertenecian al grupo tropi-
cus (con n=18) y tampoco del В. forskalii у В. scalaris (ambas del grupo forskalii)
aunque en scalaris esporocistos maternos crecieron y persistieron por 2 meses Sin
librar otra progenie de esporocistos. Aunque el B. globosus sudafricano mostró un
mayor grado de infección, (76%), B. guernei de Gambia (35%) resultö ser el huésped
mas adaptable para la mantenciön del paräsito en lo que concierne a su cria facil,
supervivencia, e infectividad en la producciön de carcarias. El orden de acomodaciön
para establecer el ciclo vital entre caracoles receptores en grupo truncatus fue: bueno

BULINUS AND SCHISTOSOMA HAEMATOBIUM

- B. guernei (Gambia), B. sericinus (W. Aden), y B. truncatus (Iran); regular - B. t.
rohlfsi (Mauritania), B.t. truncatus (Corsica), В. t. truncatus (Sudan), В. Е. rohlfsi
(Ghana) y B. coulboisi (Tanzania); pobre - B. t. truncatus (Egipto) y Bulinus sp. (n=72,
Ethiopia). El hecho de que, entre otros caracoles receptivos, В. t. truncatus de
Egipto haya sido menos susceptible (excepto B. globosus de Mozambique con 2%), con
sdlo 3% infectados, demuestra que no se desarrolla ninguna especificidad local entre
caracol y parasito.

Una especie de amiba, Hartmannella biparia se encontró infectando ejemplares de
Bulinus globosus; posiblemente esto reduce la infecciön esquistosomatica en esos
caracoles,

Bajo un patrön de condiciones regularizadas -variando sölo el factor investigado-
se estudiaron varios factores de susceptibilidad en Bulinus guernei para determinar
el que favorecia mejor al parasito. Infecciones altas, generalmente se obtuvieron
bajo las siguientes condiciones: alta alcalinidad (Óptimos resultados a 49% a pH 9. 6);
temperatura elevada (67% a 30° C, pero a más altas temperaturas el resultado fué
menor, y negativo debajo los 10° с); grandes dosis miracidiales (70% а 60+ por caracol);
en caracoles jOvenes (maximo 67% en caracoles de 3 dias; sin embargo, debido a la
gran mortalidad, caracoles de 1-2 semanas de vida dieron el maximo de los ejemplares
infectados); en caracoles extendidos exponiendo asi la mayor area del cuerpo (54%),
y más en los anestesiados (81%) presumiblemente a causa de menor secreción mucosa
agravada por inmobilidad.

La infección no retardó el crecimiento de los caracoles. En los de tres dias de
vida infectados, la mortalidad no fué mayor que en los no infectados, pero ninguno
de aquellos sobrevivió más de 32 semanas. El número de huevos en la puesta se
redujo de 7 a 100 veces (promedia 15) en los infectados, así como las anormalidades
fueron 17 veces más frequentes; las anormalidades fueron de varios tipos, simples o
en combinación, tales como falta de huevos en la matriz gelatinosa, pequeño tamaño
del ovulo, falta de embrión o colocación del embrión fuera de la membrana del huevo,
poliembrionia, y presencia de caracarias en el huevo o masa ovigera,

Los periodos de incubación cercarial fueron más cortos y uniformes cuando se
guardaron altas temperaturas (23 dias a 30°C; 35-49 dias a 24°C). El periodo álgido
de emergencia cercarial se alconzó 1-2 semanas despues de la primera muda o
derrame y el número esparacido fluctuó diariamente mucho, posteriormente, depen-
diendo de la temperatura (Óptima a 35°C, e interrumpida a 40°) y luz, así como de la
intensidad de la infección, estado de salud del caracol y condiciones acuáticas. La
infección fue parcialmente. “curada” cuando los caracoles se conservaron а 35° -37°C
por una semana, que se evidenció por el reducido rendimiento cercarial y aumento de
oviposición. El rendimiento máximo de cercarias fué estimado a 2500 diarias por
caracol, y 20.000 en total por caracol. Caracoles infectados, de gran tamaño sobre-
vivieron más, pusieron más huevos y produjeron mayor número de cercarias que los
individuos de menor tamaño.

Caracoles machos produjeron más cercarias que las hembras, la proporción
hembra-macho siendo 1:2.6. Sólo cuando un caracol fué expuesto intensamente a
miracidios, aparecieron infecciones bisexuales, a una frecuencia de 7% (10 miraci-
dios) y 9% (20 miracidios).

J. J. Po

ABCTPAKT

СОВМЕСТИМОСТЬ И ОТНОШЕНИЯ ХОЗЯИН-ПАРАЗИТ МЕЖДУ ВИДАМИ РОДА
BULINUS (BASOMMATOPHORA: PLANORBIDAE) И ЕГИПЕТСКОЙ ЛИНИЕЙ
SCHISTOSOMA HAEMATOBIUM (TREMATODA: DIGENEA)

Y/H- TCOHT-JIO

Изучалась способность различных видов Bulinus служить промежуточным
хозяином для египетской линии кровяной двуустки Schistosoma haematobium, a
также факторы, влияющие на восприимчивость моллюска к заражению и на
воздействие паразита на инфицированных моллюсков.

28 выведенных в лаборатории популяций, включающих около дюжины видов и
подвидов Bulinus из различных частей Африки и прилежащих районов, были
подвергнуты заражению Schistosoma haematobium при стандартных условиях.
Размер моллюсков варьировал от 2 до 4мм в высоту; температура колебалась

279

280

CHILD

в пределах 24-2600; каждая особь подвергалась воздействию 10-20 мирацидиев;
на 1 моллюска шло 2 мл воды. Для всех случаев использовали покупную
родниковую воду. Церкарии появлялись в группе truncatus y Bulinus truncatus
truncatus, В. t. rohlfsi, В. sericinus (Зап. Аден), В. coulboisi, В. guernei (все с
гаплоидным числом хромосом n=36) и. У Bulinus sp. (n=72); и y группы
africanus y В. globosus. Не было получено церкариев от В. tropicus и
нескольких популяций Bulinus sp., принадлежащих к группе tropicus (с n=18),
и OT В. forskalii и В. scalaris (оба из группы forskalii), хотя в последних
видах материнские спороцисты росли и оставались в течение 2 месяцев, не
освобождая дочерние спороцисты. Хотя В. globosus из Южной Африки показали
наивысшую скорость заражения (76%), В. guernei из Гамбии (35% заражения)
оказались наиболее подходящим хозяином для поддержания существования
паразита с точки зрения легкости размножения, выживания, способности

заражать и ‘выпуска церкарий. Порядок пригодности воспринимающих
моллюсков для осуществления жизненного цикла среди группы truncatus
следующий: хорошие - В. guernei (Гамбия), В. sericinus (Зап. Аден) и
В. t. truncatus (Иран); неплохие - B.t. rohlfsi (Гана) и В. coulboisi (Танзания);
плохие - В. ЕЁ, truncatus (Египет) и В. sp. (п=72, Эфиопия). То, что наша
лабораторная линия В. truncatus из Египта (3% заражения) была менее

восприимчивой, чем практически любые другие моллюски-рецепторы (кроме
В. globosus из Мозамбика с 2%), показывает, что локальная специфичность
моллюска к паразиту не всегда имеет место.

Обнаружено, что некоторые особи Bulinus globosus заражены амебой
Hartmanella Брата, что возможно снижает зараженность этих моллюсков
Schistosoma.

Для определения наибольшей успешности воздействия паразита Ha Bulinus
guernei изучали некоторые факторы, влияющие на восприимчивость моллюска
при стандартных условиях, варьируя лишь исследуемый фактор. Обычно
более высокая зараженность достигалась при следующих условиях: высокая
зелочность (оптимальные результаты 49% при pH 9,6); высокая температура
(67% при 30°C, но меньше при еще более высоких температурах и
температурах ниже 10°C); ‹ большая доза мирацидиев (70% при 60+ на 1
моллюска), у молоди моллюсков (максимум 67% у выживающих моллюсков в
возрасте 3 дней; однако из-за высокой смертности, среди моллюсков 1-2
недельного возраста наблюдалось максимальноё число зараженных особей); у
моллюсков, фиксированных в определенном положении (54%), когда вытянутое
тело моллюска представляет максимум площади для внедрения паразита, а
также при анестезии (81%) вероятно из-за меньшей секреции слизи
одновременно с вытяженнем и неподвижностьью.

Инфекция не задерживает роста моллюска. Смертность инфицированных
моллюсков в возрасте более 3 дней перед началом выпуска церкариев была
не выше, чем у незараженных моллюсков. Ни один из зараженных моллюсков
не выжил свыше 32 недель. Зараженные моллюски производили в 7-100 раз
(в среднем в 15 раз) меньше яиц, чем незараженные, а аномалии
встречались в 17 раз чаще. Обнаружено несколько типов аномалий в
кладках, единичные, либо в комбинациях: отсутствие яиц в студенистой
строме, меньший размер яиц, отсутствие эмбрионов, расположение эмбриона
вне яйцевой капсулы, полиэмбриония, присутствие церкариев в кладке или
яйце.

Периоды инкубации церкариев были короче и более однородны, если
моллюски содержались при высокой температуре (23 дня при 30°C, 35-49
дней при 24%). Пик появления церкариев достиганся 1-2 недели спустя
после их первого выхода и количество выходов в день затем сильно
варьировало в зависимости от температуры (оптимальное-при 35°C,
подавленное при 40°C) и света, а также интенсивности заражения,
состояния моллюска и качества воды. Инфекция частично излечивалась,
если зараженных моллюсков держали при 35-3796 в течение недели,
доказательством чему был сниженный выход церкариев и увеличение
выметанных яиц. Вычисленный максимальный дневной и общий выход Ha
одного моллюска был соответственно 2500 и 20000 церкариев. Зараженные
моллюски более крупного размера выживали дольше, откладывали большё яиц
и производили церкариев больше, чем моллюски меньшего размера.

Большинство моллюсков производило больше мужских церкариев, чем
женских, отношение женских к мужским было 1:2,6. Лишь в случае, когда
моллюск был сильно подвергнут атаке мирацидиев, возникала бисексуальная
инфекция, составлявшая 7% (10 мирацидиев) и 9% (20 мирацидиев).

7. A. Е.

MALACOLOGIA, 1972, 11(2): 281-286

METABOLISM OF BROODING YOUNG FROM AESTIVATING ADULTS OF THE

BANDED POND SNAIL VIVIPARUS BENGALENSIS

D. Balakrishna Rao, M. C. Venkatasubbaiah, R. Sarvajagannadha Reddy,
A. Narasimha Raju, P. Venkateswara Rao and K. S. Swami!

ABSTRACT

Young snails were collected from the uterine brood pouches of active or aes-
tivating adult specimens of Viviparus bengalensis. Glycogen, pyruvic acid,
lactic acid and inorganic phosphorus were estimated. Differences are explained
as due to reduced carbohydrate utilization during aestivation. Succinate dehy-
drogenase, cytochrome oxidase, and adenosine triphosphatase have been as-
sayed, and evidence has been presented for depressed oxidative metabolism and
aerobic carbohydrate consumption. Increased lactate was observed and ex-
plained as due to accumulation of lactic acid over the period of aestivation, as
there is no corresponding increase in lactate dehydrogenase activity. It is con-
cluded that the brooding juveniles in an aestivating adult avoid burdening the
parent by considerably reducing their aerobic carbohydrate consumption, and
by not indulging in any extra anaerobic activity other than that which occurs in

juveniles in active adults.

INTRODUCTION

The common banded pond snail Vivi-
parus bengalensis (Lamarck) is known to
be ovoviviparous and to retain the young
in the uterine brood pouch to the crawl-
ing stage. It aestivates under drought
conditions as do many other freshwater
operculate snails. Annandale (1921)
reported live young of various ages
from the uterine brood chambers of
aestivating adults. Encysted embryos
of the brine shrimp, Artemia salina,
appear to enter a state of dormancy
when subjected to desiccation (Clegg,
1967). The problem of anabiosis or
latent life has been reviewed by Keilin
(1959). Apparently the juveniles in the
uterus of an aestivating snail are able
to lead a similarly quiescent life so
that they may not become a metabolic
burden on their parent. In the present
investigation an attempt is made to
understand certain metabolic aspects
of the quiescent life of the young ones,

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‚lReprint requests should be directed to Dr. Karumuri S. Swami,
Zoology, Sri Venkateswara University, Tirupati (А.Р), India.

MATERIALS AND METHODS

Adult specimens of Viviparus bengal-
ensis of uniform size were collected
from a Selected local temple tank and
acclimated tolaboratory conditions. Fif-
ty specimens wereforcedinto aestivation
for a period of 3 months by burying
them in dry sterile sand in glass con-
tainers. Active laboratory acclimated
adults and 3-month aestivated adults
were removed from their shells, their
brood pouches opened and the young ones
collected separately. Juveniles in the
10-12 mg range were blotted free of
uterine fluid, weighed on a torsion bal-
ance and homogenized with a hand pestle
in a mortar at 5°C in appropriate media
as recommended in the assay methods.
The homogenates were centrifuged for
15 min. at 2,500 rpm at 16°C and the
fractions subjected to different proce-
dures.

For glycogen estimation juveniles
were homogenized in 80% methanol and

Head of the Department of

(281)

282 RAO, ET AL.

the methanol-insoluble fraction usedac-
cording to the method of Kemp, Andienne
& Heijhingen (1954). Pyruvic acid con-
tent was determined colorimetrically as
1,2-dinitrophenyl hydrazone complex
(Friedemann & Haugen, 1943) in the
supernatants derived from the 10% tri-
chloroacetic acid (TCA) precipitation.
Lactic acid content was estimated colo-
rimetrically by the method of Hullin &
Noble (1953) in supernatants of homo-
genates prepared in the deproteinising
solution recommended in the procedure,
To reduce the possibility of altered
lactic acid levels the following pre-
cautions were taken: a) The young were
homogenized in deproteinizing solution
at 5°C within 15 min. of the time of
their collection from adults. b) Glass-
ware was maintained acid free and con-
tact by hand avoided. c) Blanks were
always run through the complete pro-
cedure,

The incubation mixture for the assay
of adenosine triphosphatase (Enzyme
Commission No. EC. 3.6.1.4) consisted
of 2 „М adenosine triphosphate (Nutri-
tional Biochemical Corporation, Ohio),
2uM MgCl,, 0.2 ml of 0.5 М sodium
diethyl barbiturate buffer at pH 7.4 and
80-100 pgm enzyme protein in a total
volume of 0.6 ml. The mixture was in-
cubated at 37°C for 15 min. The reaction
was stopped by adding 0.4 ml cold 30%
TCA. Phosphorus was determined by
the method of Fiske & Subbarau (1925)
using 1,2,4 amino-naphthol sulfonic acid
as reducing agent.

Succinate dehydrogenase (EC.1.3,99,1)
activity was assayed by the method of
Hiat (1961). The reaction at room tem-
perature (35°C) was initiated by adding
N-methyl phenazonium sulphate. The
rate of reduction of sodium-2-6 dichlor-
ophenol indophenol was measured at a
wavelength of 600 my.

Lactate dehydrogenase (EC. 1.1.1.27)
activity was assayed colorimetrically
(Cabaud, Wroblewski & Ruggiero, 1965)
by estimating pyruvate in the reacting
system, and enzyme activity was ex-
pressed in Wroblewski units.

Cytochrome oxidase (EC. 1.9.3.1) ac-
tivity was assayed spectrophotometric-
ally by the method of Smith (1955),
where the drop in optical density at
15 sec. intervals was measured,

Protein in the homogenate superna-
tants was estimated by the Folin phenol
method of Lowry et al. (1951) using bo-
vine albumin as standard,

All colorimetric measurements were
made with a Spectronic 20 colorimeter
and spectrophotometric measurements
with a Hilger and Watts (England) spec-
trophotometer.

RESULTS

The results are given in the form of
2 tables for comparison. From Table 1
it is clear that both glycogen and lac-
tate accumulate in the young in aesti-
vating adults, The extent of this accu-
mulation over a period of 3 months is
3-fold and 8-fold for glycogen and lac-
tate respectively, There is an appreci-
able drop of 61% in the pyruvate level
of the young from aestivating adults and
an increase in inorganic phosphorus by
37% over the young from active adults.
As seen in Table 2, the enzyme activity
in general drops in the young from
aestivating adults, the drop being parti-
cularly high for succinate dehydrogen-
ase,

DISC USSION

Comparison of glycogen levels of
brooding young isolated from the active
and aestivating Viviparus bengalensis
shows a large difference (Table 1),
suggesting that the rates of carbohydrate
utilization differ under these 2 different
conditions, Low levels of life activities
and decreased metabolic ratesare gene-
rally reported for hibernating (Lyman &
Chatfield, 1955), aestivating (Meenakshi
1956, 1958, 1964; Visser 1965, Reddy
1967; Reddy & Swami 1967; Coles 1968)
and hypobiotic (Keilin 1959) animals,
The adult aestivating snail Pila virens
is reported to have a very low glyco-
lytic rate as suggested by the fact that

METABOLISM OF YOUNG VIVIPARUS 283

TABLE 1. Lactate, pyruvate, glycogen and inorganic phosphorus levels* in young from normal
and aestivating Viviparus bengalensis.

Lactic acid
ug/gm protein

135. 00
+ 9.00

Young from active
adults

1089. 70
+162. 00

Young from aesti-
vating adults

*Each value is the mean of 6 separate estimations

Pyruvic acid
ug/gm protein

Glycogen
ug/mg protein

Inorganic phosphorus
ug/mg protein

39.85
+4.92

54.80
+4, 26

TABLE 2. SDH, LDH, cytochrome oxidase and ATPase activities* in young from normal and
aestivating Viviparus bengalensis.

Succinic
dehydrogenase
activity

(a)

Young from active
adults

Young from aesti-
vating adults

Percent decrease

Lactate
dehydrogenase
activity

(b)

Cytochrome Adenosine
oxidase tryphosphatase
activity activity

(с) (9)

* Each value is the mean of 6 separate estimations.

(a) One unit of enzyme activity is defined as the amount which will cause an optical density de-

crease of 0. 01/min/mg protein at 35°C.

(b) Wroblewski Units

35°C!

24 mg of glycogen lasted for a period
| of 6 months aestivation while the same
quantity is exhausted within 20 hrs of
normal active life (Meenakshi, 1958).
The 3-fold increase in glycogen content
of the young from aestivating adults
may Similarly be explained as due to
lowered carbohydrate utilization. It is
likely that the young had fallen in line
with the aestivating parent in cutting
down their carbohydrate consumption.

(с) One unit of enzyme activity is defined as a drop in optical density by 0. 01/min/mg protein at

(d) Expressed as micrograms of inorganic phosphorus/mg protein/hr.

Complying with this, the pyruvic acid
content in young from aestivating adults
is very low (Table 1) as compared to
young from active parents. The lower
metabolic activity of the young from the
aestivating adults is further evidenced by
the decreased adenosine triphosphatase
activity (Table 2). Aestivating snailsare
also known to have reduced adenosine
triphosphatase activity (Reddy, 1967).
The higher inorganic phosphorus in the

284

young from the aestivating adults (Table
1) indicates the low level of esterifica-
tion,

The lactic acid content of the young
from aestivating adults is 8X that of the
young from active adults. There is,
however, no corresponding increase in
the lactate dehydrogenase activity in the
former (Table 2). Evidently the higher
lactate content in these young withlower
lactate dehydrogenase activity must have
resulted from accumulation of lactic acid
over the entire aestivation period of 3
months. In the young from normal
adults there is no such accumulation of
lactate. This suggests reconversion of
lactic acid to pyruvic acid as evidenced
by the higher pyruvate level and further
oxidation of this pyruvate through the
citric acid cycle. This could take place
probably because of better capacities of
cellular oxidations in the young from
active adults as shown by the higher
succinate dehydrogenase and cytochrome
oxidase activities (Table 2). The young
from the aestivating adults do not appear
to have much capacity for cellular oxi-
dation. Both succinate dehydrogenase
and cytochrome oxidase activites are
very low in them, the former only 32%
and the latter only 60% of the corres-
ponding activities in the young from
active adults (Table 2). Similar de-
pressed respiratory enzyme activity is
known in aestivating adults (Michejda
Kasprjach & Obuchowicz, 1958; Eck-
stein & Abraham, 1959, Reddy, 1967).
This necessarily leads to accumulation
of lactate.

It appears that the young from aesti-
vating adults lower their respiratory
enzyme activity and thereby the aerobic
carbohydrate consumption. They seem
to refrain from indulging in any extra
anaerobic activity other than that exist-
ing in young from active adults, They
thus avoid burdening the aestivating
parents,

ACKNOWLEDGEMENTS

This research has been financed in
part by a grant (FG-IN-395, project

RAO, ET AL.

A7-ADP-31) made by the United States
Department of Agriculture under P.L,
480.

LITERATURE CITED

ANNANDALE, N., 1921, The banded pond
snail of India. Rec. Ind. Mus., 22.

CABAUD, Р. G., WROBLEWSKI, Е. €
RUGGIERO, V., 1965, in Hawk's Phy-
siological Chemistry, Edited by Ber-
nard L. Oser, McGraw-Hill Book Co.,
New York, 14th Edition, 1965, p 1128.

CLEGG, J. S., 1967, Metabolic studies
of cryptobiosis in encysted embryos
of Artemnia salina, Comp. Biochem.
Physiol., 20(3): 801-809,

COLES, G. C., 1968, The termination of
aestivation in the large fresh water
snail, P. ovata (Ampullariidae) -1.
Changes in oxygen uptake. Comp.
Biochem. Physiol., 25: 517-522,

ECKSTEIN, B. & ABRAHAM, M., 1959,
Succinic dehydrogenase activity in
aestivating and active snails (Helix)
Levantina hierosolynia. Physiol.
Zool., 32: 310-312,

FRIEDEMANN, T. E. & HAUGEN, G. E.,
1965, in Hawk's Physiological Chem-
istry, Edited by Bernard L, Oser,
McGraw-Hill Book Co., New York,
14th Edition, 1965. p 1108,

FISKE, C. H. € SUBBARAU, Y., 1925,
The colorimetric determination of
phosphorus, J. biol. Chem., 66: 375-
400.

HIAT, A. J., 1961, Preparationand some
properties of soluble succinic dehy-
drogenase from higher plants. Plant
Physiol., 36(5): 552-557,

HULLIN, В.Р. € NOBLE, В. L., 1953,
The determination of lactic acid in
microgram quantities. Biochem. J.,
55: 287-291.

KEILIN, D., 1959, The problem of ana-
biosis or latent life.
current concepts. Proc. Roy. Soc. B,
150: 149-191.

KEMP, A., ANDIENNE, J. M. & HEIJH-
INGEN, J., 1954, A colorimetric micro
method for the determination of gly-
cogen in tissues. Biochem. J., 56:
646-648,

History and |

METABOLISM OF YOUNG VIVIPARUS 285

LOWRY, O. H., ROSEBROUGH, J. J.,
FAR, A. L. & RANDELL, R. J., 1951,
Protein measurement with the Folin-
phenol Reagent. J. biol. Chem., 193:
265-275.

LYMAN, C. P. & CHATFIELD, P. O.,

1955, Physiology of hibernation in
mammals. Physiol. Rev., 35: 403-
425.

MEENAKSHI, У. R., 1956, Physiology of
hibernation of the apple snail Pila
virens. Curr. Sci. (India)., 25: 321-
322.

MEENAKSHI, V. R., 1958, Anaerobiosis
in the South Indian Apple snail Pila
virens during aestivation. J. Zool.
Soc. (India)., 9: 62-71.

MEENAKSHI, V. R., 1964, Aestivation
in the Indian Apple snail, Pila. I.
Adaptations in natural and experi-
mental conditions. Comp. Biochem.
Physiol., 11: 379-386.

MICHEJDA, J., KASPRJACH, L. & OBU-

CHOWICZ, L., 1958, Oxidative phos-
phorylation in snails. Proc. 4th Inter-
national Congress. Biochem Sec. 5:
81. Pergamon Press, New York.

REDDY, S. R., 1967, Respiratory en-
zymes during aestivation of the Indian
Apple snail, Pila globosa. Life. Sci.,
6: 341-345,

REDDY, S. В., € SWAMI, K.S., 1967,
Adenine nucleotide and adenosine tri-
phosphatase activity during aestiva-
tion of the Indian Apple snail, Pila

globosa. Can. J. Biochem., 45: 603-
607.
SMITH, L., 1955, Spectrophotometric

assay of cytochrome C oxidase. in
“Methods in biochemical analysis”.
Edited by Glick, John Willy & Sons.,
Inc., New York, 2: 427-434,

VISSER, S. A., 1965, A study of meta-
bolism during aestivation of the am-
phibious snail, Pila ovata. West Afr.
J. Biol. appl. Chem., 8: 41-50.

ZUSAMMENFASSUNG

STOFFWECHSEL DER JUNGEN DER GEBANDERTEN TEICHSCHNECKE
VIVIPARUS BENGALENSIS LAMARCK IN DER BRUTTASCHE DER ERWACHSENEN
WAHREND DES SOMMERSCHLAFES

D. В. Rao, М. С. Venkatasubbaiah, В. S. Reddy, A. N. Raju, P. У. Rao, К. 5. Swami

JungeSchnecken aus den Bruttaschen aktiver und sommerschlafender erwachsener
Individuen von Viviparus bengalensis Lamarck wurden untersucht und verglichen,
Glykogen, Brenztraubensäure, Milchsäure und anorganischer Phosphor wurden be-
stimmt. Unterschiede werden dadurch erklärt, dass während des Sommerschlafes
der Kohlehydratverbrauch geringer ist. Succinat-Dehydrogenase, Cytochrome-
Oxidase und Adenosin-Triphosphatase wurden quantitativ bestimmt und der Beweis
für verminderten Sauerstoff-Verbrauch und aerobischen Kohlenhydrat-Abbau erbracht.
Zunahme von Lactat wurde beobachtet und damit erklärt, dass sich Milchsäure währ-
end der Zeit des Sommerschlafes ansammelt, weil keine entsprechende Zunahme der
Wirksamkeit der Lactat-Dehydrogenase vorliegt. Es wird daraus geschlossen, dass
die Jungen in der Bruttaschen sommerschlafender Erwachsener das Muttertier nicht
durch ihren Stoffwechsel belasten sondern ihren aerobischen Kohlehydratverbrauch
beträchtlich einschränken und keinen weiteren anaerobischen Stoffwechsel vornehmen,
als den, der auch bei Jungen aktiver Erwachsener stattfindet.

Н. 2.

RESUME

METABOLISME DE JEUNES EN INCUBATION CHEZ DES ADULTES EN ESTIVATION
DE LA PALUDINE VIVIPARUS BENGALENSIS

D. В. Rao, М. С. Venkatasubbaiah, В. 5. Reddy, A. N. Raju, P. У. Rao, К. S. Swami

Des jeunes ont été extraits de la poche utérine d’incubation à partir de spécimens
adultes, actifs ou en estivation, de Viviparus bengalensis Lmk. Le glycogène, l’acide

286

RAO, ET AL.

pyruvique et le phosphore non organique ont été estimes. Les differences notées
sont expliquées comme dues à une utilisation réduite d’hydrates de carbone pendant
l’estivation, Les succinate deshydrogénase, cytochrome oxydase et adénosine tri-
phosphatase ont été testées, ce qui a mis en évidence la faiblesse du métabolisme
d’oxydation et de la consommation aerobie d’hydrates de carbone. Une augmentation
du lactate a été observée et on l’explique comme due à l’accumulation de l’acide lac-
tique pendant la période d’estivation, alors qu’il n’y a pas une augmentation corres-
pondante de la lactate deshydrogénase. On en conclut que les jeunes en incubation
dans des adultes en estivation évitent d’épuiser le parent en réduisant considérable-
ment leur consommation aérobie d’hydrates de carbone et en ne s’adonnant pas a.
d’autres activités anaérobies que celles qui ont lieu chez les juvéniles de parents
actifs.
A. L.

RESUMEN

METABOLISMO DE JUVENILES INCUBADOS DURANTE LA
ESTIVACION DE ADULTOS DE VIVIPARUS BENGALENSIS (LAM.)

D. B. Rao, M. C. Venkatasubbaiah, R. S. Reddy, A. N. Raju, P. V. Rao, K. S. Swami

Individuos juveniles fueron extraidos del saco incubatorio uterino de los adultos de
Viviparus bengalensis, y se calculö la proporciön de glicogeno, acidos pirüvico y
láctico, y el fósforo inorgánico. Las diferencias encontradas se explican como obede-
ciendo a la reducción, durante la estivación, del uso de carbohidratos. Se verificaron
ensayos con sucinato de dehidrogenasa, oxidasa citocromatica y trifosfatasa de ade-
nosina, presentado evidencia de un metabolismo oxidativo deprimido y consumo de
carbohidrato aeróbico. Se observó aumento lactático que se debe a la acumulación
de ácido láctico durante el periodo estivatorio, sin aumento correspondiente de
actividad de dehidrogenasa láctica. Se concluye que los juveniles incubados durante
el periodo de estivación del adulto, evitan agravar al progenitor reduciendo con-
siderablemente el consumo de carbohidrato aeróbico, y no participando en actividades
aeróbicas extras más que las conocidas en los juveniles incubados por adultos en
actividad.

J. J. P.

ABCTPAKT

МЕТАБОЛИЗМ Y МОЛОДИ МОЛЛЮСКОВ, ВЫНАШИВАЕМЫХ ВЗРОСЛЫМИ ПРУДОВИКАМИ
VIVIPARUS BENGALENSIS (L.) ВО ВРЕМЯ ПЕРИОДА ИХ ЭСТИВАЦИИ

I. БАЛАКРИШНА-РАО, M. ВЕНКАТАСУБАЙА, Р. САРВАДЖАГАННАДХА-РЕДДИ,
А. НАРА-ЗИМХА-РАДЖУ, П. ВЕНКАТЕСВАРА-РАО, К. СВАМИ

Молодь моллюсков собиралась из маточных выводковых карманов взрослых
активных или находящихся в стадии летней спячки Viviparus bengalensis L.

У них определялись - гликоген, пировиноградная и молочная кислоты и
неорганический фосфор. Полученные различия объяснялись как результат
уменьшения потребления углеводов во время эстивации взрослых моллюсков.
Определяись также сукцинат дегидрогеназа, цитохром-оксидаза и
аденазин-трифосфотаза. Полученные данные указывают на депрессию
оксидативного метаболизма и на аэробное потребление углеводов.

Увеличение количества молочной кислоты объясняется тем, что в течение
периода эстивации, происходило ее накопление, поскольку соответствующее
увеличение активности лактатгидрогеназы отсутствовало.

Был сделан вывод, что молодь, вынашиваемая взрослыми во время их летней

спячки, избегает излишне "нагружать" родительские особи, путем
значительного снижения аэробного потребления углеводов и путем
недопущения экстра-анаэробной активности, т.е. иной, чем обычно

наблюдается у ювенильных особей, вынашиваемых взрослыми моллюсками,
находящимися в активном состоянии. Prine

MALACOLOGIA, 1972, 11(2): 287-294

SUR LA BIOLOGIE DE LA REPRODUCTION DES PATELLES DE LA
FAMILLE TECTURIDAE (GASTROPODA: DOCOGLOSSA) ET SUR LA
POSITION SYSTEMATIQUE DE SES SUBDIVISIONS

Alexandre N. Golikov et Oleg G. Kussakin

Institut Zoologique, Académie des Sciences de l’URSS,
Leningrad, et Institut de Biologie Marine, Vladivostok.

RESUME

Une étude d’écologie et de morphologie sur les patelles (famille des Tecturi-
dae) en provenance de la zone littorale des mers d’Extréme-Orient a révélé
l’ovoviviparité chez Rhodopetala rosea Dall et chez “Acmaea” sybaritica Dall.
La présence, chez cette derniere et chez une espece nouvellement décrite, d’un
penis bien développé et, en conséquence, du phenomene de fécondation interne,
nous а permis de distinguer et de décrire un nouveau genre Problacmaea ayant
comme espece type Problacmaea moskalevi sp. n. et incluant Problacmaea
sybaritica.

Il y a 2 tendances évolutives distinctes à l’intérieur de la famille des Tecturidae.
Corrélativement, 2 sous-familles ont été distinguées qui sont caractérisées par
un ensemble de caractéristiques morphologiques particulières. Au cours de
l’évolution de la sous-famille Patelloidinae, qui comprend les genres Patelloida,
Collisella, Notoacmea et Testudinalia, l’appareil radulaire a subi des compli-
cations considérables. Dans la famille Tecturidae, qui comprend Tectura,
Acmaea, Rhodopetala et Problacmaea, l'appareil radulaire n’a que légèrement
changé et le changement évolutif principal a été l’élimination du stade pélagique
en faveur d’un développement direct ou de l’ovoviviparité. Pour cette raison un

appareil reproducteur et une sexualité plus compliqués ont été acquis.

Plusieurs recherches ont montré que
les gastéropodes inférieurs ont beaucoup
de caractères communs avec les poly-
placophores par la manière de leur re-
production et de leur développement.
Typiques pour les 2 groupes sont la
fécondation externe et le développement
a métamorphose, avec stade pélagique
caractéristique obligatoire - la trocho-
phore. Mais Па été établi sur une série
d’especes de polyplacophores (Kussakin,
1960; Smith, 1966; et autres), qu'on ob-
serve dans quelques familles de ce
groupe de mollusques une transition de
la métamorphose complexe au dévelop-
pement directe, la maturation des oeufs
et des embryons ayant lieu sur le corps
de la femelle, habituellement dans les
cavités branchiales et, enfin, la transi-
tion a l’ovoviviparité (Plate, 1899, 1901),
quand le développement entier se passe

dans l’oviducte de la femelle.

On observe un phénomène analogue
chez les représentants des gastéropodes
prosobranches primitifs, comme le sont
les patelles - Docoglossa.

Le plus grand nombre d’especes de
cet ordre est à fécondation externe,
habituellement avec pseudocopulation, et
un développement avec métamorphose
par le stade pélagique. Pourtant Thor-
son (1935) a montre que les oeufs
fécondés chez les Tectura rubella(Fabr.)
restent dans la cavité palléale de l’ani-
mal, ou se passe leur développement.
Nous avons observé un phénomène pa-
reil chez le Rhodopetala rosea Dall aussi.
Ici le développement est réalisé sur le
corps de l’organisme du parent pres de
l’entrée de la cavité palléale, entre la
tête et l’extrémité antérieure du pallium.
Nous avons trouvé des embryons avec

(287)

288 GOLIKOV ET KUSSAKIN

coquille développée, d’une taille de 0,4
mm, dans cette position sur l’organisme
parental sur le littoral de l’île Para-
mouchir (Iles Kouriles Nord) le 6 aoüt
1967, a une température d’eau de 9,1°.
La fécondation dans les deux cas, chez
T. rubella comme chez R. rosea, parait
etre externe, comme celle des polyplaco-
phores étudiés, et il y a simplement un
arrêt des oeufs fécondés à l’entrée de la
cavité palléale.

Enfin, on observe le stade suivant
dans l’évolution de la reproduction et du
développement dans le genre Acmaea de
la famille Tecturidae, duquel nous sépa-
rons Problacmaea gen. n. dans l’article
présent. C’est déjà un cas de vraie
ovoviviparité qu’on observe, car tout son
développement se passe à l’intérieur de
l’organisme parental sous sa coquille.

On a trouvé chez l’espèce que nous
avons étudiée a cet égard, Problacmaea
sybaritica (Dall), dans la partie dorsale
du sac intestinal immédiatement sous
ses téguments fins, un grand nombre
d’embryons avec une coquille tout à fait
développée (Fig. 2). Les embryons ont
une coquille d’une taille de 0,45 mm. Le
sommet de la coquille blanche, arrondi,
est beaucoup plus déplacé en avant que
chez les individus adultes (Fig. 3); la
surface dorsale de la coquille autour
du sommet est rose. Nous avons trouvé
l’animal avec les embryons sur le littoral
de l’île Paramouchir (Iles Kouriles) le 17
août 1967, pour unetempérature d’eau de

8,7°. La présence chez ces animaux
d’un pénis pleinement développé témoigne
incontestablement que l’ovoviviparité
chez P. sybaritica se réunit поп pas avec
la fécondation externe, mais avec la
fécondation interne. Le pénis assez
long et mince (Fig. 4), se trouve sur
la tête et prend son part immédiate-
ment sous le tentacule droit.

Ainsi, on peut considérer comme éta-
blie l’apparition de la fécondation interne
à l’aide de l’appareil de l’accouplement
chez quelques Docoglossa.

En étudiant les matériaux complémen-
taires de la zone littorale de l’île
B. Chantar (mer d’Okhotsk), que nous
avons reçus de l’Université de l’Extréme
Orient pour le travail, nous avons dé-
couvert une espèce de patelle nouvelle
pour la science, qui se rapporte par la
construction de la radule et des parties
molles à la famille Tecturidae, mais qui
possède aussi un pénis. Puisque nous
n’avons pas trouvé de pénis par l’étude
attentive du corps de Tectura virginea
(Müller), Acmaea mitra Eschscholtz, A.
pallida (Gould) et de toutes les especes
accessibles des genres Rhodopetala Dall,
Collisella Dall, Notoacmea Iredale et
Testudinalia Moskalev, nous sommes
obligés de rapporter les espéces posse-
dant cet organe a un nouveau genre,
dont la description est donnée plus bas.

Problacmaea Golikov & Kussakin, gen. n.

La coquille est relativement petite,

FIG. 1. Rhodopetala rosea Dall, vue d’en bas.

A la sortie de la cavité palléale au dessus de la

téte se trouvent les embryons avec des coquilles bien développées.

FIG. 2. Problacmaea sybaritica (Dall), la coquille est enlevée, vue du haut.

Sous les tégu-

ments fins de la partie dorsale du sac intestinal se trouvent les embryons avec des coquilles

bien développées.

FIG. 3. Individu juvénile de Problacmaea sybaritica (Dall) enlevé de l’organisme parental.

FIG. 4. Partie de téte de Problacmaea sybaritica (Dall).

un pénis bien développé.

FIG. 5. Holotype de Problacmaea moskalevi sp.n.

Sous le tentacule droit, se distingue

a. Vue du haut. b. Vue de côté.

FIG. 6. Partie de téte de Problacmaea moskalevi sp.n. En dessous du tentacule droit se dis-

tingue le pénis.

BIOLOGIE REPRODUCTIVE DES TECTURIDAE 289

290

fine, assez haute, à base arrondie-ovale;
la position du sommet est presque cen-
trale chez les adultes. La teinte de la
coquille est claire, unicolore ou avec
des raies radiales divergentes. La
tache près du sommet est vague et de
forme irrégulière. La sculpture de la
coquille ne se compose que des lignes
de croissance concentriques. La cténi-
die est petite et ne dépasse pas les
limites de la cavité palleale. A droite,
sous le tentacule, il y a un grand pénis
musculeux courbé. La papille urogeni-
tale est bien développée, elle est grande
et dépasse les limites de la cavité pal-
léale. La radule, engénéral, est pareille
à celle des représentants des genres Ac-
maea Eschscholtz et Tectura Gray.
Toutes les dents de la radule sont a peu
pres de la méme taille, et les dents
marginales sont absentes. Les repré-
sentants du genre prédominent a l’étage
infralittoral de la partie nord-ouest de
l’Océan Pacifique.

Génotype: P. moskalevi nov. sp. Nous
rapportons aussi augenre décrit Acmaea
sybaritica Dall.

Problacmaea moskalevi
Golikov & Kussakin, Sp. n.
(Fig. 5, 6, 7F)

La coquille est fine, assez fragile, a
base arrondie-ovale et 4 sommet sub-
central, soulevé. La coquille est blanche.
La sculpture est représentée seulement
par de nettes lignes de croissance con-
centriques et par des anneaux annuels
fortement en relief. La surface in-
terne de la coquille a une petite tache
pres du sommet, d’un gris clair. La
radule est typique pour le genre. La
hauteur de la coquille holotype est de 4,7
mm, la longueur de 10,5 mm et l’épais-
seur de 9 mm. L’emplacement type: la
cuvette a l’horizon moyen de l’&tage
mésolittoral à l’île В. (Grand) Chantar,
mer d’Okhotsk (récolte de M. B. Ivanova,
10 août, 1966). L’holotype se trouve
dans les collections systematiques de
l’Institut de Zoologie de l’Académie des
Sciences de l’URSS. L’espece est nom-

GOLIKOV ET KUSSAKIN

mée en honneur de L. Moskalev, un
spécialiste connu des les patelles.
Problacmaea moskalevi ressemble
extérieurement à l’Acmaea apicina Dall,
mais elle se distingue par une coquille
beaucoup plus basse, C’est un indice
constant chez les exemplaires de tout
âge. Ainsi la longueur de la coquille
d’A. apicina surpasse sa hauteur de 1,5

fois et sa largeur de 1,25 fois, tandis !

que la longueur de P. moskalevi ne sur-
passe son hauteur et sa largeur pas
moins de 2,1-2,3 et de 1,7-1,9 fois.
Comme P. sybaritica, l'espèce que
nous décrivons est ovovivipare. Chez
le paratype recueilli en même temps
que l’holotype,

nombre considérable avec des coquilles
déjà developpées.
coquilles des embryons est de 0,3 mm.
Les individus prélevés du côté conti-
nental de la mer du Japon à une pro-
fondeur de 36 m avaient sous leur man-
teau de grands oeufs d’un diamètre
d’environ 0,15 mm. En tout nous avons
examiné 11 individus de P. moskalevi
de 3 prélèvements.

Chez les deux espèces rapportées au
genre Problacmaea, qui sont probable-
ment des hermaphrodites protandres,
comme tous les autres Docoglossa
étudiés à cet égard, ce sont seulement
les individus de moyenne taille qui ont
le pénis relativement bien développé,
pendant qu’ils fonctionnent comme mâles
adultes. Puis à mesure que l’animal se
transforme en femelle et grandit, le
pénis, qui ne croft plus, paraît con-
sidérablement plus petit.

A la lumière des données qui existent
sur l’anatomie, sur la systématique et
sur l'écologie des patelles de la famille
Tecturidae on peut y remarquer 2 ten-
dances d’évolution. Si, dans les genres
Patelloida Quoy & Gaimard, Colisella
Dall, Notoacmea Iredale et Testudinalia
Moskalev, groupe se composant sur-
tout deformeslittorales, l’évolution a
produit généralement un perfectionne-
ment de l’appareil radulaire, l’évolution

on a trouvé au fond |
de la cavité palléale des embryons en |

La longueur des |

BIOLOGIE REPRODUCTIVE DES TECTURIDAE 291

FIG. 7. Structure de la radula dans les sousfamilles Patelloidinae (A-D) et Tecturinae (E-H).
A. Testudinalia tesselata. B. Notoacmea concinna. C. Collisella cassis. D. Patelloida sac-
charina. Е. Acmaea mitra. Е. Problacmaea moskalevi. G. Problacmaea sybaritica. H.
Rhodopetala rosea. A-E. D’après Moskalev, 1966. F-H. Dessins originaux.

dans les genres Acmaea Eschscholtz,
Tectura Gray, Rhodopetala Dall et Pro-
blacmaea g. nov., groupe plutdt sub-
littoral, a progresse dans le sens de la
reproduction. En partant d’un dévelop-

pement compliqué, y compris les stades
pélagiques, il menait au développement
direct et à l’ovoviviparité, tandis que
la radule restait plus constante.

En rapport direct avec le developpe-

292

ment simplifié, le procédé sexuel se
perfectionne: notamment on observe la
transition de la fécondation primitive
externe a la fécondation interne; il en
résulte un organe copulateur mäle.

Ces différences dans les tendances
du procédé de l’évolution, et les dif-
férences morphologiques, liées à elles
dans les groupes de genres étudiés,
nous permettent de les grouper en 2
sous-familles:

La sous-famille Patelloidinae Allan,
1950, qui est représentée dans les eaux
froides et tempérées de l’hémisphère
boréal par les genres Collisella, Noto-
acmea et Testudinalia, se caractérise
à l’égard de la morphologie par la
coquille de couleur disparate, par le dé-
veloppement faible ou par l’absence
des lobes parabuccaux, et par des dents
latérales de la radule de tailles forte-
ment différentes (Fig. 7, A-D).

La sous-famille Tecturinae qui est
représentée dans les eaux froides et
tempérées de l’hémisphère boréal par
les genres Acmaea, Tectura, Rhodo-
petala et Problacmaea se caracterise
par une coquille unicolore ou ayant des
lignes radiales, par des lobes para-
buccaux bien développés et par des dents
latérales de la radule, approximative-

GOLIKOV ET KUSSAKIN

ment égales (Fig. 7, E-H).
BIBLIOGRA PHIE

KUSSAKIN, O. G., 1960, Biological pe-
culiarities of the Far Eastern mollusk
Schizoplax brandtii (Middendorff).
Zool. J. Acad. Sci. U.S.S.R.r 38):
1145-1150. (Enrusse, avec resume
anglais),

MOSKALEV, L. I., 1966, De la diagnos-
tique des genres de la famille Acmae-
idae (Gastropoda, Prosobranchia) sui-
vant la radula (en russe). Zool. J.
45(12): 1767-1772.

PLATE, L., 1899, Die Anatomie und
Phylogenie der Chitonen. Fauna Chi-

lensis, 2, 1. Zool. Jahrb., Suppl. 4:
15-216.
PLATE, L., 1901, Die Anatomie und

Phylogenie der Chitonen. Fauna Chi-
lensis, 2, 2. Zool. Jahrb., Suppl. 5:
221-600.

SMITH, A. G., 1966, The larval develop-
ment of Chitons (Amphineura). Proc.
Calif. Acad. Sci., 32(15): 433-446.

THORSON, G., 1935, Studies on the egg
capsules and development of Arctic
marine Prosobranchs. Medd. om
Greenland, 100(5): 1-71.

ABSTRACT

ON THE REPRODUCTIVE BIOLOGY OF A SEA LIMPET
OF THE FAMILY TECTURIDAE (GASTROPODA: DOCOGLOSSA)
AND THE SYSTEMATIC POSITION OF ITS SUBDIVISIONS

A. N. Golikov and O. G. Kussakin

A study of the ecology and morphology of the limpets (family Tecturidae) from the
littoral zone of the Far-East seas has revealed ovoviviparity in Rhodopetala rosea

Dall and in “Acmaea” sybaritica Dall.

The presence in the latter and in a newly-

described species of a well-developed penis and, accordingly, of internal fertilization
enabled us to distinguish and describe a new genus Problacmaea with the type species
Problacmaea moskalevi sp. n. and including Problacmaea sybaritica.

There are 2 distinct evolutionary tendencies within the family Tecturidae. Corres-
pondingly, 2 subfamilies are distinguished which are characterized by a complex of
special morphological features. During the evolution of the subfamily Patelloidinae,
including the genera Patelloida, Collisella, Notoacmea and Testudinalia, the radula

apparatus has undergone considerable complication.

In the family Tecturidae,

including Tectura, Acmaea, Rhodopetala and Problacmaea, the radula apparatus has
changed only slightly and the main evolutionary change was the elimination of the
pelagic larval stage in favour of direct development or ovoviviparity. For this rea-
son a more complicated sexual process and reproductive apparatus was acquired,

BIOLOGIE REPRODUCTIVE DES TECTURIDAE

ZUSAMMENFASSUNG

UBER DIE FORTPFLANZUNGSBIOLOGIE EINER MEERES-NA PFSCHNECKE
DER FAMILIE TECTURIDAE (GASTROPODA: DOCOGLOSSA) UND DIE
SYSTEMATISCHE STELLUNG IHRER UNTERGRUPPEN

А. М. Golikov und O. а. Kussakin

Eine Untersuchung der Okologie und Morphologie der Napfschnecken aus der
Familie der Tecturidae von der Littoralzone der fernöstlichen Meere ergab, dass
Rhodopetala rosea Dall und “Acmaea” sybaritica Dall ovovivipar sind. Das Vorhan-
densein eines gutentwickelten Penis bei der letzteren und einer neubeschriebenen Art
und demgemäss innerer Befruchtung ermöglichte es uns, eine neue Gattung Problac-
maea abzutrennen und zu beschreiben, mit der Typus-Art Problacmaea moskalevi
spec.nov., zu der auch Problacmaea sybaritica gehört.

Es gibt zwei verschiedene Entwicklungstendenzen innerhalb der Familie Tecturidae.
Dementsprechend werden zwei Unterfamilien unterschieden, die durch einen Komplex
morphologischer Züge charakterisiert werden. Während der Evolution der Unter-
familie Patelloidinae, die die Genera Patelloida, Collisella, Notoacmaea und Testudi-
nalia umfasst, wurde der Radula-Apparat beträchtlich komplizierter, Bei der Unter-
familie Tecturinae, die ausdenGenera Tectura, Acmaea, Rhodopetala und Problacmaea
besteht, hat sich der Radula-Apparat nur wenig verändert; in der Entwicklung der
Individuen dagegen wurde das pelagische Larvenstadium zugunsten einer direkten ovo-
viviparen Fortpflanzung aufgegeben, Deshalb wurden kompliziertere sexuelle Verhal-
tensweisen und Organe entwickelt.

RESUMEN

SOBRE LA BIOLOGIA REPRODUCTORA DE UNA LAPA DE LA FAMILIA
TECTURIDAE (GASTROPODA: DOCOGLOSSA) Y LA POSICION SISTEMATICA
DE LA SUBDIVISIONES EN LA FAMILIA

Golikov y Kussakin

Un estudio ecolögico y morfolögico de las lapas (familia Tecturidae) del Lejano
Oriente, revelö ovoviparidad en Rhodopetala rosea Dall y en “Acmaea” sybaritica
Dall. La presencia, en la segunda especie mencionada asi como en otra de reciente
descripciön de un pene bien desarrollado y por consiguiente de fecundaciön interna,
nos capacita para distinguir y describir un nuevo género Problacmaea, con la especie
tipo Problacmaea moskalevi sp. n., e incluyendo Problacmaea sibaritica.

Entre los Tecturidae hay dos tendencias evolucionarias distintas. Asi, se pueden
distinguir dos subfamilias, caracterizadas por peculiares complejos morfolögicos.
Durante la evoluciön de la subfamilia Patelloidinae, incluyendo los generos Patelloi-
dea, Collisella, Notoacmea y Testudinalia, el aparato radular sufrió considerables
complicaciones. En la subfamilia Tecturinae, que incluye Acmaea, Tectura, Rhodo-
petala and Problacmaea, la rádula tuvo muy ligero cambio y el aspecto evolutivo más
importante fué la eliminación de la larva pelágica en favor de un desarrollo directo
u ovoviparidad, y en consecuencia un proceso sexual más complicado, asi como del
aparato sexual, fué adquirido.

JJ. В.

293

294

GOLIKOV ET KUSSAKIN

ABCTPAKT

К ЭКОЛОГИИ MOPCKUX БЛКЛЕЧЕК СЕМЕЙСТВА TECTURIDAE (GASTROPODA:
DOCOGLOSSA) И СИСГЕМАГИЧЕСКОМУ ПОЛОЖЕНИК ЕГО ПОПРАЗПЕЛЕНИЙ.

А.Н. ГОЛИКОВ, О.Г. КУСАКИН

Изучение экологии и морфологии морских блюдечек сем. Tecturidae
литоральной зоны дальневосточных морей позволило обнаружить
яйцеживорождение у Rhodopetala rosea Dall и “Acmaea” sybaritica Dall. Наличие у
последнего вида и описываемого нового вида хорошо развитого пениса и,
соответственно, внутреннего оплодотворения позволило выделить и описать
новый род Problacmaea с типовым видом Problacmaea moskalevi sp. n., включающий
в себя и Problacmaea sybaritica. В пределах сем. Tecturidae наблюдается 2
отчетливых тенденции в эволюционном развитии и соответственно выделяется
2 подсемейства, характеризующиеся комплексом своеобразных морфологических
признаков. В процессе эволюции подсемейства Patelloidinae, включающего в
себя роды Patelloida, Collisella, Notoacmea и Testudinalia, наблюдается усложнение
радулярного аппарата. У подсемейства Tecturidae, включающем в себя роды
Acmaea, Tectura, Rhodopetala и Problacmaea, радулярный аппарат изменялся
незначительно, а эволюция шла по пути перехода от развития через
пелагическую личинку к прямому развитию и яйцеживорождению, в связи
с чем происходило усложнение полового процесса и воспроизводителбной
системы.

Z. A, Е.

MALACOLOGIA, 1972, 11(2): 295-342

THE MORPHOLOGY OF SOME MITRIFORM GASTROPODS WITH
SPECIAL REFERENCE TO THEIR ALIMENTARY AND
REPRODUCTIVE SYSTEMS (NEOGASTROPODA)

W. F. Ponder !
Dominion Museum, Wellington, New Zealand

ABSTRACT

The alimentary canal and reproductive systems of Strigatella paupercula
(Linnaeus), Austromitra rubiginosa (Hutton) and Peculator hedleyi (Murdoch)
are described in detail and compared with those of several allied species. The
main features ofthe head-foot, pallial cavity, renal organ and circum-oesophag-
eal ganglia are briefly indicated.

The species described fall into 3 families, the Mitridae, Vexillidae and Volu-
tomitridae, each family having a very distinctive type of alimentary canal. A
peculiar epiproboscis, present in the proboscis of the Mitridae, serves as a
vehicle for the salivary ducts. Accessory salivary glands and a gland of Leib-
lein occur in the Vexillidae and the Volutomitridae, but are both absent in the
Mitridae. Whereas the alimentary canal of the Vexillidae and Volutomitridae
have several features in common, their genital tracts are quite distinct. The
reproductive structures in the Vexillidae and Mitridae are very similar. Com-
mon features of the species considered include an anal gland, columellar plaits
and lack of an operculum, as well as an overall similarity of their shells, fea-
tures the author considers to be of secondary importance in assessing their
relationships at the family level. Other features of the Mitridae (s.s.) not
found in the other 2 families include a purple hypobranchial secretion, vase-
shaped egg capsules, and a ventral pedal gland in the female. The egg capsules
of Austromitra and Microvoluta are hemispherical. The renal organ has the
primary and secondary lamellae in separate areas in the Mitridae, but they are

interdigitated in the other 2 families.

There do not appear to be any significant

differences in the circum-oesophageal ganglia of the 3 groups.

INTRODUCTION

The mitrids have long been objects of
curiosity and pleasure to conchologists
and their colourful shells are often
prized incollections of Indo-Pacific mol-
luscs. Very little, however, is known of
the morphology of these animals which
are classically placed together in 1
family and are distinguished by their
heavy, often small shells with strong
columellar folds and relatively small
apertures,

Cernohorsky (1966, 1970) and Coan
(1966) have recently reviewed the genera

of the family Mitridae which, according
to Cernohorsky, is composed of 4 sub-
families in which are included about
500 Recent species.

The mitrids, as a group, are found
most abundantly in the Indo-Pacific re-
gion, although many species are known
from other areas. Some species inhabit
rocky shores or coral reefs where they
nestle under boulders or coral blocks,
or in crevices, whereas others burrow
in sand. The biology of the vast majority
of mitriform gastropods is very poorly
known and practically no information is
available on their feeding habits.

lPresent address: Australian Museum, Sydney, Australia.

(295)

296 W. F. PONDER

The first account of mitrid anatomy
is that of Quoy & Gaimard (1833) on the
gross anatomy of Mitra mitra (Linnaeus)
(=episcopalis Linnaeus) and the exter-
nal features of several species. Vay-
ssiere (1901) described the structure
of the proboscis of Mitra zonata Marryatt,
and later (1912) the external features of
the living animal. The first work of
importance, however, was that of Risbec
(1928) who described various aspects of
the morphology of 5 species of mitrid.
These included Mitra scutulata (Gmelin)
(=Strigatella scutulata), M. crenulata
(Gmelin) (=Pterygia crenulata), M. re-
tusa Lamarck (=Strigatella retusa), M.
microzonias Lamarck (=Pusia sp., pro-
bably P. consanguinea Reeve), and M.
luculenta Reeve (=Vexillum luculentum).
In 1955 Risbec compared Vexillum hebes
(Reeve) with these species. Cernohorsky
(1965, 1966) and Cross (1967) described
the living animal of some species and
made brief mention of some of their
habits. Cernohorsky (1970) briefly re-
viewed the anatomy of the group. Cate
(1968) gave an account of the mating
behaviour of Mitra idae Melville and its
egg capsules. Egg capsules have also
been described for Strigatella scutulata
(Habe, 1944), Mitra astricta Reeve and
Strigatella auriculoides (Reeve) (Oster-
gaard, 1950) and M. filaria (Linnaeus)
(Cernohorsky, 1966). Cernohorsky
(1970) described the egg capsules of 4
additional species. The radulae of the
mitrid gastropods have received special
attention from Troschel (1868-1869),
Cooke (1920), Peile (1922, 1936, 1937),
Barnard (1959), Azuma (1965), Cerno-
horsky (1966, 1970) and Cate (1967).

Risbec (1928) and Quoy & Gaimard
(1833) have commented on the difficulty
of dissecting these animals.. Their very
thick shells, into which the animal re-
tracts to a considerable degree, make it
very difficult to extract an undamaged
specimen,

In the present study the anatomy of
Strigatella paupercula (Linnaeus), Aus-
tromitra rubiginosa (Hutton) and Pecula-
tor hedleyi (Murdoch) are describedand,
where material was available, compared

briefly with allied species. Particular
stress is given to the morphology of the
alimentary canal and reproductive sys-
tems, but the main features of the head-
foot, pallial cavity, circum-oesophageal
ganglia and renal organ are also briefly
outlined. Because of the lack of anato-
mical and cytological information about
this group most of the information avail-
able to the writer is presented in this
account.

The main object of this study was to
provide a firmer basis for familial
classification of the mitriform gastro-
pods on anatomical grounds,

The terminology used here follows
Carriker (1943) for the proboscis and
its associated structures and Fretter
(1941) for the genital systems.

None of the shells of the species
described are figured as in each case
adequate illustrations can be readily
found elsewhere in the literature as
indicated. Representative specimens of
the material used in these observations
are housed in the Dominion Museum.

MATERIAL AND METHODS

The localities from which material
was collected are mainly in New Zealand
and the New Hebrides, S.W. Pacific
Ocean. More detailed collection data
are entered preceding the description of
each species. Specimens were fixed for
histological examination in Bouin’s fluid,
Material was double embedded by Peter-
fi’s celloidin-paraffin method (see Pan-
tin, 1962) and sections were cut at 7-9 u
and stained with Mallory’s triple stain,
Other specimens were dissected after
fixation in Bouin’s fluid, formalin or
after preservation in alcohol and, in some
cases, dissected alive.

PART 1

STRIGATELLA PAUPERCULA
(Linnaeus)

1758 Voluta paupercula Linnaeus, Syst.
Nat. ed. 10, p 731.

1965 Strigatella paupercula; Cernohor-
sky, Veliger, 8: 112, pl. 17, fig. 59.

MORPHOLOGY OF MITRIFORM GASTROPODS 297

A full synonymy and description of the
shell of this species is given by Cer-
nohorsky (1965), and the radula is also
described by that author (1966). The
material used for the following account
was collected at Port Vila, Efaté Island,
in the New Hebrides, in January, 1967.
The species was abundant in the upper
part of the shore where they clustered
in crevices amongst coral blocks.

The rather short foot is dark-brown
above, and has a white sole. The snout,
Siphon and tentacles are white distally,
and dark brown proximally. A long slit
across the anterior edge of the foot
forms the opening to the anterior pedal
gland. In female specimens a broad,
white, transverse strip runs down the
right side of the foot from the pallial
cavity, and anteriorly, a small ventral
pedal gland is present. A columnar
epithelium covers the foot above where
it is cuticulate and the distal halves of
the epithelial cells are filled with pig-
ment granules. The ciliated sole epi-
thelium is thicker, and rich in mucous
cells.

The long pallial cavity contains a very
large, brown osphradium and a slightly
longer ctenidium on the left side, anda
narrow, thick hypobranchial gland is
wedged between the ctenidium and the
gonoduct. This gland has a smooth in-
ternal surface and in life produces a
purple secretion similar to that seen in
some other mitrids(Cernohorsky, 1965).
The much larger Mitra mitra has the
hypobranchial gland pleated as in Buc-
cinum (Dakin, 1912) and Alcithoe (Pon-
der, 1970 ), and also produces a pur-
ple fluid that stains the hands and has
a pungent odour (Quoy & Gaimard, 1833).
The ctenidial filaments are triangular,
with the width of their bases slightly
less than their height. The curved os-
phradium has about 40 filaments on its
concave lower (left) side and 70 onits
upper side.

No close study was made of the cir-
culatory, renal, or nervous systems,
although it was noted that the renal
organ has a very similar structure to
that of Perrier's (1889) “meronephri-

diens,”with the primary and secondary
glandular lamellae separated. The cir-
cum-oesophageal ganglia show a marked
concentration, and are of the normal
rachiglossan pattern (Fig. 6H).

The Alimentary Canal

The most conspicuous feature of the
alimentary canal is the massive probo-
scis. The external shape of this struc-
ture has been indicated in several species
by Quoy & Gaimard (1833), who also
gave a brief description of its morpho-
logy in Mitra mitra. Vayssiere (1901)
described the internal structure of the
proboscis of Mitra zonata, as did Risbec
(1928) in the species that he examined.
All of these authors commented on the
prominent and unique structure of the
mitrid (s.s.) proboscis which has gen-
erally been regarded as a poison gland
(Risbec, 1928; Thiele, 1929; Cernohor-
sky, 1965, 1966). It was referred to as
a “tongue” by Quoy & Gaimard (1833)
and as a protractile organ by Vayssiere.
The present investigation shows that
there is no glandular tissue inthis struc-
ture and that it is in fact a muscular
rod that acts as a vehicle for the sali-
vary ducts. To avoid ambiguity a new
term, epiproboscis, will be used here.
The Proboscis. In preserved material
the pleurembolic proboscis measures
up to about ?/3 of the length of the shell
when extended and as little as 1.6 mm
when fully retracted. The wrinkled
appearance of the extended organ shows
that it is capable of further elongation.
Retraction of the proboscis, as revealed
in preserved material, is achieved in 2
ways, although it is probable that 1 of
these may be due to an unnaturally vio-
lent contraction brought about by con-
tact with the preserving fluid. Specimens
preserved in alcohol usually have the
proboscis irregularly folded into the
proboscis sac. Its walls are heavily
pleated and its overall diameter is only
Slightly greater than the average dia-
meter of the protracted organ. Practi-
cally none of the proboscis wall is
inverted to form part of the proboscis
sac. In formalin-fixed material the pro-

298 W. F. PONDER

boscis was usually considerably short-
ened and showed a subsequent increase
in diameter to nearly twice that of the
extended organ (Fig. 9A). The longitu-
dinal muscle layers in the wall were
correspondingly thicker due to the severe
and possibly unnatural contraction and
much of the basal part of the proboscis
behind the epiproboscis was inverted to
form part of the proboscis sac. Many
specimens preserved in alcohol still had
the proboscis extended, thus suggesting
a sluggish withdrawal similar to that
mentioned by Quoy & Gaimard (1833) in
Mitra mitra.

The proboscis sac is very thin-walled
and spacious. When filled with the re-
tracted proboscis it causes the roof of
the cephalic cavity to bulge into the ante-
rior half of the pallial cavity. A wide,
powerful series of muscles, continuous
with the inner longitudinal layer of the
proboscis wall, run to the floor of the
cephalic cavity and become confluent
with the columellar muscle, whereas 2
lateral muscles with a similar origin,
attached to the roof of this cavity, make
up the main proboscis retractor muscles,
A powerful sphincter muscle guards the
small rhynchostome (opening to the pro-
boscis sheath) through which the unpig-
mented proboscis is everted,

The rather thin proboscis wall con-
sists of an outer layer of circular
muscles, which are sharply separated
from a thicker, inner layer of longi-
tudinal fibres. A basement membrane
lies beneath the outer cuticularized cu-
boidal epithelium.

Sections through the buccal mass and
the middle part of the proboscis can be
seen in Figs. 1B, C, and a lateral view
of the anterior region of the proboscis
in Fig. 1A. The mouth is overhung by
an outer muscular rim, the peristomal
rim (p.r ) which is very similar to that
in the muricacean Urosalpinx cinerea
(Say) (Carriker, 1943). Short, powerful
muscles (p.r.m ) control this rim and
have their origin in the proboscis wall.
It does not appear that this rim can be
flattened to expose the mouth completely,

so that it may function, therefore, asa
sucker or a cushion. Running between
the mouth and the buccal cavity is a
ring of weaker oral retractor (o.r )
muscles. The oesophagus is loosely
bound to the proboscis wall by thread-
like buccal tensor muscles which become
heavier and much more abundant around
the buccal cavity.

The buccal wall is composed of a
thick mass of circular muscles and a
Superficial layer of longitudinal ones,
whereas its lining epithelium is covered
ventrally with stout cuticle over which
the odontophore moves. Bordering this
thick cuticular plate are the anterior
extensions of the dorsal folds (d.f ).

The odontophore (Fig. 2A) is pink in
life, short and wide, and covered dor-
sally by a thin sheet of transverse mus-
cle (Fig. 1B; d.t.m ). Wide odontophoral
cartilages (od.c ) extend the length of
the odontophore and come close together
in front, although they do not join. The
triangular, dorsal subradular membrane
protractor muscles (d.sm.p) are at-
tached to the ventral edge of the ante-
rior portion of the cartilages and to the
radular sac. Below these muscles lie
the large dorsal subradular membrane
retractor muscles (d.sm.r ) which are
attached to the inner ventral edges of
the cartilages along the posterior 7/3 of
their length. As well as being fixed to
the subradular membrane these muscles
are fixed to the radular sac. The odonto-
phoral protractor muscle sheets (1.p.od )
lie laterally, being inserted inthe poste-
ro-lateral buccal wall, and run to the
posterior end of each cartilage. Below
these muscles lie the lateral subradular
membrane retractor muscles (l.sm.r )
which are attached to the dorsal edge of
each cartilage, and to the subradular
membrane after passing around the ven-
tral edge of the cartilages. Lying below
and near the anterior end of the odonto-
phore, and attached to the anterior end
of the odontophoral cartilages from
where they pass into the latero-ventral
wall of the buccal cavity, is a pair of
short, odontophoral divaricator muscles,

MORPHOLOGY OF MITRIFORM GASTROPODS 299

B an Dann Vodir

AN

FIG. 1. A-D. Strigatella paupercula (Linnaeus): A. Lateral view of the anterior end of the pro-
boscis opened from the left side; B. Transverse section of the proboscis through the odontophore;
C. Transverse section of the proboscis behind the epiproboscis; D. Radular teeth from 2 speci-
mens from Port Vila, Efaté Island, New Hebrides, showing variation. E. Imbricaria conovula
(Quoy & Gaimard). Radular teeth (Port Meslep, Efaté Is. , New Hebrides).

A transverse muscle (+. ) runs ven- odontophoral retractor muscles (d.od.r )
trally between the anterior portions of are fixed to the odontophoral cartilages
the odontophoral cartilages to which it along the posterior 7/3 of their length,
is attached. A series of short, dorsal their area of attachment coinciding with

300

р
u
= 99

0.4

W. F. PONDER

KEY TO LETTERING ON FIGURES

anus

opening to anterior digestive gland
duct

anal gland

albumen gland

accessory salivary gland duct
accessory salivary gland
antero-ventral lobe of capsule gland
buccal ganglion

pale blue staining area of capsule
gland

bursa copulatrix

blue-staining gland cells

blood vessel

cerebral ganglion

caecum of stomach

capsule gland

common opening of digestive gland
ducts

circular muscle

ciliated region

dorsal channel

dorsal fold

duct of gland of Leiblein

dorsal odontophoral protractor muscle
dorsal odontophoral retractor muscle
dorsal subradular membrane
protractor muscle

dorsal subradular membrane
retractor muscle

dorsal transverse muscle
ejaculatory duct

gland cells

gland of Leiblein

ingesting gland duct

ingesting gland

intestine

intestinal region of stomach

left fold of ventral channel
longitudinal muscle

lateral odontophoral protractor
muscle

lateral subradular membrane
retractor muscle

mucous secretion area of capsule
gland

mucous cells

glandular epithelium of the section
of the mid-oesophagus behind the
valve of Leiblein

muscular region of stomach

nerve

orange-staining area of capsule
gland

od.
od.c

odontophore

odontophoral cartilage
odontophoral retractor muscle
oesophagus

outer longitudinal muscle strip
operculum

oral retractor muscle

oral tube

oral tube retractor muscle
pleural ganglion
purple-staining area of capsule
gland

pallial opening of oviduct
gonopericardial canal
opening to posterior digestive
gland duct

pedal ganglion

penis

buccal cavity

penial groove

penial duct

epiproboscis

posterior oesophagus
epiproboscis retractor muscle
epiproboscis sheath
peristomal rim

prostate gland

prostatic cells

peristomal rim muscles
pallial opening of prostate
proboscis sheath

rectum

radula

red-staining gland cells
rhynchostome

radial muscle

radular sac

sub-oesophageal ganglion
salivary duct

salivary gland

seminal groove

sperm

supra-oesophageal ganglion
supporting sheath

seminal vesicle

testis

transverse muscle

typhlosole

vagina

ventral channel

valve of Leiblein

ventral odontophoral retractor
muscle

vestibule

MORPHOLOGY OF MITRIFORM GASTROPODS 301

FIG. 2. Strigatella paupercula (Linnaeus). A. A schematic diagram of the odontophore and the
epiproboscis and its associated muscles viewed dorsally. B. Dorsal view of the buccal appara-
tus showing the epiproboscis and its associated dorsal muscles. C. Transverse section of the
posterior part of the mid-oesophagus to show the “typhlosole”. D. The stomach opened dorsally.
E. A transverse section of the muscular portion of the stomach. The cuticle lining is shown in
black. F. A transverse section of the intestinal region of the stomach.

TABLE 1. Radula variation in S. paupercula

of cusps
oat pane Е и = : с
central : the insertion of the dorsal subradular
ent tooth in ee membrane retractor muscle (d.sm.r ).
microns The former muscles radiate dorsally and

tooth denticles)

ventrally and slope obliquely backwards
before becoming attached to the pro-
boscis wall. The posteriorly placed
strands of this muscle are longer anda
little heavier than those in front. A
pair of narrow, ventral odontophoral re-
tractor muscles (v.od.r ) are fixed to
the posterior end of the odontophoral
All specimens from Port Vila, Efaté Is. cartilages, and extend back through the

302 W. F. PONDER

proboscis to eventually anchor them-
selves in the floor of the cephalic cavity.
In addition, a pair of thin, broad, ventral
odontophoral protractor muscles lie be-
low the odontophore and are fixed to the
floor of the buccal cavity in front, andto
the posterior ends of the odontophoral
cartilages behind.

The radular sac (r.s ) is only slightly
longer than the odontophore and opens
out in the usual manner just before
bending downwards over the anterior
ends of the odontophoral cartilages.
The worn radular teeth are presumably
loosened by the subradular membrane,
being resorbed in the ventral pocket at
the distal end of the radula. A thin
strip of muscle runs backwards from
this distal pocket and is attached to the
ventral surface a little in front of the
proximal end of the radular sac.

The radula of Strigatella paupercula
has been described by Cernohorsky
(1966, p 110, fig. 17) but comparisons
of the radulae of several specimens
(see Table 1) has shown that an unusual
amount of variation exists (Fig. 1 D).
Peile (1936) has also shown radular vari-
ation in Mitra cucumerina (Lamarck).

The salivary ducts (s.d ) are narrow
convoluted tubules which lie alongside
the oesophagus and, just before the
oesophagus opens into the buccal cavity,
they enter its walls to lie beneath the
dorsal folds in the usual manner. How-
ever, instead of opening into the buccal
cavity, they pass ventrally as exceedingly
fine ducts which merge just above the
thin-walled sheath of the epiproboscis
(Fig. 3).

The Epiproboscis. This muscular rod
is the most conspicuous feature of the
buccal mass (Figs. 1A, 3, 9A). Itgradu-
ally tapers anteriorly and when retracted
forms an introvert which lies ina sheath
(p.o.s ) beneath and behind the buccal
mass with its posterior portion arching
up to the end of the buccal mass, Thus
the epiproboscis forms a U behind, and
about 1 /2 times the length of, the odon-
tophore. It is translucent yellow in life
with smooth, glossy walls, and is at-

tached to the odontophore just above the
end of the radular sac by a short, bulky
retractor muscle (p.o.r ). This in turn
is fixed to the base of a pair of power-
ful dorsal odontophoral protractor mus-
cles which (Figs. 1A, B; 3B; d.od.p )
are incorporated in the wall of the
buccal cavity and lie on the dorsal sur-
face of the odontophore where they meet.
These muscles appear to have no homo-
logues in other neogastropods,

The whole of the U-shaped portion of
the epiproboscis lies loosely in the
proboscis cavity, except where it passes
through the 2 ventral odontophoral re-
tractor muscles (v.od.r ) to which the
epiproboscis sheath is loosely bound on
its inner (anterior) face by a transverse
muscular connection, It is this connec-
tion, and the posterior continuation of
the ventral odontophoral retractors that
Risbec (1928) refers to asa “horse-shoe
shaped muscle”, although it could more
appropriately be termed hairpin-shaped.
It appears as though this modification
of the odontophoral retractor muscles
serves to aid in the retraction of the
epiproboscis in harmony with the rest
of the buccal mass. It is not essential
in the manipulation of this organ how-
ever as its absence is noted in Pterygia
crenulata (Risbec, 1928) and Imbricaria
spp. (herein).

The structure of the epiproboscis is
shown in Fig. 3, Throughout most of
the posterior U-shaped portion (Fig. 3),
the retracted organ is composed of an
outer sheath containing an external longi-
tudinal layer and an inner layer of cir-
cular fibres. The inner surface of the
ventral part of the sheath (Figs. 3b-d)
is lined with a very thin epithelium

- covered with cuticle, but at the bend in

the U the epithelium crosses the gap
between organ and sheath and becomes
confluent with the epithelium of the non-
introvertible part of the epiproboscis,
which is thus, also, naked behind this
point (Fig. 3a). The epiproboscis has a
central core of longitudinal muscle(l.m ) ©
which is surrounded by circular muscles,
The circular muscle is thick distally,

MORPHOLOGY OF MITRIFORM GASTROPODS 303

FIG. 3. Strigatella paupercula (Linnaeus). Semi-diagrammatic lateral view of the buccal appa-

ratus and the epiproboscis.
epiproboscis (see text).

but longitudinal muscles predominate in
the dorsal arm of the U. A strip of
longitudinal muscle fibres (o.l.m ) lies
dorsally along the whole ventral arm of
the retracted epiproboscis and has its
origin in the posterior mass of longi-
tudinal muscle fibres. This muscle
probably serves to bend the organ, while
the circular fibres cause it to elongate

The positions of the sections a-h are indicated.

a-h sections of

and the central longitudinal muscle core
withdraws it. Small blood spaces (b.v )
lie beneath the epithelium and these
would supply the turgor necessary in
protraction. The sheath remains dis-
connected from the buccal mass almost
to its opening below the mouth where it
is fixed to the outer integument by a few
muscle fibres. The combined outer

304 W. F. PONDER

integument and sheath can form a short
cone (s.s ) which projects forwards and
surrounds a portion of the epiproboscis,
thus acting as a Supporting Sheath. Be-
low the buccal mass the sheath has very
thin walls composed only of the epithe-
lium anda few longitudinal muscle fibres,
but below the buccal cavity itis enclosed
by a muscular tunnel of longitudinal
fibres (Fig. 3c, d).

The salivary ducts (s.d) run on the
upper side of the sheath, just inside the
epithelium, to the bend in the U where,
along with the epithelium, they cross to
the non-invaginable portion of the epi-
proboscis. They then extend, as exceed-
ingly fine ducts, along this organ (Figs.
3b-e) until, just behind its tip, they be-
come embedded in a mass of connective
tissue and scattered longitudinal fibres
(Fig. 31). Here they expand and become
confluent (Fig. 3g) and the combined
duct opens at the tip of the organ, ap-
pearing to be an invagination of the
outer epithelium at this point (Fig. 3h).

The epiproboscis thus functions as an
extensile vehicle for the salivary ducts.
It is likely that the saliva is administered
only in small amounts. The ducts are
very long and narrow, without cilia or
peristaltic muscles to aid the delivery
of the secretion.

On extension the epiproboscis is in-
verted at its posterior end and the re-
tractor muscle becomes surrounded by
the outer sheath. Only partial inversion,
up to the point where the hairpin muscle
is joined to the outer sheath, was ob-
served. Further protraction probably
includes the incorporation of the ventral
odontophoral protractor muscle into the
longitudinal core of this organ, Thus
retraction of the epiproboscis is probably
a 2 stage process, the first being achieved
by the withdrawal, by its contraction, of
the ventral odontophoral retractor mus-
cle from the introvert, and the second by
using this muscle as a pivot, by the
contraction of the epiproboscis retrac-
tor muscle.

The Oesophagus. The anterior oeso-
phagus (Fig. 1, oes ) is adapted for the

passage of large pieces of food. Itisa
wide, oval tube with low, longitudinal
ridges. Above the odontophore the
laterally placed dorsal folds (d.f ) are
readily distinguishable but they become
indistinguishable in the posterior por-
tion of the anterior oesophagus which
is nearly circular in section. The short,
ciliated epithelium has abundant mucous
goblet cells, although these are more
Sparse ventrally in the anterior portion
which lies above the buccal mass, The
oesophageal wall is rather thin and con-
sists of a few outer longitudinal muscle
fibres and an inner circular muscle
layer.

A pair of oblique, glandular pads which
are inclined forwards from the dorsal
surface lie just in front of the nerve
ring and represent the valve of Leiblein,
They are lined with tall mucous cells
of the same type as those occurring in
the valve of Leiblein of other neogastro-
pods. There is no definite indication of
torsion such as occurs in some other
rachiglossans (Graham, 1941). The
anterior oesophageal ridges, however,
terminate at the glandular pads and are
inclined a little to the right, but, as the
dorsal folds are not distinguishable at
this point, and there is no distinct ven-
tral groove, no further direct indication
of torsion could be observed. There
are, however, mid-dorsally in the mid-
oesophagus, a pair of somewhat more
prominent ridges which have a non-
ciliated groove between them. These
ridges are covered with a slightly taller
epithelium than the rest of the mid-
oesophagus and are more richly supplied
with mucous cells. They probably re-
present the dorsal folds in their post-
torsional position, Before the oesopha-
gus leaves the nerve ring, a peculiar
swelling (Fig. 2c), resembling a short
typhlosole, appears in the mid-dorsal
line and is bordered on either side by
the low dorsal folds. These folds
cease at the commencement of the pos-
terior oesophagus immediately behind
the swelling. The swelling which con-
sists of an irregular cluster of small

MORPHOLOGY OF MITRIFORM GASTROPODS 305

cells was observed in all 12 sectioned
Specimens, and in dissected material.
It is sited where the gland of Leiblein
normally opens. That gland is absent
in this species, and the function of the
swelling is obscure, The remainder of
the mid-oesophagus is weakly ridged
and is lined with short, ciliated cells,
and mucous cells.

Behind the nerve ring the oesophagus
rapidly increases in diameter and forms
a wide storage crop behind the cephalic
cavity. The narrower anterior section
has tall, longitudinal ridges covered
with short, columnar cells with pale
cytoplasm and dense, red staining nu-
clei. These cells bear short cilia, and
mucous cells are abundant. At the end
of the pallial cavity the oesophagus
narrows a little below the posterior
pallial floor. Here it is buried in dense
connective tissue, and the epithelium
changes to weakly ciliated cuboidal cells
having dense cytoplasm and large cen-
tral nuclei with prominent nucleoli. Oc-
casional large goblet cells occur, but
otherwise no glandular tissue is present.
In addition the longitudinal ridges be-
come narrower and more irregular than
those in front but when the crop is dis-
tended with food these flatten out to
form a uniformly oval structure. The
outer wall of the oesophagus is very
thin and composed of only a few longi-
tudinal muscle fibres, and a little con-
nective tissue.

The Salivary Glands. These form a
relatively large mass about 0.8 mm in
length which lies over the cerebral
ganglia. They form a single compact
body which can be fairly readily sepa-
rated into 2 lobes. The cells are of 2
types. One has a bluish Staining granu-
lar cytoplasm, and the other is filled
with purplish-red staining granules.
Both types occur with equal frequency
and are arranged in narrow, irregular
tubules. Although the salivary ducts
(Figs. 1B, С; 3; 2B, s.d ) have a ciliated
pavement epithelium near the glands,
they lose this where they come to lie
alongside the oesophagus, and have only

a wall of fibrous tissue.

The Stomach. The oesophagus opens
into a muscular gizzard-like structure
with 10-14 longitudinal ridges lined with
thick cuticle (Figs. 2D; m.r; 2E). A
thick layer of circular muscle surrounds
these ridges which have an epithelium
of cuboidal cells. This region of the
stomach presumably effects the initial
breaking up of the food. As there is no
gland of Leiblein the first important
digestive enzymes commence the break-
down of the food in the stomach. A small
posteriorly pointing area, all that re-
mains of the main gastric lumen, lies
between the oesophageal and intestinal
arms of the stomach and is lined with
columnar cells, the irregular height of
which forms low, broad ridges. The
Opening to the posterior digestive gland
(p.d.o) lies mid-ventrally immediately
behind the muscular region and a trans-
verse channel runs from this opening
across the posterior edge of the mus-
cular area, The anterior digestive
gland duct (a.d.o ) opens near the inner
end of the intestinal region. The intes-
tine (int ) emerges from the stomach on
the right, above the oesophagus. The
intestinal region (i.r ) corresponds tothe
style sac of many prosobranchs. It has
numerous, tall ridges running obliquely
into a shallow groove, while on the
posterior face lies a pair of small folds
or typhlosoles (Fig. 2F; ty). These
typhlosoles are formed by columnar
cells with a few large goblet cells con-
taining refringent secretory masses.
The dorsal epithelium of the intestinal
region consists of small cuboidal cells
with relatively large nuclei, whereas
laterally and ventrally the cells are
even smaller and flattened.

The Digestive Gland. The large poste-
rior (left) lobe of the digestive gland
lies behind the stomach, and the rela-
tively minute anterior (right) lobe in
front. Their short ducts are lined
with a columnar epithelium continuous
with that of the stomach. The digestive
cells vary from 50-70 y in height when
mature, and appear to be of 1 type only,

306 W. F. PONDER

having orange-red-staining granules of
irregular size in the mature state.
“Immature” cells which lie between the
bases of the larger cells have colour-
less granules, and similar granules
occur in the distal borders of mature
cells. Some of the digestive cells have
weak cilia, but the majority are uncili-
ated. Islands of amoebocytes, containing
darkgreen refringent granules, are scat-
tered through the digestive gland. Cells
similar to these are a common occur-
rence in the digestive glands of steno-
glossans (Smith, 1967).

The Intestine. The opening to the in-
testine from the style sac isnot guarded
by a sphincter muscle but an abrupt
change in the epithelium occurs, The
intestine curves downwards beneath the
renal organ, which encompasses it, be-
fore emerging on the right side of the
pallial cavity. A tall columnar epi-
thelium, which contains occasional gland
cells, lines the upper intestine, and
variations in its height form about 6 low,
irregular ridges which differ appreciably
from those of the style sac region. As
the intestine enters the pallial cavity,
red-staining glandular cells suddenly
become abundant in its walls. In the
middle part of the pallial cavity the
gland cells become less numerous and
the cilia longer. This rectal region
(Fig. 4A, Е; г) has many low folds and
continues unchanged to the anus which
is placed some distance back from the
mantle edge.

The Anal Gland. As typical of many
neogastropods, Strigatella has an anal
gland (Fretter, 1946: Smith, 1967). It
is composed of 1-4 tubules which extend
through most of the right pallial wall
(Fig. 4F; a.g ). The weakly cilated cells
are like those in the anal gland of most
other neogastropods and contain brown-
staining granules. These granules are
accumulated in their distal ends which
are eventually nipped off. Amoebocytes
with similar granules are found around
the bases of the cells. The gland opens
just in front of the anus by way ofa

very narrow, ciliated duct lined with
cuboidal cells.

Smith (1967) suggests that amoebo-

cytes carry the granules produced inthe
digestive gland to the anal gland which
then excretes them, and cites as evidence
the presence of amoebocytes carrying
granules around bases of the cells of
the anal gland. In Strigatella, however,
the large, dark green-staining granules
in the digestive gland amoebocytes are
quite different from those in the amoe-
bocytes of the anal gland.
Food. Fragments of sipunculid worms
were found in the crop of several speci-
mens. Strigatella paupercula has also
been observed feeding on sipunculid
worms near Honiara, Solomon Islands,
by Prof. J. E. Morton (pers. comm.).
[After this paper was written, Kohn
(1970) reported on the feeding behaviour
of Strigatella litterata (Pacif. Sci., 24:
483-486), which also feeds on sipun-
culids. |

The Male Genital System

The Testis. The tubules of the testis
ramify through the digestive gland, al-
though they are concentrated on the
ventral side of the visceral mass. Sper-
matozoa are collected into a wide, tight-
ly coiled seminal vesicle (Fig. 4A; s.v )
which is lined with cells varying from
cuboidal to columnar in its upper region.
These cells often contain brown spher-
ules and in some areas their distal
ends are budded off, these being added
to the mass of sperm. Sperm ingestion
was observed taking place in some
groups of cells that had pseudopodial
processes developed on their distal ed-
ges. The anterior coils of the seminal
vesicle are wider and lined with pave-
ment epithelium,

The Vas Deferens. The renal vas defe-
rens has a ciliated epithelium which
forms longitudinal ridges and is sur-
rounded by avery thin layer of connective
tissue. There is no sphincter muscle

MORPHOLOGY OF MITRIFORM GASTROPODS 307

FIG. 4. A-G. Strigatella paupercula (Linnaeus): A. The male genital system, excluding the testis
B. A transverse section of the penis; C, D. Transverse sections of the anterior (C) and poste-
rior (D) parts of the prostate gland; E. The pallial oviduct opened dorsally and viewed from the
right; F. A transverse section of the pallial opening of the oviduct and of the bursa copulatrix.
С. A transverse section of the capsule gland. H. Imbricaria conularis Lamarck: A transverse
section of the ventral channel.

308 W. F. PONDER

separating it from the seminal vesicle
and no gonopericardial duct, eventhough
it is buried in connective tissue of the
pericardial wall.

The Prostate Gland. A prostate gland
(pr ) commences at the posterior end
of the pallial cavity where it receives
the vas deferens, and is lined with tall,
narrow, ciliated cells with small blue-
staining granules and, inaddition, a mass
of similar staining cellsliesbelow. This
posterior portion, which is rather short,
is broader than the remainder of the
gland, and communicates with the pallial
cavity by way of a ciliated slit (Figs. 4A,
D; pr.o ). The rest of the gland (Figs.
4A, C) has an enclosed duct, and the
glandular cells have larger, round nu-
clei. Their secretory granules stain
pale pink. There is no indication ofa
line of fusion of an originally open
groove as seen in some muricids (Fret-
ter, 1941). Nearer the penis the gland
becomes narrower and consists of the
duct lined with short columnar cells, and
a few blue-staining sub-epithelial cells
scattered around it. This portion of the
male system corresponds to the ejacu-
latory duct. Itis about 150 »indiameter,
with a wide lumen, and continues un-
changed bulging from the pallial wall,
into the base of the penis.

The Penis. The penis (pen ) lies behind
the right cephalic tentacle. It is rather
elongate when at rest, oval in section,
slightly narrower at its base than in
the middle region, and tapers to a blunt
point. Its outer epithelium consists of
small cuboidal cells which are covered
with a thin layer of cuticle in the basal
portion, but have very short cilia dis-
tally. The penial duct (Fig. 4B; pn.d )
resembles the ejaculatory duct, apart
from being a little narrower, and fol-
lows a rather irregular path until it
opens at the distal tip of the penis.
This duct lies just outside a wide, cen-
tral area loosely filled with variously
orientated muscle fibres and surrounded
by a ring of circular muscle. This cen-
tral area is primarily a blood space
and probably plays a major part in the

elongation of this organ. The rest of
the penis consists of a mass of connec-
tive tissue and muscle fibres in which
lie loosely packed, blue-staining cells
like those surrounding the ejaculatory
duct (Fig. 4B).

The Female Genital System

Risbec (1928) and Quoy & Gaimard
(1833) both briefly mention the pallial
oviduct of the mitrids they examined,
but no detailed account has been given
of the reproductive apparatus of any
mitrid,

The Ovary. The ovarian tubules of S.
paupercula ramify through the digestive
gland and tend to occupy most of the
upper visceral mass when mature. The
eggs are of moderate size (up to0.3 mm
diam.) and are filled with large yolk
granules.

The Upper Oviduct. The upper oviduct
is a straight tube lined with irregular,
non-cilated columnar cells with central
nuclei. These become cilated and form
longitudinal ridges as the oviduct passes
along the wall of the pericardium,
but there is no gonopericardial duct.
A few muscle fibres surround the
walls of this rather short portion of the
oviduct which is a little narrower (140-
160 y in diameter) than the upper ovi-
duct. The renal oviduct enters the
albumen gland (Fig. 4E; alb ) a little in
front of its posterior end.

The Albumen Gland. A more or less
straight, ciliated channel lies on the
floor of the albumen gland and its thick
glandular walls have the same type of
histology as certain other rachiglossans
(Fretter, 1941). This gland is taller
than it is long, and its ventral, ciliated
channel continues as a short, wide, non-
muscular duct into the capsule gland
(cap), as the ventral channel of that
organ.

The Ingesting Gland. The duct of the
ingesting gland (i.d) is a dorsal out-
growth of the duct between the capsule
and albumen glands and both are lined
with a ciliated, cuboidal eipthelium.
This duct arises on the outer (right)

~

MORPHOLOGY OF MITRIFORM GASTROPODS

side of the oviduct and opens into the
ingesting gland (i.g ) dorsally. The upper
portion of the duct, about 250 y wide,
is surrounded by a thin muscle layer,
absent from the more ventral portion,
and contains masses of orientated sperm,
The ingesting gland is a spacious cavity
divided into 2 lobes by the intervention
of its duct. It is lined withlarge colum-
nar cells very like those seen in most
other Neogastropoda (Fretter, 1941).
They have yellowish-brown-staining cy-
toplasm and are 100-200 и in height.
Sperm lie in irregular masses, or in
large orientated bundles like those in
the upper part of the duct, and are in-
gested, along with yolk granules, by the
epithelium.

The Capsule Gland. The capsule gland
(Figs. 4E, G; cap ), which occupies most
of the pallial oviduct, is oval in section,
with thick lateral lobes which have the
epithelium organized in the same way as
in the rachiglossan species investigated
by Fretter (1941). Several glandular
regions in the capsule gland are indi-
cated by their different staining proper-
ties, although these are variable in
extent in different specimens. A pale-
blue-staining area (b.a) lies in the
posterior region of the gland, this being
bordered in front by 2 transverse strips
of non-staining mucous cells(m.a ) which
are followed by a purple-staining zone
(p.a ). The middle part of the gland
(Fig. 4G) has a lateral reddish-orange-
staining area (0.a ) bordered above and
below on both sides by a narrow wedge
of blue-staining cells (b.a ) and, on the
dorsal wall, by a wide strip of colour-
less mucous cells (m.a ). This latter
zone is unlike the other glandular areas
in being a simple epithelium which is
folded into shallow alveoli and has cili-
ated cells throughout. The other areas
have ciliated cells only in the outer
layer of columnar epithelium and have
thick, multicellular glands lying below.
The ventral channel (v.c ) is rather
wide, lined with a cuboidal, strongly
ciliated epithelium 20-25 y thick and is
overhung by a Single fold on the left

309

(1f). A low ridge on the right (a.v.1 )
is also distinguishable and is probably
homologous with the right foldin Alcithoe
(Ponder, 1970) and the antero-ventral
lobe in Nucella (Fretter, 1941). There
is no trace of a right ciliated fold. In
the anterior part of the capsule gland
the dorsal mucous zone migrates down-
wards to occupy all of the lateral gland-
ular surface at the anterior end of the
gland. A ciliated channel lined with
blue-staining gland cells only 50 y high
commences in the mid-dorsal line near
the anterior end of the capsule gland
and rapidly spreads to occupy all of its
dorsal wall.

The Vestibule and Vagina. The oviduct
narrows in front of the capsule gland
and is lined by simple, ciliated, colum-
nar cells and scattered mucous cells.
This portion of the oviduct (Fig. 4E;
vest ) is longitudinally ridged and quite
short. It lies on the inner side of the
bursa copulatrix and corresponds to the
vestibule in the species investigated by
Fretter (1941).

The vestibule rapidly narrows until
only the ventral channel remains, At
this point it is surrounded by a thick
layer of circular muscle fibres and be-
comes the vagina (va). Two dorsal
ridges of ciliated cells persist which
represent the 2 lateral walls of the
vestibule, and they contain occasional
large goblet cells. The ventral wall of
the vagina is lined with a non-ciliated,
pavement epithelium. The interior of
the whole structure is only 0.1 mm in
diameter,

The short vagina opens into the pallial
cavity (Fig. 4F) a little behind the anus,
and the gonopore is surrounded by a thick
muscular lip covered with small cuboidal
cells containing fine, brownish-staining
granules and very elongate nuclei. These
cells are strongly ciliated and merge
with the epithelium of the distal section
of the vagina which consists of cells
with longer cilia, pale blue-staining
cytoplasm, and oval nuclei.

The Bursa Copulatrix. The opening to
the bursa copulatrix (b.c ) lies above the

310 W. F. PONDER

gonopore. Its short, ciliated duct is
made up of a series of irregularly folded,
low muscular ridges which extend, with-
in the bursa, almost to the anterior
limit of this organ. These ridges in-
crease in size and gain additional mus-
culature as they approach the inner
bursal aperture, but do not extend much
behind it. The bursa copulatrix is an
oval body, circular in section and about
0.7 mm in diameter in its middle, It
commences just behind the anus and its
rather thin, but muscular, walls contain
both longitudinal and circular fibres. The
lumen is subdivided by a number of ir-
regular lamellae which are penetrated
by muscle fibres and lined with small,
dense, cuboidal cells covered with cuti-
cle. Occasionally it is packed with
orientated and unorientated sperm, the
former attached by their heads to the
cuticle, This structure thus presumably
acts as a Sperm receiving organ.

The Pedal Gland. A small ventral
pedal gland is present but is not obvious
in preserved material. It is a deep
depression situated a little behind the
anterior edge of the foot and has 3-4
layers of red-staining subepithelial gland
cells clustered above the pedal epithe-
lium which is, in this region, a little
shorter than that over the rest of the
sole.

IMBRICARIA SPECIES

Imbricaria conularis (Lamarck)

1811 Mitra conularis Lamarck, Ann,
Mus. Hist. Nat., 17, p 219.

1965 Imbricaria conularis; Cernohor-
sky, Veliger, 8: 154, pl. 23, fig. 131,
text fig 11;

Material was collected at Port Havan-
nah, Efate. Is., New Hebrides, on sand-
strewn coral rock just below low tide,

Imbricaria conovula (Quoy & Gaimard)

1833 Mitra conovula Quoy & Gaimard,
Voy. Astrolabe, Zool., 2: 655, pl. 45b,
figs. 18-22.

1963 Imbricaria conovula; Cate, Veliger,
6: 41, pl. 8, figs. 55-56.

Material collected at Meslep, Efaté
Is., New Hebrides, just below low tide
on coral sand,

All of the specimens were, unfor-
tunately, in a fairly fragmentary state
owing to the difficulty of removing the
animal from the shell without damage.
Four specimens of I. conularis were
sectioned and 1 of J. conovula was dis-
sected,

The external appearance of the living
animal and the radula of J. conularis
have been described by Cernohorsky
(1965, p 155). The animal differs from
Strigatella species in not having the
dorsal side of the foot heavily pigmented
and in details of the radula. The absence
of considerable head-foot pigmentation
was also noticed in /. conovula and in
Mitra species.

The mantle cavity is similar to that
of Strigatella and although the overall
plan of the alimentary canal and repro-
ductive systems is very similar, there
are some differences. The proboscis
has only been observed in the retracted
state, in which it is relatively wider
and shorter than in Strigatella and a
greater development of the retractor
muscles and thickness of the proboscis
walls are apparent. The buccal mass,
which is contained within the fully re-
tracted proboscis in Strigatella, pro-
trudes into the cephalic cavity in /m-
bricaria (Fig. 9C) and the much longer
epiproboscis is loosely folded behind.
This organ is attached to the posterior
end of the odontophore by several thin
muscles which run to several points on
the odontophore, including the base ofthe
large dorsal odontophoral protractor
muscles, The ventral odontophoral re-
tractor muscles are not connected tothe
epiproboscis as they are in Strigatella,
but a muscular cavity houses the organ
below the entire length of the odonto-
phore, whereas in Strigatella it is only
enclosed below the buccal region. The
detailed structure of this organ, how-
ever, is very like that of Strigatella.
The salivary ducts are relatively much
wider and less convolute than in Striga-

MORPHOLOGY OF MITRIFORM GASTROPODS 311

tella and the glands have fewer red-
staining cells than pale cells.

The radula of J. conularis (=I. conica)
has been figured by Thiele (1929, p 341,
fig. 402) and Cernohorsky (1965, 1966),
and that of J. conovula, which has not
previously been illustrated, is here fig-
ured for comparison with that species
(Fig. 1E).

There is no sign of the peculiar
“typhlosole” or of a valve of Leiblein
in the mid-oesophagus, andthe glandular
epithelium of that region is more thickly
developed than in Strigatella. The sto-
mach and crop are similar to those in
Strigatella, although the crop does not
appear to be ciliated, and the intestinal
region of the stomach has only a fewlow
ridges developed. The digestive gland,
rectum and anal gland are like those of
Strigatella. The crop and rectum con-
tained radula teeth of what appear to
be turrid and rhipidoglossan gastropods,

The genital systems of I. conularis
differed in some respects from those
of Strigatella. No information about
these systems was obtained from the
specimen of 1. conovula. The tightly
coiled seminal vesicle was lined with
an epithelium varying from cuboidal to
Squamous, but no indication of sperm
ingestion was seen. A gonopericardial
canal could not be identified inthe avail-
able material. The prostate gland, al-
though relatively narrower, hadthe same
structure as in Strigatella. The ejacula-
tory and penial ducts, however, are sur-
rounded by a thick layer of circular
muscle, and also retain the ciliated
epithelium seen in Strigatella. The penis
is relatively much longer than in Striga-
tella, and has the same structure.

The ovary and ova are like those of
Strigatella. The presence or absence
of a gonopericardial canal could not be
verified. The albumen gland, ingesting
gland and its duct, and the capsule gland
all appeared to be the same as in Stri-
gatella, although the ventral channel of
Imbricaria (Fig. 4H) has an additional

short, ciliated fold on the right. In
marked contrast to Strigatella, the bursa
copulatrix of Imbricaria has a massive,
muscular, internally ridged wall and the
pallial opening is wider. It opens directly
into the bursa and to the vestibule by
way of a short, but very narrow vagina
buried in the bursal wall. The pedal
gland, as far as can be judged from
sectioned material, is relatively larger
than that structure in Strigatella.

In summary the anatomy of Imbricaria
Species differs from that of Strigatella
in the relatively longer epiproboscis,
shorter proboscis, small differences in
the buccal musculature and in the lack
of a typhlosole and valve of Leiblein on
the mid-oesophagus. The muscular
sperm duct and the massive, internally
ridged bursa copulatrix are the main
features of the reproductive tracts that
differ from Strigatella.

MITRA SPECIES

The proboscides of several species of
Mitra have been examined and these are
of the same general plan as that of
Strigatella paupercula. These species
include: M. mitra (Linnaeus), Apia, Sa-
moa (Fig. 9B); M. stictica (Link) Nuie;
M. eremitarum Röding, Malekula Is.,
New Hebrides; M. chrysostoma Brode-
rip, Port Vila, Efaté Is., New Hebrides;
M. nigra (Gmelin), Long Reef, New
South Wales. Some variation in the
relative size of the buccal mass and
epiproboscis and in the development of
the peristomal rim was observed (Table
2), but there was remarkable conformity
to the plan found in Strigatella. Inall
cases, the proboscis was long and, when
retracted, folded into the proboscis sac.
The proboscis of M. chrysostoma was
sectioned and found to be of nearly iden-
tical structure to that of Strigatella.

The peristomal rim reaches its great-
est development in M. stictica where it
overhangs the relatively minute mouth,
Its anterior surface is strongly pleated
and has quite a different appearance
from the outer surface. This rim also
reaches a greater development in the

312 W. F. PONDER

TABLE 2. Relative dimensions of the shell, buccal mass and epiproboscis
in Mitra species.

Species

. mitra
M. stictica
M. eremitarum

. nigra

Length of buccal
mass (excluding
buccal cavity)

Length of retracted
epiproboscis behind
buccal cavity

4mm

4 mm

Each measurement based on a single specimen.

other species of Mitra in comparison
with Strigatella.

PART 2

AUSTROMITRA RUBIGINOSA (Hutton)

1873 Columbella (Atilia) rubiginosum
Hutton, Cat. Mar. Moll. N.Z., p 20.

1913 Vexillum rubiginosum; Suter, Man.
N.Z. Moll., p 366, pl. 18, fig. 7.

1927 Austromitra rubiginosa; Finlay,
Trans.“ N. АВЕ, 57-410:

1970 Austromitra rubiginosa;C ernohor-
sky, Bull. Auck. Inst. Mus, 8: 57, pl.
10, figs. 5-10.

Austromitra rubiginosa lives beneath
stones in the lower littoral throughout
New Zealand. It feeds, as also recorded
by Morton & Miller (1968), on various
species of tunicate, both solitary and
compound, and its egg capsules are
found embedded in their tests.

The black shell is usually about 8 mm
in length, although it occasionally reach-
es a height of 10 mm, has a tall spire
with weak axial ribs, and a narrow white
band just below the periphery. The
orange columella has 4 strong plaits,
and the aperture has a short anterior
canal. This species shows considerable
regional variation, particularly in shell
colour and in the strength of axial rib-

bing. The material examined was col-
lected at Leigh, northof Auckland, where
it occurs with a closely allied species,
A. rubiradix Finlay?

The living animal has a moderately
long, slender siphon which projects well
beyond the short anterior canal of the
shell aperture, A broad, black band en-
circles the basal half of the siphon, the
rest being white. There are black,
radiating patches which are variable in
number and pattern onthe dorsal surface
of the foot, and the rest of the foot is
translucent-white with opaque-white
spots. Long tentacles with black or
grey bases lie on either side of the head
which is black or grey dorsally, the
rest being white. There is no trace of
an operculum. The foot has short
lateral projections anteriorly and a slit,
the anterior mucous gland aperture,
across the front edge. The head-foot
of A. rubiradix differs from rubiginosa
in having much more black pigmentation.

The mantle cavity has no unusual fea-
tures. A large, pale brown osphradium
lies on the left alongside the ctenidium
which has triangular filaments, their
bases slightly narrower than their height.
The hypobranchial gland secretes a
dense, pale yellow-green secretion, and
cells of this colour are scattered amongst
opaque-white and colourless cells. All

2Cernohorsky (1970: 57) regards A. rubiradix as a synonym of A. rubiginosa.

MORPHOLOGY OF MITRIFORM GASTROPODS 313

cell types occur in approximately equal
numbers and have a rather even distri-
bution throughout the gland, The mantle
ciliation is normal in pattern, with a
particularly strong exhalant current on
the right side which carries waste ma-
terial to the exterior.

The circum-oesophageal ganglia are
shown in Fig. 6D (p 319). Concentration
is fairly advanced although all of the
ganglia except for the pleurals are
separate. The supra-oesophageal gang-
lion has a rather long connective but
the sub-oesophageal ganglion is very
close to the right and left pleural gang-
lia. The cerebral ganglia are joined by
a very short, broad commissure,

The renal organ resembles that of
Nucella and Buccinum in Perrier’s (1889)
pycnonéphridiens in having the primary
and secondary renal lamellae intermin-
gled.

The Alimentary Canal

The Proboscis. When retracted the
short, broad pleurembolic proboscis
(Figs. 5A, 9D) has the posterior part
of the buccal mass projecting from its
inner end. The rather muscular pro-
boscis sheath is attached in front to
the cephalic cavity by a ring of retrac-
tor muscles and forms the basal part
of the proboscis when it is protracted.
Although repeated attempts were made
to induce the animal to feed in the labo-
ratory, they were not successful, so the
total length of the extended proboscis
and the feeding mechanism were not
observed. It appears, however, that
the proboscis is not capable of great
elongation.

Cuboidal cells covered with cuticle,
and abundant goblet cells make up the
outer epithelium of the proboscis and
its sheath, apart from the anterior por-
tion of the latter which is ciliated. The
proboscis wall consists of a thin outer
layer of circular muscle and an inner
longitudinal layer. This wall is thinner
at the anterior end and there are a few
Subcutaneous gland cells amongst the
underlying connective tissue and longi-

tudinal fibres. When the proboscis is
opened the delicate, narrow oral tube
(o.t ) leading from the minute mouth can
be seen. A thin-walled oral invagination
has a cuboidal epithelium continuous with
that of the outer wall, and this short
tube opens into a rather muscular, very
narrow part of the oral tube. The minute
accessory Salivary gland duct opening is
on the antero-ventral edge of this mus-
cular part of the oral tube, which is
also rather short and is joined to the
proboscis wall by a series of thin,
radiating retractor muscles(o.t.r ). The
anterior invaginated portion is connected
by only a few thread-like fibres. The
muscular part of the oral tube has a
ciliated, cuboidal epithelium, but behind
this region the cuboidal epithelium is
non-ciliated and the oral tube very thin-
walled and concertinaed against thebuc-
cal cavity. This part of the tube lies
loose in the proboscis cavity, but the
buccal cavity is firmly fixed to the pro-
boscis wall by numerous, thin, short,
buccal tensor muscles. The buccal
walls are very muscular, and are lined
with cuticle ventrally, whereas those
above remain ciliated. Presumably the
odontophore traverses the entire oral
tube, but it is not clear how this is
achieved,

The salivary ducts migrate down the
sides of the small buccal cavity to open
latero-ventrally near its anterior end.
The moderately large odontophore (od )
protrudes into the buccal cavity. Well-
developed muscles surround the large
cartilages and a rather slender odonto-
phoral retractor muscle (Fig. 9, p 331
od.r ) runs from the posterior end of
the odontophore to the floor ofthe cepha-
lic cavity. Although functionally a single
muscle, it consists of partially fused
right and left elements. The rather
broad radular sac is the same length
as the odontophore and the teeth are
very like those of the genus Vexillum.
These consist of 2, curved, simple,
lateral teeth and a broad central tooth
in each row. The central is slightly
arched and has 15 pointed cusps (Fig.

314 W. F. PONDER

5B). A. rubiradix has the same number
of cusps on the central, but the lateral
teeth bear very minute denticles (Fig.
SE). There is no epiproboscis.

The Oesophagus and Salivary Glands,
The first portion of the anterior oeso-
phagus has muscular walls consisting
of an inner longitudinal and an outer
circular layer, but the posterior part
has very thin walls. Short, ciliated
cuboidal cells cover the prominent dor-
sal folds of the anterior oesophagus,
while the non-ciliated ventral channel and
the longitudinally ridged dorsal food
gıoove are lined with cuboidal epithe-
lium. Only a few goblet cells can be
found in the anterior oesophagus, this
being in marked contrast to the situation
found in Strigatella.

The wide salivary ducts are about
50 y in diameter and lie buried in the
dorsal folds which they enter just in
front of the valve of Leiblein. They
are lined with ciliated cuboidal cells,
and the short, free sections of the ducts
are surrounded by a few circular mus-
cle fibres. The ducts enter the large
glands (s.g ) near their antero-median
edges. They lie mostly on the left and
in the middle of the cephalic cavity and
cover most of the anterior, and some of
the mid-oesophagus. Each gland con-
sists of close-packed, semi-discrete
tubules which are made up of cells
containing masses of purple-red-stain-
ing granules,

The accessory salivary glands(a.s.g )
are large vesicles up to 250 и in dia-
meter which are lined witha non-ciliated
pavement epithelium, and outside this,
a coat of inner longitudinal muscles and
outer circular muscles, Each vesicle
is filled with a pale-blue-staining se-
cretion derived from a mass of gland
cells lying outside the muscle layers.
These cells are in 2-3 layers and stain
bluish-purple. The structure of these
glands is thus very like the accessory
salivary glands of Alcithoe (Ponder,
1970 ) and many other rachiglossans.
The ducts of the accessory salivary
glands (a.s.d) are lined with a non-

ciliated, cuboidal epithelium and are
surrounded initially by a few circular
muscle fibres, outside of which is a
Single layer of gland cells. As the
ducts approach the proboscis they lose
the glandular tissue, become narrower
and eventually join below the odonto-
phore to form a single, very narrow,
coiled duct.

The valve of Leiblein (v.l) is a rela-
tively large bulb about 260 и in diameter.
Its thick glandular walls consist of 2
different-staining regions as is normal
in this structure (Graham, 1941; Wu,
1965). The anterior portion consists of
tall, colourless to pale blue-staining
cells which bear very long cilia, whereas
the posterior portion has taller cells
that stain dark purplish-red to purplish-
blue and have short cilia. Very long
cilia, which arise from a ring of colum-
nar cells at the posterior rim of the
anterior oesophagus, mingle with those
of the first glandular region to forma
cone-like mass in the middle of the
valve, but there is no projecting rim
derived from the anterior oesophagus as
there is in the muricids (Graham, 1941;
Wu, 1965) and in Alcithoe (Ponder,
1970). The ventral groove of the ante-
rior oesophagus remains as a ventral,
non-ciliated slit throughout the valve of
Leiblein, Just behind the valve the mid-
oesophagus suddenly narrows and passes
through the nerve ring and its walls
become thin with weak longitudinal rid-
ges. The ventral groove is represented
by a narrow, non-ciliated ventral strip
with low dorsal folds lying on either
side. The remainder of the epithelium
is ciliated and has abundant goblet cells,
but as the mid-oesophagus nears the
posterior side of the nerve ring these
become less common, Behind the nerve
ring the mid-oesophagus suddenly ex-
pands, its walls becoming thick and
glandular. This epithelium is made up
of tall gland cells containing irregular
granules that appear semitranslucent
white in life, but stain purplish-red,
and these alternate with short, wedge-
Shaped ciliated cells. Torsion occurs

MORPHOLOGY OF MITRIFORM GASTROPODS 315

0.5mm

FIG. 5. A-D. Austromitra rubiginosa (Hutton): A. Anterior alimentary canal; B. Radular teeth
(Leigh, north of Auckland); C. The portion of the mid-oesophagus just behind the nerve ring
showing torsion; D. The stomach opened dorsally. E. Austromitra rubiradix Finlay. Radular
teeth (Leigh, north of Auckland). Е. Vexillum luculentum (Reeve). Mid-oesophagus ventral
view. G-H. Vexillum plicarium (Linnaeus): G. Mid-oesophagus, dorsal view; H. Radular teeth
(Port Vila, Efaté Island, New Hebrides).

316 W. F. PONDER

just behind the commencement of the
glandular region (Fig. 5C) so that the
now weakly ciliated, thin-walled, dorsal
food channel (d.c ) lies ventrally. The
ventral groove is completely obliterated
by the glandular epithelium covering
the entire pretorsional ventral and la-
teral walls. The pretorsional upper
edges of the dorsal folds persist as
columnar ciliated cells throughout the
remainder of the mid-oesophagus, this
being rather long and folded up in the
cephalic cavity behind the salivary glands
and in front of the gland of Leiblein.

The very short duct of the gland of
Leiblein opens on the right ventral side
of the mid-oesophagus at the end of the
glandular region. This position is unu-
sual in the Neogastropoda, since inmost
other species the duct opens dorsally.
The duct has the 2 pretorsional ventral
oesophageal folds lying on its posterior
surface, and these run obliquely into
the dorsal side of the posterior oeso-
phagus where they disappear. The duct
is lined with a continuation of the epi-
thelium making up the gland of Leiblein
and the ventral folds, the latter nearly
entering the gland before they terminate.
The unusual orientation of this duct
suggests that it has beenforced ventrally
by the glandular development of the mid-
oesophagus following the occlusion of the
ventral groove.

The gland of Leiblein (g.1 ) lies on the
right side of the posterior oesophagus
and is an elongate, pyriform body, dark
greenish-brown in life, transversely
wrinkled, with the anterior end, from
which the duct leaves, bent back on
itself on the left side of the gland. Its
lumen is subdivided into semi-tubular
compartments by thin, muscular parti-
tions. The whole of the gland is lined
with tall gland cells which nearly fill
the lumen and it is surrounded by a
thin, muscular coat. The gland cells
have basal nuclei and many bear short
cilia. They appear to undergo a secre-
tory cycle commencing with short cells
with orange-red to brownish-staining
granules in a purplish-blue-staining cy-

toplasm, As the cells enlarge the
granules increase in quantity, and when
almost at full size green-staining gran-
ules appear. These accumulate with
the other granules at the distal ends of
the cells and at this stage the cilia
appear to be lost. A vacuole then
generally appears below the distal gran-
ular mass which is budded off while the
red granules re-accumulate in the basal
part of the cell and the cycle recom-
mences. The distal end of the gland
is a Single tubule, the epithelium of
which is not actively glandular but other-
wise resembles that of the rest of the
gland,

The posterior oesophagus (p.oes) is a

narrow, thin-walled tube with no dis-
tinct crop region. It is surrounded by
a few muscle fibres and there are about
6 longitudinal ciliated ridges. There
are afew large goblet cells, but other-
wise it is non-glandular. The spherules
from the gland of Leiblein and the gran-
ular secretion from the mid-oesophagus
can be observed in its lumen,
The Stomach and Digestive Gland. The
rather small, U-shaped stomach (Fig.
5D) has a very delicate outer wall. The
oesophagus (oes ) opens into the stomach
on the left side and the intestine emer-
ges alongside on the right. Posteriorly
there is a short caecum (cae ) whichhas
numerous radiating folds on its walls.
The intestinal half of the stomach is
occupied largely by a style sac (i.r ).
This has 2 dorsal typhlosoles and a low
transverse ridge which marks its poste-
rior limit. Alongside the posterior edge
of this ridge a groove leads to the single
digestive gland aperture (c.d.o ) which
lies in the middle of the stomach at the
bend in the U. Thus it lies in close
proximity to both the style sac and the
opening to the oesophagus. The ciliated
gastric epithelium consists mainly of
columnar cells, and there are no cuticle-
lined surfaces.

The digestive gland duct divides into
2 just below the stomach, the dorsal
branch passing to the small anterior
lobe of the gland which lies above the

MORPHOLOGY OF MITRIFORM GASTROPODS 317

intestinal part of the stomach, and the
other branch running to the massive
posterior lobe. The epithelium of the
digestive gland is like that of Striga-
tella, but there were none of the amoebo-
cytes, which characteristically store
greenish granules, present in the diges-
tive glands of the 4 specimens sectioned.
The Intestine and Anal Gland. The in-
testine runs from the stomach through
the renal organ and along the right
pallial wall. It is lined with columnar
cells bearing long cilia. Numerous yel-
low to orange-staining gland cells occur
in the rectum,

The anal gland (Fig. 6C; a.g ) is re-
presented by only a Single tubule which
lies above the rectum and opens into it
at the level of the anal aperture. Its
cells are cuboidal or short-columnar
and non-ciliated, with large spherical
nuclei and dense yellowish-brown gra-
nules in the cytoplasm. Unlike the usual
type of anal gland epithelium they do
not appear to bud off their apices.

The Male Genital System

The Testis and Vas Deferens. The
testis lies on the ventral surface of the
visceral mass where its tubules form
a compact mass and do not ramify
through the digestive gland. The vas
deferens is swollen into a coiled seminal
vesicle which is lined with pavement
epithelium and does not appear to ingest
sperm. It is confluent witha moderately
wide, ciliated duct, the renal vas defe-
rens, which is longitudinally ridged and
opens into the prostate gland at the
posterior end of the pallial cavity. There
is no gonopericardial canal.

The Prostate Gland. The initial portion
of the large prostate gland (Fig. 6A; pr )
has an enclosed, non-ciliated lumen with
the renal vas deferens buried in its
inner wall. At the point where this
opens, the lumen of the prostate gland
‚becomes ciliated and a short fissure is
formed ventrally. The greater part of
the prostate is, however, an enclosed
tube, circular or oval in Section and
about 0.34 mm in diameter with a very

narrow, ciliated lumen. There is no
trace of a line of fusion such as that
seen in Ocenebra (Fretter, 1941). The
prostatic cells which contain purple-red-
Staining granules, are arranged in an
irregular mass around an inner epithe-
lial layer. This inner layer is similar
in staining properties to the rest of the
prostatic cells, but its cells are colum-
nar in shape and alternate with ciliated
cells.

The prostate becomes narrower inthe

anterior part of the pallial cavity where
it passes on to the floor of the cephalic
Sinus as the ejaculatory duct. This duct
is not muscular and is surrounded by a
glandular epithelium which stains blue
near the base of the penis,
The Penis. The massive penis (pen )
lies on the right side of the body at the
base of the pallial cavity. It is oval in
section and tapers to a blunt point at
which the duct opens. The outer surface
is covered with a thick layer of cuticle
which is secreted by a cuboidal epithe-
lium. Immediately belowthis epithelium
is a thin layer of circular muscle which
surrounds the bulk of the penial tissue.
This consists of an interwoven mass of
variously orientated muscle fibres
amongst which are minute blood spaces
and connective tissue, The ciliated
penial duct has a fairly wide lumen and
is central in position.

The Female Genital System

The Ovary. The ovary contains large
ova up to about 300 и in diameter which
have large yolk granules. The ovarian
tubules remain separate from the diges-
tive gland. The upper oviduct is short
and straight, and has an irregular, non-
ciliated columnar epithelium. The rather
short renal oviduct is lined with tall
ciliated cells and, althoughit crosses the
pericardial wall, there is no gonoperi-
cardial duct.

The Albumen Gland. The posterior end
of the albumen gland (Fig. 6B; alb )
bulges into the anterior wall of the renal
organ and has a simple glandular epi-
thelium up to 140 u thick consisting of

318 W. F. PONDER

a Single layer of cells. The renal ovi-
duct opens near the anterior end of the
albumen gland and, at this point, the
glandular epithelium changes from pur-
plish-blue to very pale pink-staining
cells. These give way ventrally to a
groove lined with a cuboidal epithelium,
This groove is continuous with the ventral
channel of the capsule gland. The pale
pink-staining lateral walls are continuous
between the capsule gland and the albu-
men gland, though there is a change to
a bright red-staining region at the com-
mencement of the capsule gland.

The Ingesting Gland. The ingesting
gland duct opens into the ventral chan-
nel between the junction of the albumen
and capsule glands on their outer side,
It is like that of Strigatella, but has 1 or
2 very prominent longitudinal folds inthe
upper half. As inStrigatella it opens into
the ingesting gland dorsally. This gland
(1.5) is also like that of Strigatella,
being a simple pouch lined with tall
cells with large spherical, basal nuclei.
Groups of orientated spermatozoa from
the bursal duct lie in the lumen of the
gland amongst masses of unorientated
sperm which are ingested by the epi-
thelial cells. These cells contain bluish-
purple-staining vacuolate cytoplasm, but
have no yellow granules like those typi-
cally seen in many rachiglossans.

The Capsule Gland, The capsule gland
(cap ) closely resembles that of Striga-
tella and shows similar zones in the
posterior part. Owing to the smaller
size of this species, however, the epi-
thelium is nearly all of the simple
glandular type, only the mid-lateral
walls of the middle region of the capsule
gland having a complex glandular epithe-
lium such as that seen in most larger
rachiglossan species. The middle re-
gion of the gland differs slightly from
that of Strigatella as there is anorange-
red-staining zone in the lower half
separated by a narrow wedge of blue
cells from a dorsal, pale pink-staining
area,

The ventral channel is lined with a
ciliated epithelium and differs from
that of Strigatella in having a bilobed
left, and a single right ciliated fold

overhanging it. In addition, through
most of its length there is a low ciliated
ridge along its centre.

The Vestibule, Vagina and Bursa Copu-
latrix, The anterior region of the
oviduct is also like that of Strigatella
in general plan. An anterior, vertical
strip of pale pink-staining glandular epi-
thelium up to 120 y in thickness, gives
way suddenly to a thin-walled vestibule
with narrow, longitudinal ridges and is
lined with short columnar and cuboidal
cells which have only a few mucous
cells amongst them. The vestibule
rapidly narrows until it is only a nar-
row, ventrally placed tube (va ). This
has a thin muscle coat and is lined
with columnar cells laterally and dor-
sally, but cuboidal cells ventrally. These
latter cells are continuous with the ven-
tral channel of the capsule gland, This
tube, the vagina, lies below and on the
outside of a long muscular bulb, the
bursa copulatrix (b.c ). Both the vagina
and the bursa copulatrix open at the
large pallial opening or gonopore, which
is located just behind the anterior ex-
tremity of the bursa. The walls of the
gonopore are heavily folded and lined
with ciliated columnar cells. Behind
the gonopore the cells are covered with
cuticle. Masses of spermatozoa lie with
their heads embedded inthe bursal walls,
but are also found free in the bursal
lumen and attached to the walls of the
anterior part of the vagina. There was
no indication of a ventral pedal gland in
either of the 2 mature females sectioned,
The Egg Capsules. Egg capsules (Fig.
6E) are found throughout most of the
year embedded in the tests of various
species of compound and colonial tuni-
cates. They are transparent, horny
and hemispherical, with the flat side
outermost. Usually 3-5 eggs are in-
cluded in each capsule and as many
embryos develop, so that no cannibalism
appears to occur. The juveniles escape
by making an irregular rent in the outer
surface of the capsule. They are white |
and have no operculum. The shells
consist of the pink protoconch of 2
whorls, and at this stage they have 3
columellar plicae.

MORPHOLOGY OF MITRIFORM GASTROPODS 319

0-2 5mm 5р.о

FIG. 6. А-Е. Austromitra rubiginosa (Hutton): A. A diagram of the pallial part of the male genital
system, including a transverse section of the prostate; B. A diagram of the pallial oviduct seen
from the right; C. A transverse section of the bursa copulatrix and vagina; D. A diagram of
the circum-oesophageal ganglia viewed dorsally with the cerebral ganglia separated and spread
apart; E. Dorsal and lateral view of egg capsule. F. Vexillum plicarium (Linnaeus). A dia-
gram of the pallial part of the male genital system. G. Vexillum luculentum (Reeve). A dia-
gram of the right side of the pallial oviduct. H. Strigatella paupercula (Linnaeus). A diagram
of the circum-oesophageal ganglia viewed dorsally with the cerebral ganglia separated and
spread apart (for explanation see fig. D).

320

VEXILLUM LUCULENTUM (Reeve)

1845 Mitra luculenta Reeve; Conch. Icon.
pl. 30 sp. 245.

1965 Pusia luculenta; Cernohorsky, Ve-
liger, 8: 147, pl. 22, fig. 122.

1966 Vexillum luculentum; Cernohorsky,
Veliger, 9: 120, text fig. 41.

Cernohorsky (1965, 1966) has de-
scribed the external colouration of the
animal, the shell, habitat preferences
and radula of this species. Risbec
(1928) also described the shell, radula
and external features of V. luculentum
as well as the gross anatomy of the
alimentary canal and pallial cavity.

The material described here was col-
lected in the middle intertidal zone at
Port Vila, Efaté Island, New Hebrides.

This species is small for the genus,
being 8-15 mm in height (Cernohorsky,
1965). A few differences in the alimen-
tary canal and genital systems exist
between У. luculentum and Austromitra
yubiginosa and these are summarised
below.

The retracted proboscis is a little
longer than that of Austromitra but the
buccal mass still projects into the ce-
phalic cavity. A very narrow, short
oral invagination recalls that of Austro-
mitra in structure, but the muscular part
of the oral tube behind it is not ciliated,
although it is lined with cuboidal cells.
The posterior part of the oral tube is
even more muscular than the middle
portion and is ciliated, both of these
features being in contrast to the situation
in Austromitra. The posterior part of
the oral tube, as in Austromitra, is not
attached in any way, and the middle
part is fixed to the proboscis wall by
slender retractor muscles,

The mid-oesophagus (Fig. 5F) shows
the greatest differentiation from Austro-
mitra of any structure in the alimentary
canal. The long glandular part has
become mostly separated from the con-
ducting tube and forms a long, convolute
structure that is attached to the short,
triangular gland of Leiblein. The de-
tached portion of the mid-oesophagus is

W. F. PONDER

surrounded by a thin layer of muscle
and the growth of its glandular walls
has apparently outpaced that of anarrow
thin-walled ventral channel (v.c ) which
runs between them. This channel is lined
with a very thin, non-ciliated epithelium
which contains minute greenish granules

Similar to those in the cells of the gland ©

of Leiblein, The original duct of this
gland (d.g.l) is still apparent as a nar-

row portion between the mid-oesophageal |
section and the true gland of Leiblein, |

but all traces of the pretorsional ventral
folds have been lost. The gland of

Leiblein has a thick, muscular wall |

with an outer longitudinal and inner
circular layer. The glandular epithe-

lium is not as well developed as it is !

in Austromitra and secretory activity

is much less pronounced. The torsional |

area and general cytology are otherwise
like the those of Austromitra. Although
the posterior oesophagus (p.oes) has a
somewhat greater diameter than that of

Austromitra no crop-like structure is |
The remainder of the ali- |

developed.
mentary canal is very like that of Aus-
tromitra except that the 2 digestive gland
ducts open into the stomach separately,
although these are close together in the

same area as the opening of the single

duct in Austromitra.

The male genital system is very like |
that of Austromitra but the female differs |

in some respects. Because ofthe some- |
what larger size of this species the |
glandular epithelium of the albumen |
gland and capsule gland is arranged in |
complex, multicellular units, except for |

the dorsal glandular strip of the capsule
gland. The capsule gland (Fig. 6G; cap)
is short in relation to the length of the
bursa copulatrix, but is similar to that
of Austromitra except that the. ventral
channel has a short right ciliated fold
and 2 left folds. The lower left fold is
about the same size as that on the right,
but the upper one is considerably longer.
The very long vagina (va) is divided
into upper and lower halves by a long
left fold and short right folds and opens,
together with the bursal duct, ata small,

MORPHOLOGY OF MITRIFORM GASTROPODS 321

muscular gonopore.

The bursa copulatrix (b.c ) is much
longer than that of Austromitra and it
differs in several other respects. Only
unorientated sperms are stored there
and its thinly muscular wall is not
internally ridged. It is lined with tall
columnar cells, about 50 y in height,
containing red-staining globules which
are secreted, along with blue-staining
granules, into the bursal lumen and ap-
pear in considerable quantities amongst
the masses of spermatozoa. This secre-
tion is possibly responsible for sperm
breakdown as intact spermatozoa could
only be seen in the proximal end of the
bursa, whereas irregular masses of
sperm that had undergone changes in
appearance and staining properties were
found distally. Thus the bursa may
Supplement the function of the ingesting
gland, that is to rid the gonoduct of
excess Sperm. Glandular bursal epi-
thelia have also been recorded in Oce-
nebra erinacea (Linnaeus) (Fretter,
1941) and in Oliva sayana Ravenel (Mar-
cus & Marcus, 1959). The bursal duct
is a moderately long, rather twisted,
very muscular canal lined with a cili-
ated epithelium. There was no sign of
a ventral pedal gland.

The renal organ of this, and the fol-
lowing species, is like that of Austro-
mitra,

VEXILLUM PLICARIUM (Linnaeus)

1758 Voluta plicaria Linnaeus; Syst.
Nat. ed. 10, p 732, no. 366.

1965 Vexillum plicarium; Cernohorsky,
Veliger, 8: 132, pl. 20, fig. 94.

The shell of this handsome species
has been described and figured by Cer-
nohorsky (1965) and the radula by Tro-
schel (1856, pl. 9, fig. 15). The material
described here was collected at Port
Vila, Efaté Is., New Hebrides.

The adult shell is 34-50 mm in height
(Cernohorsky, 1965) and is thus much
larger than both of the foregoing species,
The head-foot is like that of other
species of the genus, but details of the

considerable external pigmentation could
not be determined adequately in the
preserved material.

The mantle cavity has a relatively
smaller osphradium and a larger gill
than either of the other 2 much smaller
Species, the osphradium being about
2/3 of the length of the gill, and about
!/2 its width. Differences in the pro-
portions of pallial structures are, how-
ever, usual in allied species that show
a considerable discrepancy in size.

The retracted proboscis of this species
is relatively much longer than that of
V. luculentum. It lies in a muscular
Sheath on the right side of the cephalic
cavity and is then bent to the left. It
thus displaces the large salivary glands
to the left so that the right gland over-
lies the left, whereas in Strigatella the
reverse situation is found. The long,
muscular anterior oesophagus runs along
most of the proboscis sheath, but at the
edge of the salivary glands it descends
beneath them. Four powerful retractor
muscles lie below the sheath, continuous
with the rather thick longitudinal mus-
cles in its wall. The slender proboscis
lies with its pointed distal end some-
times protruding into the snout. The
structure of the proboscis (Fig. 9E) is
Similar to that of the 2 preceding spe-
cies and is particularly like that of V.
luculentum. The outer epithelium, how-
ever, is columnar and most of the oral
tube is lined with columnar cells. Un-
like that of V. luculentum, the oral in-
vagination, which is exceedingly narrow,
is ciliated, but the next portion, to which
the retractor muscles are attached, has
a non-ciliated cuboidal epithelium. The
posterior part of this tube is relatively
wider and much folded, and has a cili-
ated columnar epithelium. The very
narrow, common duct of the accessory
salivary gland opens on the anterior
extremity of this latter region.

The mid-oesophagus (Fig. 5G) closely
resembles that of У. luculentum, al-
though the gland of Leiblein (g.l) is
shorter than in that species, being about
as broad as it is long and having a

322 W. F. PONDER

thicker muscular coat with variously
orientated fibres, In addition the glan-
dular lining is much reduced and deli-
cate, although the cells are of the same
type as in Austromitra and occasional
budding of their distal ends occurs,
The lumen of the gland is not sub-
divided, is relatively wide and contains
granules of secretion from the Separated
mid-oesophageal region attached to the
gland. The gland of Leiblein presumably
acts aS a pump in the Same manner as
the poison bulb in the Toxoglossa.

The posterior oesophagus (p.oes) is
much wider than that of either of the
other 2 species in this group. Its walls
have very high lamellae which develop
secondary and, posteriorly, tertiary
folds, which consequently occupy much
of the lumen. The function of these
lamellae is possibly absorptive as they
are rather vascular, especially posteri-
orly.

The stomach is relatively smaller than
that of V. luculentum and Austromitra,
and has 2 digestive gland openings. The
narrow intestine resembles that of the
other 2 species and the anal gland is
also similar, although the single tubule
develops short side-branches,

The male genital system follows the
same plan as that of Austromitra but
the prostate (Fig. 6F; pr.) is relatively
shorter, and the posterior opening ap-
pears to be restricted to a small pore.
The penis (pen.) is long and slowly
tapering and its duct is centrally placed
as in the other 2 species. Unfortunately,
no male specimen was available for
histological examination,

The female genital structures were
examined histologically in 1 specimen
and, although there was no female avail-
able for dissection, the general plan
of the genital tract appears to be like
that of V. luculentum. The mature
ovary is massive, sharply differentiated
from the digestive gland and contains
ova up to 240 » in diameter. There is
no gonopericardial duct and the renal
oviduct is embedded in the pericardial
wall as in the 2 allied species and

Strigatella. The larger size of this
Species has resulted in a much greater
development of the lateral walls of the
albumen and capsule glands than was
observed in the smaller, preceding spe-
cies, Larger size has also resulted in
the subdivision of the ingesting gland
into several compartments, andits rela-
tively narrow duct is surrounded by a
massive layer of circular muscle. In
other features, however, this gland has
the same structure as that of Austro-
mitra and У. luculentum. The ventral
channel of the capsule gland has a long
left fold, with 2 low ridges on its under
surface, and a low median fold lying
immediately below the innermost secon-
dary ridge of the left fold. Thus a
Sperm channel on the left is separated
from an ovarian channel on the right.
The vagina also shows a division into
2 separate channels as in V. luculentum,
but the folds on either side are of equal
length. The bursa copulatrix does not
appear to be as long as it is in V. lucu-
lentum, but it is lined with the same
epithelium as seen in that species, the
cells being about 50 y high. The bursal
walls, however, have low, longitudinal
folds, and the muscular bursal duct is
like that of V. luculentum. No orientated
spermatozoa were observed inthe bursa.

The differences inthe mid-oesophagus
and bursa copulatrix suggest that generic
separation is justified for Austromitra,
despite its radula being similar to Vex-
illum species, The simple structure of
the mid-oesophagus, including the primi-
tive nature of the gland of Leiblein in
Austromitra, suggest that it is less
advanced than Vexillum species interms
of evolutionary development.

PART 3

PECULATOR HEDLEYI (Murdoch)

1905 Velpecula (Pusia) hedleyi Murdoch;
Trans. N.Z. Inst., 37: 228, pl. 8, fig. 21.

1937 Peculator hedleyi; Powell, Dis-
covery Rept. 15: 212,

The shell of P. hedleyi is adequately de-

MORPHOLOGY OF MITRIFORM GASTROPODS 323

scribed and figured by Cernohorsky (1970:
116, pl. 14, figs. 15-16) but no informa-
tion on the soft parts has been published.

Living specimens of P. hedleyi were
obtained in shell sand from just below
extreme low water to about 2 fathoms
deep in Taurikura Bay, Whangarei Heads
and in 6-18 fathoms in the entrance to
Port Fitzroy, Great Barrier Island, It
is not a common species and appears
to be restricted to the north eastern
coast of the North Island of New Zealand,

The shell (Fig. 7G) reaches 6.2 mm
in height, is inflated, with a short spire
which is only 4/2 the height of the aper-
ture. The only sculpture is fine axial
growth lines and weak spiral grooves,
The disproportionately large protoconch
of 2 whorls is uniform brown, but the
remainder of the shell has the brown
colour broken up by irregular spiral
rows of white spots. The long aperture
has 4 columellar plaits.

The living animal (Fig. 7G) is trans-
lucent white and studded with minute,
opaque white spots. Along the lateral
parts of the foot there is a pair of
opaque white strips which are some-
times broken up into a series of patches.
A short siphon projects a little beyond
the shell and the rather short tentacles
have rounded ends, with the eyesbulging
from their outer bases. A minute oper-
cular rudiment lies onthe dorsal surface
of the posterior end of the broad foot
which has a wide, straight anterior end
with short lateral projections. The
strongly ciliated sole is richly supplied
with mucous secretion.

The pallial cavity presents few diffe-
rences from the species discussed pre-
viously. The broad, yellowish-brown
osphradium has about 16 filaments which
are longer on the right side, and the
ctenidium has triangular gill filaments
which have bases a little narrower than
their height. The hypobranchial gland
covers the pallial roof, gonoduct and
rectum and has 4 types of cells, all of
which are distinguishable inlife. Trans-
parent cells occur abundantly throughout
the gland while black cells and translu-

cent “crystalline” cells lie over the
rectum and gonoduct and are replaced
by brown cells throughout the rest of the
gland. There is no purple hypobranchial
secretion.

The pale greenish renal organ opens
posteriorly into the pallial cavity andthe
mid-oesophagus bulges into the lumen
of the cavity from below the thin floor.
The single tubule of the anal gland can
be seen externally, lying on the right
side of the anterior half of the pallial
roof.

The circum-oesophageal ganglia (Fig.
8G) are similar in arrangement to those
of the foregoing species, although the
supra- (sp.o) and sub-oesophageal
(sb.o) ganglia are connected to the
pleural ganglia (p.) by moderately long
connectives. The buccal ganglia (b.)
are somewhat displaced to the left. The
renal organ is like that of Austromitra
in having the 2 types of renal lamellae
interdigitated.

The Alimentary Canal

The Proboscis. The extended pleurem-

bolic proboscis is moderately long and
is of the same colour as the external
parts of the animal. It is short when
retracted (Figs. 7A, 9G) and the basal
portion forms a proboscis sheath, The
distal part does not lie entirely within
the sheath, but extends forward into a
short, ciliated, anterior proboscis cavity
which represents an expansion of the
rhynchostome (Fig. 9G). The outer epi-
thelium of the proboscis is non-glandular
and ciliated, but the sheath is devoid of
cilia. The proboscis wall is rather thin
anteriorly and consists of a very narrow
zone of circular muscles and, inside
these, a few longitudinal fibres, the
latter being much more prominent in
the wall of the sheath. Longitudinal
fibres and connective tissue occupy the
proboscis cavity and some irregular
clusters of red- and blue-staining gland
cells lying in this cavity send their
ducts to the outer surface of the probo-
scis.

The buccal cavity has thick, muscular

324

walls and lies above the narrow odonto-
phore which extends nearly to the tip of
the proboscis in the resting position. A
thick cuticular plate lies below the ante-
rior end of the odontophore just under
the small mouth. There is no other
appreciable cuticular thickening although
the buccal walls are covered with a thin
chitinous layer. Weakly ciliated but
prominent dorsal folds lie laterally in
the buccal cavity and have the salivary
ducts embedded in them. These ducts
pass laterally and then ventrally to dis-
charge near the anterior end of the
odontophore. A very short, unpaired
accessory salivary gland (a.s.g ) dis-
charges below the anterior end of the
odontophore by way of a short, narrow,
muscular duct. This glandis surrounded
by a thin layer of circular muscle and
has an irregular glandular epithelium
which stains pale blue. There are no
gland cells lying outside the muscle,
contrary to the usual condition in the
accessory salivary glands of other neo-
gastropods.

The odontophoral cartilages (od.c )
are rather small and extend to the inner
end of the retracted proboscis. They
are attached to a mass of muscle which
extends well beyond the inner end of the
retracted proboscis, and thus behind the
odontophoral cartilages. This muscular
rod is circular in section (Fig. 7C) and
is made up of a thick coat of circular
muscle about 50 y in thickness. It con-
tains a core of longitudinal muscle in
which is buried, for about 1/2 of its
length, the radular sac (r.s). Behind
the end of the radular sac the muscular
core continues to the endof the muscular
rod to which a short odontophoral re-
tractor muscle (od.r )isattached. There
is no epiproboscis.

Each radular row (Fig. 7D) consists
of a large central tooth, and a pair of
smaller, needle-like lateral teeth. Each
central tooth has a long median cusp
with a transversely concave anterior
surface. This suggests that each tooth
acts, in part, as a spoon rather than as
a simple cutting tool. The base of each
tooth has a pair of anteriorly bent, long,

W. F. PONDER

narrow plates, the lower portions of
which are curved laterally.

The Oesophagus and Salivary Glands. A
thick wall of circular muscle surrounds
the anterior oesophagus (Fig. 7Ba). Its
non-glandular epithelium is only weakly
ciliated within the dorsal food groove, but
the dorsal folds have moderately strong
cilia. The salivary ducts lie embedded
in the dorsal folds throughout the ante-
rior oesophagus and enter it just in
front of the valve of Leiblein. They are
ciliated and lined with a squamous epi-
thelium and, where free from the oeso-
phagus, they have a thin outer coat of
muscle, The small salivary glands
(s.g ) lie below the anterior part of the
mid-oesophagus. They are lobed bodies
which are composed of a few semi-
discrete tubules made up of reddish-
staining cells similar to those found in
most neogastropods. These tubules do
not have any outer muscles and do not
appear to contain any ciliated cells,

The mid-oesophagus (Fig. 7A) is the
most conspicuous part of the alimentary
canal as it forms a long, convolute,
swollen tube lying within the cephalic
cavity. It commences well in front of
the nerve ring as the valve of Leiblein
(v.1), which is slightly wider than the
rest of the mid-oesophagus. A non-
ciliated channel (v.c ), continuous with
the ventral channel in the anterior oeso-
phagus, lies ventrally and a zone of
radial muscles (r.m) on either side
extend from it into the now reduced
dorsal folds. These muscles persist
right through the valve. Above the
folds lies the glandular pad usually
found in this structure (Fig. 7Bb). The
most anterior glandular epithelium
stains red (r.c ) but a dorsal zone of
mucous cells (m.c) alittle behind rapidly
spreads to surround the dorsal glandu-
lar area (Fig. 7Bc). Cells bearing
very long cilia between the mucous
cells and these cilia extend backwards
into the lumen of the gland but there is
no cone-like valve such as is normally
found in this region. The dorsal folds
remain as a distinct, though reduced,
region throughout the “valve”, Their

MORPHOLOGY OF MITRIFORM GASTROPODS 325

FIG. 7. A-G. Peculator hedleyi (Murdoch): A. The anterior alimentary canal showing the probos-
cis opened. The muscular portion of the mid-oesophagus is cross-hatched; B. (a-h) Transverse
sections of oesophagus near and through the valve of Leiblein (for explanation see text); C. A
transverse section of the muscular posterior extension of the odontophore; D. Radular teeth,
face and lateral view; E. A transverse section of the muscular part of the oesophagus with posi-
tion of section indicated on fig. A; F. A transverse section of the gland of Leiblein and the pos-
terior oesophagus; G. A dorsal view of the living animal and the shell showing the re-
duced operculum. H. Microvoluta marginata (Hutton). A transverse section of the proboscis.

326

lower surfaces are lined witha squamous
epithelium which covers the muscles
referred to above. Their upper surfaces
consist of the red-staining gland cells
which have persisted from the anterior
zone and these reach a maximum height
of 40 u. The supporting cells between
these gland cells have only short cilia.
About 7/3: of the way through the valve
the red cells on the dorsal folds, and
the mucous lining in the dorsal groove,
are suddenly replaced by blue-staining
gland cells (Fig. 7Be; Ы.с ), the sup-
porting cells between which bear short
cilia. This latter region is short and is
replaced by a glandular lining of tall,
pale blue-staining cells and occasional
red-staining cells (Fig. 7Bf-h; m.o )
which continue through the next region
of the mid-oesophagus. Torsion occurs
at the commencement of the blue-staining
area, the ventral groove (v.c ) moving
up the right side (Fig. 7Bd, e). When
in a dorsal position, the Squamous epi-
thelium is replaced by red-staining gland
cells like those in the anterior part of
the “valve”. These cells occlude the
ventral groove and the radial muscles
beneath the dorsal folds disappear. This
narrow zone of red-staining cells per-
sists through the next portion of the
mid-oesophagus. The gland cells in the
pretorsional dorsal “food groove” are
replaced by a cuboidal epithelium which
forms a ventral thin-walled, weakly
ciliated channel. The mid-oesophagus
narrows only slightly as it passes be-
tween the circum-oesophageal ganglia,
and there is no appreciable change in
cytology or structure behind this point
for a distance equal to that which lies
in front. In the next regionthe glandular
epithelium is reduced in height and the
pretorsional ventral channel is lost;
correspondingly, the muscular coat,
which was rather thin through the ante-
rior part of the mid-oesophagus, sud-
denly increases in thickness, An irre-
gular epithelium containing greenish-
staining granules abruptly replaces the
gland cells of the anterior section of
this muscular region, although there is

W. F. PONDER

also a narrow, ventral ciliated strip
which is continuous with the dorsal food
groove and is bordered by the 2, low,
ciliated dorsal folds (Fig. 7E). This
epithelium probably represents the ante-
rior part of the oesophageal gland(gland
of Leiblein.. The muscular coat is
very thick at this point and the lumen
of the oesophagus rapidly narrows. An
outer circular layer makes up the bulk
of this coat, but there is also a thin,
inner layer of longitudinal muscle. The
ventral ciliated strip disappears near
the posterior end of this portion of the
mid-oesophagus, but the pretorsional
ventral groove reappears dorsally and
leads to the opening of the minute gland
of Leiblein. The duct of this gland is
embedded in the muscular oesophageal
wall up to the posterior limit of the mid-
oesophagus. The gland itself (g.1) is
a short, finger-like caecum, much nar-
rower than the mid-oesophagus although
of a Similar diameter to the posterior
oesophagus (Fig. 7F). It is a simple
tube with a very thin, outer muscular
coat and is lined with irregular cells
containing greenish granules of the same
type normally seen in this gland, al-
though the characteristic budding of
their distal ends is rather infrequent.
The lumen of the mid-oesophagus is
divided into 2 by the formation of a
partition where the dorsal groove is
closed off to become the duct of the
gland of Leiblein. The lower portion
becomes ciliated and is continuous with
the posterior oesophagus.

In contrast to the mid-oesophagus, the
posterior oesophagus (p.oes) is very
narrow and has only athin external layer
of muscle in all but its most anterior
section. It has aciliated, non-glandular,
columnar epithelium and a few longitu-
dinal ridges result from variation in the
height of these cells, there being about
6 ridges initially and 4near the stomach,
The Stomach and Digestive Gland. The
oesophagus becomes confluent with the
stomach on its posterior side, and the
intestine lies alongside. Two very
short digestive gland ducts open near

MORPHOLOGY OF MITRIFORM GASTROPODS 327

the oesophageal aperture, the larger on
the posterior wall leading to the large
left lobe of the digestive gland, whereas
the other, the duct of the small right
lobe, is situated ventrally. A short
caecum forms the right (upper) part of
the stomach and has tall, strongly cili-
ated, closely spaced ridges which run
in a direction parallel to the oesophagus
and intestine. Below this region, on the
anterior side is the main gastric lumen
with ciliated folds running from the
oesophagus to the anterior gastric wall.
A distinct style sac region is separated
from the gastric lumen and has 2 large
typhlosoles bordering a ventral groove.
A small, cuticulate gastric shield pro-
jects into the gastric lumen on the
anterior edge of the stomach, just be-
hind the style sac.

A small anterior (right) lobe of the
digestive gland lies in front of the sto-
mach but most of the gland comprises
the posterior (left) lobe behind. There
are 2 types of digestive cell, the major-
ity being elongate and having long cilia
and variably staining granules whichare
mostly contained in the proximal half
of the cell. A less abundant type is
very broad. These cells contain densely
staining red granules and have very
narrow distal ends whichare not ciliated.
The Intestine and Anal Gland, Thereare
no glandular cells in the posterior part
of the intestine, this having only a
ciliated columnar epithelium and a mo-
derately wide lumen compared with the
posterior oesophagus, and it narrows
towards the anus, At the beginning of
the rectum the epithelium becomes
shorter and numerous epithelial gland
cells with large, orange-staining gran-
ules occur amongst the ciliated cells.
The cells take on a cuboidal form when
the rectum is distended with faecal
material. The narrow distal portion of
the rectum has only ciliated columnar
cells and, consequently, a very narrow
lumen.

The anal gland opens directly at the
anus (Fig. 8D) and is a Single tube with
short side branches. It has a typical

epithelium of irregular columnar cells
containing greenish - brown - staining
granules and these aggregate in the
distal ends of the cells which are then
budded off.

The Male Genital System

The testis lies above the digestive
gland and does not ramify into it. Sperm
is stored in the swollen, convolute semi-
nal vesicle (Fig. 8A) which is lined with
Squamous epithelium. There is a very
short ciliated gonopericardial canal
(p.d ) at the commencement of the renal
vas deferens. The renal section of the
vas deferens is a very narrow duct that
opens into a pallial seminal groove
(s.gr ). This ciliated groove is formed
by a flap on the lower edge of the right
pallial wall which lies against the pallial
floor (Fig. 8B). Two ridges, which bor-
der this groove near the base of the
penis, are occupied by blue-staining
Subepithelial gland cells, although the
epithelium is composed of only ciliated
cuboidal cells.

The penis (pen) is short and thick
and has a Shallow, ciliated groove con-
tinuous with the sperm groove, situated
on the left. A central rod of red-
staining prostatic gland cells liberates
its secretion into a narrow ciliated duct
that runs through them, and this opens
at the distal end of the penis at the point
where the penial groove terminates. A
mass of sub-epithelial blue-staining
gland cells are continuous with those in
the anterior part of the seminal groove,
and these lie amongst the connective
tissue and muscle fibres comprising the
bulk of the penis. The outer epithelium
consists of short, ciliated cells and a
few gland cells.

The Female Genital System

The Ovary and Upper Oviduct. The
large ovary contains large yolky eggs

up to 400 y in diameter and remains
quite separate from the digestive gland.
The upper oviduct is constructed in the
same way as that of Strigatella and Aus-
tromitra. The short, ciliated, non-

328

muscular renal portion passes next to
the pericardial wall and there is no
gonopericardial duct. A long, narrow
arm of the renal organ, however, opens
into the oviduct by way of a very narrow
aperture. This unusual phenomenon has
also been recorded in Marginella des-
jardini Marche-Machad (Graham, 1966).
The Albumen Gland and Ingesting Gland.
A posterior glandular mass, the albumen
gland (Fig. 8C; alb ), has short cells
containing red-staining granules instead
of the normal blue-staining tissue. This
gland is constructed in the normal fash-
ion and the oviduct opens ventrally near
its anterior end. A short, median region
(Fig. 8F; c.r ), with thin, slightly mus-
cular walls which are heavily folded and
lined with a ciliated cuboidal epithelium,
lies between the posterior gland and the
capsule gland. A considerable number
of ciliated tubules (i.d ) branch off from
this area both dorsally and laterally,
especially from the right side. These
tubules are irregularly coiled and open
into vesicles (i.g ) lying mostly on the
left side of the oviduct, although in this
median region they also lie dorsally.
The vesicles extend almost to the ante-
rior and posterior extremities of the
gland and usually contain small bundles
of loose sperm. They are lined with
large cells of very variable form and
size which have pale blue, non-glandular
cytoplasm and large, central nuclei.
Although the vesicles are probably ho-
mologous with the ingesting gland of other
stenoglossans they present a totally
different appearance to those that have
been described and, in addition, there
is no sign of sperm ingestion. They
might more appropriately be termed
seminal receptacles. The ciliated tu-
bules are lined with cuboidal cells and
are not muscular.

The Capsule Gland and Anterior Struc-

tures. The capsule gland (Fig. 8E; cap)
begins infront of the ciliated region, their
walls being continuous. The ventral
channel (v.c ) which had become very
subdivided in the ciliated region, retains
a single fold initially but this quickly
disappears until only a ciliated ventral

W. F. PONDER

channel remains, overlapped by a short
glandular fold on either side. The walls
of the capsule gland show only 2 types
of glandular cells. A short posterior
region stains blue and both walls are of
equal thickness, whereas the remainder
of the gland stains red, and the cells,
which are larger than those ofthe poste-
rior red-staining gland, have relatively
smaller granules. In addition, the outer
(right) wall is only a quarter as thick
as the inner wall in this region. Near
the anterior end of the capsule gland a
short, ciliated right fold appears above
the narrow ventral channel, Just behind
the bursa copulatrix the walls of the
capsule gland become thin by the shor-
tening of the epithelial cells, although
they still contain red-staining granules,
The vestibule (Fig. 8D; vest) lies on
the outside of the short bursa copula-
trix (b.c ) and has a simple ciliated
epithelium. A small gonopore (Fig. 8D)
is confluent with that of the bursal open-
ing and lies just behind the anterior end
of the oviduct. There is no true vagi-
nal region apart from the ciliated lips
of the gonopore.

The bursa copulatrix (b.c ) is, along
most of its ventral side, open to the
pallial cavity. Its inner walls are lined
with a non-ciliated red-staining glandu-
lar epithelium, but a thick lobe, lined
with pavement epithelium and consisting
of connective tissue and a few muscle
fibres, projects from the right dorsal
wall and nearly fills the lumen. This
lobe diminishes in size and disappears
before reaching either end of the bursa.
Only a few muscles surround the cili-
ated bursal lips and the remainder of
the bursa is not very muscular, No
Sperm were observed in the bursa in any
of the specimens sectioned.

No pedal gland was found in the fe-
male, either in the living animal or in
sectioned material.

MICROVOLUTA MARGINATA (Hutton)
1885 Turricula marginata Hutton, Trans.

N. Z. Inst., 17: 315, pl. 18, fig. 4.
1905 Vulpecula (Pusia) biconica; Mur-

|
|

MORPHOLOGY OF MITRIFORM GASTROPODS 329

FIG. 8. A-G. Peculator hedleyi (Murdoch): A. A diagram of the male genital system; B. Atrans-
verse section of the posterior part of the seminal groove; C. A diagrammatic lateral view of
the pallial oviduct. The sections d-f correspond to figs. D-F; D. A transverse section of the
bursa copulatrix, vagina and vestibule and showing the anus and anal gland opening; E. A trans-
verse section of the posterior end of the pallial oviduct showing the ingesting gland and its cili-
ated ducts; F. A transverse section of the ciliated, median part of the pallial oviduct showing
the ingesting gland; G. A diagram of the circum-oesophageal ganglia viewed dorsally with
the cerebral ganglia separated and spread apart. H-J. Microvoluta marginata (Hutton):
H. A diagram of the male genital system; I. A transverse section of the anterior part of the
seminal groove. J. A transverse section through the middle region of the penis.

330

doch & Suter, Trans. N. Z. Inst., 38:
289, pl. 23, fig. 22.

1927 Microvoluta biconica; Finlay,
Trans. N. Z. Inst., 57: 410.
1930 Microvoluta cuvierensis Finlay,

Trans. N. Z. Inst., 61: 242, pl. 43,
figs. 19, 21.

1970 Microvoluta marginata; Cernohor-
sky, Bull. Auck. Inst. Mus., 8: 122,
pl. 15, figs. 14-19, pl. 16, figs. 1-2.

The radula of Microvoluta australis
Angas is figured by Peile (1922) but no
description of any aspect of the animal
of M. marginata has previously been
available. The shell is figured in the
original diagnosis by Finlay (1930), and
by Cernohorsky (1970).

М. marginata lives in moderately deep
to deep water (15-270 fathoms) around
the coasts of New Zealand, extending to
the Snares Islands and to the Chatham
Islands. The shell attains a length of
about 7 mm and usually has strong axial
ribs and spiral cords, although the de-
gree and detailed pattern of sculptural
development is variable.

Living specimens were obtained from
several localities off the north east
coast of the North Island. These were
all collected by the writer on the Marine
Department vessel “Ikatere” from: 25
fathoms off Bergens Point, south of
Doubtless Bay; 24 fathoms off Cone Rock,
Whangaroa; 85 fathoms south east of the
Cavalli Islands; and 29 fathoms 4 miles
west of Little Barrier Island.

The living animal is translucent white
with small clusters of yellow, orange and
white pigment cells on the dorsal sur-
face of the foot. A moderately long
siphon projects from beneath the siphonal
notch of the shell and has pale yellow or
orange pigment cells scattered over its
surface. The’ eyes are about 4/3 of the
way along the slender tentacles which
have a few yellow spots. The foot is
broad and is evenly rounded behind,
with short expansions in front and a
slightly indented anterior edge. There
is no opercular rudiment,

The mantle cavity is like that of Pe-
culator, though it was not examined

W. F. PONDER

while the animal was alive, The osphra-
dium has about 14 filaments, those onthe
left side being shorter. The ctenidium
is relatively large, with about 30 tri-
angular filaments.

The renal organ is like that of Austro-
mitra and Peculator.

The Alimentary Canal

The retracted proboscis (Fig. 9F) is
Similar in structure and shape to that of
Peculator, but a compact cluster of
gland cells lies on each side beneath the
proboscis wall (Fig. ТН; g.c ). These
do not extend into the dense muscle and
connective tissue surrounding the buccal
cavity but terminate behind at the end
of the odontophore. These cells stain
blue, or red, the latter type having
large granules, and clearly represent a
further development of the loose sub-
epithelial gland cells seen in Peculator.
The outer epithelium of the proboscis is
ciliated dorsally and laterally but is
covered with cuticle on its ventral and
anterior surfaces. Unlike the situation
in Peculator the muscles of the proboscis

wall are not arranged into distinct zones ©

but are a mixture of variously orientated —

fibres. A short, muscular tube lies in
an invagination behind the minute mouth
and is lined with very thick cuticle. This
tube is attached to the proboscis wall
by a dense series of short retractor

muscles and the odontophore lies just |

behind it. Protrusion of the odontophore
is probably accompanied by the eversion
of this inner mouth, The weakly cuti-
culate oral invagination surrounding the
oral tube is loosely bound to the thin,
outer proboscis wall by many tangential
fibres which may act as retractors and/
or dilators. There is no oral invagina-
tion or separate tube in Peculator.
Lying mostly within the retracted
proboscis behind the oral tube is the
odontophore. Massive subradular mem-
brane retractor muscles are attached to
the narrow odontophoral cartilages
(od.c ) while a short odontophoral re-
tractor muscle is attached directly to

their ends and ascends to the floor of |

the cephalic cavity.

Thus there is no :

MORPHOLOGY OF MITRIFORM GASTROPODS 331

m
0-25mm E

0.5.9 F

un
A 0-25mm
0-25mm

FIG. 9. Comparative diagrams of the buccal mass (shown stippled) of the mitriform gastropods
to show the relationships of the main structures. The proboscis wall is solid black and the radu-
lar sac is shown densely stippled where it protrudes from the odontophoral muscles. A. Striga-
tella paupercula (Linnaeus). B. Mitra mitra (Linnaeus). C. Imbricaria conovula (Quoy and
Gaimard). D. Austromitra rubiginosa (Hutton). E. Vexillum plicarium (Linnaeus). (Muscle
fibres are shown running from the oral tube to the buccal mass and proboscis wall). F. Micro-
voluta marginata (Hutton). G. Peculator hedleyi (Murdoch).

332

development of the elongate muscular
rod seen in Peculator. The radula is
very similar to that of Peculator except
that the lateral teeth are relatively
larger and a little heavier.

The single accessory salivary gland
(Fig. 9F; a.s.g ) is longer than in Pecu-
latory as it commences opposite the valve
of Leiblein. Its coiled duct (Fig. 7H;
a.s.d ) opens just in front of the odon-
tophore after passing below it as a mi-
nute tube. A short posterior portion
about 60 y wide has a wall consisting
of thin layers of inner circular, and
outer longitudinal muscles, and an inner
epithelium of small, irregular, pale
bluish-staining gland cells with granu-
lar contents. A similar type of cell
forms a Single layer outside the mus-
cular tube a little further anteriorly
where the tube reduces in width. At
the same time the inner epithelium be-
comes more pronounced, but at the base
of the proboscis the glandular epithelium
is replaced by squamous cells and the
tube becomes very narrow.

The buccal cavity, anterior, mid- and
posterior oesophagus are like those of
Peculator and, although the salivary
glands are rather larger, they have the
same structure.

The stomach differs from that of
Peculator innot having a definite caecum,
although the posterior part is expanded,
The style sac is especially well-devel-
oped with the typhlosole on the anterior
wall being mainly composed of large,
blue-staining gland cells. The digestive
gland, rectum and anal gland are like
those of Peculator. Fine mineral par-
ticles, diatom cases and spicule-like
fragments have been Seen in the faecal
material.

The Male Genital System

There are few differences from the
system described in Peculator. The
seminal groove (Fig. 8H; s.gr )is shorter
and is replaced about halfway along the
pallial cavity by glandular ridges (Fig.
8I) similar to those situated further in
front in Peculator. The penis is much

W. Е. PONDER

longer than in Peculator although there
is a similar penial groove (Fig. 8J;
p.gr ) and a central rod of prostatic
tissue (pr.c ). The prostatic tissue is
surrounded by a ring of circular muscle
and a ciliated prostatic duct opens dis-
tally at the end of the seminal groove as
it does in Peculator. Two lateral tracts
of blue-staining cells (g.c ) lie on either
side of the prostatic mass, and the outer
penial epithelium is ciliated and contains
abundant mucous cells.

The Female Genital System

Only a single female was available
for examination and although the general
features of the female system resemble
those of Peculator, no detailed compari-
son could be made. The ovary is like
that of Peculator but the albumen gland
cells stain blue and are very short,
being only 20-30 y in height. The gland
also has a wide lumen and is of an
irregular shape. Between the albumen
and capsule glands the ciliated sac is
found, but in this species it is smaller
than in Peculator and is clearly just a

swelling of the ventral channel. Only 2
non-muscular, ciliated ducts are given
off from this area and both open into
the “ingesting gland” or seminal recep- |

tacles. These vesicles have the same
cytological structure as those in Pecu-
lator.

no indication of sperm ingestion was
observed. The capsule gland appears to

be similar to that of Peculator but no _
detailed observations were possible. A |

short, ciliated fold lies on the left of

the ventral channel in the anterior part |
A thin-walled |
vestibule is on the right of the bursa

This is lined with mucous |

of the capsule gland,

copulatrix,
cells and opens into a wide, muscular
vagina which extends along the anterior
half of the bursa to open distally along-

side the bursal opening. The vagina has |

an orange-staining cuboidal epithelium
which bears long cilia.

The bursa copulatrix has a thick wall |

Long cilia in the ducts mould о
sperm into coherent masses which are :
visible in the lumen of the vesicles, but .

|

MORPHOLOGY OF MITRIFORM GASTROPODS 333

of circular muscle and its interior is
irregularly folded. Although the bursal
Opening is ciliated the remainder is
lined with columnar cells about 18 y in
height which are covered with a “soft”
cuticle. The differences in the anterior
female genital structures of Peculator
and Microvoluta can, no doubt, be at-
tributed to the relative size of the penis
in these 2 species.

As in Peculator there was no indica-
tion of a pedal gland. Single egg cap-
sules have been observed attached to
the dorsal or lateral surfaces of the
Shells of a few specimens of Micro-
voluta. Each capsule consists of rather
fragile, transparent, horny material and
is about 0.7 mm in diameter. The cap-
sules are hemispherical in shape anda
Single embryo develops within each.
When emergence takes place the crawl-
ing juvenile breaks away most of the
top of its capsule.

DISC USSION

There is a general uniformity in the
Shells of mitriform neogastropods that
has resulted in considerable difficulty
in placing them in genera and higher
taxa. Most of the mitriform species
have solid shells with rather elongate
apertures which are ornamented with
columellar plaits, and no operculum.
Various authors have shown that de-
Spite the similarity of their shells, the
mitriform gastropods fall into several
well defined groups based upon radular
pattern. Risbec (1928) found that the
anatomy of several species also showed
considerable differences and Thiele
(1929), presumably using this work as a
basis, listed the anatomical characters
of each of his subfamilies and arrived
at the following classification:

Superfamily Volutacea
Family Mitridae
Subfamily Mitrinae (Mitra, Imbri-
са а)
Subfamily Vexillinae (Pusia, Уех-
illum)
Subfamily Cylindrinae (Cylindra)

Thiele further suggested that the
structure of the anterior alimentary
canal is so different that 2 families,
Vexillidae and Mitridae, should probably
be distinguished, Risbec (1955) arranged
the species he investigated into several
different families. The true mitrids he
aligned with the Toxoglossa, as he sug-
gested that the epiproboscis (poison
gland) is homologous with the toxoglossan
poison gland. His arrangement was as
follows:

Suborder Toxoglossa
Superfamily Mitracea
Family Mitridae
Subfamily Mitrinae (Mitra, Stri-
gatella)
Subfamily Cylindrinae (Cylindra)
Suborder Stenoglossa
Superfamily Muricacea
Family Purpuridae
“new subfamily” (Pusia)
Superfamily Buccinacea
Family Nassidae
“new subfamily” (Vexillum)

This classification has been subse-
quently accepted only by Taylor & Sohl
(1962) who used it in their summary of
gastropod classification.

The next major attempt to classify
the family Mitridae was that of Cerno-
horsky (1966) which was based primarily
on radular and shell features. This
author made no reference to Risbec’s
work and used the same scheme as
Thiele except for the use ofanadditional
sub-family, Imbricariinae. Cernohors-
ky’s scheme is summarised below: 3

3Since the above account was prepared Cernohorsky (1970) has published a comprehensive re-
view of the “Mitridae and Volutomitridae”. The classification that he adopts is essentially that

of his earlier (1966) work.

334 W. F. PONDER

Superfamily Volutacea
Family Mitridae
Subfamily Mitrinae (Mitra, Stri-
gatella, Neocancilla,
Charitodoron)
Subfamily Imbricariinae (Imbri-
caria, Cancilla, Scab-
ricola, Swainsonia)
Subfamily Vexillinae (Vexillum,
Pusia, Austromitra)
Subfamily Cylindromitrinae
(Pterygia = Cylindra)

Azuma (1965) raised the Vexillinae to
family rank because of its radular char-
acters.

A small group of species around Volu-
tomitra have been variously placed in
the Volutidae (Powell, 1951) or in the
subfamily Volutomitrinae of the Voluti-
dae (Thiele, 1929; Smith, 1942; Cerno-
horsky, 1966) and in the Mitridae (Cot-
ton, 1957; Powell, 1962). It appears
that Microvoluta and Peculator belong
in this group so that the families Micro-
volutidae and Peculatoridae erected by
Iredale & McMichael (1962) are syno-
nyms.

The present investigation suggests an
arrangement that is not entirely in
accordance with any of the previous
schemes. Of the species examinedthere
appear to be 3 very distinct groups; the
true mitrids (Strigatella, Mitra, Imbri-
caria); the “Vexillum group” (Vexillum,
Austromitra); and the “Volutomitra
group” (Microvoluta, Peculator). Ana-
tomical differentiation between each of
these groups, particularly in the ali-
mentary canal, is so marked that their
separation at the family level appears
to be fully justified. There do not
appear to be sufficient differences to
separate Imbricaria from the true mi-
trids, even at the subfamily level. Cer-
nohorsky (1966) does not indicate how
the Imbricariinae can be separatedfrom
the Mitrinae. The radula, shellfeatures
and anatomy of the Cylindromitrinae
indicate that this group is related to the
Mitrinae and for the present should be
regarded as a Subfamily of the Mitridae.

The Volutomitridae has generally been

associated with the Volutidae because
of the similarity of the radular teeth of
Volutomitra and Scaphella species. This
resemblance is only superficial as the
Shells and the morphology of the animals
have very few features in common, Sars
(1878) has described the radula and the
gross features of the proboscis of Volu-
tomitra grönlandica (Beck), the type of
that genus, and these structures very
closely resemble those of Microvoluta
and Peculator. Peile (1922) described
the radula of Microvoluta australis An-
gas, the type species of Microvoluta,
and states that there are no lateral
teeth, whereas all other members of the
family, including Paradmete (see Thiele,
1929; Powell, 1951) have these teeth,
The radula of the type species of Pe-
culator, P. verconis Iredale, is unknown,
Probably some generic rearrangement
is require to take the radular features
into account, but more species should
first be examined.

The anatomy of a species of Pusia
was described by Risbec (1928) and his
description of the shell suggests that it
was P. consanguinea (Reeve) rather than
the closely allied P. microzonias, the
type species of the genus. The central
tooth of the radula has only 3 cusps but
otherwise it is similar to that of Vexzl-
lum and Austromitra species and the
alimentary canal is also similar. It
would thus appear that Pusia and Vexil-
lum are related genera andcanbe placed
together in 1 family. Risbec (1955)
suggested Pusia be placed in the Nas-
sariidae, a decision with which the
writer finds no merit whatsoever,

The scheme adopted here for the
classification of the mitriform gastro-
pods can be summarised as follows:

Family Mitridae
Subfamily Mitrinae (=Imbricarii-
nae)
Subfamily Cylindromitrinae
Family Vexillidae
Family Volutomitridae (=Microvol-
utidae, Peculatoridae)

A synopsis of the chief distinguishing

features of the 3 families is given in

MORPHOLOGY OF MITRIFORM GASTROPODS 335

tabular form below (Table 3). The main
differences between the Mitrinae andthe
Cylindromitrinae are given in Table 4,
The anatomical data on the Cylindro-
mitrinae are obtained from Risbec’s
(1928) account of the anatomy of Ptery-
gia crenulata.

The whole question of the relationships
of the families of the Neogastropoda
will be discussed elsewhere, but there
can be little doubt that the 3 groupings
suggested here are of family level. The
morphological characters show a level
of differentiation similar to or greater
than that seen in other neogastropod
family groups.

Despite the considerable differences
in the alimentary canal between the
Mitridae and the Vexillidae, their re-
productive and nervous systems are
generally similar which may suggest a
close relationship. Both the male and
female genital systems of the volutomi-
trids Microvoluta and Peculator, how-
ever, show considerable differences
from those of the other 2 families,
There are some common features of
the alimentary canal between the Vexil-
lidae and the Volutomitridae. They both
have a gland of Leiblein, a glandular
mid-oesophagus, a valve of Leiblein and
accessory Salivary glands. These fea-
tures, however, are found in many neo-
gastropod families and do not necessarily
indicate a close relationship. Graham
(1941) has suggested that a different
position of torsion in the mid-oesophagus
indicates a different origin. In the
Vexillidae the torsion of the alimentary
canal seems to occur just behind the
nerve ring whereas in the Mitridae it
probably takes place near the position
of the valve of Leiblein. Torsion in the
Volutomitridae occurs on the posterior
side of the valve of Leiblein but in front
of the nerve ring. Thus, on this evi-
dence alone, the 3 families are well
separated.

The renal organ in the Mitridae is
like that of the Olividae (Marcus &
Marcus, 1959) and the Volutidae (Per-
rier, 1889) in having the primary and

secondary renal lamellae separated into
2 distinct glandular areas, whereas inthe
Vexillidae and the Volutomitridae these
2 types of lamellae are interwoven as
in Buccinum (Perrier, 1889; Dakin, 1912)
and Nucella (Perrier, 1889; Fretter &
Graham, 1962).

The ability of the Mitridae to secrete
a purple hypobranchial fluid similar to
that seen in the Muricidae and the Volu-
tidae is not shared by the Vexillidae or
the Volutomitridae, but does occur in
some Terebridae. When more informa-
tion is available, egg capsules may prove
to have a consistently distinctive form
for each of the families.

Although the Mitridae resembles the
Buccinidae and its allied families in the
absence of accessory salivary glands,
the reduction or absence of a valve of
Leiblein, and the multicuspid lateral
teeth of the radula, the presence of a
purple hypobranchial secretion and an
anal gland suggest affinity with either
the Muricidae or the Volutidae. Other
features of the family such as the colu-
mellar plaits of the shell, the absence of
an operculum, and the very elongate
proboscis, fit the Volutidae better than
the Muricidae. A long proboscis is also
found in the Buccinidae and related fami-
lies.

One of the most puzzling questions
concerning the Mitridae is how the epi-
proboscis was evolved, Probably this
was brought about by an elaboration of
a trend towards the ventral migration
of the salivary ducts, such as that seen
in the Vexillidae. As the buccal mass
lies just behind the mouth, this may
have resulted in the openings of these
ducts being pushed to the edge of the
mouth, Eventually these may have been
placed on a small papilla, but the advan-
tages of this are not known, Invagination
of this papilla would probably accompany
its further elongation. The salivary
glands have a second type of secretory
cell not seen in the Vexillidae or the
Microvolutidae and it is possible that
these cells are responsible for the pro-
duction of a toxic substance. It is quite

336

TABLE 3.

Feature

Shell
Size

Predominant
sculpture

Radula

Lateral teeth

Central teeth

Hypobranchial
secretion
Alimentary canal

Proboscis

Epiproboscis

Mouth

Oral tube

Accessory salivary
glands

Salivary ducts

Valve of Leiblein

Region of torsion

Gland of Leiblein

Mid-oesophagus

Stomach

Genital system

Gonad

W. F. PONDER

The chief distinguishing features of the 3 families of mitriform gastropods.

MITRIDAE VEXILLIDAE VOLUTOMITRIDAE

large to medium

smooth or spiral

usually multicuspid
or absent

usually relatively
small, multicuspid

long

present

large, with
peristomal rim

absent

absent

free or in oeso-
phageal wall

small or absent

valve of Leiblein (?)

absent

very short, not con-
spicuously glandular

often with muscular
gizzard, a modified
style sac and no
caecum

tubules intermingle
with digestive gland

large to small

axial

simple, curved

relatively large, 3
or more cusps

moderately long or
short

absent

small, no
peristomal rim

long

large, paired

in oesophageal wall

large

behind nerve ring

moderately large or
small

moderately short or
long, glandular

simple, with short
posterior caecum
and style sac

medium to small

smooth or axial

needle-like or absent

relatively large, 1 cusp,
long basal processes

colourless

short

absent

small, no
peristomal rim

very short or absent

small, single

in oesophageal wall

large

behind valve of Leiblein
but in front of
nerve ring

very small, only parti-
ally separated from
oesophagus

very long, glandular

with style sac and
gastric shield, with
or without caecum

tubules separate from | tubules separate from

digestive gland

digestive gland

MORPHOLOGY OF MITRIFORM GASTROPODS 337

Table 3 (continued)

Feature

Ingesting gland or
seminal receptacle

cells columnar,
ingest sperm
and yolk

Pedal gland

present

Egg capsules

vase-shaped

Prostate gland large pallial gland,
closed except for
small posterior
pallial opening
Renal organ primary and
secondary lamellae
interdigitate

possible that a more primitive member
of the Mitridae exists which may give a
definite indication of the evolution of

this organ.

Maes (1971) has shown in Miira nodu-
losa (Gmelin) that the epiproboscis de-
posits the toxin against the soft parts
of the prey and that the toxin permeates
unbroken epidermis (presumably killing
the prey).

The structure of the mid-oesophagus
in the Volutomitridae is different from
that of any other neogastropods that
have been described. It has the oeso-
phageal gland (gland of Leiblein) appar-
ently only partially separated from the
mid-oesophagus, the anterior portion
being incorporated in the oesophagus
itself. Thus the gland was probably
partially separated from the oesophagus
from behind forwards. There is, how-
ever, no trace of any ventral folds in
the gland to confirm this supposition.
The gland of Leiblein in the remainder
of the neogastropods was, as shown by
Graham (1941), removed backwards from
the mid-oesophagus and thenturned over
so that its dorsal surface, along which
run the ventral (oesophageal) folds, lies
immediately above the oesophagus. The
glandular area behind the valve of Leib-
lein in the volutomitrids represents a

MITRIDAE VEXILLIDAE

cells columnar,
ingest sperm

absent

large pallial gland,
closed except for
small posterior

pallial opening

primary and
secondary lamellae
separate

VOLUTOMITRIDAE

cells cuboidal, no
sperm ingestion

absent

inverted hemispherical] hemispherical
(Austromitra)

(Microvoluta)

open pallial groove,
prostatic tissue in
penis

primary and
secondary lamellae
separate

secondarily elongated part of the mid-
oesophagus from which the oesophageal

gland retreated. This part appears to
have been largely pulled through the
nerve ring so that the area where tor-
sion occurs lies just behind the valve
of Leiblein.

Cernohorsky (1965, 1966) suggests
that the Mitridae feed on micro-organ-
isms grazed or swept from surface de-
tritus, and that the Vexillidae feed on
dead or living flesh. The gut contents
of the animals described above indicate
that Strigatella and Imbricaria feed on
Sipunculids and molluscs, although they
may well feed onother animals, and Aus -
tromitra has been observed feeding on
ascidians. The faecal residue of Micro-
voluta shows only fine particulate mate-
rial that could have been derived from
the accidental inclusion of detritus while
feeding, or from the gut contents of its
prey. The food of Strigatella, Imbri-
caria and presumabley Mitra is swal-
lowed in chunks that are stored in the
crop region and then triturated by the
muscular gizzard of the stomach. Vex-
illum and Austromitra appear to be
adapted for swallowing small pieces of
food which are then moved rapidly to
the mid-oesophagus and are broken down
by the digestive juices secreted by the

338

W. F. PONDER

TABLE 4. The main differences between the 2 subfamilies, Mitrinae and Cylindromitrinae

Feature

Shell

Radular formula 1-1-1

Head-foot

i D ASS

Alimentary canal

Proboscis long, rather broad

Epiproboscis
Salivary ducts

Stomach
oesophageal region

gland of Leiblein and possibly the mid-
oesophageal glands. Cernohorsky (1965)
has observed Vexillum species envelop-
ing prey with the foot after the manner
of some Olividae. The Volutomitridae
probably scrape particles of flesh or
may even feed on body fluids which are
sucked into the proboscis by the power-
ful buccal walls. Again preliminary
breakdown of food may occur by a
secretion from the mid-oesophageal
glands, but in addition some of the
epithelium of the gland of Leiblein is in
direct contact with the food as this epi-
thelium is incorporated in the oesopha-
gus. Possibly a protostyle is sometimes
formed in the style sac, which may ac-
count for the retention of that part of
the stomach, and for the presence of a
gastric shield.

Raeihle (1969) has shown that Thala
floridana (Dall) feeds on a variety of
gastropods which it kills by a sting
from its extended proboscis. Cerno-
horsky (1970) also notes an observation
(but does not give a source) of a species
of Thala “killing another mollusc with
the extendable poison gland”. This
genus has a vexillid type of radula and
Shell and may eventually prove to be

MITRINAE

variable in outline, often
elongate

| small in relation to shell

moderately large in relation
to the powerful buccal mass

free from oesophageal wall

with muscular gizzard in

CYLINDROMITRINAE

cylindrical, with depressed
spire

0-1-0

large in relation to shell

very long, narrow

very large in relation to the
minute buccal mass

apparently within wall of
oesophagus

apparently no muscular
region

an atypical mitrid when anatomical in-
formation is available.

Risbec (1955) has noted the advantage
of columellar plaits in providing “slip
free traction” for the columellar muscle.
This shell feature has been evolved
independently in many groups including,
within the Neogastropoda, the Volutidae,
Olividae, Fasciolariidae, Turridae (Bor-
soniinae), Marginellidae and the Turbin-
ellidae, and may well have evolved
separately in the 3 families of mitri-
form gastropods,

ACKNOWLEDGEMENTS

The writer wishes to express his
thanks to Dr. R. K. Dell and Professor
J. E. Morton for their help and encour-
agement throughout the course of this
work. Some of the material used in
this investigation was collected by the
writer on the New Zealand Marine De-
partment vessel “Ikatere”, and for the
use of this facility the writer is grate-
ful to the then Acting Director of Fish-
eries Research, Mr. J. Brodie. Other
material was provided by Dr. A. W. B.
Powell and Dr. R. K. Dell. The work
was supported in part by a Post-gradu-

MORPHOLOGY OF MITRIFORM GASTROPODS 339

ate Scholorship and a Research Grant
(A.G.140 Zool.38) awarded by the Uni-
versity of Auckland and also by a re-
search grant, GB-3974 from the National
Science Foundation, Washington, D.C.
Thanks are also due to Dr. M. J. Win-
terbourn and Mr. R. G. Ordish for their
critical reading of the manuscript and
to Dr. J. B. Burch and Mr. L. D, Ross
for their assistance in the field.

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ZUSAMMENFASSUNG

DIE MORPHOLOGIE EINIGER MITRIFORMER GASTROPODEN UNTER
BESONDERER BERUCKSICHTIGUNG IHRES VERDAUUNGS-
UND GESCHLECHTSAPPARATTS (NEOGASTROPODA)

W. F. Ponder

Verdauungskanal und Geschlechtsapparat von Strigatella paupercula (Linnaeus),
Austromitra rubiginosa (Hutton) und Peculator hedleyi (Murdoch) werden ausführlich
beschrieben und mit denen einiger verwandter Arten verglichen. Die hauptsächlichen
Merkmale von Kopf, Fuss, Mantelhöhle, Nieren und Schlundring-Ganglien werden

kurz angegeben.

Die Arten gehören zu 3 Familien, den Mitridae, Vexillidae und Volutomitridae,
wobei jede Familie einen besonderen Typus des Verdauungskanals aufweist. Eine
besondere Epiproboscis an der Proboscis der Mitridae dient als Träger der Speichel-

gänge.

Zusätzliche Speicheldrüsen und eine Leibleinsche Drüse sind bei den Vexilli-

MORPHOLOGY OF MITRIFORM GASTROPODS

dae und Volutomitridae vorhanden, fehlen aber beide in den Mitridae. Während der
Verdauungskanal der Vexillidae und Volutomitridae manche Züge gemeinsam haben,
sind ihre Geschlechtswege ganz verschieden. Die Geschlechtsapparate der Vexillidae
und Mitridae sind sehr ähnlich. Gemeinsame Merkmale der besprochenen Arten sind
u.a. eine Analdrüse, Columellarfalten und Fehlen eines Operculums, ebenso eine
allgemeine Ähnlichkeit der Schalen, welche Ähnlichkeiten der Autor für weniger aus-
schlaggebend für die Beurteilung der Verwandtschaft der Familien hält. Andere
Merkmale der Mitridae (s.s.), die bei den anderen 2 Familien nicht vorkommen sind
eine hypobranchiale Purpursekretion, vasenförmige Eikapseln und eine ventrale
Fussdrüse bei den Weibchen. Die Eikapseln von Austromitra und Microvoluta sind
halbkugelig. Die Niere der Mitridae hat die primären und sekundären Lamellen an
getrennten Stellen, sie greifen bei den anderen 2 Familien ineinander. Es scheinen
keine wesentlichen Unterschiede der Schlundringganglien der 3 Gruppen zu bestehen.

HZ:

RÉSUMÉ

LA MORPHOLOGIE DE QUELQUES GASTÉROPODES MITRIFORMES
AVEC RÉFÉRENCE SPÉCIALE À LEUR APPAREIL
DIGESTIF ET REPRODUCTEUR (NÉOGASTROPODA)

W. F. Ponder

Les appareils digestif et reproducteur de Strigatella paupercula (L.), Austromitra
rubiginosa (Hutton) et Peculator hedleyi (Murdoch) sont décrits en détail et comparés
a ceux de plusieurs especes voisines. Lesprincipaux caracteres de la téte et du pied,
de la cavité palléale, du rein et des ganglions périoesophagiens sont brièvement
indiques.

Les especes decrites se rapportent ä 3 familles, les Mitridae, Vexillidae et Voluto-
mitridae, chaque famille ayant un type distinctif d’appareil digestif. Un épiproboscis
particulier, présent dans le proboscis des Mitridae, sert de véhicule aux conduits
salivaires. Des glandes salivaires accessoires et une glande de Leiblein se rencon-
trent chez les Vexillidae et les Volutomitridae, mais sont toutes deux absentes chez
les Mitridae. Tandis que les appareils digestifs des Vexillidae et des Volutomitridae
ont plusieurs traits communs, leurs tractus génitaux sont tout a fait distincts. Les
structures de l’appareil reproducteur des Vexillidae et des Mitridae sont tres sem-
blables. Les traits communs des espéces considérées sont: glande anale, plis colu-
mellaires et absence d’opercule, ainsi que similarité générale de leur coquille,
caractéres que l’auteur considere comme d’importance secondaire, vu qu’il évalue
leur parenté au niveau de la famille. D’autres caractéres des Mitridae (s.s.), non
rencontrés dans les 2 autresfamilles, comprend une sécrétion pourpre hypobranchiale,
des capsules ovigéres enforme de vase et une glande pédiale ventrale chez les femelles,
Les capsules ovigeres d’Austromitra et Microvoluta sont hemispheriques. Le rein a
des lamelles primaires et secondaires nettement séparées chez les-Mitridae, mais
elles sont interdigitées chez les 2 autres familles. Il ne semble pas y avoir de dif-
férence significative entre les ganglions circum-oesophagiens des 3 groupes.

А. Г.

RESUMEN

MORFOLOGIA DE ALGUNOS NEOGASTROPODA MITRIFORMES CON
REFERENCIA ESPECIAL A SUS SISTEMAS DIGESTIVO Y REPRODUCTOR

W. F. Ponder
El canal alimenticio y sistema reproductor en Strigatella paupercula (L.),

Austromita rubiginosa (Hutton) y Peculator hedleyi (Murdoch), se describe ye se com-
para en detalle, con aquellos de otras especies aliadas. Se indicanbrevemente los

341

342

W. F. PONDER

aspectos principales de la cabeza, pié, cavidad paleal, órganos renales y ganglios
circunesofágicos.

Las especies así descriptas pertenecen a tres familias: Mitridae, Vexillidae y
Volutomitridae, cada una con un tipo de canal alimenticio distinto. Una epiproboscis
peculiar, presente en la proboscis de los Mitridae, sirve de vehículo a los conductos
salivares. Glándulas salivares accesorias aparecen, asi como una glándula de
Leiblein, en los Vexillidae y Volutomitridae, pero estan ausentes en los Mitridae.
Aunque el canal alimenticio en Vexillidae y Volutomitridae tienen muchos aspectos
comunes sus conductos genitales son muy distintos. Caracteres comunes a las espe-
cies consideradas incluyen una glándula anal, placas columelares, y ausencia de
opérculo, asi como similaridad general en las conchas que el autor considera de
importancia secundaria en la apreciación de las relaciones al nivel de familia. Otros
caracteres de los Mitridae (s. 5.) que по se encuentran en las otras familias son:
secreciön hipobranquial purpurea, capsulas ovigeras vasiformes, y una glandula
pedal ventral en las hembras. Las capsulas ovigeras de Austromitra y Microvoluta
son esféricas. El Órgano renal tiene las lamelas primarias y secundarias en areas
separadas en los Mitridae, pero son interdigitadas en las otras dos familias. Los
ganglios circunesofágicos en los tres grupos parecen no tener diferencias de signi-
cación.

J. J. P.

ABCTPAKT

МОРФОЛОГИЯ НЕКОТОРЫХ МИТРИДООБРАЗНЫХ GASTROPODA (NEOGASTROPODA),
ОСОБЕННО ИХ ПИЩЕВАРИТЕЛЬНОЙ И ПОЛОВОЙ СИСТЕМ

В.Ф. ПОНЛЕР

Детально описывается строение пищеварителвной и половой систем у
Strigatella paupercula (L.), Austromitra rubignosa (Hutton) и Peculator hedleyi (Murdoch)

Y проводится их сравнение с некоторыми близкими видами. Вкратце
приводится описание основных черт строения области голова-нога,
мантийной полости, почечного органа и вокругглоточно го ган глия.

Рассмотренные виды относятся к трем семействам - Mitridae, Vexillidae и
Volutomitridae. Виды каждого семейства имеют различный тип строения
пищеварительного канала. Особый epiproboscis, имеющийся Ha proboscis Митрид
служит путепроводом для слюнных протоков. Дополнительные слюнные железы
и железа Леблейна имеются y Vexillidae и Volutomitridae, но отсутствуют y
Митрид. В то время, как пищеварительная система y Vexillidae и
Volutomitridae имеют некоторые обшие черты, строение их половых протоков
совершенно различно. Строение половой системы у Vexillidae и Mitridae очень
сходно. Общим для них является наличие анальной железы, колюмеиллярных
складок и отсутсвие operculum, а также имеется сходство в общем строении
их раковин. Эти признаки считаются второстепенными при установлении их
родственных связей на уровне семейства. Другие признаки Mitridae (s.s.),
He найденные у двух других семейств, - это гипобранхиальная секреция
пурпура, вазообразные яйцевые капсулы и (y самок) наличие с брюшной
стороны ножной железы. Яйцевые капсулы y Austromitra и Microvoluta -
полусферические. Почечный орган у Mitridae имеет раздельные первичную и
вторичную пластинки, в то время, как у двух других семейств они имеют
пальцевидные выросты. Видимо, никаких значительных различий у всех
трех групп в строении вокругглоточного ганглия нет.

Z. A. Е.

MALACOLOGIA, 1972, 11(2): 343-350

DISTRIBUTION AND AGE OF MARGARITIFERA MARGARITIFERA (L.)
IN A MADISON RIVER (MONTANA, U.S.A.) MUSSEL BED!

Quentin J. Stober?

Department of Zoology and Entomology
Montana State University, Bozeman, Montana, U.S.A.

ABSTRACT

The distribution of Margaritifera margaritifera (L.) in a Madison River mus-
sel bed 26 x 130 m was investigated during the winter of 1968. Mussels were
found to be concentrated in small scoured depressions and were not randomly
distributed. They preferred stony bottom areas with sufficient water velocity
to prevent deposition of sand, silt and detritus.

The annuli in the ligaments of 4 relatively young mussels (ages 10, 11, 16 and
16 years) were measured and averaged to obtain a ligament growth curve for the
Madison River population. Ages for 84 mussels were determined on the basis
of this curve. The minimum and maximum ages were 10 and 67 years respec-
tively, with an average of 47.9 years. Of 171 mussels examined, total length
measurements of 86.5% were between 80 and 95mm. The slope (0.745) of the
regression of shell weight versus age was considered to reflect the average
annual weight increase. A comparison of growth curves for the Madison River,
Arctic, and Southern Sweden indicated that Madison River mussels grew ata

faster rate than those collected in Sweden.

INTRODUC TION

The North American freshwater pearl
mussel, Margaritifera margaritifera(L.)
has received relatively less attention
than other large freshwater pelecypods.
Several investigators have estimatedthe
extreme ageattainedby M. margaritifera
(Comfort, 1957). A reliable aging tech-
nique was developedby Hendelberg (1960)
to determine the age of pearl mussels
from Arctic Sweden. Bjork (1962), fol-
lowing Hendelberg’s method, determined
the age and growth of the pearl mussel
in Southern Sweden. No information
was found for age of North American
mussels using this technique. Chamber-
lain (1931) used the common method of
counting annuli on the valves in aging

freshwater mussels.

It has been established that the fresh-
water pearl mussel exhibits a holarctic
distribution, inhabiting northern Europe,
northern Asia, Japan, Iceland, and north-
ern North America (Simpson, 1900).
The North American distribution has
been described to include the Eastern
Seaboard from Labrador to Pennsyl-
vania, and western North America west
of the Rocky Mountains from Alaska to
California. Two exceptions to this
general distribution pattern have been
discussed (Walker, 1910), one of which
describes the pearl mussel in the head-
waters of the Missouri River above the
Great Falls. Van der Schalie (1945)
described the region of Yellowstone Park
as an area where confluence probably

lContribution of Zoology and Entomology Department, Montana Agricultural Experiment Station,

Project No. 410, Journal Series No. 257.

2Present Address: Fisheries Research Institute, College of Fisheries, WH-10, University of

Washington, Seattle, Washington 98195, U.S.A.

(343)

344 Q. J. STOBER

occurred between the Missouri (Missis-
sippi River-Gulf of Mexico drainage)
and Snake Rivers (Columbia River-Pa-
cific Ocean drainage) over Two Ocean
Pass, accounting for the present mus-
sel distribution. The Gallatin River in
Montana is the only tributary to the
Missouri River which has been speci-
fically cited in the previous literature
to contain M. margaritifera (Walker,
1910).

From casual observation, it was ap-
parent that the pearl mussel was rela-
tively abundant in the Madison River.
The Madison and Gallatin Rivers join
with the Jefferson River at the Three
Forks of the Missouri River. This
study was designed to determine the age
composition and distribution of amussel
population in a single area of the Madi-
son River, Madison County, Montana,
U.S.A}

Field observations were made from
January 15-March 23, 1968 and on Aug-
ust 27, 1969. The mussel bed studied
was 0,6 km upstream from the conflu-
ence of Hot Springs Creek below Ennis
Lake at about 45°35'N latitude, 111°36'
W longitude and 274 m elevation M.S.L.

METHODS

Observations of mussels in the river
were made with the aid of a waterglass
and by diving. Mussels were collected
with a small rake to dislodge them from
the substrate or by handpicking while
diving. Specimens were preserved in
70% ethanol. Water velocities were
measured with a Pygmy current meter,

Ages of older mussels were not readily
obtained because of erosion of the liga-
ment and shell. The method of counting
annuli on the valves could not be used
as a reliable aging technique of M.
margaritifera due to excessive shell
erosion, Therefore, age determinations
were made using the method described
by Hendelberg (1960). The valves of
each mussel were separated by cutting
the ligament in sagittal section. A
growth curve for the ligament was devel-

oped from 4 young individuals by mea-
suring the distance from the center of
the umbo to the posterior margin of each
annual layer. These measurements were
averaged to obtain a ligament growth
curve which was used to determine the
age of all other mussels with an eroded
ligament distance of less than 32 mm,
A correlation of the ligament annuli with
the annular growth lines of the shell was
made for the 4 young individuals, This
was done by cutting through the umbo to
the ventral margin to expose the valve
annuli. This insured accuracy equiva-
lent to the valve annuli counting tech-
nique for the ligament growth curve.
Each mussel was aged by counting the
annual layers of the existing ligament
and measuring the distance (in mm) of
eroded ligament from the umbo to the
posterior margin of the first existing
annual layer of the ligament. The age
equivalent of the eroded ligament was
determined from the ligament growth
curve. The total age was obtained by
the addition of the number of existing
annual ligament layers counted and the
equivalent age of the eroded ligament
determined from the growth curve.

Shell measurements were taken with
calipers following the method of Hendel-
berg (1960) and Bjork (1962) with the
periostracum intact. Shell weights were
determined on air-dried shells with a
Mettler balance.

RESULTS
Description of the Study Area

The study area in which the fresh-
water pearl mussel was most abundant
was 26 m wide and extended 130 malong
the west shore ofthe river. Water veloc-
ities and scouring of the bottom were
generally less due tothe nearshore loca-
tion and presence of several large boul-
ders which tended to divert the main
flow of the river and to reduce velocities
to less than those observed at midstream.
Ice covered the area on January 15,
1968 except for a few open holes where
high water velocities occurred; however,

|

|

direction did not seem to

BIOLOGY OF FRESHWATER MUSSEL

the main river channel remained open
during the entire winter. The study
area was ice-freeafter January 31, 1968.
Water temperatures increased from 1-
5°C during the winter period. Air
temperatures fluctuated from 5-12°C.
Discharge during the winter observation
period ranged from 29.4-55.5 m°/sec
and averaged 44.9 m°/sec (Anon., 1968)
measured approximately 11.3 km above
the study area.

Distribution

Mussels were found to be restricted
to small scoured depressions 0.6-1.2 m
wide by 1.5-3.7 m long and were not
randomly distributed. The scoured de-
pressions, free of silt and fine sand,
existed between beds of submerged root-
ed aquatic vegetation. All mussels were
removed from 10 scoured areas; how-
ever, many other areas were observed,
Mussel density ranged from 1-32 and
averaged 11.6 per scoured area. Water
velocity in the scoured depressions
ranged from 0.12-0.21 m/sec at 0.02 m
above the substratum, and from 0.38-
0.69 m/sec at 0.3-0.5 m above the sub-
stratum. All mussels were collected
in water ranging in depth from 0,5-
0.8 m.

The substratum type in the scoured
depressions ranged from coarse sand
to rubble 38 cm in diameter, with the
major substratum type being rubble
10-15 cm in diameter and coarse sand
in which most of the mussels were
found. Mussels were seldom found in
areas where rooted aquatic vegetation
tended to collect fine sand, silt and
detritus.

Most mussels were anchored with the
foot firmly in the substratum, However,
some were completely exposed and un-
attached, while others were buried with
only the siphons visible. A few mussels
were found partially buried near areas
of deposition of sand and silt. Current
influence
mussel orientation on the bottom. Fila-
mentous algae were frequently attached
to the valves around the siphons, and

345

Aufwuchs composed largely of diatoms
commonly covered the valves of the
exposed mussels, Areas of stable sub-
stratum, without deposition of sand and
silt, appeared to be most conducive to
mussel survival.

The study area was observed once on
August 27, 1969; no differences in mus-
sel distribution or orientation were de-
tected from prior winter observations,

Age and Ligament Growth

Age determinations were made on 84
of 171 mussels collected. Severe erosion
of the ligament and shell precluded aging
more than 50% of the sample. The 4
individuals selected for the ligament
growth curve were determined to be 10,
11, 16 and 16 years old with respective
total lengths of 69, 72, 73 and 88 mm.
These were the youngest mussels col-
lected and exhibited the least erosion
of ligament and shell. A special effort
was made to obtain additional young
mussels from the study area, but none
were found. Measurements ofthe annual
growth lines of the ligament from these
4 mussels were plotted and averaged to
form a Madison River aging curve (Fig.
1). The year in which the mussel passed
the glochidium stage was not included.
Ages for all other mussels were deter-
mined using this curve plus the number
of existing ligament annuli. The greatest
error of the curve was estimated to be
+ 3 years for a mussel with 32 mm ero-
ded from the ligament. This could
result in an error of approximately 4%
for a 67 yr old mussel, The error in
the aging curve is reduced with a de-
crease in length of eroded ligament, Of
the 84 mussels aged, the minimum age
was 10 years and the maximum age was
67 years. The average age was 47.9
years. The standard deviation and stan-
dard error of the mean are given in
Table 1. The dominant age class was
47 years with 9 individuals.

Ligament growth curves for Arctic
Sweden, about 66°30" N latitude (Hendel-
berg, 1960) and Southern Sweden, about
56°15'N latitude (Bjork, 1962) have been

346 Q. J. STOBER

40

36

32

28

24

20

Distance umbo-posterior margin of ligament growth layer,mm

16
12
В
и С Madison River
8 ; D
; Mean
Mean Arctic Sweden (Pärlälven)
4 Mean Southern Sweden (Silletorpsan)
O

4 8 12 16 20 24
Age (Years)

FIG. 1. Ligament growth curve developed and used to determine the ages of Madison River
pearl mussels, and mean curves for Arctic (Hendelberg, 1960) and Southern (Bjork, 1962)
Sweden pearl mussels.

BIOLOGY OF FRESHWATER MUSSEL 347

10
9
8
г:
2:6
5 ===" Not Aged
zZ
4
3
2
| [ yt [
| H - 1
O
60 70
Length(mm)

хо © &

00
О
©
O
Q
O

FIG. 2. Length-frequency relationship of aged and unaged Madison River mussels.

included in Fig. 1 for comparison with
Madison River mussels.

Length Frequency

Length frequency analysis of all the
mussels collected is shown in Fig. 2.
Fifteen mussels (8.8%) were less than
80 mm in length and 86.5% of the total
sample was between 80 and 95 mm.
Eight mussels (4.7%) were greater than
95 mm. Aged mussels are distinguished
from unaged mussels for each length
class and the former are represented
over the length frequency except above
95mm. Mussels of a length greater
than 95 mm may have been older than
the maximum age determined; however,
aging was not possible due to excessive
ligament and shell erosion.

| Shell Analysis

Shell analysis is given in Table 1.
The mean total length was 86.7 mm.
Shell thickness (width) averaged 28.4 mm
and mean shell umbonal height was

43.8 mm.
grams,

Shell weight was found to increase
over the life of the freshwater pearl
mussel, The slope of the regression
line (0.745), fitted by the method of
least squares, is the average annual
shell weight increase per year in grams
(Fig. 3).

Mean Shell weight was 49.6

DISC USSION

The habitat of Margaritifera marga-
ritifera was very well defined and limi-
ted to the scoured areas of the mussel
bed. Stony bottom areas with sufficient
water velocity to prevent deposition of
sand and silt were preferred. The distri-
bution and habitat requirements of Madi-
son River mussels were similar to those
reported for Swedish streams by Hen-
delberg (1960) and Bjork (1962). Acom-
parison of the ligament growth rates
in Fig. 1 suggests that Madison River
mussels grew at a faster rate thanthose

348 Q. J. STOBER

TABLE 1. Analysis of shell measurements of Margaritifera margaritifera from the Madison
River.

Statistic

n=
Range
Mean
Standard deviation

Standard error of mean

80
ff OR
e
mal
ee
e
60|-
= sor y=14.1+ 0.739x
5 = pe ore e
= 40+ e ... =
no e
5 5
=
3 30H
=
20H e
.
10 |
fe) L Je 1 1 Sit l J
10 20 30 40 50 60 70
Age (Years)
FIG. 3. Regression of age versus shell

weight of Madison River mussels.

collected in Arctic or Southern Sweden.
Pearl mussels in Southern Sweden have
a faster growth rate than those in the
Arctic. The lower latitude of the Madi-
son River may account for a faster
growth rate, as demonstrated for the
razor clam (Weymouth, McMillin & Rich,
1931); however, differences in altitude
and water quality have not been examined.
Bjork (1962) found a difference in growth

Total length Width Umbonal height
(mm) (mm) (mm)

Age
(years)

rates in 2 streams, Brünnestadsän and
Silletorpsan, in Southern Sweden. Mus-
sels from the former streamapproached
the Madison River growth curve closely.
Madison River mussels attain a shorter
total length and none were found that
had reached the extreme age of 116
years reported by Hendelberg (1960)
for Arctic Sweden pearl mussels. The
lack of mussels approaching an age of
100 years in Southern Sweden may be due
to 2 factors pointed out by Bjork (1962);
pearl fishing and accelerated growth
rates.

The age and length analyses indicate
the Madison River population is domi-
nated by the older year classes witha
lack of very young mussels. This con-
dition has been found to occur in Arctic
Sweden and in most pearl mussel popu-
lations investigated. Mussels of the
Madison River have not been exploited
as those in Sweden,

A thorough field investigation of M.
margaritifera in the Madison River is
needed to determine reasons for the lack
of younger age classes,

ACKNOWLEDGEMENTS

Thanks are due Dr. C. J. D. Brown
who suggested this investigation and re-
viewed the manuscript, and to Angie
Stober who provided assistance in data
analysis,

BIOLOGY OF FRESHWATER MUSSEL 349

LITERATURE CITED

ANONYMOUS, 1968, Geological Survey,
U.S. Dept. of Interior, Water Resour-
ces Data for Montana. Part 1. Sur-
face Water Records. 41 p.

BJORK, S., 1962, Investigations on Mar-
gavitifera margaritifera and Unio
crassus. Acta Limnologica (4) 109 p.

CHAMBERLAIN, T. K., 1931, Annual
growth of freshwater mussels, Bull.
U.S. Bur. Fish., 46: 713-739.

COMFORT, A., 1957, The duration of
life in molluscs. Proc. malacol. Soc.
London, 32: 212-241.

HENDELBERG, J., 1960, Thefreshwater
pearl mussel, Margaritifera marga-
ritifeva (L.). Rep. Inst. freshw. Res.,

Drottningh., No. 41: 149-171.

SIMPSON, C. T., 1900, Synopsis of the
Naiades. Proc. U. $. natin. Mus., 22:
501-1044,

VAN DER SCHALIE, H., 1945, The value
of mussel distribution in tracing
stream confluence. Mich. Acad. Sci.,
Arts and Letters, 30: 355-373.

WALKER, B., 1910, The distribution of
Margaritifera margaritifera. (Linn.)
in North America. Proc. malacol.
Soc. London, 9: 126-145.

WEYMOUTH, F. W., MCMILLIN, H. C.
& RICH, W. H., 1931, Latitude and
relative growth in the razor clam,
Siliqua patula. J. exp. Biol., 8: 228-
249,

ZUSAMMENFASSUNG

VERTEILUNG UND ALTER DER MARGARITIFERA MARGARITIFERA (L.)
IN EINER MUSCHELBANK DES MADISON RIVER (MONTANA, U.S.A.)

Q. J. Stober

Die Verteilung der Margaritifera margaritifera (L.) in einer Muschelbank des
Madison River in einer Ausdehnung von 26 x 130 m wurde in Winter 1968 untersucht.
Die Muschel befanden sich in kleinen ausgewaschenen Vertiefungen zusammengedrangt
und waren nich regellos verteilt. Sie bevorzugten steinige Bodenstellen unter genügend
starter Strömung, die den Absatz von Sand, Schlamm und Detritus verhinderte,

Die Zuwachsstreifen im Ligament von 4 verhältnismässig jungen Muscheln (10, 11
und 2 Stück 16 Jahre alt) wurden gemessen und ihr Durchschnitt errechnet, um eine
Ligament-Wachstumskurve für die Population des Madison River zu erhalten. Das
Alter von 84 Individuen wurde auf Grund dieser Kurve bestimmt. Die Muscheln waren
zwischen 10 und 67 Jahre alt, im Durchschnitt 47,9 Jahre. Von 171 untersuchten
Muscheln waren 86% zwischen 80 und 95 mm lang. Der Gewichtsverlust der Schale im
Alter entsprach dem durchschnittlichen jährlichen Gewichtszuwachs. Ein Vergleich
der Wachstumskurven für den Madison River, sowie das arktische und südliche
gebiet Schwedens zeigte, dass die Muscheln des Madison River schneller wuchsen als
die in Schweden gesammelten.

H. 2.

RESUME

DISTRIBUTION ET ÄGE DE MARGARITIFERA MARGARITIFERA (L.)
DANS UN BANC MOULIER DE LA RIVIERE MADISON (MONTANA, U.S.A.)

Q. J. Stober
La distribution de Margaritifera margaritifera (L.) dans un banc moulier de la

rivière Madison de 26 x 130 m a été étudiée pendant l’hiver 1968. Les mulettes se
concentrent dans de petites dépressions d’affouillement et ne sont pas régulièrement

350

Q. J. STOBER

distribuées. Elles préfèrent les fonds rocheux avec assez de vitesse de courant pour
éviter le dépôt de sable, argile et détritus.

Les anneaux de croissance du ligament de 4 spécimens relativement jeunes (Age
10, 11, 16 et 16 ans) ont été mesurés et étalonnés de façon à obtenir une courbe de
croissance du ligament pour la population de la rivière Madison. Les âges de 84
mulettes ont été déterminés d’après cette courbe. Les 4ges minimum et maximum
ont été 10 et 67 ans respectivement, avec une moyenne de 47,9 ans. Sur 171
échantillons mesurés, la longueur totale de 86,5% d’entre eux était comprise entre
80 et 95 mm. On estime que la pente (0,745) de régression du poids de la coquille en
fonction de l’âge, reflète la moyenne annuelle del’augmentation de poids. Une compa-
raison des courbes de croissance pour la riviére Madison, le sud, et la région arctique,
de la Suède, montre que les mulettes de la rivière Madison s’accroissent selon un
taux plus rapide que celles récoltées en Suede.

IES

RESUMEN

DISTRIBUCION Y EDAD DE MARGARITIFERA MARGARITIFERA (L.)
EN UNA CAMADA DE ALMEJAS DEL RIO MADISON (MONTANA, U.S.A.)

Q. J. Stober

En el invierno de 1968 se investigó la distribución de Margaritifera margaritifera
(L.) en el Río Madison, en un área de 26x 130 metros, donde las almejas se encontra-
ron no esparcidas sino concentradas en fondos pedregosos y donde la corriente era
lo suficientemente veloz como para prevenir sedimentación arenosa, limosa o de
detritos.

Los anillos en el ligamento de 4 ejemplares relativamente jóvenes (10, 11, 16 y 16
años) se midieron para obtener la curva de crecimiento para el ligamento, en la
población del Río Madison. Las edades de 84 almejas fueron determinadas en base
a esa curva. Las edades mínimas y máximas fueron 10 y 67 años respectivamente,
con un promedio de 47.9 años. En 171 almejas examinadas, el 86.5% tenian una
longitud total de 80-95 mm. El descenso regresivo (0.745) del peso de la concha versus
edad, se consideró que reflejaba el promedio anual del aumento de peso. Una com-
paración de las curvas de crecimiento del ligamento de las almejas del Río Madison,
y de las regiones del sur y ártico de Suecia, indican que las del Río Madison crecieron
más rápido que aquellas colectadas en Suecia.

J.J. Р.

ABCTPAKT

РАСПРОСТРАНЕНИЕ И ВОЗРАСТ MARGARITIFERA MARGARITIFERA
НА МОЛЛЮСКОВЫХ БАНКАХ Р.МЭДИСОН ( США)

К. СТОБЕР
Зимой 1968 года исследовалось распространение Margaritifera margaritifera

(L.) на банках в р.Мэдисон, площадью 26х130 метров. Было отмечено, что
моллюски сконцентрированы в небольших углублениях дна и распространены

неравномерно. Моллюски предпочитали каменистое дно и течение
значительной силы, которое препятствовало накоплению песка, ила
и детрита. Измерялись годовые кольца в лигаменте у относительно

"молодых" моллюсков (в возрасте 10, 11 и 16 лет), чтобы получить данные
по росту лигамента в популяциях моллюсков в р.Мэдисон. На основании
полученной кривой был определен возраст у 84 моллюсков. Наименьший и
наибольший возраст был 10 и 67 лет, соответственно, среднее - 47.9 лет.
У 171 исследованного моллюска 86.5% общей длины было между 80 и 95 мм.
Угол регрессии (0.745) веса раковин в сравнении с возрастом отражал
среднее годовое увеличение их веса. Сравнение кривых роста моллюсков из
р.Мэдисон, Арктики и Ю. Швеции показало, что моллюски из р.Мэдисон
росли быстрее, чем в Южной Швеции.

7. А. Е

| MALACOLOGIA, 1972, 11(2): 351-364

LIFE HISTORY OF PLEUROBEMA CORDATUM (RAFINESQUE 1820)
(BIVALVIA: UNIONACEA)

Paul Yokley, Jr.

Department of Science
Florence State University
Florence, Alabama 35630, U. S. A.

ABSTRACT

The Ohio pigtoe mussel, a commercially valuable species, inhabits the largest
rivers of the Ohio River drainage system and also occurs in concentrations or
“mussel beds” in the Tennessee River. Oogenesis and spermatogenesis follow
an annual cycle, with spawning and fertilization in April and May. The seasonal
changes in gonad histology are described. Four to 6 weeks after fertilization,
the marsupial outer demibranchs are found to contain glochidia. Larval devel-
opment to this stage is dependent on water temperatures above about DIG. In
the laboratory experiments the parasitic glochidia, released mainly in June,
attach to the gill filaments of the rosefin shiner, Notropis ardens (Cope), en-
cyst, and transform into independent mussels in 14-18 days. A motile foot de-
velops during encystment but no increase in overall size results. Within 3 weeks
after dropping from the host fish, the free-living naiads double in size. Sexual
maturity is reached within 4 years, and the gonads remain functional throughout

the mussel’s remaining 25-30 years of life.

INTRODUCTION

The Ohio pigtoe mussel, Pleurobema
cordatum (Rafinesque, 1820), (Unionidae:
Ambleminae) is a widely distributed ovo-
viviparous naiad in the Tennessee River.
Its economic history dates back to 1883
when it was a source of raw material
for a short-lived pearl button plant at
Knoxville, Tennessee, U.S.A. In 1914
the Tennessee River furnished nearly
650 tons of mussel shells to the pearl
button industry (TVA, 1966).

After the mainstream dams were built
by the Tennessee Valley Authority (TVA)
in the late 1930’s and early 1940’s,
mussel fishermen and many biologists
predicted mussels would die out in the
river. But, in 1945 many species were
still alive, and the shell harvest was
resumed after a lapse of 9 years, rising
from 3,700 tons in 1945 to nearly 10,000
tons in 1947. The mainstream reser-
voirs of the Tennessee River became
the most important source of fresh-
water mussel shells in the United States

(TVA, 1966).

Pearl buttons were gradually replaced
by synthetics, but the cultured pearl
industry created a new demand for the
freshwater mussel shells. Again, P.
cordatum possessed the desired char-
acteristics, including color, luster, and
toughness, (Figs. 3, 4) required by this
industry (Yokley, 1968).

The shell harvest rose annually during
the decade following 1945, but in 1956
it was much reduced. Subsequently,
the United States Fish and Wildlife
Service conducted studies on the species
(Scruggs, 1960). This survey revealed
that adult pigtoes were being harvested
23 times faster than they were being
replaced by younger ones. Also, it
showed that the majority of the mussels
were older than 12 years. The exact
cause of this could not be determined
since the life history of this species, in
particular the host fish, was largely un-
known, After reviewing the literature
of Surber (1912), Lefevre & Winterton
(1912), Howard (1913), Coker, et al.

(351)

352

MUSSEL
(FIRST DAY FROM HOST FISH) =

bora,
= 217 оон

Y ez

7 E, A y
Æ à 7 i

e у AS

$ 220) ze
A a

rs = Bobs

era =

(Host

FIG. 1.

(1921), Baker (1921), and Jones (1950,
1952) on the subject of hosts of fresh-
water mussels, it appears that none of
these authors were working with P.
cordatum, and therefore this species
has not had its complete life cycle re-
corded. No past records of specific
host fish for P. cordatum have been
found. Scruggs (1960) recorded the
Spawning habits of the pigtoe mussel
as occurring from April through August,
and therefore he may have been working
with more than a single species. Other
studies on the most closely related
species of P. cordatum have recorded
inconclusive evidence of possible host
fish relationships.

The mussel harvest has continued to
drop annually even though more har-
vesting effort has been expended and
more boats and equipment used (Yokley,
1968). In 1963 the TVA began an ex-
tensive study in an attempt to uncover
the reasons for this decline in harvest.
The goals were to determine (1) the
distribution and the density of the mus-
sels, (2) the quality of the habitat, (3)

MATURE MUSSELS

0

P. YOKLEY

GRAVID
Gill

GLOCHIDIUM ATTACHES
ro FISH GILL

Life cycle of Pleurobema cordatum (Ohio pigtoe mussel).

the physical quality of the naiads, and
(4) the life history relationships of the
more important commercial species,
In the present paper the life cycle of
the Ohio pigtoe mussel is described.

EQUIPMENT AND TECHNIQUES

At the outset of this study, specimens
were collected with commercial equip-
ment (variously called by local fisher-
men a “brail”, “dredge”, or “crowfoot
dredge”) which was drawn slowly along
the river bottom. Coker, et al. (1921)
described this equipment indetail. How-
ever, diving proved to be a more effi-
cient method, and many sizes and age
groups were collected by skin diving.

The potential host fish were seined
from the Tennessee River or its tribu-
taries. The rosefin shiners were caught
in Lindsey Branch which empties into
Cypress Creek, Holding tanks for the
potential host fish species were variously
modified until the spring of 1968 when
“Living Stream” tanks were used. These
commercially built tanks were purchased

LIFE HISTORY OF PLEUROBEMA CORDATUM 353

FIGS. 2-3. Shell and gills of Pleurobema

cordatum. Fig. 2. Left valve. Fig. 3. a,
Mantle; b, gravid outer demibranch; d, trans-
parent inner demibranch.

by TVA (Fish and Wildlife Branch) from
a Toledo, Ohio, manufacturer (Frigid
Units, Inc.). The temperature, aeration
and filtration of the water may be regu-
lated in these tanks. Rosefin shiners
retained in the controlled tanks and
individually handled many times re-
mained vigorous and healthy for several
months,

A small, narrow aquarium (1'w x 6"1)
was constructed of cemented pieces of
plate glass. This tank reduced moving
and turning of the fish during exposure
to the glochidia. Concentrations of
glochidia in a pipette weve placed near
the mouth of each fish. As the water
entered the mouth of the fish and passed
over the gills, the suspended glochidia

clamped onto the gill filaments. The
fish were removed from the container
within 3-5 minutes to prevent over-
infestation. Each fish was examined by
placing it under a dissecting microscope
and carefully lifting the operculum to
expose the gill filaments. This was
done very quickly and preferably with
the fish immersed in a container of
water. The glochidia may be easily
observed and counted on each gill. No
attempt was made to determine how
many of the glochidia successfully trans-
formed after attaching to the gills of the
host shiner. Those, however, which were
encysted after 2-3 days usually con-
tinued development through metamor-
phosis.

The parasitized fish were returned
to the holding tanks for 13 days before
being captured by a hand-net and placed
in small plexiglas containers constructed
with round bottoms. Each container
held approximately 3 gallons of water
and 6 parasitized fish. These containers
were placed in the larger tank of water
to maintain the constant water temper-
ature. Individual air supply tubes were
provided for each container, Thetrans-
formed glochidia began leaving the fish
after 14 days of parasitism and con-
tinued to do so through the 18th day.

The independent naiads, settling tothe
lowest area of the containers, were
Siphoned into a tube and placed in small
evaporating dishes (Fig. 14) into which
a constant flow of water was pumped
from the bottom of the holding tank.
Thus, the water temperature remained
equal to that in the holding tank. Oxygen
was provided by the constant dripping
and overflow from the evaporating dish-
es.

Adult naiads were collected during
each month of the year from the Tenne-
ssee River in the vicinity of Muscle
Shoals, Alabama, and pegged (valves
wedged open slightly to allow preserva-
tive to enter) in 10% formalin. These
were later histologically sectioned
through the gonads to determine the
seasonal stages of gametogenesis.

354 PY YOKEEY

FIG. 4. Shell and animal of Pleurobema cordatum. a, White lustrous mother-of-pearl; b,shows
the thickness of the outer gravid demibranch. |

FIG. 5. Glochidia attached to the gill filaments of a fish (the fish operculum has been removed).

LIFE HISTORY OF PLEUROBEMA CORDATUM 355

..
FA
É

yom
NL м м
r

ZT © ”
Я
hay,
VA,
My Y
Mn к i
i wn
Y .
h d'à
m ” *
i ”

Wy

FIG. 6. The acini of the testes, showing several spermatogenic acini and their ducts.
FIG. 7. The acini of the testes, showing the sperm morulae (a).

| FIG. 8. Spermatozoa.

| FIG. 9. The alveoli of the ovary in the spring with large ovocytes.

FIG. 10. The alveoli of the ovary in the late summer, showing atretic material.

FIG. 11. The alveoli of the ovary in the fall (note the thicker walls and numerous cells in the
lumen of each alveolus).

356

GA ME TOGENESIS
Spermatogenesis

The acini (Fig. 6) of the testes are
the sites of spermatogenesis. This
process evidently occurs in the Ohio
pigtoe during all the warm months since
different spermatogenic stages are most
frequently found in the spring, summer
and fall. However, mature spermatozoa
are much more plentiful in the lumina
in early spring when spawning and ferti-
lization occur,

Each acinus may differ slightly from
another in spermatogenic progress, but
typically the following parts are ob-
served. The epithelium contains a
single layer of spermatogonia, recog-
nized by their large but vesicular nu-
clei. Toward the lumina of the acini
are many primary spermatocytes which
have round, morechromatic nuclei and
are a little smaller than the spermato-
gonia. Among the primary spermato-
cytes which fill much of the acini may
be seen small clumps of secondary
spermatocytes, which give rise to sper-
matids by meiosis. Large numbers of
dividing cells showing the various chro-
mosome figures are characteristic of
this area in the fall months. Sertoli
cells appear either yellow or pinkish in
the lumina of the acini when hematoxylin-
eosin stains (H-E) are used. Spermatids
are arranged in clumps, sperm-morulae
(Fig. 7), around the slightly stainedSer-
toli cells. From 2-20 or more may
occur in 1 clump. Spermatids develop
into spermatozoa which remain in the
lumina attached to Sertoli cells until
they pass outside. Each acinus, overall,
stains quite basic with H-E preparations
because of the concentration of chroma-
tic material at this time. Spermatozoa
are elongated rods (Fig. 8) rounded on
one end and slightly concave onthe other,
A very long flagellum has been observed
at the concave end of each spermatozoan
in material from fresh testes,

The condition of the testes in the
Spring months reveals the following
characteristics:

P. YOKLEY

1. Acini enlarged and close to each
other with little tissue separating
them.

2. Lumina of acini filled with mature
spermatozoa.

3. Periphery of acini filled with many
secondary spermatocytes undergo-
ing meiosis,

4, Spermatozoa migrating through the
externally directed tubules.

Summer appears to be a recovery

period for the testes, and they can be
described as follows:

1. Acini reduced in size (Fig. 6) leav-
ing a good deal of space occupied by
connective tissue between acini.

2. Very few mature spermatozoa in
the lumina,

3. Acinus wall build-up begins with
many spermatogonia and primary
spermatocytes, and fewer later sta-
ges.

4. Accumulations of nutrient matter,
possibly stored protein, in the Ser-
toli cells and division of these cells.

The fall condition of the testes is

characterized by the following observa-
tions:

1, The acini are enlarged but not as
large as they appear in the spring.

2. Lumina of acini with few mature
spermatozoa.

3. Division of primary spermatocytes
to secondary spermatocytes preva-
lent.

4, Clusters of these spermatocytes

and Sertoli cells throughout the
acini.

5. Spermatids occupy the lumina of the
acini.

The winter condition of the testes
reveals little change from late fall,
evidently a result of the reduced water
temperature.

There is some overlap in these sea-
sonal differences, but the above condi-
tions prevail in the majority of examined
specimens.

Oogenesis

The female gonopores are located just

posterior to the nephridiopores and ven- |

LIFE HISTORY OF PLEUROBEMA CORDATUM 357

‘tral to the anterior end of the kidneys.
The gametes enter the dorsal mantle
cavity just posterior to the point where
the inner reflected gill lamellae lose the
connection to the dorsal wall. Many of
these gametes are evidently carried in
the current of water flowing posteriorly
in the suprabranchial canals. Exactly
how these sex cells passfrom the supra-
branchial chambers to the outer gill is
not known by the author. Like the
spermatozoa, they may be caught up in
the incurrent flow of water through ostia
of the outer gill, and they may then
lodge in the water tubes. A definite
limiting factor in the successful propa-
gation of this mussel would seem to be
the synchronous requirements of sperm
and egg meeting within the mantle cavity
of the female which is an infinitisimal
fraction of the very large environment
of water surrounding them.

The alveoli of the ovaries are found
to be sufficiently different in the spring,
summer, and fall to warrant description.
In the spring months the following char-
acteristics prevail:

1. The alveolar walls are very thin

(Fig. 9).

2. The lumina of the alveoli are crowd-
ed with large ovocytes (ova).

3. The ovocyte nuclei possess 1 or
more nucleoli.

4. The alveoli are crowded close to
each other in the available space
of the visceral mass,

The summer characteristics are sim-

ilar, but the following generally apply:

1. The alveolar walls are beginning to
rebuild with oogonia.

2. The lumina are almost empty of
large ovocytes,

3. The oocytes and ootids remaining
in the cavities are usually seen to
be smaller and devoid of nucleoli.

4. More space now exists between
the smaller alveoli.

Conditions in the fall may be charac-

terized as follows:

1, Alveolar walls are restored in
thickness as a result of the numer-
ous mitoses.

2. The lumina of the alveoli are crowd-
ed with early oocytes and earlier
meiotic figures (Fig. 11).

3. Most of these newly divided cells
are uniformly small at this season.

4. Atretic material representing older
ovocytes occupy the centers of many
lumina (Fig. 10). These materials
are in the process of break-down,

5. The alveoli again are enlarging in
the visceral mass thus occupying
proportionately more of the avail-
able space.

The colder water in the winter season
reduces the visible changes to a mini-
mum so that late fall conditions are
characteristic throughout the winter.

SYNGAMY AND EMBRYOGENY

The method of reproduction in P.
cordatum is best characterized by the
term ovoviviparous because not only is
fertilization internal but development
occurs while the embryo is retained
within the mother. The animals may
also be termed larviparous since the
offspring are released as glochidial
larvae,

It appears that a freshwater environ-
ment may promote ovoviviparity and dis-
courage most free-swimming larvae.
The river flow and low density of fresh-
water are important factors to support
this inference. Needham (1950) states
that “The existence of minute free-
Swimming larvae in the plankton is a
positive bar to the colonization of flu-
viatile fresh water.” Freshwater is
less buoyant than salt water and greater
energy expenditure would be required of
Swimming larvae. Pennak (1953) notes
the paucity of freshwater invertebrates
that have planktonic young. Theabsence
of a planktonic state has the disadvan-
tage of reducing opportunities for dis-
persal. This has led to a selective ad-
vantage for those species of freshwater
mussels with a temporary parasitic
period on fish. The time spent within
the brood pouch permits the develop-
ment of structural adaptations, including

358 P. YOKLEY |

hooks and byssi, for this next transient
mode of life. The pigtoe mussel pro-
duces large numbers of glochidia and
this high fecundity is doubtlessly linked
to the hazards of parasitism.

The physiological relationship of the
embryo to the maternal organism has
not been studied in this species; however
there is some evidence that the embryos
of Anodonta absorb amoebocytes which
cross the gill epithelium (Pelseneer,
1935). Amoebocytes are abundant in
the loose tissues of the gills of the pigtoe.

Of 318 Ohio pigtoe mussels histologi-
cally examined for sex determination,
nearly 53% were males, 43% were fe-
males, and 4% were sterile (or indeter-
minate in sex).

Sexual maturity, basedonthe presence
of mature gametes in the gonads, is
attained in this species before 4 years
of age. Since specimens younger than
4 years were not available, this study
does not reveal the earliest age of
sexual maturity for the pigtoe. However,
all of the 4- and 5-year-old classes
were sexually mature. The oldest speci-
mens which were examined had func-
tional gonads. The average ages of
these 318 pigtoes were found to be 12-
18 years. These data agree with the
findings of Scruggs (1960).

The Ohio pigtoe is tachytictic, which
means that the embryos are retained
in the parent’s gill for only a short
term. Embryos and larvae have been
found in the enlarged outer gills (Figs.
3, 4) in late April, May, June, and early
July. Slight disturbances may cause
the females to abort, thus emptying the
demibranchs containing the embryos.
These white aborted masses, often called
conglutinates, include unfertilized eggs,
zygotes, and later embryonic stages
developing into glochidia. These stages
indicate that a female produces glochi-
dia which mature and are deposited in
the water a few at a time, rather than
all maturing and leaving at one moment.

Syngamy may occur in the suprabran-
chial tubes of the inner gills just as
the primary oocytes leave the oviduct

openings, or possibly anywhere in the ©
mantle cavity. In addition, the oocytes «
may be fertilized as they move from the |
cloacal chamber to the suprabranchial «
chambers of the outer gills. While ©
examining the contents removed from *
the gravid outer demibranchs of pigtoe «
mussels in May 1967, I observed а’
primary oocyte that had just been ferti- |
lized. The unequal 2, 4 and 8-celled |
stages, as well as the morula and blas-
tula, have been observed,
Pigtoe mussels collected during the
first weeks in May 1967 had enlarged |
outer demibranchs which were examined |
microscopically; most of the cells and |
embryos were just beginning develop- «
ment. In the water tubes of the gills |
there were unfertilized eggs, zygotes and À
early embryos, but no fully develope |
glochidia. |
Motility and spawning of mussels are »
apparently related to a rising water |
|

ae, ST ee

temperature. On March 3, 1967, a 25- |
square-yard area of the Tennessee Riv-
er known to be a “mussel bed” was |
carefully examined for pigtoe mussels
and 7 specimens were found. On April |
2, 1967, the same area yielded 22 pigtoes |
along with several other species. The |
temperature of the water changed from |
8°C on March 3 to 19°C on April2. The
first indications of gravid demibranchs |
were recorded on April 30, 1967, with
3 individuals out of 20 collected having |
swollen outer demibranchs. Thetempe- |
rature was 20°C on this date. The!
average temperature for May 1967 was
approximately 20 °c; and during this |
period 12 of 14 pigtoes had swollen
outer demibranchs which contained early |
developmental stages and only a small |
percentage of mature glochidia. The
mean temperature for June 1967 was |
23 C, and during that month the per- |
centage of gravid females was greatest. |
Examination of the widened demibranchs |
revealed that more than 50% contained |
mature glochidia. The temperature of :
the water in July 1967 averaged below
normal at 26.5°C, and in the first 10
days of that month a few gravid females

LIFE HISTORY OF PLEUROBEMA CORDATUM 359

were found but none thereafter from
early July through the summer of 1967.

These 1967 data indicate that June is
the peak month for glochidia maturation
and release. Similar results have been
noted for 1964, 1965, and 1966. In
this portion of the Tennessee River, no
gravid pigtoes have been found after
July 15. Fertilization and embryonic
development occur in late April and
May. Roughly 4-6 weeks elapse be-
tween fertilization and glochidial re-
lease, and the change in the development
is probably controlled by the rise in
water temperature. Evidently water
temperature must reach a minimum of
20°C before the embryos continue devel-
opment in the marsupial gill.

In the summer of 1965 several gravid
female pigtoes were held in stainless
steel tanks supplied with cool spring
water. The water temperature never
exceeded 20°C through the monthof July.
The average temperature in June was
18°C. Gravid demibranchs examined 2
weeks after mussels had been placed in
the tanks indicated little change beyond
fertilized eggs. The comparatively low
temperatures apparently slowed the de-
velopment of embryos.

Glochidia are most abundant in June
each year or approximately 3-4 weeks
after the water temperature rises to
PIC.

At the time glochidia are mature and
are being released into the water, the
natural fish host should be over the beds.
However, the rosefin shiner appears to
be more common in smaller, more
Shallow, and swifter-flowing streams.
Impoundment may have encouraged this
host fish of the pigtoe mussel to move
out of the main channel of the Tennessee
River, thus reducing the chances of
completing the mussel’s life cycle. Pleu-
robema cordatum is confined to the lar-
gest rivers, but today natural reproduc-
tion may have been interrupted without
a suitable riffle habitat for the rosefin
Shiner along the lower Tennessee River,
Pigtoe populations are becoming older
in average age, and recruitment is ob-

viously decreasing.
THE PARASITIC PERIOD

The glochidium (Figs. 12, 13) of P.
cordatum is small and hookless, mea-
suring about 0.14 mm in length and
0.15 mm in height.

Glochidia are dispersed upward into
the water from the female naiad through
the excurrent aperture. These glochi-
dia possess no byssus but do become
temporarily suspended in a network of
mucus threads flowing through the aper-
ture along with the glochidia. Possibly
rosefin shiners are visually attracted to
these suspended particles and thus be-
come parasitized. These minnows are
Omnivorous and have been observed
schooling near spawning longear sun-
fish. Bits of food dropped or suspended
by the sunfish may attract the shiner
minnows,

Several unsuccessful attempts tofind
the host fish were made before Notropis
ardens (Cope), the rosefin shiner, was
tried. Every fish species used was ex-
perimentally parasitized, but the un-
natural host species sloughed off the
glochidia within a few days. The glochi-
dia were probably destroyed by host
action.

The fish appear to experience an un-
favorable reaction to the initial attach-
ment of the glochidia (Fig. 5). This is
probably not the case in nature since
fewer glochidia per unit volume occur
in the water. The few glochidia that
attach to the gill filaments in nature
probably do not disturb the fish. Micro-
Scopic examination of the gills of the
fish exposed to the glochidia showed many
of the parasites clamped firmly into the
smallest gill filaments, pinching the
small blood vessels so that blood did
not flow.

The glochidia were evenly distributed
over the gills, and 100 or more may
attach to each side of a small minnow
without noticeable damage or injury.
A list of the fish species that have been
parasitized and the results appear in

360 PS YOKUEY

ALES oe 4 3 Re BRENNEN ARE ARE

к DNS eu A SE Y dsd
FIG. 12. The glochidia of Pleurobema cordatum. (a)shows the single adductor muscle from the
lateral view and (b) shows the same muscle from dorsal view of the glochidia.

FIG. 13. The glochidium of Pleurobema cordatum in a position to attach to the gills of a fish.

FIG. 14. The circulating system for raising the young mussels. The young mussels were held
in the evaporating dishes into which a constant flow of water was pumped from the bottom of a
Living Stream tank. The water overflowed back into the tank.

FIG. 15. A young of Pleurobema cordatum the day after dropping from the host fish gill.

LIFE HISTORY OF PLEUROBEMA CORDATUM 361
TABLE 1. Results of fish infections

No. of fish infected Species of fish een | Walt. ae
of glochidia holding tank
25 Largemouth bass 4-5 days ne
Micropterus salmoides
20 Smallmouth bass 3-4 days ACC
Microptevus dolomieui
65 Longear sunfish 4-8 days 21°C
Lepomis megalotis
8 Black crappie 3-6 days 20°C
Pomoxis nigromaculatus
9 White crappie 3-6 days 20°C
Pomoxis annularis
20 Bluegill sunfish 4-5 days 2196
Lepomis macrochiris
8 Redear sunfish 2-3 days 21°C
Lepomis microlophus
12 Green sunfish 2-3 days 21°C
Lepomis cyanellus
81 Rosefin shiner 14-18 days 21°C
Notropis ardens
3 Tennessee snubnose darter few hours ACE
Etheostoma simoterum
3 Logperch darter few hours AE
Percina caprodes
2 Black bullhead few hours DAO
Ictalurus melas
il Smallmouth buffalo 2-3 days ZC

Ictiobus bubalus

Table 1. The artificial infections were
attempted several times with these spe-
cies of fishes. The longest glochidial
infections on the longear and crappie
were on individuals weakened by fungal
infections.

The rosefin shiner was the only host
found for pigtoe musselglochidia. Young
mussels (Fig. 15) have been collected
from the bottom of containers after 14-
18 days of infection on this species.
Four different infections with different
glochidial sources and different rosefin
shiners have provided conclusive data.
The parasitic period in controlled tem-
perature of 21°C is 14-18 days. Young

mussels begin dropping from the demi-
branchs on the 14th day and are gone
by the 19th day, except for rare in-
stances. Recovery of the young mussels
is greatest on the 15th and 16th days
(Fig.s1):

Young mussels were maintained in
small evaporating dishes (Fig. 14) with
constant water flow into and out of the
dishes from the bottom of the Living
Stream tanks. Mortality rate was high,
but the young mussels that survived
were still developing in the dishes after
36 days. Equipment failure caused
their death at this time.

Further studies are needed to learn

362 P. YOKLEY

how to increase survival. Histological
sections of the young individuals would
reveal new data on organ and system
development. Glochidial infections of
still other fishes should be tested to
determine if the rosefin shiner is the
only possible host for the pigtoe mussel.

SUMMARY

1. In Pleurobema cordatum, sperma-
tozoa are formed during all warm
months but are most abundant in
April.

2. Spawning occurs in April and early
May.

3. Syngamy occurs as the oocytes pass
from the oviducts to the water tubes.

4, Fertilized eggs undergo early divi-
sion in the water tubes of the outer
demibranchs,

5. Embryogeny is dependent upon a
rising water temperature which
must reach about 21°C before ma-
ture glochidia are. formed,

6. Infective glochidia are most abun-
dant in June,

7. The glochidia of pigtoes are hook-
less and can anchor firmly to gill
filaments of small fish only.

8. The rosefin shiner (Notropis ar-
dens) is a host fish for the glo-
chidia of the pigtoe mussel.

9. The parasitic period extends over
approximately 14-18 days.

10. Glochidia do no apparent harm to
either the host fish or its gills.

ACKNOWLEDGEMENTS

The Tennessee Valley Authority, Fish
and Wildlife Branch, furnished equip-
ment, advice, and financial assistance.
Mr. Billy B. Carroll, Area Supervisor,
has been especially helpful in every way
during this study, as has his secretary,
Mrs. Dorothy Stansell, who assisted in
arranging and typing the final copy.

Mr. Charles Gooch assisted in diving
and collecting specimens. Mrs. Nancy
G. Unger drew the sketches, and my
wife, Betty, typed the original manu-
script.

LITERATURE CITED

BAKER, Е. C., 1921, Freshwater Mol-
lusca of Wisconsin. Part II. Pelecy-
poda. Bull. Wis. geol. natur. Hist.
Surv., 70: 1-495, 76 pls., 96 figs.

COKER, В. E., SHIRA, A. F., CLARK, |
H. W. & HOWARD, A. D., 1921, Na-
tural history and propagation of fresh- |
water mussels. U.S. Bur. Fish. Bull.
No. 893. p 71-181.

HOWARD, A. D., 1913, Experiments in
Propagation of Fresh Water Mussels |
of the Quadrula group. Bureau of !
Fisheries Document 801.

JONES, R. O., 1950, Propagation of
Freshwater Mussels. U.S. Fish Wildl.
Serv., р 13-25.

JONES, В. O., 1952, Progress Report--
Mussel Propagation Project, 1951
Field Season, p 1-4.

LEFEVRE, G. & WINTERTON, C. C.,
1912, Studies on the Reproduction and |
Artificial Propagation of Freshwater
Mussels, Bull. Bur. Fish., 756: 105-
201, 17 pls., 70 figs.

NEEDHAM, J., 1950, Biochemistry and
morphogenesis. Cambridge Univer-
sity Press, London. 787 p.

PELSENEER, P., 1935, Essai d’ethologie
zoologique d’après l'étude des mol- |
lusques. Palais des Académies, Brux-
elles, 662 p. |

РЕММАК, ВБ. W., 1953, Freshwater in- |
vertebrates of the U.S. RonaldPress, |
New York. 769 p.

SCRUGGS, G. D. Jr., 1960, Status of
fresh-water mussel stocks inthe Ten- |
nessee River: U.S. Fish Wildl. Serv., |
Spe. Sci. Rep. Fish., 370: 1-41.

SURBER, T., 1912, Notes on the natural |
hosts of fresh-water mussels. Bull.
Bur. Commerc. Fish., p 103-119.

TENNESSEE VALLEY AUTHORITY, |
1966, The mussel resource of the
Tennessee River. Fish and Wildl.
Br., T.V.A. p 1-32.

YOKLEY, P. Jr., 1968, A study of the |
anatomy of the naiad Pleurobema cor-
datum (Rafinesque, 1820) (Mollusca: |
Bivalvia: Unionoida). Unpubl. dissert., |
Ohio State Univ. |

LIFE HISTORY OF PLEUROBEMA CORDATUM

ZUSAMMENFASSUNG
BIOLOGIE VON PLEUROBEMA CORDATUM (BIVALVIA: UNIONACEA)
P. Yokley Jr.

Pleurobema cordatum, die “Schweinehuf-Muschel” des Ohio, eine Art von wirt-
schaftlicher Bedeutung, lebt in den grössten Flüssen im Einzugsgebiet des Ohio und
kommt ausserdem in Kolonien oder Muschelbänken im Tenesseefluss vor. Die Fort-
pflanzung geschieht in jährlichem Rhythmus, Samenausstoss und Befruchtung im April
und Mai. Die wechselnde histologische Beschaffenheit der Gonaden während des
Jahreslaufes werden beschrieben. Vier bis sechs Wochen nach der Befruchtung
wurden in den äusseren Kiemen Glochidien gefunden. Die Entwicklung der Larven
bis zu diesem Stadium findet nur statt, wenn die Wassertemperatur Über ca. 21°C
ansteigt. Bei Zuchtversuchen setzten sich die parasitischen Glochidien an den Kiemen
des rotflossigen Notropis ardens (Cope) fest, encystieren sich und verwandeln sich
innerhalb 14-18 Tagen in freilebende Muscheln. Ein beweglicher Fuss entwickelt sich
während dieser Zeit, ein Grössenwachstum erfolgt aber nicht. Innerhalb 3 Wochen
nach Verlassen des Wirtsfisches verdoppelt die freilebende Najade ihre Grösse. Sie
wird in 4 Jahren geschlechtsreif, und die Gonaden bleiben funktionstüchtig durch die
weiteren 25-30 Lebensjahre des Individuums,

H. 7.

RESUME
BIOLOGIE DE PLEUROBEMA CORDATUM (BIVALVIA: UNIONACEA)
P. Yokley Jr.

La moule d’eau douce “pied de porc” de l’Ohio, espèce commerciale, habite les
plus grandes rivières du réseau hydrographique de l’Ohio et se rencontre aussi en
concentrations ou “bancs mouliers” dans la riviére Tennessee. Ovogenése et sperma-
togenése subissent un cycle annuel, avec émission des gamétes et fécondation en
avril ou mai, Les changements saisonniers dans l’histologie de la gonade sont
decrits. Pendant 4 ä 6 semaines apres la fécondation, on trouve des glochidiums dans
les branchies externes marsupiales. Le développement larvaire jusqu’a ce stade
nécessite une température de l’eau d’au moins 21°C. Dans les expériences de labora-
toire, les glochidiums parasites, expulsés en général en juin, s’attachent aux fila-
ments branchiaux du poisson Notropis ardens (Cope), s’enkystent et évoluent en
coquilles libres en 14-18 jours. Un pied mobile se développe pendant l’enkystement,
mais il n’en résulte aucun accroissement de taille d’ensemble. Trois semaines
après avoir quitté le poisson hôte, les mollusques ont doublé de taille, La maturité
sexuelle est atteinte en 4 ans et les gonades demeurent fonctionnelles pendant les
25 à 30 ans que vivent encore ces mollusques.

А. Г.

RESUMEN
BIOLOGIA DE PLEUROBEMA CORDATUM (BIVALVIA: UNIONACEA)
P. Yokley Jr.

La almeja “pata de cerdo” Pleurobema cordatum, especie de valor comercial,
habita los grandes ríos del sistema del Ohio y también aparece en concentraciones o
“camadas” en el río Tennessee. Ovogénesis y espermatogenesis tienen ciclo anual y
la fertilización se produce de abril a mayo. Se describen los cambios estacionales en
la histología de la gonada. Decuatroa seis semanas post-fertilización se encontraron
gloquidias en las semibranquias externas del marsupio. Desde ese estado el desarro-
llo larval depende la temperatura del agua, favorable cuando es alrededor de 21°. En

363

364

P. YOKLEY

experimentos de laboratoiro, las gloquidias libradas en abril se adhieren a los fila-
mentos branquiales del pez plateado de aletas rosadas, Notropis ardens (Cope), se
enquistan y después de 14-18 dias se transforman en almejas independientes. Durante
el enquistamiento se desarrolla un pié, pero el tamaño intergral no aumenta. Tres
semanas después de haber desprendido del pez, las almejitas doblan el tamaño,
Madurez sexual es alcanzada dentro de los 4 años y las gonadas continuan funcionando

por el resto de la vida del molusco que es de 25 a 30 años.
J. J.P.

СТРАКТ

u1

БРАЗ ЖИЗНИ PLEURONEMA CORDATUM (RAFINESQUE, 1820)
(BIVALVIA: UNIONACEA)

I. WOKJM

Промысловый вид моллюска из района Огайо, где он обитает в самых
больших притоках системы реки Огайо, а также в реке Теннесси, где
образует большие "моллюсковые банки". Овогенез и сперматогенез имеет
годовую цикличность, спаривание и оплодотворение происходит в
апреле-мае. В работе даются описания сезонных изменений в гистологии
гонад. Через 4-6 недель после оплодотворения в марзупиях (на внешних
полужабрах) уже содержатся глохидии. Развитие личинок на этой стадии
зависит от температуры воды, превышающей 21°C.

В лабораторных экспериментах паразитические глохидии, выходящие
главным образом в июне, прикрепляются к жаберным нитям Notropis ardens
(Соре), инцистируются и через 14-18 дней превращаются в самостоятельных
моллюсков. Подвижная нога у них развивается во время инцистирования, но
не увеличивается в размере. Через три недели после выхода 13
рыбы-хозяина свободноживущие моллюски увеличиваются в размере вдвое.
Половозрелость у них наступает через 4 года; гонады продолжают
функционировать в течение 25-30 лет жизни.

Z. A. Е.

| nomenclature is chaotic.

MALACOLOGIA, 1972, 11(2): 365-389

THE GENUS THYASIRA IN WESTERN CANADA (BIVALVIA: LUCINACEA)

F. R. Bernard

Fisheries Research Board of Canada
Biological Station
Nanaimo, B. C., Canada

ABSTRACT

A brief review of the systematics and anatomy of the 4 species of the bivalve
genus Thyasira Lamarck occurring in the seas of Western Canada is presented.
Based upon the collections of the many hundred stations of the faunistic survey
of the Fisheries Research Board of Canada taken since 1950, it is concluded that
T. trisinuata Orbigny, 1846 is extraterritorial.

Anatomical studies reveal marked modification of the digestive system con-

nected with the macrophagous behavior.

Hypertrophy of the foot and arrange-

ment of the pallial openings and water currents are secondary adaptations to a
deep infaunal habitat. The genus is closely related to the lucinids and repre-
sents a terminal branch of the Heterodonta.

INTRODUCTION

The position of the genus Thyasira in
the higher categories has not been stable.
Thiele (1935) placed it in the Family
Ungulinidae, while Grant & Gale (1931)
assigned it to the Superfamily Coda-
kiacea. Knudsen (1967) returned to the
earlier usage of Ungulinidae. Anatomi-
cally, it is related to the lucinid complex
and in this paper the classification sum-
marized by Vokes (1967) is used, placing
Thyasira within the Family Thyasiridae,
Superfamily Lucinacea, Order Veneroi-
dea.

While the position within the higher
categories has vacillated, the generic
Thyasiva is
a Leach manuscript name employed by
| Lamarck in 1818 in the synonymy of
| Amphidesma flexuosa (Montague 1803)
and fully acceptable under the Interna-
tional Code of Zoological Nomenclature.
Axinus Sowerby 1821 is a synonym, as
is Cryptodon Turton 1822. Conchocele
Gabb 1866 should also be considered a
Synonym, though some workers (Oyama

& Mizuno, 1958) use it as a subgenus of
Thyasira. The subgenus Axinulus Ver-
| rill € Bush 1898, displays a number of

interesting anatomical and conchological
differences and Axinulus will be accorded
full generic rank in a Subsequent paper.

Four species of Thyasira Lamarck
exist in the Canadian Pacific, consisting
of Thyasira bisecta (Conrad, 1849), T.
cygnus (Dall, 1917), T. disjuncta (Gabb,
1866), and T. flexuosa (Montagu, 1803).
T. cygnus and T. flexuosa are clearly
distinguishable, but controversy has
characterized the status of the 2 largest
species. Venus bisecta Conrad 1849 was
adequately described and accompanied by
a fine illustration. After describing
Conchocele disjuncta, Gabb (1869) stated
that he collected topotypes of V. bisecta
and referred to Conrad’s 1849 and 1865
papers. Gabb considered his species
sufficiently distinct from T. bisecta to
warrant specific status. Dall (1895)
illustrated T. bisecta and synonymized it
with C. disjuncta. The majority of
later workers followed Dall. Tegland
(1928) drew attention to the separation
of the 2 species, considering T. bisecta
a fossil species and T. disjuncta refer-
able to living individuals. Tegland’s
paper appears to have been largely neg-
lected by later workers. Yabe & Namura
(1925) described from Japan fossil ma-

(365)

366 F. R. BERNARD

terial which they correctly referred to
T. bisecta, but considered bisecta and
disjuncta as synonymous, Nakazima
(1958) in a superficial anatomical des-
cription of C. disjuncta returned to
Gabb’s nomenclature. Knudsen (1967),
followed Dall (1895), placing C. investi-
gatoris Smith 1895 in the synonymy of
T. bisecta. If these reports are accep-
ted then T. bisecta has an extraordinary
geographical range consisting of the
entire Pacific and Indian Oceans and
portions of the South Atlantic, with a
bathymetric range of nearly 2000 metres.

Extraterritorial species

Thyasiva excavata Dall 1901. A south-
ern form extending from Oregon to Mex-
ico. The holotype was collected in
1005 fathoms; Hertlein & Strong (1946)
discussed 2 shells collected in 43-45
fathoms off Mexico referable to this
species, Dall (1921) gave the range as
extending from Oregon to the Gulf of
California. Some forms of T. flexuosa
possess radial flexuosities, Further
study may well place T. excavata as a
form of T. flexuosa.

Thyasira trisinuata Orbigny 1846.
Dall (1921) gave the range as Alaska to
San Diego. Oldroyd (1924) and LaRocque
(1953) simply quoted Dall. Dall’s (1901)
record from Sitka Harbour is referable
to T. trisinuata Orbigny, a striking glo-
bular shell, limited to the West Indies.
(It appears to merge with T. flexuosa in
the northern Atlantic distribution.) The
status of T. trisinuata polygona Jeffreys
1863 is not clear. The validity of the
Species is doubtful since the small
thyasirids have been extensively dif-
ferentiated and further study may rele-
gate many to synonymy.

TAXONOMIC ACCOUNT

Class Bivalvia
Order Veneroidea
Superfamily Lucinacea
family THYASIRIDAE
1901 Thyasiridae Dall
Genus Thyasiva Lamarck 1818

Thyasira Lamarck (Leach MS), 1818,
p 492, Type (Monotypy) Tellina flexuosa
Montague, 1803; Lamy, 1915, p 19;
Thyassiva, Blainville, 1829, p 33 (err.
pro. Thyasira); Thyatira, Jeffreys, 1839,
р 42 (err. pro. Thyasira); Thiatyra,
Sowerby, 1842, p274(err. pro. Thyasira);
Thiatisa, Gray, 1847, p 195 (err. pro.
Thyasiva); Thyaseiva, Gray, 1851, p
100 (err. pro. Thyasira); Thyasira, Try-
on, 1884, p 211 (err. pro. Thyasira);
Thyarsiva, Pallary, 1912, p 174 (err.
pro. Thyasira); Axinus Sowerby J., 1821,
p 11, Type (Original designation) Axinus
angulatus Sowerby, 1821; Cryptodon Tur-
ton, 1822, p 121, Type (Original desig-
nation) Tellina flexuosa Montagu, 1803;
Ptychina Philippi, 1836, p 15, Type(Ori-
ginal designation) Ptychina biplicata
Philippi, 1836; Clausina Jeffreys, 1847,
p 18 (non Brown 1827), Type (Subsequent
designation) Kellia ferruginosa Forbes,
1843; Conchocele Gabb, 1866, p 27, Type
(Original designation) Conchocele dis-
juncta Gabb, 1866; Schizothaerus Locard,
1896, p 180 (non Conrad 1853), Type (Ori-
ginal designation) Tellina flexuosa Mon-
tagu 1803; Prothyasira Iredale, 1930, p
393, Type (Original designation) Prothy-
asira peroniana Iredale, 1930.

Type. (monotypy) Tellina flexuosa (Mon-
tagu 1803) = Venus sinuosa Donovan, 1802
= Lucina sinuata Lamarck, 1818, = Pty-
china biplicata Philippi, 1836 = Crypto-
don bisinuatus Wood, 1840 = Axinus
sinuatus, Philippi, 1845. (Dall 1901).

Description

Valves with edentulous hinge, the an-
terior dorsal area more or less im- !
pressed, the posterior more or less |
radially sulcate or plicate (Dall 1903).

General characteristics

Shell: Shell thin, white, fragile, Um-
bones prosogyrate. Sculpture absent,
except for incremental lines, Charac-
terized by a radial sulcus adjacent to
the lateral median lines of the body.
Hinge edentulous,

Anatomy: Mantle thin, periphery much
thickened, muscular, bearing 3 distinct

THYASIRA IN WESTERN CANADA 367

folds, posteriorly fused at 1 point, gen-
erally forming a small anal and large
inhalant aperture though a secondary
anterior fusion may occur, All species
are asiphonate; no vestige of siphonal
retractors are present, therefore a true
pallial sinus is absent. Adductor muscles
unequal, the anterior large, elongate and
adjacent to mantle edge. Posterior
small, subcircular in outline. Foot
vermiform with distal tip bulbous. A
prominent byssal groove is present but
the function appears to be modified to
mucus production, No byssal threads
could be found and histological sections
showed the presence of underlying mucus
cells but no typical byssal gland. Mouth
large, situated above anterior adductor
muscle which is covered by a ciliated
epithelium. Labial palpi small, con-
sisting of 2 plates with few folds. The
palpi are dorsal to, and removed from,
the mouth, joined by a long oral groove.
Ctenidia thick, dark brown due to de-
posits in the tissues, homorhabdic, con-
sisting of a small outer, and a larger
inner demibranch. The mouth leads to
an elongated oesophagus bearing promi-
nent longitudinal ridges. The oesophagus
opens antero-ventrally into the globular
thin-walled stomach. The ducts of the
digestive diverticula consist of 2 long
tubes. The digestive diverticula and
gonadial tissues form lateral arbores-
cent tufts connected to the body by a
narrow isthmus of tissue. Intestine:
thin-walled, with large ventral typhlo-
sole. The gut pierces the ventricle;
then proceeds dorsally to the posterior
adductor. Pericardial glands form dark
masses on the anterior walls of the
auricles and on portions of the pericar-
dium. The large kidney is postero-
dorsal, underlying the intestine. The
heart is proportionately large; the ven-
tricle gives off a prominent anterior
aorta and vestigial posterior aorta.

Discussion

All species are laterally compressed
to a marked degree; the anterior portion
of the body consists of a mere envelope

containing the stomach. Together with
the compression of the body and the
development of the lateral pouches, there
has been a postero-ventral elongation
of the anterior adductor muscle and
displacement of the mouth to its dorsal
surface. This elongation has caused a
partial rotation of the anterior end of
the body and the mouth has come to lie
below the orifices of the digestive diver-
ticula (Fig. 13C). The oesophagus has
lengthened and the orifices of the diges-
tive diverticula are no longer opposite,
but the left one is well in advance of the
right. The placement of the digestive
gland in lateral pouches with only a
narrow isthmus fused to the body resulted
in the great prolongation of the digestive
ducts, which are also of remarkable dia-
meter. The stomach has lost most of
its ciliated areas and has been freed
from surrounding connective tissue. The
wall of the stomach is not muscularized,
but at the junction of the oesophagus and
in the style-sac mid-gut regiona number
of muscular supporting fibres suspend
the organ (Fig. 16F). While it is ap-
parent that the wide ciliated digestive
ducts would permit the passage of large
particles, none were found in any of the
dissections. Stomach contents consisted
of detritus with numerous diatom frus-
tules and Foraminifera tests, many bro-
kendown polychaete setae and arthropod
remains. Despite the sand and mud in
the substrate, no rock fragments were
found, indicating a thorough sorting sys-
tem prior to ingestion.

Sars (1851) first notedthe arborescent
digestive gland and gonad housed in
lateral pouches in Axinus sarsi andcom-
pared them to similar structures of the
Brachiopoda. The possession of lateral
pouches may be associated with macro-
phagy as they are also present in the
Septibranchia. It has been suggested by
a number of workers that the Lucinacea
consist of a monophyletic line of bivalves
specializing in the colonization of im-
poverished habitats. Allen (1958) felt
that a natural series is displayed, with
the Ungulinidae most like the ancestral

368 F. R. BERNARD

stock, and the Lucinidae the most ad-
vanced, basing his conclusion partly up-
on the reduction in the size of the palpi
and upon studies (Allen, 1960) of the
comparative ligamental structure of the
3 taxa.

McAlester (1966) considered that the
adaptations demonstrated in the Lucini-
dae, together with the fossil record, in-
dicated an ancient and separate branch
of the bivalvia not related to the Hetero-
donta. While only the Leptonacea show
morphologic features suggestive of an
evolutionary connection with the Lucina-
cea (Oldfield, 1955; Morton, Boney &
Corner, 1957), it is premature to assign
high categorical rank to lucinaceans.
McAlester based his reasoning upon the
premise that the Ordovician bivalve
Babinka was not only related to the
Monoplacophora but was also a lucinoid,
There is no evidence to connect Babinka
with living lucinaceans, or indeed with
the earliest undoubted lucinoid genus,
the Silurean Prolucina Dall.

While a high degree of specialization
in habitat and macrophagy is displayed,
the basic characteristics are those com-
mon to the Heterodonta. The nervous
system, circulatory system, shell mor-
phology, and complex excretory system,
coupled with the presence of both inhalant
and exhalant posterior openings in ad-
dition to the anterior (inhalant) aperture
and the basic eulamellibranchiate struc-
ture of the ctenidia, all point to an
advanced organism modified to meet
specialized conditions. The argument
has been ably summarized by Boss
(1969).

Despite the reduction of openings of
the digestive diverticula to the stomach,
there has been no hesitation in placing
the Thyasiridae inthe Polysyringia (Pur-
chon, 1960). Secondary reduction in
numbers of openings is not uncommon;
it is probable that the Verticordidae,
placed inthe oligosyrigianSeptibranchia,
are secondarily modified polysyrigian
(stomach type IV-Purchon, 1960) bi-
valves adapted to macrophagy (Bernard,
MS). It is interesting to note that lateral

arborescent pouches containing the di-
gestive diverticula and gonadia are often
associated with macrophagous and car-
nivorous feeding behavior. The septi-
branchs Myonera, Cuspidaria and, to a
lesser extent, Poromya all possess ar-
borescent digestive diverticula projec-
ting laterally from the body.

In conclusion, it may be stated that
although species of the Thyasiridae are
a distinct offshoot of the bivalvia modi-
fied for macrophagous existence in the
Substrate, the family is unmistakably
related to other Heterodonta,

KEY TO THE WESTERN CANADIAN
SPECIES OF THYASIRA

1. Beaks anteriorly placed. .......2
Beaks subcentrally placed.......3
2. Anterior margin concave. .....+.o..
OO ov ee « PRODISecCta
Anterior margin straight I
en na Are, TI ASTUNELA
3. Radial furrow pronounced,.......
RS . ol flexuosa
Radial furrow slight......7. Cygnus

oeeeeee

Thyasira bisecta (Conrad, 1849)
(Figs. 3, 4, and 9)

Venus bisecta Conrad, 1849, p 724, pl.
17, figs. 10, 10a; Cyprina bisecta, Con-
rad, 1865, p 153; Cryptodon bisectus,
Dall, 1892, р 189 (part); Dall, 1895,
p 713(part); Cryptodon bisecta, Knudsen,
1967, p 289 (doubtful); Thyasira bisecta,
Dall, 1901, p 789 (part); Dall, 1919,
p 103 (part); Dall, 1921, p 33 (part);
Oldroyd, 1924, p 120(part); Yabe & Na-
mura, 1925, p 84, pl. 23, 24; Tegland,
1928, p 121; Grant & Gale, 1931, p 281,
pl. 13, fig. 15 (part); LaRocque, 1953,
p 56 (part); Conchocele disjuncta, Habe,
1958, p 26, pl. 2, fig. 5; Nakazima, 1958,
p 186; Habe, 1961, p 124, pl. 56, fig. 15;
Okutani, 1962, p 23, pl. 2, fig. 9; Habe,
1964,,.p.181, pl... 56,: fig, 15. Mae
bisecta).

Type locality: Astoria, Oregon. Mio-
cene fossil.
Holotype: Unknown, not inAcademy of

THYASIRA IN WESTERN CANADA 369

FIGS. 1-2 Thyasira disjuncta (Gabb, 1866).

Natural Sciences, Philadelphia.

Original description: Oblique, sub-
rhomboidal, ventricose, with robust lines
of growth, Anterior side very short,
truncate, angulate below, having a sub-
marginal vertical furrow, and the in-
ferior margin at its termination slightly
excavate. Posterior surface strongly
excavate from the upper side of the
beak to the posterior margin, and sub-

FIGS. 3-4. Thyasira bisecta (Conrad, 1849).

carinate below the excavation; ligament
and supero-posterior margin forming
together a regular curve. Basal margin
arcuate, a little tumid behind the middle,
Length 5 cm, distance anterior to beak
0.85 cm; apical angle 120°. Valves
quite thin.

Range: North Pacific

Material examined: National Museum
of Canada - 1 specimen (Cat. No. 47342).

370 F. R. BERNARD

Fisheries Research Board of Canada
-2 lots consisting of 5 specimens col-
lected alive off British Columbia in 220
and 160 metres, mud,

Discussion

The species is closely related to, but
easily distinguished from, T. disjuncta
(Gabb, 1866) by the concave outline of
the anterior surface and the more pro-
minent umbones, Invariably in the
eastern Pacific, T. bisecta is of rare
occurrence, though Oyama & Mizuno
(1958) reported a Lower Oligocene sub-
species from Japan and designated it as
Thyasira (Conchocele) bisecta omarui.

Anatomy

In general form this species is simi-
lar to T. disjuncta; only the differences
will be discussed here. The mantle is
generally thicker апт T. disjuncta and
the edges are not so developed. The
anal aperture is comparatively large and
much of the posterior adductor is ex-
posed; fusion of the mantle is in one
small area and involves the inner and
middle folds only. The anal aperture
is not provided with tentacles or other
processes but a number of small pro-
tuberances, doubtfully of a sensory na-
ture, are visible (Allen, 1958). The
adductor muscles are unequal, but the
anterior muscle is not as prolonged
and is more verticalthanin T. disjuncta.
The foot is extremely elongate and the
tip is slightly dorso-ventrally flattened.
Labial palpi small, subtriangular, set
close to the mouth. The mouth is large
and lies in contact with the dorsal sur-
face of the adductor muscle. Digestive
diverticula present the familiar arbores-
cent tufts, but individual processes are
proportionately smaller than in T. dis-
juncta. The stomach is not globular,
but forms a thin-walled egg-shaped body
leading to the short fused mid-gut and
style-sac. The intestine describes an
acute dorsal flexure and pierces the
ventricle of the heart before running
in a posterior median direction over
the adductor muscle tothe anal aperture,

A small dorsal hood and sorting area
occur on the dorsal anterior wall of
the stomach. A large typhlosole runs
the length of the intestine and enters
the floor of the stomach, The arrange-
ment of the digestive tubules is radically
different from T. disjuncta. Inthe latter
species the long ducts are sparsely
branched into the digestive tubules. In
T. bisecta the ducts are shorter and the
tubules branch off in large numbers al-
most immediately. The kidneys are
small and their openings do not appear
to be connected as is the case with Т.
disjuncta. The heart and circulatory
systems are Similar, but the ventricle
is thinner and the first part of the
aorta is bulbously thickened.

Thyasira cygnus Dall, 1917
(Figs. 7, 8, and 10)

Thyasira cygnus Dall, 1917, p 409; Dall,
1921, p 33; Oldroyd, 1924, p 121, pl. 3,
fig. 10; LaRocque, 1953, p 56.

Type locality: Station 4224, Cygnet
Inlet, Boca de Quadra, Alaska, in 160
fathoms,

Type: (Holotype). United States Na-
tional Museum No, 222618.

Original description: Shell white, with
a pale straw-coloured periostracum,
moderately convex, sharply compressed
behind, the beaks prominent, prosocoe-
lous over a large cordate lunule, the
escutcheon long and very narrow, bound-
ed by a sharp keel; general form rounded,
quadrate, the compressed posterior area
narrow and basally falling notably short
of the basal curve of the disk, posterior
Slope slightly convexly arcuate, anterior
distinctly concave, meeting the basal
arc in an obtuse angulation. Length 14;
height 13.5, diameter 8.5 mm.

Range: Alaska - Vancouver Island,
British Columbia, in 290-1537 metres,

Material examined: Fisheries Re-
search Board of Canada - 1 lot consist-
ing of individuals from 47°58.2N 125°
47.4W in 1537 metres. Deposited in
National Museum of Canada (Cat. No.
47341).

THYASIRA IN WESTERN CANADA

371

Y.

lom

tom

FIGS. 5-6.

Anatomy

This rare, small species has not been
previously studied. Unfortunately the
material was poorly preserved and only
superficial examination could be under-
taken. In general appearance the spe-
cies is Similar to other members of the
genus, although the mantle is fused in
2 places, giving rise to 3 distinct aper-
tures. The nature of the fusion is ano-
malous; in the general thyasiran plan,

Thyasira flexuosa (Montagu, 1803).

FIGS. 7-8. Thyasiva cygnus Dall, 1917.

the fusion primarily involves the middle
mantle fold only. In T. cygnus the anal
and inhalant apertures are the product
of middle fold fusion only, but the pedal
Opening is formed by a total fusion
except for a small “lip” in the outer
fold. The mantle boundary around the
pedal opening is much thickened and
muscularized. The anal opening is
guarded by 4 small papillae, probably
of a sensory function. Thyasiva cygnus
is the only representative of the West

372 Г. В. BERNARD

KEY TO LETTERING IN FIGURES

A Anus

AA Anterior adductor muscle

AAp Anterior aperture

ALOD Ascending lamella of outer
demibranch

CA Ciliated area

CE Ciliated epithelium

CE Ctenidium

CtA Ctenidial axis

CT Connective tissue

DDD Duct to digestive diverticula
DGG Digestive gland and gonad

DLOD Descending lamella of outer
demibranch

DT Digestive tubule

Ex Exhalant aperture

F Foot

Fol Follicle

G Gonad

H Heart

I Intestine

ID Inner demibranch

In Inhalant aperture

IM Inner fold of mantle

LDD Left digestive duct

LP Labial palp

M Mouth

American genus to possess 3 distinct
mantle cavity openings, and it issimilar
to species of the genus Diplodonta in
this respect. The adductor muscles are
not equal, the posterior muscle being
elongated, but not as much as in other
species. The labial palpiarenarrowand
produced, large for the genus. Mouth
wide, with deep oral groove running to
the palpi. Digestive diverticula and
gonads are contained in many short sac-
like protuberances which demonstrate a
much larger fusion area to the body and
are partially fused together dorsally,
rather than 2 separate bodies joined to
the stomach by a narrow isthmus as in
other Thyasiva. The internal anatomy
was not investigated.

Thyasiva disjuncta (Gabb, 1866)
(Figs. 1, 2, 11, and 13)

Conchocele disjuncta Gabb, 1866, p 27,
pl. 7, figs. 48, a, b; non, Habe, 1958,

Man Mantle

MF Muscle fibre

MG Marginal groove

MS Mid-gut and style sac
Mus Muscle

N Nucleus

O Ovum

OD Outer demibranch

Oe Oesophagus

OG Oral groove

OM Outer fold of mantle

Ovd Oviduct

PA Posterior adductor muscle
PG Pedal gape

Pro Processes of exhalant aperture
R Rectum

RDD Right digestive duct

Ren Renal tissue

RM Rejection track of muscle
5 Shell

SA Sorting area

St Stomach

Srs Subrenal sinus

T Typhlosole

TB Terminal bulb

TDG Tubule of digestive gland
VM Visceral mass

p 26, pl. 2, fig. 5; non, Nakazima, 1958,
р 180; non, Habe, 1961, р 124, pl. 56,
fig. 15; non, Okutani, 1962, p 23, pl. 2,
fig. 9; non, Habe, 1964, p 181, pl. 56,
fig. 15. (all T. bisecta). Cryptodon
bisectus, Dall, 1892, p 189 (part); Dall,
1895, p 713 (part); Cryptodon bisecta,
Knudsen, 1967, p 284, pl. 2, figs. 7, 8
(doubtful); Thyasira bisecta, Dall, 1901,
p 789 (part); Dall, 1919, p 103 (part);
Dall, 1921, p 33 (part); Oldroyd, 1924,
p 120, pl. 10, fig. 1; Grant & Gale, 1931,
p 281, pl. 13, fig. 15 (part); LaRocque,
1953, p56 (part); Thyasira disjuncta,
Tegland, 1928, p 129.

Deadman Island, near
Pliocene

Type locality:
San Pedro Bay, California.
fossil.

Type: (Lectotype -Stewart 1930) Aca-
demy of Natural Sciences, Philadelphia.

Original description: Shell subquad-
rate, beaks terminal, anterior; anterior
end abruptly and angularly truncated;

THYASIRA IN WESTERN CANADA 373

FIG. 9. Thyasira bisecta (Conrad, 1849).
mantle removed.

A. Lateral view from right side, right valve and
B. Inhalent and exhalent posterior apertures.

C. Anterior inhalent gape.

D. Labial palpi and mouth in right aspect. For lettering see p 372.

base broadly rounded; cardinal margin
arched, sloping downwards towards the
posterior end. Surface marked only by
lines of growth, except near the poste-
rior part where the peculiar truncation
takes place, the surface suddenly des-

cending at a right angle to the curve of
the shell, for a short distance, and then
resuming its former direction.

Range: Alaska - Oregon, Caribbean
Sea, Japan, in 150-750 metres.

Material examined: National Museum

374 F. R. BERNARD

D
N \ NAS
\ NS

A

FIG. 10. Thyasiva cygnus Dall, 1917. A. Lateral view from right side, right valve and mantle
removed. B. Posterior view of inhalent and exhalent apertures. C. Labial palpi and mouth in

right aspect. For lettering see p 372.

of Canada, 5 specimens (Cat. No. 47343).
Fisheries Research Board of Canada -
6 lots consisting of 22 valves and 97
live specimens collected off Northeas-
tern Vancouver Island in 190-200 metres,
Los Angeles County Museum of Natural

History -1 specimen (Loan №. 3293),
collected off Alaska.

Discussion

Individuals of this species are the
largest representatives of the genus,

|

THYASIRA IN WESTERN CANADA 379

cm

FIG. 11. Thyasiva disjuncta (Gabb, 1866). A. lateral view from right side, right valve and
mantle removed. В. Inhalent and exhalent posterior apertures. С. Anterior inhalent gape.
D. Labial palpi and mouth in right aspect. For lettering see p 372.

Boss (1967) reported a single large
valve from 421-641 metres in the Gulf
of Darien and commented upon the dis-
tinctive natures of T. bisecta and T.
disjuncta. This firmly placed the living

_ species in the Caribbean,

|
|

Anatomy

Many specimens preserved in various
fixatives and fresh were available for
study, so new features were brought to
light. Nakazima (1958) published a

376 F. R. BERNARD

PA

N

ak
N

NN

DGG

FIG. 12. Thyasira flexuosa (Montagu, 1803).
mantle removed.

short paper on a poorly preserved spe-
cimen collected off Japan, with which
this study is not in complete agree-
ment, particularly in details of stomach
structure, which were investigated by
means of dissection and the preparation

B. Posterior view of inhalent and exhalent apertures.
mouth in right aspect. For lettering see p 372.

A. Lateral view from right side, right valve and

C. Labial palpi and

of internal plastic casts with the diges-
tion of surrounding tissues.

The body is laterally compressed and
hidden by the two large lateral arbores-
cent masses of digestive and gonadal
tissues (Fig. 13B).

THYASIRA IN WESTERN CANADA 377

FIG. 13. Thyasira disjuncta (Gabb, 1866). A. Right lateral schematic showing principal water
and ciliary current directions. B. Ventral aspect of digestive gland and gonadal pouches, left
gill removed. C. Schematic of stomach and intestine in right aspect. D. Distal end of digestive

gland duct in Thyasira bisecta (Conrad, 1849). For lettering see p 372.

The mantle margins are thickened into
sisting of a double layer of epithelium a muscularized band consisting of 3
with scattered patches of mucocytes. pronounced folds, well described by
The dorsal regions of the mantle con- Allen (1958) and characteristic of the
tain connective fibres and haemocoeles, family. The inner fold bears cilia-

The mantle is extremely thin, con-

378 F. R. BERNARD

FIG. 14.

cm

Thyasira disjuncta (Gabb, 1866). Transverse sections through body; gills and foot re-

moved. A. Section through anterior portion of stomach. B. Section through mid-stomach region.
C. Section througn mid-gut and style pouch. D. Section through mid-region of the foot. Mate-
rial fixed in Formol-alcohol stained in Harris’ alum hemotoxylin counterstained eosin; 15 u sec-

tions. For lettering see p 372.

ted tracks and a region supplied with
a thick secretory epithelium, similar
to that found in Cuspidaria. The cen-
tral position of the mantle edge is
occupied by a large haemocoele, Mantle
fusion is limited to a small area around
the anal aperture. Nakazima (1958)
noted that this fusion involves the inner
and middle folds only. The anus, after
passing over the posterior adductor,
projects for a short distance into the
aperture, The outer fold formsa simple
fringe around the anal aperture; no pro-
cesses or sensory areas are evident.

The posterior apertures fall above and
below the radial sulcus of the shell, so
that the exhalant aperture is directed
posteriorly but the inhalant aperture
faces almost directly upwards, Obser-
vation of living individuals suggests that
both the apertures are used as exhalant
apertures, The anterior aperture is not
separate from the pedal gape, but is
supplied with a slightly more muscular
band than the ventral mantle margin and
appears asa distinct aperture (Fig. 11B).
The adductor muscles are very unequal,
the anterior one greatly elongated and

FIG. 15. Thyasira disjuncta (Gabb, 1866). Corrosion model of digestive tract made by injection

of liquid plastic and digestion of the tissues.

diverticula and digestive tubules.

A. Stomach and intestine. B. Duct of digestive

379

THYASIRA IN WESTERN CANADA

Cy

Е

+

г
74

Ping

CRC

LT

380 F. R. BERNARD

running along the mantle edge for ap-
proximately 1/4of its total length. The
dorsal surface of the anterior adductor
is invested with a ciliary covering and
probably serves as a rejection area
together with the mantle edge tracks.
The lateral areas of the muscle’s upper
surface bear longer cilia beating towards
the mouth, which probably function to
maintain the powerful anterior current
bringing water into the mantle cavity.
The posterior adductor is small. Both
sets of muscles are divided into “quick”
and “catch” portions. The foot as des-
cribed by Allen (1953) is elongate, ver-
miform in outline, but is not as pro-
portionately long as in other thyasirids.
The entire surface of the foot is annu-
larly plicated and the distal portion is
bulbous. The bulbous tip contains many
secretory cells which give a mucin-
positive histochemical reaction. The
ctenidia are extremely thick and dark,
due to abundant intrafilamentory tissue
containing many dark pigment granules,
and terminal patches of mucocytes are
present. Two nonplicate demibranchs
occur with the outer rather smaller
than the inner (Fig. 17A). Adjacent
filaments unite at intervals. Both la-
mellae of the outer demibranch are fused
to the body in their anterior portions.
In the inner demibranch only the ascend-
ing lamella is fused, the descending
lamella joining by ciliary junction only.
A marginal food groove is present in
the ventral margin of the inner demi-
branch, Ciliary currents are ina
ventral direction and towards the mouth
at the free edge of both demibranchs
(Fig. 13A). Labial palpi are small, con-
sisting of 2 subtriangular plates situated
above the mouth, communicating with it
via a deep oral groove. Six to 8 trans-

verse ridges are visible on each palp.
The mouth is a wide slit situated on the
distal portion of the “snout”, fringed by
the free folds of the oral groove. Diges-
tive diverticula consisting of 2 large
complex arborescent masses extend into
the pallial cavity. The anterior portion
consists of glandular tissues intermixed
with some gonadial tissues; posteriorly,
gonadial tissue predominates. The di-
gestive system is highly modified and
quite unlike that found in other bivalves.
The oesophagus consists of a curving
tube joining the mouth antero-ventrally
(Fig. 13C, oe.). The oesophagus extends
dorsally to the stomach; on the floor
of the stomach, anterior to its bulbous
expansion, are the 2 large (2 mm dia-
meter) openings of the ducts to the
digestive diverticula. As a result of the
strong lateral compression of the body
and the downward flexure and prolonga-
tion of the mouth, the right duct is
placed anteriorly to the left duct. The
ducts run posteriorly and then dichoto-
mise after entering the arborescent
mass of the digestive gland. The walls
of the anterior portion of the digestive
system are provided with numerous
longitudinal folds and several complex
ciliary areas. The stomach is thin-
walled and globular in shape (Fig. 14).
The small dorsal hood has anassociated
sorting area. The gastric shield is thin
and small in extent. The mid-gut and
style-sac are fused and extended poste-
riorly as a tapered tube. The crystalline
style is short and thick. The intestine
turns a 3/4 dorsal flexure and passes
through the ventricle of the heart before
running posteriorly over the posterior
adductor muscle to the anus, Pericar-
dial glands are present, consisting of 2
patches on the margins of the auricles

FIG. 16. Microscopic sections of digestive system of Thyasira disjuncta (Gabb, 1866). A. Wall
of mouth. B. Wall of stomach. C. Ductof digestive diverticulum and digestive tubule. D. Style-
sac and mid-gut. E. Mid-gut. F. Stomach, ventral sorting area. G. Intestine. H. Rectum.

Material fixed in Aceto-formol-alcohol, stained in Harris’ alum hematoxylin, counterstained |
eosin; 10 u sections. For lettering see p 372.

381

THYASIRA IN WESTERN CANADA

382 F. R. BERNARD

and covering part of the pericardial
wall. The kidneys arelarge, spongiform
bodies occupying a considerable area
posterior to the pericardium (Fig. 17F).
The large gonadal and renal apertures
are fused and open via a cloaca to the
anal cavity. The heart possesses a
highly muscularized ventricle, joined by
2 extensive subtriangular flattened au-
ricles. The posterior aorta is vestigal
as expected in this asiphonate species.
The mantle edge and the anterior adduc-
tor muscle are supplied by large bran-
ches off the anterior aorta. The gonad
consists of a layer of tissue overlying
and surrounding the digestive diver-
ticula. The interfollicular tissue is
poorly developed and the follicles large.
A complex system of ciliated ducts ram-
ify throughout the gonad and fuse to
form a definite duct passing dorsally
through the isthmus of tissue connecting
the digestive gland-gonad complex to
the body and discharging in the exhalant
region of the pallial cavity. The species
is a protandric hermaphrodite, sexual
maturity occurring at approximately the
size of 1 cm. Individuals less than 3 cm
in length were male, larger animals were
all female. Thenervous system is simi-
lar to the general form of the rest of
the order. The cerebral ganglia have
migrated ventrally and consist of 2
small commissural bodies situated be-
tween the mouth and anterior adductor
muscle. The anterior adductor muscles
and mantle are innervated by the pallial
nerve. The pedal ganglia are large and
richly supplied with red tissues, prob-
ably containing haemoglobin. Statocysts
were not found. The visceral ganglia
are small and difficult to locate.

Thyasira flexuosa (Montagu, 1803)
(Figs. 5, 6, and 12)

Venus sinuosa Donovan, 1802, pl. 42,
fig. 2 (non Pennant, 1777); Tellina
flexuosa Montagu, 1803, p 72; Amphi-
desma flexuosa, Lamarck, 1818, p 128;
Lucina sinuata Lamarck, 1818, p 230;
Cryptodon flexuosum, Turton, 1822, p
121, pl. 7, figs. 9, 10 (non Möller, 1842);
Ptychina biplicata Philippi, 1836, p 15,
pl. 2, fig. 44; Lucina flexuosa, Gould,
1841, p 71, fig. 52; Forbes & Hanley,
1850, p 54, pl. 35, fig. 4; Lucina gouldii
Philippi, 18453, p. 74, pl. 2: НЕЕ
Axinus sarsii Philippi, 1845b, p 91;
Axinus flexuosus, Loven, 1846, p 39;
Jeffreys, 1863, p 247; G. Sars, 1878,
p 59, pl. 19, figs. 4a, b; Cryptodon
gouldii, Gould in Binney, 1870, p 100,
fig. 406; Cryptodon flexuosus, Dall, 1874,
p 297; Cooper, 1888, p 237; Axinus
gouldii, G. Sars, 1878, p 60, pl. 19, figs,
6a, b; Cryptodon barbarensis Dall, 1890,
p 261, pl. 8, fig. 9; Thyasira gouldii,
Dall, 1901, p 790; Arnold, 1903, p 135;
Dautzenberg & Fischer, 1912, p 485;
Dall, 1921, p 33; Oldroyd, 1924, p 120,
pl. 34, fig. 5; Oldroyd, 1925, p 5; Water-
fall, 1929, p 78; Thiele, 1928, p 620;
Grant & Gale, 1931, p 282; Johnson,
1934, p 39; LaRocque, 1953, p57; Clarke,
1962, p 64; Thyasira barbarensis, Dall,
1901, p 790; Dall, 1921, p 34; Oldroyd,
1924, p 120, pl. 53, fig. 3; LaRocque,
1953, p 56; Parker, 1964, p 159; Thy-
asiva flexuosa, MacGinitie, 1959, p 171,
pl. 4, fig. 12.

Type locality:
of Britain.

Type: (Lectotype) Royal Albert Mu-
seum, Exeter, England. Montagu Col-

South and east coasts

|
Thyasira disjuncta (Gabb, 1866). Microscopic sections. A. Vertical section through
right gill. B. Vertical section through base of left oral palp. C. Transverse section through
digestive tubules and gonad. D. Longitudinal section through ciliated gonoduct and follicles.
E. Transverse sectionthrough upper mantle tissue. F. Vertical section through excretory organ.
Material fixedin Aceto-formal-alcohol, stained in Harris’ alum hematoxylin counterstained eosin.
For lettering see p 372.

FIG. 17.

10 u sections.

THYASIRA IN WESTERN CANADA 383

= gr na Lente à

== gees

384

lection, No. 3894-9. Type lot consists
of 7 single valves and 2 complete shells.
A lectotype was designated by Ockel-
mann (1961) and is registered as 3894.

Original description: Tellina with a
thin, pellucid, fragile, convex, sub-orbi-
cular, white shell: from behind the umbo
to the lower angle of the margin, a
sulcus runs parallel to the cartilage
Slope, and forms a sinus or flexure at
the edge. It is finely, but irregularly
striated concentrically, and is not very
glossy: umbo placed central, much pro-
duced, and turns to one side at the apex:
hinge with an obsolete tooth; along the
margin, from behind the umbo, a groove
in which is fixed the connecting carti-
lage: inside smooth, glossy white.

Range: Point Barrow, Alaska, to San
Diego, California. Atlantic, Greenland
to Connecticut. Iceland, Europe, Medi-
terranean, in 35-450 metres,

Material examined: National Museum
of Canada -49 valves (Cat. No. 1302); 2
valves (Cat. No. 45580). Fisheries
Research Board of Canada - 14 lotsfrom
various stations along the British Co-
lumbian coast, live collected.

Discussion

Gould (1841) identified Tellina flexuosa
from off Massachusetts; however, Phil-
ippi (1845b) considered the American
species to be sufficiently distinct to
warrant separation and applied the name
Lucina gouldii. Jeffreys (1863) ques-
tioned Philippi’s species but did not
synonymize the 2 names, Madsen(1949)
and Soot-Ryen (1932), followed by Mac-
Ginitie (1959) regarded T. gouldi and
T. sarsi as junior synonyms of T.
flexuosa. Intergradations with the simi-
lar T. barbarensis Dall 1890 occur, par-
ticularly to the south of the range and
are here considered synonymous, Ockel-
mann (1961) considered T. plana and T.
inaequalis, both Verrill & Bush, to be
junior synonyms of T. gouldi. The form
gouldi is clearly identifiable both in the
Pacific and Atlantic, and the discoidal
form sarsi may be separated from most
long series. Separation into various

F. R. BERNARD

forms of this highly plastic and variable
species is confusing and does not clarify
the systematics. Miloslavskaja (1970)
confirmed the observations of Ockelmann
(1958) concerning the absence of T.
flexuosa from the high arctic and con-
sidered it a boreal-lusithanian species.
The hinge and ligament have been well
described by Allen (1960). Though he
describes a small tooth in the right
valve of T. flexuosa, these are not always
present, the majority of adult specimens
being entirely edentulous,

Anatomy

An excellent description has been
given by Allen (1958), so only a short
addition to his description will be given
here. Mantle thin, transparent, mar-
gins thickened similarly to other Thy-
asiridae. Mantle fusion limited to a
small section below the anal aperture.
Mantle fusion around the anal aperture
is limited to the middle fold only (Allen,
1958). Inhalant aperture large. Ad-
ductor muscles markedly divided into
“quick” and “catch” portions. The an-
terior adductor is elongate, curvedalong
the ventral border of the mantle. Foot
extremely elongate, distal portiontumid.
Ctenidia heavily pigmented dark brown,
thick, non-plicate, consisting of a small
outer andlargerinner demibranch. Mar-
ginal groove deep, running anteriorly.
Labial palpi reduced, bearing 5-8 lateral
folds. Mouth small, situated on the
distal tip of a snout-like prolongation,
connecting with the palps via a strong
oral groove. Digestive diverticula con-
sist of arborescent tufts situated on
either side of the body, communicating
with the stomach by 2 large apertures,
Gonadial tissue surrounding the digestive
diverticulum tubules and predominating
in the posterior portions of the lateral
tufts. The speciesis dioecious, Stomach
thin-walled, mid-gut fused with style-
sac. Crystalline style short, hard,
Gastric shield thin, small. The stomach
structure of T. flexuosa has been studied
by Purchon (1958a, 1958b) and agrees
well with our interpretation. Mid-gut

THYASIRA IN WESTERN CANADA 385

short, direct, passing through the ven-
tricle of the heart. The circulatory
system agrees in general with T. dis-
juncta and was not studied in detail.

ACKNOWLEDGEMENTS

I wish to express my gratitude for
assistance and advice received from
the following: Dr. A. H. Clarke of the
National Museum of Canada; Dr. P. J.
Boylan of the Royal Albert Museum,
Exeter; Dr. L. G. Hertlein of the Cali-
fornia Academy of Sciences; Dr. J. Mc-
Lean of the Los Angeles County Museum
of Natural History; Dr. K. Van Winkle
Palmer of the Paleontological Research
Institution, Ithaca; Dr. D. B. Quayle of
the Fisheries Research Board of Canada,
Nanaimo; Dr. H. G. Richards of the
Academy of Natural Sciences in Phila-
delphia; Dr. J. D. Taylor of the British
Museum (Natural History).

Thanks are extended to Mrs. J. Bain
and Miss D. Blake for careful typing of
the manuscript.

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ZUSAMMENFASSUNG

DIE GATTUNG THYASIRA IN WESTKANADA (BIVALVIA: LUCINACEA)

F. R. Bernard

Eine kurze Übersicht der Systematik und Anatomie der 4 Arten der Muschelgattung
Thyasira Lamarck, die in den Merren von Westkanadaleben, wird gegeben. Auf Grund
der Aufsammlungen an den vielen hundert Stellen der faunistischen Aufnahme der
Fischerei-Forschungsstelle von Kanada, die seit 1950 gemacht worden sind, wird
geschlossen, dass T. trisinuata D’Orbigny 1846 nördlich nicht Uber Britisch Columbia

hinausgeht.

Anatomische Untersuchungen ergaben deutliche Modifikation des Verdauungssystems

im Zusammenhang mit der macrophagen Ernährung.

Hypertrophie des Fusses und

die Anordnung der Mantelöffnungen und Wasserströmungen sind sekundäre Anpassungen

an ein tiefgründiges Substrat.

Die Gattung ist nahe verwandt mit den Luciniden und

ist ein hochentwickelter Zweig der Heterodonta.

H° 2.

THYASIRA IN WESTERN CANADA

RESUME
LE GENRE THYASIRA DANS L’OUEST CANADA (BIVALVIA: LUCINACEA)
F. R. Bernard

L’auteur présente un bref exposé de systématique et d’anatomie de 4 espèces du
genre Thyasira Lamarck, se trouvant dans les mers de l’Ouest Canada. En se basant
sur les collectes de plusieurs centaines de stations de la prospection faunistique du
Fisheries Research Board du Canada, réalisées depuis 1950, on en conclut que T.
trisinuata Orbigny 1846, ne se rencontre pas plus au nord que la Colombie Britannique.

Les études anatomiques révélent une modification profonde de l’appareil digestif,
en relation avec le comportement macrophagique. L’hypertrophie du pied et la dis-
position des ouvertures palléales et des courants d’eau, sont des adaptations secon-
daires a l’habitat hypogé profond. Le genre est étroitement apparenté aux Lucinidés

et représente une branche terminale des Hétérodontes.
A. L.

RESUMEN
EL GENERO THYASIRA EN CANADA OCCIDENTAL (BIVALVIA: LUCINACEA)
F. R. Bernard

Esta trabajo presenta una breve revisiön, sistemätica y anatömica, de las cuatro
especies del género de bivalvos Thyasira, que habitan en el oeste de Canada. En base
a las colecciones hechas por la Dirección Canadiense de Estudios Pesqueros, en
varios cientos de estaciones desde 1950, se concluye que T. trisinuata d’Orbigny,
1846, no aparece tan al norte como la Columbia Británica.

Estudios anatómicos revelan marcada modificación del sistema digestivo en con-
nexión con el comportamiento macrófago. Hipertrofia del pié, y el ordenamiento de
las abertura paleales y corrientes aquiferas, son adaptaciones secundarias a un
habitat faunístico de profundidad. El género esta estrechamente relacionado con los

Lucinidos y representa una rama terminal de los Heterodonta. ran

ABCTPAKT
РОД THYASIRA Y ЗАПАПНОЙ КАНАЛЫ (BIVALVIA: LUCINACEA)
Ф.Р. БЕРНАР

Работа представляет собой обзор систематики и анатомии 4 видов

двустворчатых моллюсков из рода Thyasira Lamarck, встречающихся y
восточной Канады. Работа основана Ha изучении сборов этих моллюсков,
сделанных BO время фаунистических исследований В экспедициях
Fisheries Research Board of Canada, начиная с 1950 г. Судя по результатам

обработки этих материалов Т. trisinuata Orb., 1846 не заходит так далеко на
север, до Британской Колумбии. Анатомические исследования видов Thyasira
показали наличие значительной изменчивости их пищеварительной системы,
что связано e образом жизни их, как макрофагов. Гипетрофия
ноги, расположение мантийных отверстий и токи воды представляют собой
вторичную адаптацию этих моллюсков к обитанию глубоко в толще осадков
(инфауна). Род близок к Люцинидам и является концевой ветвью Heterodonta.

Z. A. F.

389

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MALACOLOGIA, 1972, 11(2): 391-406

NEW DATA ON THE SQUIDS (CEPHALOPODA: OEGOPSIDA)
FROM THE SCOTIA SEA (ANTARCTIC)

J. A. Filippova

All-Union Research Institute of Marine Fisheries and Oceanography
17 Verkhne-Krasnoselskaja
Moscow B - 140, U.S.S.R.

ABSTRACT

A collection of squids (Cephalopoda, Oegopsida) is described which was ob-
tained during cruises I and III in the Scotia Sea by the research vessel (R/V)
“Academician Knipovitch”. The collection contains 33 specimens representing
5 genera and 6 species, of which 3 species and 1 genus are new to science;
Moroteuthis knipovitchi, Galiteuthis aspeva, and Kondakovia longimana; the
latter is the type species of a new genus belonging to family Onychoteuthidae.
Among the species found, Psychroteuthis glacialis is of especial interest, since
this rare antarctic species, known previously only from fragments taken from
seal and penguin stomachs, was encountered for the first time in 50 years. The
most common species found inthe Scotia Sea was the Brachioteuthis sp. (?riisei).

INTRODUCTION

The cephalopod fauna of Antarctic wa-
ters (especially the squids) is still far
from being adequately studied. Those
scant data which are presently available
come mainly from certain expeditions
realized by the “Alert”, “Valdivia”,
“Scotia” and some other shipsinthe past
century and in the first quarter of the
present one. Results connected with
cephalopods were published in a number
of works (Smith, 1881; Chun, 1910;
Hoyle, 1912; Thiele, 1921; Odhner, 1923;
Robson, 1925). After a fairly long re-
cess some informative articles have
appeared (R. Clarke, 1956; Dell, 1959;
M. Clarke, 1966; Korabelnikov, 1959),
and recently American malacologists
have started the study of cephalopods of
the Antarctic (Voss, 1967; Roper &
Young, 1968; Young & Roper, 1968;
Roper, Young & Voss, 1969).

Since 1965 ВНИРО (All-Union Research
Institute of Marine Fisheries and Ocean-
ography) has been carrying out investi-
gations within the Atlantic sector of the

Antarctic Ocean, making use of the re-
search vessel “Academician Knipo-
vitch”,

The present communication deals with
a description of a rather modest collec-
tion gathered on board this ship during
its cruises I and III in the Scotia Sea,
This latter is located between the Falk-
land, S. Shetland, S. Orkney and S.
Georgia Isles and lies predominantly
south of the Antarctic convergence; con-
sequently, it forms an integral part of
the Antarctic waters.

The collection contains 33 specimens
from 14 stations (Fig. 1) captured by
use of various commercial trawls of
both the benthic and pelagic types.

The animals were measured according
to the Adam’s scheme (Adam, 1952).
The absolute magnitude is given for the
mantle length only, all other sizes are
given as a % of this first value. Their
Symbols are as follows : ML - mantle
length; MWI - mantle width index; FLI -
fin length index; FWI - fin width index;
CLI - club length index; I, II, Ш, IV -
arms length index.

(391)

392

J. A. FILIPPOVA

FIG. 1. Map of the stations of R/V “Academician Knipovitch” in the Scotia Sea from which the |

squids were caught.
SYSTEMATIC SECTION

Family Onychoteuthidae
Moroteuthis ingens (E. Smith, 1881)

Sta. 203, March 17, 1965. Trawling depth
30-50 m. 13; ML - 212 mm.

This species is endemic to the South-
ern hemisphere. It has been taken in
Magellan Strait (E. Smith, 1881; Lonn-
berg, 1898), near the S. Orkney Isles
(Hoyle, 1912), and off New Zealand
(Massy, 1916; Filippova, unpublished).
It was considered to be a rare species
because of its paucity in the trawls.
However data on the feeding of sperm
whales show that it forms the principal
part of the diet of these whales in ant-
arctic waters (R. Clarke, 1956; M.
Clarke, 1965, 1966). This suggests that
M. ingens is abundant, as whales gener-
ally feed on the schooling animals, at
least in summer (Klumov, 1963).

In our collection this species is re-

presented by a single specimen, the
characters of which fully coincide with
those described by Pfeffer (1912), with
the exception of the relative length of
the fins. They are shorter (FLI-48)
than the fins of specimens described by
Pfeffer (FLI-49-58). Our specimen is
a male with a ripe gonad and with sper-
matophores in Needham’s sac. The
genital organ is a long narrowtube which
reaches the middle of the funnel carti-
lage. There are no traces of the hecto-
cotylus. The radula has 7 rows of teeth.

The central teeth are tricuspid, thefirst |

lateral ones bicuspid, and the others
unicuspid.
Moroteuthis knipovitchi, sp. nov.

Sta. 176, March 3, 1965. Trawling depth
550-400 m. 1%; ML - 225 mm

The structure of the gladius is with

short rhachis, long wide vane and ter- |

minal cartilaginous conus; the presence

SQUIDS FROM THE SCOTIA SEA 393

of rows of hooks on the clubs, and suckers
with smooth rings onthe arms; а rounded
funnel groove; the absence of nuchal
folds and photophores.

These characters allow this squid to
be placed in the genus Moroteuthis.
However as it differs from the other
known species of this genus, it is here
referred to as a new species.

Description. (Fig. 2,3). The mantle,
cylindrical in its anterior half, tapers
from the base of the fins toward the
posterior end (Fig. 2a). The anterior
dorsal margin of the mantle is slightly
produced while the ventral margin is
emarginated in a gentle curve,

The fins are large and united together
into a rhombus. They are broadest in
the middle of their length. The skin is
thin and smooth. The head is narrower
than the mantle width. The funnel,
broad at its base, is gradually attenuating
and reaches the lower margin of the eye
opening. The funnel organ (Fig. 2d)
consists of the inverted V-shaped dorsal
pad and 2 oval ventral pads. The locking
apparatus (Fig. 2c) consists of a longi-
tudinal cartilaginous groove on the fun-
nel and a long narrow ridge on the
mantle,

The arms are stout, in order 2-3 =
4-1. The suckers have smooth horny
rings (Fig. 2e). The suckers of the
ventral arms are smaller (d-1.8 mm)
than those on the others (d-2.0-2.3 mm).

The tentacles are long with the stalks
compressed laterally. At the base of
the club there is an adhesive organ con-
sisting of 9 minute, closely sitting suc-
kers and 9 pads. The club (Fig. 2b) is
slightly expanded withthe swimming keel
on the aboral surface. The oral surface
is occupied by 13 pairs of long narrow
hooks, those of the ventral row being
larger than those of the dorsal. The
largest is 1cm in length. The hooks
are wrapped in skin hoods. The base
of each large hook is asymmetrical due
to the presence of a semi-circular appen-
dage on 1 side (Fig. 2f). There is a
small patch of 16 minute suckers at the
distal extremity of the club.

The gladius (Fig. 3) with the vane

running along its larger part has a ter-
minal cartilaginous conus, which occu-
pies about 1/6 ofthe length of the gladius.
The terminal conus is triangular in
cross section with a sharp ventral edge
and flattened dorsal one.

The radula has 7 rows of teeth. All
of the teeth are uniform unicuspid with
narrow bases. There are no additional
cusps (Fig. 2g). Photophores are absent.
The color of the preserved animal is
light violet.

The squid described above is a young
female with minute eggs in the ovaries
and moderate-sized nidamental glands,
the length of which is 34 mm, i.e., 16%
of mantle length.

The Holotype of Moroteuthis knipo-
vitchi, sp. nov. is inthe Zoological Insti-
tute of the Academy of Sciences of the

U.S.S.R. Its measurements and indices
are as follows:
ML - 225 mm
FLI - 60%
FWI - 69%
ArmsI 44%
Il 54%
II 53%
IV 253%
СШ =" 450%

Locality: near South Georgia Island.

Discussion. This species is allied to
M. aequatorialis Thiele, 1921, by the
presence of the thin, smooth skin while
the other species of Moroteuthis (M.
robusta, M.ingens, M. lonnbergii, M.
robsoni) have warty skin. However M.
knipovitchi is distinguished from these
and M. aequatorialis by the peculiarities
of the radula, the teeth of which are
unicuspid while the radulae of other
Species are characterized by the pre-
sence of additional cusps: 2 on the teeth
of the central row and 1 on the Ist
lateral teeth.

Hoyle (1912) illustrated the radula of
a species which, in his opinion, was M.
ingens. At the same time he pointed
out its differences from that of M. ingens
described by Smith (1881). Iaminclined
to think that this radula is related to M.
knipovitcht. I have had the opportunity

394 J. A. FILIPPOVA

{cm

1ст

FIG. 2. Moroteuthis knipovitchi sp. nov. a, dorsal view; b, tentacular club; с, funnel and |

mantle cartilages; d, funnel organ; e, armsucker; f, large hook of tentacular club; g, radular
teeth; h, mandibles.

SQUIDS FROM THE SCOTIA SEA 395

2

FIG. 3. Moroteuthis knipovitchi, sp. nov.
The gladius.

to examine the radula of M. ingens from
specimens caught in different parts of its
range - in the Scotia Sea and off New
Zealand. The radula has median teeth
distinctly tricuspid, and the 1st lateral
ones bicuspid.

Diagnosis. M. knipovitchi is charac-
terized by the smooth, thin skin, pecu-

liar radula, the asymmetrical base of
hooks of the club, and the large rhombic
fins. This species is named in honour
of the famous Russian oceanologist acad-
emician N. M. Knipovitch.

Kondakovia, gen. nov.

Since this new genus presently in-
cludes a single species, it is impossible
to delimit the generic characters sepa-
rately from the specific ones; the diag-
nosis of the genus coincides with that of
a species. The genus is named after
the noted Russian malacologist М. М.
Kondakov.

Kondakovia longimana, sp. nov.

Sta. 835, February 17, 1967. Trawling
depth 50 m. 12 ; ML - 138 mm

Sta. 969, March 20, 1967. Trawling depth
50 m. 12; ML - 210mm

Sta. 970, March 20, 1967. Surface. 19;
ML - 260 mm.

Description. (Fig. 4) The mantle is
broadly cylindrical, shaped like a bag,
slightly tapering posteriorly. Its walls
are soft andfleshy. The anterior mar-
gin is slightly produced dorsally into a
moderate prominence, while forming a
shallow notch ventrally.

The head and arms are more massive
and longer than the mantle portion (Fig.
4a). The fins are soft and feeble with a
slightly extended tail. Their length is
less than half that of the mantle and
their width somewhat exceeds the length.

The head is narrower than the mantle.
The funnel, broad at the base, reaches
the lower edge of the eye opening. The
funnel groove is rounded infront. The
mantle-locking cartilage is longitudinal
with nearly parallel margins and a deep,
slightly curved groove. Its frontal end
is more acute than the posterior one,
The corresponding mantle cartilage is
shaped like a thin longitudinal ridge
(Fig. 5a). The nuchal cartilage consists
of 2 marked ribs separated by a longi-
tudinal groove. The funnel organ con-
sists of an inverted V-shaped dorsal
pad and 2 oval ventral pads (Fig. 5b).

The skin on the dorsal surface of the

396

FIG. 4.

mantle, of the head and the base of the
arms is vesicular, The arms are mas-
sive and fleshy, equalling or exceeding
the mantle in length. While stout at
their bases, they thin out progressively
to become nearly thread-like at thetips.
The distal part of the ventral arms re-
veals a swimming membrane, The oral

Kondakovia longimana, gen. nov. sp. nov.
dius; Cy, transversal section of terminal conus of gladius; d, mandibles.

J. A. FILIPPOVA

surface of the arms is bordered on
either side by a protective wavy mem-
brane with muscular supports. The
suckers on the arms have smooth horny
rings (Fig. 5c). The suckers on the
ventral arms are smaller than those on
the other arms. The tentacles are long,
being 1 1/2 times longer thanthe mantle.

a, dorsal view; b, tentacular club; с, gla- |

SQUIDS FROM THE SCOTIA SEA 397

=

E
i
SE

Е
E
%

d

FIG. 5. Kondakovia longimana. a, funnel
and mantle cartilages; b, funnel organ; c,
armsucker; d, hook of tentacular club.

Their stalks are strongly flattened from
both sides, ribbon-shaped. The fixing
apparatus at the base of the club is not
as compact as the one of the genus
Moroteuthis and its boundaries are
less distinctly defined. It consists of
10 suckers and 7 pads on the right club,
and 10 pads and 9 suckers on the left
one.

The club is slightly expanded (Fig. 4b);
the bordering protective membrane and
the swimming keel running its whole
length are indistinctly pronounced. The

club is equipped with 2 rows of hooks
and 2 series of minute suckers arranged
peripherally. Each club is armed with
33 hooks and an equal number of mar-
ginal suckers. The distal portion of the
club is occupied by 28 closely fitted,
minute suckers.

The general pattern of the gladius is
much the same as that of Moroteuthis;
that is a short rachis, a vane running
nearly the whole length of the gladius
and a cartilaginous rostrum at the end.
Yet the gladius discussed has a number
of distinguishing features. It is thinner,
more fragile and furnished with 3 pairs
of narrow longitudinal ribs (Fig. 4c).
The first pair, shaped like narrow, deep
grooves, border the rachis onboth sides,
while those of the second pair follow the
marginal rim, and the third pair (the
least distinct) are located between the
first 2. The rostrum, shaped like a
thin, semitransparent plate, begins with-
in 15 mm from the end of the gladius,
on its dorsal surface; it extends back-
wards ending in a trihedral point. There
is a convex rib over the full length of
its flat dorsal surface. Incross-section
this rostrum shows a laminated structure
(Fig. 4c,).

The lower mandible has a gentle rib
on its lateral wall, which is directed
from the upper frontal angle backwards
in such a manner as to cross midway
the back edge of the lateral wall. The
mandible is black-brown coloured ex-
cept for the cartilage-coated wings,
which are milky-semitransparent, and
the marginal rim on the lateral wall
which is transparent. The upper mandi-
ble has transparent wings and lateral
walls. There is a dark spot on the dor-
sal mandible surface (Fig. 4d). The
radula has 7 longitudinal rows of ex-
tremely minute teeth. The specimen
from Sta. 969 has only 6 rows, as it
lacks the central one. It is possible
that we have here a case of pathological
departure,

The squids were purple-brown col-
oured, and without photophores. All 3
specimens were immature females, jud-

398

ging by the size of their ovaries and
nidamental glands. These latter varied
from 14% of the mantle length to 9.8%
for the smallest specimen. All 3 squids
had their stomachs tightly packed with
semidigested remains of Euphausia su-
perba. The holotype is in the Zoological
Institute of The Academy of Sciences of
the U.S:S:R:

Discussion. Kondakovia longimana re-
sembles the genus Moroteuthis. Indeed,
the general structural pattern of the
gladius, the rounded funnel groove, the
presence of the neck folds and the ab-
sence of the nuchal folds, the gladius
being nontranslucent on the dorsal sur-
face - all these features emphasize their
affinity. On the other hand the some-
what different bodily proportions, pe-
culiar characters of the gladius, and
suckers and hooks located together on
the club of the adult squids do not allow
us to place it in the genus Moroteuthis.
Since the gladius and club structure are
the generic features for the family
Onychoteuthidae I believe I must attri-
bute these animals to a new genus with
the following characters: a massive an-
terior portion of the body with long
thick arms, weakly developed fins, a
club equipped with suckers and hooks,
and a thin, fragile gladius with narrow
longitudinal thickenings. Three speci-
mens of Kondakovia longimana were en-
countered at 3 stations somewhat north
of the S. Orkney Isles, in localities
with high krill concentrations. The
contents of squid stomachs show that
they feed upon Euphaisiids. This, along
with the peculiar bodily proportions, the
looseness of the tissues and a moderate
size of radula with very minute teeth,
is indicative of a form adapted to feed
upon macrozooplankton (Euphausiids).
An easily accessible and abundant food
is evidently responsible for the loss of
a number of features inherent to active,
predatory pelagic dwellers, such as
squids of the genus Moroteuthis. All of
this indicates that the new squid is en-
demic to Antarctic waters, and does not
extend beyond the limits of E. superba

J. A. FILIPPOVA

TABLE 1. Measurements (mm) and indices
of Kondakovia longimana gen.

nov. sp. nov.

—

Holotype Paratypes

ML 260 210 133
MWI - - 27
FLI - 42 42
FWI - 60 57
Arms I 80 110 54

Il 100 119 64

III 96 116 66

IV 100 114 65
CLI 39 40 30
distribution.

Family Psychroteuthidae
Psychroteuthis glacialis, Thiele, 1921

Sta. 91, November 5, 1965. Trawling
depth 410-396 m. 19 ; ML - 128 mm
Sta. 200, March 15, 1965. Trawling depth

560-730 m. 12; ML - 131 mm

A single species of this endemic ant-
arctic genus has been described (Thiele,
1921) from the fragments of some spe-
cimens taken from the stomachs of
Weddell seals and penguins in the Ant-
arctic.
living Specimens until now. Therefore
description of our specimens would be
useful,

Description. (Fig. 6) The mantle is
cylindrical, tapering rapidly from the
beginning of the fins. The anterior
mantle margin is slightly produced dor-
sally in the midline, while ventrally it
is emarginated beneath the funnel with
small lateral lappets (Fig. 6a).

The fins are large, rhomboidal, wider
than long, with the length slightly ex-
ceeding half the mantle length.

The head is narrower than the mantle,
with small eyes and 2 neck folds on each
side of the head,

The funnel is wide at its base, and
tapers rapidly to the safe end. It is
short and reaches to about the level of
the eyes. The funnel organ consists of

There have been no records of |

SQUIDS FROM THE SCOTIA SEA 399

lcm

5 ст

FIG. 6. Psychroteuthis glacialis. a, dorsal view; b, tentacular club; с, gladius; а, mandibles;

e, armsucker; f, large sucker of tentacular club.

an inverted V-shaped dorsal pad with a
small papilla in the middle of its ante-
rior margin and 2 ventral oval pads.
The funnel cartilage is simple with a
somewhat sinous, longitudinal groove.
The corresponding member on the man-
tle is a ridge of the same length,
The arms are moderately long, stout

in the base, gradually tapering to the
end. Their suckers are biserial and
are protected on either side by a low
protective membrane. The suckers
are provided with smooth horny rings
except the terminal ones which have
finely toothed rings (Fig. 6e).

The tentacles are considerably longer

400
TABLE 2. The measurements (mm) and in-
dices of 2 specimens of P. glacialis
2 2
ML 128 | 131
MWI - | 24. 4
FLI 577 5732
FWI | 71.8 64.8
arms I 44.5 56. 4
Il | 53:41: 59.5
III 51.5 57.2
IV 50. 7 557

than the arms, with the strong, slightly
expanded clubs curved like palms (Fig.
6b). The club bears 4 rows of suckers
with horny rings provided with sharp
teeth bent outwards (Fig. 6f). The cen-
tral suckers have 25-26 teeth. Some of
the suckers of the central rows are
distinctly larger than the outer ones.
The distal part of the club bears minute
suckers which sit in 5 rows. At the
base of the club there is a row of mi-
nute adhesive suckers and pads which
run along the tentacle stalk.

The gladius is lanceolate, weak and
transparent, with a short rachis, rather
wide and long vane, the margins of which
are fused in the distal part andforma
pocket without a bottom (Fig. 6c). The
gladius does not reach the end of the
body.

There are no photophores.
is thin and lightly coloured.

Both specimens are females withova-
ries and nidamental glands insignifi-
cantly developed.

The skin

Family Brachioteuthidae
Brachioteuthis sp. (?riisei Steenstrup,
1882)

Sta. 110. February 9, 1965. Trawling
depth 40 m, 3 sp.; ML - 90; 66; 58 mm
Sta. 186. March 11, 1965. Trawling depth
50-60 m. 3 sp; ML - 117; 110; 107mm
Sta. 201. March 16, 1965. Trawling depth
50-60 m. 3 sp.; ML - 115; 22; 26 mm
Sta. 817. February 14, 1967. Trawling
depth 30 m. 3 sp.; ML - 138; 106; 77 mm

J. A. FILIPPOVA

Sta. 957. March 18, 1967. Trawling depth
50 m. 10 sp.; ML - 132-80 mm

Our collection contains 22 specimens
of this species, taken from 5 stations,
The material suggests that this species
is one of the common squids in the sur-
face waters of the Scotia Sea. The main
systematic features allow it to be re-
ferred to Brachioteuthis riisei. How-
ever the sizes of our squids exceed
considerably those of the known speci-
mens of B. riisei. Many of our squids
are about 100 mm in mantle length, the
largest one being 138 mm, i.e., 4 times
as large as the largest specimen of B.
riisei (33.5 mm) examined up to now
(Degner, 1925).

Whether or not this squid represents
a new Species is a problem which will
be unsolved until additional specimens of
В. riisei are obtained from different
parts of its wide range, and the compar-
ison is made.

Family Cranchiidae
Galiteuthis aspera sp. nov.

Sta. 921. March 11, 1967. Trawling depth
50-60 m. 1 sp.; ML - 317 mm

Sta. 932, March 14, 1967. Trawling depth
40m. 1 sp.; ML - 137 mm

Sta. 957. March 18, 1967. Trawling depth
50 m. 2 sp.; ML - 260; 200 mm

Description. (Fig. 7) The mantle is
very long, with a form reminiscent of a
tall, conical wine-glass (Fig. 7a). The
mantle surface is closely set with small
but distinct cartilaginous tubercles, due
to which the skin feels prickly. On the
surface of the mantle, at the points of
its attachment with the funnel and the
head, there are clusters of 5-6 spines
(Fig. 7b, c).

The fins are large, festonal on their
margins; their outline may be described
as longitudinal oval (Fig. 7a, d). Their
length equals about 1/2 of the mantle-
length, their width is 1/2 their length.

The funnel is broad at the base, and
then tapers while its tubular distal end
is curved ventrally. The funnel organ
consists of a large dorsal pad, which

SQUIDS FROM THE SCOTIA SEA 401

a

FIG. 7. Galiteuthis aspera, sp. nov. a, dorsal view (paratype; the tentacles are torn away);
b, part of mantle skin; c, funnel; d, ventral view of fins; e, tentacular club (holotype’s); f,
outline of fins of С. aspera and С. armata; g, armsucker from the distal part of arm Ш; g,,
armsucker from the proximal part of arm III; h, eyeball with the large semilunar photophores.

402 J. A. FILIPPOVA

surrounds the anal conus, and is equip-
ped with 2 papillae and 2 rounded ven-
tral pads.

The arms are stout, rather short,
about 1/; the mantle length, in order
3-2-4-1. The oral surface of the arms
is bordered for its entire length on ei-
ther side by a protective membrane with
long supports. The horny rings of the
suckers are weakly toothed, but the
more distal suckers have more obvious
teeth (Fig. 7g, g,).

The tentacles are long and muscular.
The tentacular stalk is round in cross-
section and bears, along its distal °4,
pairs of small adhesive suckers alter-
nating with pairs of small pads. At the
base of the club there is afixing appara-
tus consisting of 8 suckers and 8 pads.
The club is a little expanded, and bor-
dered by a protective membrane. The
club length equals lessthan l/pthe man-
tle length. It bears 6 pairs of long, thin
hooks, which are distally replaced by
4 rows of minute suckers. Each hook,
except a proximal one, has a minute
sucker at its base (Fig. 7e). There are
11 such suckers on each club,

The gladius is clearly visible through
the mantle wall. It is very slender with
an anterior expansion and with another
about the fins, where its width equals
1/53 of the gladius length. From this
point it gradually tapers and becomes
an extremely narrow gutter. the margins
of which do not fuse.

The radula has 7 longitudinal rows of
teeth of which the central 1 is more
obvious, consisting of the teeth with 2
additional cusps. The teeth of the 1st
lateral rows have 1 cusp.

The colour of the squids is pale with
large, light violet chromatophores. The
head, buccal membrane and oral surface
of the arms are coloured more inten-
sively.

The eyeballs eachbear ontheir ventral
periphery 2 large semilunar photophores
(Fig. 7h), the outer being much larger
than the inner one, and enclosing the
latter.

TABLE 3. The measurements (mm) and indi- |
ces of G. aspera sp.nov.

Holotype Paratypes

The holotype is in the Zoological
Institute of the Academy of Sciences of
the U.S.S.R.

Distribution. The eastern part of the
Scotia Sea.
Discussion. Until recently the genus

Galiteuthis was considered to be mono-
typic (with the single species G. armata)
and widely distributed. It hasbeentaken
in the North Atlantic (Joubin, 1898;
Degner, 1925; Voss, 1960), South At-
lantic off the African coasts (Chun,
1910, Robson, 1924), and the Pacific
(Berry, 1912; Sasaki, 1929; Iwai, 1956;
Hikita & Hikita, 1956; Pearcy, 1965;
Akimushkin, 1963). As for its discovery
in antarctic waters there is very doubt-
ful evidence; 2 juveniles were caught
in the Weddell sea. These were later
referred to G. suhmi, which was later
synonymized with G. armata (M. Clarke,
1966). Until now no adult Galiteuthis
had been caught in antarctic waters.

Iwai (1956) pointed out that the squid
from the stomach of a sperm whale,
caught in the north-western Pacific,
differed from typical G. armata, and
that this suggests the existence of 2
forms of Galiteuthis - Atlantic and Pa-
cific ones.

Our specimens have a number of
characteristic features which distin-
guish it from typical forms of G. armata
and from Iwai’s specimen. There fea-
tures are: 1. prickly surface of the

SQUIDS FROM THE SCOTIA SEA 403

TABLE 4.

List of squid species from the Antartic region (based on

published data and the author’s observations)

Species

Distribution

Architeuthis spp. widespread (genus)

Onychoteuthis banksi
Moroteuthis ingens
Moroteuthis knipovitchi
Kondakovia longimana
Gonatus antarcticus
Psychroteuthis glacialis
Alluroteuthis antarcticus
Brachioteuthis riisei
Bathyteuthis abyssicola
Batoteuthis scolops
Neoteuthis sp.
Promachoteuthis sp.
Oregoniateuthis lorigera
Calliteuthis miranda
Crystalloteuthis glacialis
Teuthowenia antarctica
Taonius pavo

Galiteuthis aspera
Mesonychoteuthis hamiltoni

cosmopolitan
antarctic and notalian
antarctic

antarctic

antarctic and notalian
antarctic

antarctic
cosmopolitan
cosmopolitan
antarctic

antarctic

antarctic

antarctic

antarctic, notalian and south-subtropical
antarctic

antarctic and notalian
cosmpoolitan
antarctic

antarctic

mantle due to numerous tubercles; 2.
presence of clusters of hyaline spines
at points where the mantle attaches to
the head and funnel. 3. toothed horny
rings on the arm suckers. 4. fins longi-
tudinal oval in their outline (Fig. 7f).
5. rather wide fins, which are l/ as
wide as they are long.

All this, and its distribution in antarc-
tic waters, indicate that this squid is a
new species.

CONCLUSION

A small collection of squids (33 spe-
cimens) obtained from a somewhat lim-
ited region of Antarctic waters is, none-
theless of marked interest, inasmuch
as it enlarges our knowledge of a little-
known fauna of antarctic Cephalopods.
Out of 6 species of squids from this
collection 3 proved to be new, including
one belonging to a new genus.

The teuthofauna of the Antarctic re-
gion has been studied to a far lesser
extent than the ichtyofauna from this

same area. Therefore, it would be
quite premature at present to summarize
all data available, as might be appro-
priate for other groups of animals (Ek-
man, 1953; Andriyashev, 1964).

However poor the available data, it is
clear that the squid fauna of Antarctic
waters is quite characteristic. In fact,
out of 20 species of squids presently
known in Antarctic waters, 11 (or 55%
of the total) are endemic (Table 4). Six
genera (Psychroteuthis, Alluroteuthis,
Batoteuthis, Neoteuthis, Mesonychoteu-
this and the new genus Kondakovia) out
of 19 are undeniable Antarctic endemics
(Table 4). Considering that endemismis
rather odd for the Cephalopoda, particu-
larly for squids (Akimushkin, 1963),
these figures may be thought of as quite
significant.

It appears that the squid fauna of the
Antarctic regionis composed of 3 groups:
autochtones (not extending beyond the
Antarctic waters), squids spread to much
the same extent in Antarctic and notal-
ian waters and, finally those squids

404 J. A. FILIPPOVA

which are widespread (cosmopolitan).
Future investigations will, beyond doubt,
extend this list. It is now clear that
cephalopods, primarily squids, play an
important part in the food-chains of
antarctic vertebrates (Dell, 1959), and
this corroborates our suggestion that
the teuthofauna of this vast area is far
richer than is presently known.

ACKNOWLEDGEMENTS

The collection was obtained by the
following research workers of ВНИРО
V. N. Semenov, V. V. Shevtsov, R. R.
Makarov and Yu, E. Permitin. Ilustra-
tions for the article were executed by
V. M. Gudkov. In treating the data and
preparation of the manuscript I was
assisted by S. К. Klumov. To every per-
son mentioned above I am deeply in-
debted.

REFERENCES

ADAM, W., 1952, Résultats scientifiques
des expéditions océanographiques bel-
ges dans les eaux côtières africaines
de 1'Atlantique Sud (1948-49). Céph-
alopodes. Res. sci. Exped. ocean.
Belg. (1948-49), 3(3): 1-142.

AKIMUSHKIN, I. L, 1963, The Cephalo-
poda of the Seas of the USSR. [in
Russian]. 124. Acad. Nauk USSR. 1-
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ANDRIJASHEV, A. P., 1964, A review of
the fauna of the antarctic fishes. /ssl.
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BERRY, S.S., 1912, A review of the
cephalopods of western North Ameri-
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336.

CLARKE, M., 1965, “Growth rings” in
the beaks of the squid Moroteuthis
ingens (Oegopsida: Onychoteuthidae).
Malacologia, 3: 287-307.

CLARKE, M., 1966, A review of the
systematics and ecology of oceanic
squids. Advan. mar. Biol., 4: 91-300.

CLARKE, R., 1956, Sperm whales of
the Azores. “Discovery” Rep., 28:

237-298.

CHUN, C., 1910, Die Cephalopoden.
Wiss. Ergebn. dt. Tiefsee-Exped.“Val-
divia”, 18: 1-552.

DEGNER, E., 1925, Cephalopoda. Rep.
Dan. oceanogr. Exped. Mediterr., 2:
1-94,

DELL, R. K., 1959, Cephalopoda. Rep.
B.A.N.Z. antarct. Res. Exped., 8: 89-
106.

EKMAN, Sv., 1953, Zoogeography of the
Sea. Transl. from the Swedish, Lon-
don, Sidgwick & Jackson, 1-404.

HIKITA, T. & HIKITA, T., 1956, On the
rare striking squid Galiteuthis armata,
found in Hokkaido. Jap. zool. Mag.
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HOYLE, W. E., 1912, The Cephalopoda
of the Scottish National Antarctic Ex-
pedition. Rep. Sci. Res. “Scotia”, 48:
273-283,

IWAI, E., 1956, Notes on a rare Species
of cranchiid squid. Bull. Jap. Soc.
scient. Fish., 21(12): 1210-13.

KLUMOV, S. K., 1963, Feeding and hel-
minth fauna of whalebone whales (Mys-
tacocoti) in the main whaling grounds
of the World Ocean. Tr. Inst.Oceanol.,
71: 94-194,

KORABELNIKOV, L. V., 1959, The diet
of sperm whales in the Antarctic.
Privoda, 3: 103-104. [in Russian]

JOUBIN, L., 1898, Note sur une nou-
velle famille de céphalopodes. Ann.
Sci. nat., Ser. 8, Zool., 6: 279-292.

LONNBERG, E., 1898, On the cephalo-
pods collected by the Swedish Expe-
dition to Tierra del Fuego 1895-96,
Wiss. Erg. schwed. Exped. Magellans-
land, 2: 49-64,

MASSY, A. L., 1916, Mollusca. 2, Ce-
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Exped. 1910, Zoology, 2: 141-176.

ODHNER, N., 1923, Die Cephalopoden,
Swedish antarct. Exped., 1: 1-7.

PEARCY, W. G., 1965, Species compo-
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Oregon. Pacif. Sci., 19(2): 261-266.

PFEFFER, G., 1912, Die Cephalopoden
der Plankton-Expedition. Ergebnisse

SQUIDS FROM THE SCOTIA SEA 405

dev Plankton-Expedition der Hum-
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ROBSON, G. A., 1924, On the Cephalo-
poda obtained in South African waters
by Dr. J. D. Gilchrist in 1920-21.
Proc. zool. Soc. Lond. : 589-686.

ROBSON, G. A., 1925, On Mesonychoteu-
this, a new genus of Oegopsida, Ce-
phalopoda. Ann. Mag. nat. Hist., 16:
272-277.

ROPER, С. Е. E., € YOUNG, В. BY
1968, The Promachoteuthidae (Cepha-
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of Its Systematic Position Based on
New Material from the Antarctic and
Adjacent Waters. Antarct. Res. Ser.,
2: 203-214.

ROPER, Cay Ber Eo. YOUNG, «Rn; &
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to the Order Teuthoidea (Cephalopoda).
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SASAKI, M., 1929, A monograph of the
dibranchiate cephalopods of the Jap-

anese and adjacent waters. J. Fac.
Agri. Hokkaido Imp. Univ. 20, Suppl.
10: 1-357,

SMITH, E., 1881, Account of the Zoolo-
gical collections made during the sur-
vey of H.M.S. “Alert” in the Strait
of Magellan, and on the coast Patago-
nia. Mollusca, Proc. 2001. Soc. Lond.,
22-44,

THIELE, J., 1921, Die Cephalopoden
der Deutschen Sudpolar-Exped. 1901-
1903. Dtschl. Sudpol. Exped., 16 (Zoo-
logy Bd. 8): 433-465.

VOSS, G. L., 1960, Bermudan cephalo-
pods. Fieldiana, Zool., 39: 419-446,
VOSS, G. L., 1967, Systematics and dis-
tribution of Antarctic Cephalopods.

Antarct. J. U.S., Sept. Oct.

YOUNG, R. E., € ROPER, C.F.E., 1968,
The Batoteuthidae, a new Family of
Squid (Cephalopoda: Oegopsida) from
Antarctic Waters. Antarct. Res. Ser.,
2: 185-202.

ZUSAMMENFASSUNG

NEUE BEFUNDE VON DEN KOPFFUSSLERN (CEPHALOPODA: OEGOPSIDA)
AUS DEM SCOTIA-MEER (ANTARKTIS)

J. A. Filippova

Ein Posten Kopfftissler (Cephalopoda, Oegopsida) wird beschrieben, der von dem
Expeditionsschiff (R/V) “Akademiker Knipowitsch” während der Fahrten I und Ш im
Scotia-Meer aufgefischt worden ist. Das Material umfasst 33 Individuen von 5
Gattungen und 6 Arten, wobei 3 Arten und eine Gattung neubeschrieben sind: Moro-
teuthis knipovitchi n.sp., Galiteuthis aspera n.sp. und Kondakovia n.g. longimana n.sp.
- dieTypus-Arteines neuen Genus, das zu der Familie Onychoteuthidae gehört.

Unter den gefundenen Arten ist Psychroteuthis glacialis besonders wichtig, da
diese seltene antarktische Art, die früher nur in Bruchstücken aus den Mägen von
Robben und Pinguinen bekannt war, zum ersten Male seit 50 Jahren angetroffen wurde.
Die häufigste Art, die in dem Scotia-Meer gefunden wurde, war Brachioteuthis sp.

(aff. riisei?).
HZ

RESUME

NOUVELLES DONNEES SUR LES CALMARS (CEPHALOPODA: OEGOPSIDA)
DE LA MER SCOTIA (ANTARCTIQUE)

J. A. Filippova
L’auteur décrit une collection de calmars (Cephalopoda, Oegopsida), quia été

récoltée pendant les croisières I et III en Mer Scotia, par le navire de recherche
“Academicien Knipovitch”. La collection contient 33 exemplaires représentant 5

406

J. A. FILIPPOVA

genres et 6 espéces, parmi lesquels 3 especes et 1 genre sont nouveaux pour la
science: Moroteuthis knipovitchi, Galiteuthis aspera et Kondakovia longimana -
l’espéce type du nouveau genre appartenant a la famille des Onychoteuthidae. Parmi
les espèces trouvées, Psychroteuthis glacialis est d’un intérêt tout spécial, puisque
cette rare espèce antarctique n’était précédemment connue que d’après des fragments
trouvés dans les estomacs de Phoques et de Manchots et n’avait pas été rencontrée
depuis 50 ans. L’espèce la plus communément rencontrée dans la Mer Scotia a été
Brachioteuthis sp. (?riisei).
AVI

RESUMEN

NUEVOS DATOS SOBRE CALAMARES (CEPHALOPODA: OEGOPSIDA)
DEL MAR DE ESCOCIA (ANTARTICA)

J. A. Filippova

Se describe una colección de calamares, obtenida durante los cruceros I y II en el
Mar de Escocia, por el barco de investigación (R/V) “Acadamician Knipovitch”. La
colección contiene 33 ejemplares representando 5 géneros y 6 especies, de los cuales
3 especies y 1 género son nuevos para la ciencia: Moroteuthis knipovitchi, Galiteuthis
aspera y Kondakovia longimana - especie tipo de un nuevo género de la familia
Onychoteuthidae. Entre las especies encontradas, Psychroteuthis glacialises de es-
pecial interés, desde que esa rara especie antártica, previamente conocida sólo por
fragmentos extraídos de los estómagos de focas y pinguinos, es la primera vez que
se registra en 50 años. La especie más común en el Mar de Escocia es Brachio-
teuthis sp. (riisei?).

J. J. P.
ABCTPAKT
НОВЫЕ JAHHBE О КАЛЬМАРАХ (CEPHALOPODA:OEGOPSIDA)
ИЗ МОРЯ СКОТИЯ (АНТАРКТИКА)

Ю.А. ФИЛИППОВА

Описывается коллекция кальмаров (Cephalopoda, Oegopsida), полученная в 1 и
3 рейсах исследовательского судна "Академик Книпович". В коллекции
имеется 5 родов и 6 видов, из которых 3 вида и 1 род новые для науки:
Moroteuthis knipovitchi, Galiteuthis aspera и Kondakovia longimana - (типовой вид
нового рода из сем. Onychoteutidae). Среди найденных видов особый интерес
представляет Psychroteuthis glacialis, так как этот редкий антарктический вид,
прежде известный только по фрагментам, полученным из желулков тюленей и
пингвинов, был найден впервые за 50 лет. Наиболее обычным видом в море
Скотия был Brachioteuthis sp. (?riisei).

LRASES

MALACOLOGIA, 1972, 11(2): 407-413

FIRST REPORT OF HERCOGLOSSA ULRICHI (WHITE, 1882)
(CEPHALOPODA: NAUTILIDA) FROM THE CANNONBALL FORMATION
(PALEOCENE) OF NORTH DAKOTA, U. 5. A

Rodney M. Feldmann

Department of Geology
Kent State University
Kent, Ohio 44242, U.S.A.

ABSTRACT

A single specimen of Hercoglossa ulrichi (White), 1882, was collected from a
concretion derived from the Cannonball Formation (Paleocene) and preserved in
a Pleistocene gravel in central Morton County, North Dakota. This is the first
notice of this species in the upper midcontinent. Paleontologic evidence indi-
cates that physical connection between the marine Paleocene deposits in the
upper midcontinent and the Gulf Coast is extremely unlikely and, therefore, the
occurrence extends the range of the species through at least 30 degrees of lati-

tude.

INTRODUCTION

Ammonoid and nautiloid cephalopods
are extremely common fossils in Cre-
taceous rocks of the upper mid-North
American continent. First summarized
by Meek (1876), they have since been
studied by many other workers. No
Cenozoic cephalopods have been reported
from this same region; however, this is
perhaps not too unusual because Ceno-
zoic rocks in the upper midcontinent
are sparse. All of the post-Cretaceous
marine rocks in this region are found
in the Cannonball Formation which crops
out in several localities inCentral North
Dakota.

During the summer of 1970, Mr.
William Bauer collected the first cepha-
lopod known to the writer from the
Cannonball Formation. The single speci-
men collected was removed from a con-
cretion found in a gravel pit about 2.25
miles WNW of Fallon, southern Morton
County, North Dakota (Fig. 1). The
specimen was collected from material
interpreted (Feldman & Holland, 1971)

as a lag deposit of Pleistocene age,
The material in the lag consists of
cobble- to boulder-size material in a
matrix of coarse sand and pebbles. The
source of the coarse material is ap-
parently quite local in that most is from
the Cannonball Formation or its terres-
trial equivalent, the Tongue River For-
mation. The only other stratigraphic
unit that contains concretions similar
in form to that which enclosed the
nautiloid cephalopod is the Fox Hills
Formation, of Cretaceous age. Because
this crops out to the S and E of the
locality it could not have been a source
for this material, since the general
direction of glacial transport in this
area has been from the north.

A rich and varied fauna has been
collected and described from the Can-
nonball Formation including gastropods
and bivalves (Stanton, 1920; Cvancara,
1964; 1966; 1970), corals (Vaughan, 1920),
foraminiferans (Fox & Ross, 1942; Fox
& Olsson, 1969) and decapod crustaceans
(Holland & Cvancara, 1958; Feldmann
& Holland, 1971). Fox & Ross (1942)

1Contribution Number 65, Department of Geology, Kent State University

(407)

408

PRIMARY ROAD
— — SECONDARY ROAD

FIG. 1. Map of North Dakota showing the
location at which Hercoglossa ulrichi was
collected.

were the first to recognize the Paleocene
age of the Cannonball Formation and it
has subsequently been confirmed by the
writers indicated above. Although seve-
ral of the benthic invertebrates arecon-
generic with those of the Midway Group,
few are conspecific (Cvancara, 1966, p
281).

The unit has been correlated with the
Midway Group of the Gulf Coastal Plain,
but it is unlikely that any physical con-
nection existed between the 2areas. The
bivalves appear to have northern affi-

R. M. FELDMANN

nities (Cvancara, 1966, p 281) and, there-
fore, the Cannonball seaway probably
had its origins to the north and north-
east (Fig. 2). A similar conclusion
was drawn by Lemke (1960, p 31) based
on foraminiferal evidence developed by
Fox & Ross (1942). Although any litho-
logie evidence of a former connection
of the Cannonball seaway with the Arctic
Ocean or the North Atlantic Ocean has
been removed by erosion, the faunal
evidence strongly indicates that such a
connection must have existed during the
Paleocene. No evidence, lithologic or
paleontologic, indicates a physical con-
nection between the Cannonball seaway
and the Mississippi Embayment.

DESCRIPTION OF MATERIAL

Class Cephalopoda
Subclass Nautiloidea
Order Nautilida
Superfamily Nautilaceae
Family Hercoglossidae Spath, 1927
Genus Hercoglossa Conrad, 1886
Hercoglossa ulrichi (White), 1882

Nautilus texanus White [not Shumard], 1882,
Proc. U.S. natn. Mus., 4: 137.

Enclimatoceras ulrichi, Hyatt, 1883, Proc.
Boston Soc. natur. Hist., 22: 270. Harris,
1896, Bull. Amer. Paleont., 1: 127, 131,
139-143, 146, 236-239; pl. 13, figs. 1-3;
pl. 14, fig. 1; pl. 15, fig. 1. Deussen, 1914,
U.S. Geol. Surv. Water Supply Paper 335:
pl. 3, figs. 1-1b. Deussen, 1924, Prof.
Paps., U.S. Geol. Surv., 126: 41?; pl. 14,
figs. 1-1b. Gardner, 1926, Amer. J. Sci.,
5th Ser. , 12: 453-454. Douvillé, 1929, С.
7. somm. Séance. Soc. Géol. Fr., 12: 167
Semmes, 1929, Ala. Geol. Surv. Spec.
Rept. 15: 232-233.

Enclimatoceras (Nautilus) ulrichi, White,
1884, Bull., U.S. Geol. Surv., 4: 16-17;
pl. 7;figs. 128; pl..8, fig up cd

FIG. 2.

Map of North America showing the approximate location of exposures of marine Paleo-

cene rocks as wellas localities from which Hercoglossa ulrichi has been collected. Boundaries
of the northern seaway are strongly suggested by paleontologic data but are not documented by

a rock record in Canada.

Fossil localities in the southern United States are from Miller (1947).

HERCOGLOSSA FROM CANNONBALL FORMATION

409

LEGEND

mm PALEOCENE EXPOSURES
HYPOTHETICAL BOUNDARY OF
— — NORTHERN SEAWAY IN THE
PALEOCENE
+ LOCATIONS AT WHICH A. ulrichi
HAS BEEN COLLECTED

SCALE

200 400 600 800 1000 MILES
rt rt ta i)

т т т т т 7
200 400 600 800 1000 1200 1400 KILOMETERS

LAMBERT AZIMUTHAL EQUAL-AREA PROJECTION

410 R. M. FELDMANN

FIG. 3. Right lateral view of Hercoglossa ulrichi from the Cannonball Formation, x 1. Kent

State University paleontology collection, #1825.

Harris, 1894, Ark. Geol. Surv., Ann. Rept.
for 1892, 2: 36-39; pl. 2, figs. 1-3.

(?) Enclimatoceras hyatti?, Aldrich, 1886,
Bull. , Ala. Geol. Surv., 1: 60.

Hercoglossa ulrichi, Foord & Crick, 1890,
Ann. Mag. natur. Hist., 6th Ser., 5: 392.
Gardner, 1933, Texas Univ. Bull. 3301:
320-322. Miller € Thompson, 1933, Jd.
Paleont., 7: 308-309, 319-322. Pijpers,
1933, [part], Geog. geol. Meded., Physiog.
-geol. Reeks 8: 30, 80. Stenzel, 1940,
Texas Univ. Pub, 3945: 744-749. Stenzel,
1942, [illustrated card catalogue of North
American early Tertiary fossils of Atlantic
-Gulf Coastal Plain], Cephalopoda, cards
16a, 16b. Shimer & Shrock, 1944, Index
fossils of North America: 549; pl. 225, figs.
5-7. Miller, 1947, Mem., geol. Soc.
Amer., 23: 60-62, pl. 43, fig. 1; pl. 44,
figs. 1-4; pl. 45, figs. 1-2.

Hercoglossa (Enclimatoceras) ulrichi, Grabau
& Shimer, 1910, North American index fos-
sils, invertebrates, 2: 111-112; fig. 1343.

Hercoglossa danica, Scott, 1926, [part],

Amer. J. Sci., bth ser. 12: 157, 159,161:
Scott, 1926 [part], Univ. Grenoble, These:
115, 116 113,189:

Description

The shell is medium sized for the
genus, involute; maximum height is 102
mm; height of outer whorl is 69 mm;
width of the outer whorl is about 65 mm.
The venter is smoothly rounded, the
lateral margins are only slightly rounded
and converge on the venter at an angle
of 42° (Fig. 4). The umbilicus is nar-
row, about lcm, and rather deeply
impressed.

The suture pattern of the terminal
whorl is very similar to that described
by Stenzel (1940, p 746). The ventral
saddle is broad and gently arched (Fig.
4). The lateral lobe is broad and gently
curved with the axis just ventrad from
the midline of the lateral surface, The

HERCOGLOSSA FROM CANNONBALL FORMATION 411

FIG. 4. Line drawings of the outline of Her-
coglossa ulrichi (a) constructed in the posi-
tion of the terminal septum, and (b) of the
suture pattern of the terminal septum, x 1/2.

lateral saddle is narrow and more angu-
lar than the lateral lobe. A shallow
lobe is developed from the umbilical
shoulder to the umbilicus, The internal
suture and the siphuncle are unknown,

Although the surface of the shell is
poorly preserved, it appears to be very
smooth with finely inscribed growth
lines. No other ornamentation was ob-
served.

Discussion

The single specimen from the Can-
nonball Formation shows a portion of
the living chamber as well as all 12
camerae of the outer whorl. This
Specimen matches, in every detail, the
discussions and illustrations of this
species given by Stenzel (1940, p 478)
and Miller (1947, p 60). Both authors
give elaborate descriptions of the species
in this genus that have been described
from North America and they will not,
therfore, be summarized herein, It is
sufficient to note that the most closely
related Species appears to be Herco-
glossa gardnerae (Stenzel, 1940) which
has a much narrower lateral lobe than

that on H. ulrichi and a more rounded
outline. H. orbiculata (Toumey, 1886)
the type species of the genus, has a
suture pattern very similar to that of
H. ulrichi but has a much broader, more
rounded outline.

Herocoglossa ulrichi is one of the
most common nautiloids fromthe Paleo-
cene Midway Group in the Southern
United States, but apparently this is the
first report of its occurrence elsewhere,

Locality and stratigraphic position

The single specimen of Hercoglossa
ulrichi was collected from a concretion
in a Pleistocene lag deposit containing
concretions derived from near the mid-
dle of the Cannonball Formation of
Paleocene age in a gravel pit, NE '/4,
NE 7%, Sec: 8, № 135 Ney Re 83 Wo,
about 2.25 miles WNW of Fallon, Morton
County, North Dakota. The specimen,
KSU number 1825, is deposited in the
paleontology collection at Kent State
University, Kent, Ohio.

PALEOECOLOGY

The paleoecological setting of the
middle of the Cannonball Formation has
been described by Holland & Cvancara
(1958, p 490) and by Feldmann & Holland
(1971). Although the fauna collected
from this particular locality does not
contain a large number of species,
it does contain a relatively unusual
assemblage of animals, all of which are
normal marine organisms. They include
the lobster Nephrops buntingi Feldmann
& Holland, 1971, and a snail, ?Drepano-
chilus sp. which is considered marine
through its association with other clearly
marine organisms. In association with
these organisms are concretions formed
around large pieces of deciduous wood
which attain a diameter of about 30 cm
and a length of 50-75 cm. The wood
contains numerous borings of the ship-
worm, Nototeredo globosa (Meek & Hay-
den). These wood-bearing concretions
are similar in composition to those
containing the lobsters and Hercoglossa

412

ulrichi which would support the sup-
position that the organisms were pre-
served in a single stratigraphic horizon.

This association of marine organisms
along with large deciduous wood frag-
ments would seem to indicate that these
specimens were preserved ш a rela-
tively shallow marine environment. None
of the above-mentioned fossils were
found in outcrops of the Cannonball
Formation in the near vicinity. The
medium grain, crossbedded sandstone
that is exposed in these outcrops does,
however, contain similar, but unfossil-
iferous, concretions. Itis very probable,
therefore, that the fossiliferous concre-
tions were derived from this horizon
which would tend to confirm the environ-
mental interpretation.

LITERATURE CITED

CVANCARA, A. M., 1964, Shipworm pal-
lets from the Paleocene (Cannonball
Formation) of North Dakota. (Abst.)
Geol. Soc. America, 1964 Annual
Meeting, Program: 38-39.

CVANCARA, A. M., 1966, Revision of
the fauna of the Cannonball Formation
(Paleocene) of North and South Dakota.
Contr. Mus. Paleont. Univ. Mich., 20
(10): 277-375; Pls. 1-9.

CVANCARA, A. M., 1970, Terinid (Bi-
valvia) pallets from the Paleocene of
North America, Paleontology, 13:
619-622.

FELDMANN, R. M. € HOLLAND, F. D.,
Jr., 1971, A new species of lobster
from the Cannonball Formation (Pale-
ocene) of North Dakota. J. Paleont.,

R. M. FELDMANN

45(5): 838-843; Pls. 95-96.

FOX, S. K. € ROSS;-R. J., тт. 1942
Foraminiferal evidence for the Midway
(Paleocene) age of the Cannonball
Formation in North Dakota. J. Paleont.
16: 660-673.

FOX, S. K. & OLSSON, R. K., 1969, Da-
nian planktonic Foraminifera from
the Cannonball Formation in North
Dakota. J.Paleont., 43: 1397-1404;
Pls. 168-169,

HOLLAND, F. D., Jr. & CVANCARA, A.
M., 1958, Crabs from the Cannonball
Formation (Paleocene) of North Da-
kota. J. Paleont., 32(3): 495-505; Pl.
74,

LEMKE, R. W., 1960, Geology of the
Souris River area, North Dakota. U.
S. Geol. Survey Prof. Paper 325: 1-
138.

MEEK, F. B., 1876, Invertebrate Cre-
taceous and Tertiary fossils of the
upper Missouri country. U.S. Geol.
Survey Terr., 9: 1-629; Pls. 1-45.

MILLER, A. K., 1947, Tertiary nauti-
loids of the Americas. Mem., geol.
Soc. Amer., 23: 1-234; Pls. 1-100.

STANTON, T. W., 1920, The fauna ofthe
Cannonball Marine Member of the
Lance Formation. Prof. Paps., U.S.
Geol. Surv., 128(A): 1-60; Pls. 1-9.

STENZEL, H. B., 1940, Tertiary nauti-
loids from the Gulf Coastal Plain.
Univ. Texas Cont. Geol., 3945: 731-
795; Pls. 35-42,

VAUGHAN, T. W., 1920, Corals from the
Cannonball Marine Member of the
Lance Formation. Prof. Paps., U.S.
Geol. Surv., 128(A): 61-66; Pl. 10.

ZUSAMMENFASSUNG

ERSTER NACHWEIS VON HERCOGLOSSA ULRICHI (WHITE 1882),
(CEPHALOPODA NAUTILIDA) AUS DER “CANNONBALL”-FORMATION
(PALAOZAN) VON NORD-DAKOTA, U.S. A.

R. M. Feldmann

Ein einziges Exemplar von Hercoglossa ulrichi (White, 1882) wurde in einer
Konkretion der “Cannonball”-Formation des Paläozän gefunden, diesichin sekundärer
Lage in einen pleistozänen Kies im mittleren Morton County in Nord-Dakota befand.

HERCOGLOSSA FROM CANNONBALL FORMATION

Dies ist der Erstnachweis dieser Art in der oberen Mitte der Kontinents. Paläonto-
logische Fakten berechtigen zu der Annahme, dass eine räumliche Verbindung
zwischen den dortigen Paläozän-Ablagerungen und der Golfküste ganz unwahrschein-
lich ist und darum das Vorkommen die Verbreitung der Art um wenigstens 30

Breitengrade vergrössert,
He Ze

RESUME

PREMIERE DONNEE SUR HERCOGLOSSA ULRICHI (WHITE, 1882)
(CEPHALOPODA: NAUTILIDA) DANS LA FORMATION CANNONBALL
(PALEOCENE) DU DAKOTA NORD, U. S. A.

R. M. Feldmann

Un seul spécimen de Hercoglossa ulrichi (White, 1882) a été récolté dans une con-
crétion dérivée de la formation Cannonball et conservé dans des graviers, dans le
centre du comté de Morton, Dakota Nord. Il s’agit du premier signalement de cette
espéce dans la partie supérieure du continent moyen. Des preuves paléontologiques
indiquent qu’il est très improbable qu’une relation physique existe entre les dépôts
marins paléocénes dans la partie supérieure du continent moyen d’une part et de la
cöte du Golfe d’autre part. Par conséquent, la trouvaille étend la zone de répartition
de l’espéce a travers au moins 30° de latitude.

A. L.

RESUMEN

PRIMER HALLAZGO DE HERCOGLOSSA ULRICHI (WHITE, 1822)
(CEPHALOPODA: NAUTILOIDEA) EN LA FORMACION CANNONBALL
(PALEOCENO) DE NORTH DAKOTA, U.S. A.

R. M. Feldmann

De una concreciön de la formaciön Cannonball (Paleoceno) derivada de escombros
pleistocénicos del centro del Condado de Morton, en North Dakota, se extrajo un
ejemplar tnico de Hercoglossa ulrichi (White); esta es la primera noticia de la es-
pecie en tal zona mediocontinental. Evidencia paleontolögica indica la improbabilidad
de contactos fisicos entre los depösitos marinos paleocenos en elinterior del conti-
nente y la costa del Golfo; por consiguiente la apariciön extiende los limites de la
especie sobre los 30° de latitud.

dia de 1

ABCTPAKT

ПЕРВОЕ СООБЩЕНИЕ O HERCOGLOSSA ULRICHI (WHITE, 1882)
(CEPHALOPODA: NAUTILIDA) ИЗ ФОРМАЦИЙ КАННОНБОЛЛ (ПАЛЕОЦЕН)
СЕВЕРНОЙ ДАКОТЫ, США

Р. ФЕЛЬШМАН

Единственный экземпляр Hercoglossa ulrichi (White, 1882) сохранившийся в
плейстоценовых гравийеых отложениях центральной Мортон Каунти, Северная
Дакота, был найден среди конкреций в отложениях Канноболл (Палеоцен).
Это - первое указание о находке этого вида в верхних слоях в середине
континента. Палеонтологические данные указывают на то, что, хотя
физические связи между морскими палеоценовыми отложениями этого района и
побережьем залива крайне незначительны, общее распространение вида
охватывает по крайней мере 30 градусов по широте.

Z. А.Е.

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MALACOLOGIA, 1972, 11(2): 415-426

ABBREVIATED TITLES OF SCIENTIFIC PUBLICATIONS AND PLACE NAMES
TO BE USED IN LITERATURE CITATIONS IN MALACOLOGIA

The journals, other publications and place names listed here are many of those
cited by authors in previous issues of MALACOLOGIA, as well as those cited in our
affiliated journal, Malacological Review. These lists are by no means complete, but
they do include most of those publications and place names likely to be cited repeatedly
by our contributors, as well as some rarer ones, Authors preparing manuscripts
are requested to refer to these lists when preparing their bibliographies for MALA-
COLOGIA.

Journal Abbreviations

Abhandlungen der Deutschen Akademie der Abh.dtsch. Akad. Wiss. Berlin
Wissenschaften zu Berlin

Abhandlungen hrsg. von der Senckenbergischen Abh. Senckenberg.naturforsch. Ges.
naturforschenden Gesellschaft

Acta biologica Academiae scientiarum hungaricae Acta biol. Acad, Sci. hung.

Acta cytologica Acta cytol,

Acta geologica hispanica Acta geol. hispanica

Acta physiologica et pharmacologica néerlandica Acta physiol. pharmacol. néerl.

Acta zoologica Acta zool.

Acta zoologica fennica Acta zool. fenn.

Advance Abstracts of Contributions on Fisheries Adv. Abstr. Contr. Fish. aquat. Sci.
and aquatic Sciences in India India

Advances in Protein Chemistry Advanc. Protein Chem.

Allgemeine Forstzeitschrift Allg. Forstz.

Ameghiniana Ameghiniana

American Geologist Amer. Geol.

American Journal of Conchology Amer. J. Conchol.

American Journal of Hygiene Amer. J. Hyg.

American Journal of Science Amer. J. Sci.

American Journal of Tropical Medicine and Amer. J. trop. Med. Hyg.
Hygiene

American Malacological Union, Inc. , Annual Amer. malacol. Union, ann. Reps.
Reports

American Midland Naturalist Amer. Midl. Natur.

American Museum Novitates Amer, Mus. Novit.

American Naturalist Amer. Natur.

American Scientist Amer. Sci.

American Zoologist Amer. Zool,

Anatomical Record Anat. Rec.

Annales d’endocrinologie Ann. Endocrinol,

Annales de la Faculté des sciences de Marseille Ann. Fac. Sci. Marseille

Annales du Musée d’histoire naturelle de Marseille Ann. Mus. Hist. natur. Marseille

Annales, Musée royal de l’Afrique centrale Ann. Mus. roy. Afr. centr.

Annales du Musée royal du Congo belge Ann. Mus. voy. Congo belge

Annales de parasitologie humaine et comparée Ann. Parasitol. hum. comp.

Annales des sciences naturelles (Zoologie) Ann. Sci. natur. (Zool.)

Annales de la Société royale zoologique de Ann. Soc. roy. Zool. Belg.
Belgique

Annales zoologici Ann. Zool, `

Annals and Magazine of Natural History Ann. Mag. natur. Hist.

(415)

416 MALACOLOGIA

Annals of the Natal Museum

Annals of the New York Academy of Sciences

Annals of Scottish Natural History

Annals of the South African Museum

Annals of Tropical Medicine and Parasitology

Annotationes zoologicae japonenses

Arbeiten aus den Zoologischen Instituten der
Universitat Wien u. der Zoologischen Station
in Triest

Archiv fiir Anatomie und Physiologie

Archiv für experimentelle Zellforschung

Archiv für Hydrobiologie

Archiv für mikroskopische Anatomie und
Entwicklungsmechanik

Archiv für Molluskenkunde

Archiv für Naturgeschichte

Archives d’anatomie, d’histologie et
d’embryologie

Archives d’anatomie microscopique et de
morphologie expérimentale

Archives de biologie

Archives italiennes de biologie

Archives néerlandaises de physiologie de l’homme
et des animaux

Archives néerlandaises de zoologie

Archives de zoologie expérimentale et générale

Archivio zoologico italiano

Archivos de zoologia do Estado de Säo Paulo

Argamon

Arkiv för zoologi

Atti dell’Accademia nazionale dei Lincei.
Rendiconti

Atti della Societa toscana di scienze naturali
residente in Pisa

Auk

Australian Journal of Experimental Biology and
Medical Science

Australian Journal of Marine and Freshwater
Research

Australian Journal of Zoology

Basteria

Beaufortia

Bergens museums ärbog

Biochimica et biophysica acta

Biological Bulletin

Biological Journal of the Linnean Society of
London

Biological Journal of Okayama University

Biological Reviews

Biologische Untersuchungen

Biologisches Zentralblatt

Boletim do Instituto oceanogräfico

Boletín de la Asociación médica de Puerto Rico

Ann. Natal Mus.

Ann. N.Y. Acad. Sci.

Ann. Scot. natur. Hist.
Ann. S. Afr. Mus.

Ann. trop. Med. Parasitol.
Annot. zool. jap.

Arb, zool. Inst. Univ. Wien

Arch, Anat. Physiol.

Arch. exp. Zellforsch.

Arch. Hydrobiol.

Arch. mikrosk, Anat. Entwickl.-Mech.

Arch. Molluskenk.
Arch, Naturgesch.
Arch, Anat. Histol. Embryol.

Arch, Anat. microsc. Morphol. exp.

Arch. Biol,
Arch, ital. Biol,
Arch, néerl. Physiol,

Arch, neerl. Zool.

Arch. Zool, exp. gen.
Arch, Zool, ital.

Arch, 2001. Est. Sao Paulo
Argamon

Ark, Zool.

Atti Accad, naz, Lincei, Вс.

Atti Soc. tosc. Sci. natur. Pisa

Auk
Austr. J. exp. Biol. med. Sci.

Austr. J. mar. freshw. Res.
Austr. J. 2001.

Basteria

Beaufortia

Bergens Mus. Arb.
Biochim, biophys. Acta
Biol. Bull.

Biol, J. Linn. Soc. Lond.

Biol. J. Okayama Univ,
Biol. Rev.

Biol, Unters.

Biol. Zentralbl.

Bol, Inst. oceanogr.
Bol. Asoc. méd. P. Rico

ABBREVIATIONS

Bollettino di pesca, piscicoltura e idrobiologia

Bollettino della Societa malacologica italiana

Bollettino di zoologia, pubblicato dall’Unione
zoologica italiana

Breviora

British Birds

British Medical Bulletin

Bulletin de l’Académie polonaise des sciences

Bulletin of the American Museum of Natural
History

Bulletins of American Paleontology

Bulletin of the Azabu Veterinary College

Bulletin biologique de la France et de la Belgique

Bulletin of the British Museum (Natural History)

Bulletin of California State Mining Bureau

Bulletin of the Florida State Museum. Biological
Sciences

Bulletin of the Geological Society of America

Bulletin de l’Institut océanographique

Bulletin de l’Institut royal des sciences naturelles
de Belgique

Bulletin of the Japanese Society of Scientific
Fisheries

Bulletin of the Los Angeles County Museum of

Natural History

Bulletin of Marine Science of the Gulf and
Caribbean

Bulletin mensuel de la Société linnéenne de Lyon

Bulletin du Musée royal d’histoire naturelle de
Belgique

Bulletin of the Museum of Comparative Zoology at
Harvard College

Bulletin du Museum d’histoire naturelle

Bulletin. National Museum of Canada

Bulletin of the National Science Museum

Bulletin of the New York Academy of Medicine

Bulletin de la Société géologique de France

Bulletin de la Société d’histoire naturelle de
Toulouse

Bulletin de la Société linnéenne de Normandie

Bulletin de la Société de pathologie exotique

Bulletin de la Société zoologique de France

Bulletin of the Torrey Botanical Club

Bulletin. United States Geological Survey

Bulletin. United States National Museum

Bulletin of the World Health Organization

Bulletin of Zoological Nomenclature

Cahiers de biologie marine

Cahiers du Pacifique

California Journal of Mines and Geology
Canadian Journal of Microbiology
Canadian Journal of Zoology

Caribbean Journal of Science
Chesapeake Science

Boll. Pesca Piscic. Idrobiol.
Boll. Soc. malacol. ital.
Boll. Zool.

Breviora

Brit. Birds

Brit. med, Bull.

Bull. Acad, pol. Sci.

Bull. Amer. Mus. natur. Hist.

Bull. Amer, Paleont.

Bull. Azabu vet, Coll.

Bull. biol. Fr. Belg.

Bull. Brit. Mus. (natur. Hist.)
Bull. Calif. St. mining Bur.
Bull. Fla. St. Mus., biol. Sci.

Bull. geol. Soc. Amer.

Bull. Inst. oc&onogr.

Bull. Inst. voy. Sci. natur. Belg.
Bull. Jap. Soc. sci. Fish.

Bull. Los Angeles Co. Mus. natur.

Bull, mar. Sci. Gulf Caribb.

Bull. mens. Soc. linn. Lyon
Bull. Mus. voy. Hist. natur. Belg.

417

Hist.

Bull. Mus. comp. Zool. Harvard Coll.

Bull. Mus. Hist. natur.

Bull., natn. Mus. Can.

Bull. natn. Sci. Mus.

Bull. N.Y. Acad, Med,

Bull. Soc. géol. Fr.

Bull, Soc. Hist. natur. Toulouse

Bull. Soc. linn. Normandie
Bull. Soc. Pathol. exot.
Bull. Soc. 2001. Fr.

Bull. Torrey bot. Club
Bull., U.S. Geol. Surv.
Bull., U.S. natn. Mus.
Bull, "а. Hlth. Org.
Bull, zool. Nomencl.

Cah. Biol, mar,
Сай. Pacif.

Calif. J. Mines Geol,
Can. J. Microbiol.
Can. J. Zool.
Caribb. J. Sci.
Chesapeake Sci.

418 MALACOLOGIA

Chromosoma

Collecting and Breeding

Comparative Biochemistry and Physiology

Compte rendu sommaire des séances de la
Société géologique de France

Comptes rendus hebdomadaire des séances de
l’Académie des sciences

Comptes rendus des séances de la Société de
biologie

Comunicaciones de la Sociedad malacolögica del
Uruguay

Conchiglie

Condor

Contributions from the Laboratory of Vertebrate
Biology of the University of Michigan

Contributions from the Museum of Paleontology,
The University of Michigan

Contributions in Science

Copeia

Current Science

Cytologia

Dissertation Abstracts
Doklady Akademii nauk SSSR

Echo

Ecological Monographs
Ecology

Endeavour

Ethiopian Medical Journal
Evolution

Experientia

Experimental Parasitology

Federation Proceedings. Federation of American
Societies for Experimental Biology

Fieldiana: Zoology

Fishery Investigations. Ministry of Agriculture,
Food and Fisheries

Forma et Functio

Fossils

Fragmenta faunistica

General and Comparative Endocrinology
Genetics

Géobios

Geologie

Ghana Medical Journal

Growth

Hallesches Jahrbuch fiir mitteldeutsche
Erdgeschichte
Handbuch der Zoologie

Chromosoma

Collecting & Breed.

Comp. Biochem. Physiol.

C.r. somm. Séanc. Soc. géol. Fr.

C.r. hebd. Seanc. Acad. Sci.
C.r. Seanc. Soc. Biol.
Comun. Soc. malacol. Urug.

Conchiglie
Condor
Contr. Lab. vertebr. Biol. Univ, Mich.

Contr. Mus. Paleont. Univ, Mich,

Contr. Sci.
Copeia
CUFT. SCL.
Cytologia

Diss. Abstr.
Dokl, Akad. Nauk SSSR

Echo

Ecol. Monogr.
Ecology
Endeavour
Eth. med. J.
Evolution
Experientia
Exp. Parasitol.

Fed. Proc., Fed. Amer. Socs. exp. Biol.

Fieldiana, Zool.
Fish. Invest., Min. Agr. Food, Fish.

Forma et Functio
Fossils
Fragm. faun.

Gen. compar. Endocrinol.
Genetics

Géobios

Geologie

Ghana med, J.

Growth

Hallesches Jahrb. mitteldtsch. Erdgesch.

Handb. Zool,

ABBREVIATIONS 419

Helgoländer wissenschaftliche Meeresuntersuchungen

Heredity
Herpetologica
Hyacinth Control Journal

Illinois Biological Monographs
Image

Immunology

In vitro

Indian Journal of Medical Research
Indo-Pacific Mollusca

Ingenieur in Nederlandsch-Indié
Israel Journal of Zoology

Japanese Journal of Genetics

Japanese Journal of Parasitology

Japanese Journal of Zoology

Jenaische Zeitschrift für Naturwissenschaft

Johnsonia

Journal of the Academy of Natural Sciences of
Philadelphia

Journal of Anatomy

Journal of Animal Ecology

Journal of Bacteriology

Journal of Biophysical and Biochemical Cytology

Journal of the Bombay Natural History Society

Journal of Cellular and Comparative Physiology

Journal de conchyliologie

Journal of Conchology

Journal of the Egyptian Medical Association

Journal of Elisha Mitchell Scientific Society

Journal of Experimental Biology

Journal of Experimental Marine Biology and
Ecology

Journal of the Fisheries Research Board of
Canada

Journal of the Florida Academy of Science

Journal of Geology

Journal of Immunology

Journal of Invertebrate Pathology

Journal of the Linnean Society

Journal of the Malacological Society of Australia

Journal of Mammalogy

Journal of the Marine Biological Association of
the United Kingdom

Journal of Marine Research

Journal of Morphology

Journal of Natural History

Journal of Paleontology

Journal of Parasitology

Journal and Proceedings of the Asiatic Society
of Bengal

Journal of the Royal Microscopical Society

‘Journal of Science of the Hiroshima University,
Series B

Helgoländer wiss. Meeresunters.
Heredity

Herpetologica

Hyacinth Control J.

Illinois biol. Monogr.
Image

Immunology

In vitro

Indian J. med. Res.
Indo-Pac. Moll.

Ing. Ned. -Indié

Ist. J. Zool.

Jap. J. Genet.

Jap. J. Parasitol.

Jap. J. Zool,

Jena. Z. Naturwiss.
Johnsonia

J. Acad. natur. Sci. Philad.

. Anat.
anim. Ecol.

. Bacteriol,

biophys. biochem. Cytol.
Bomb, natur. Hist. Soc.
cell. comp. Physiol,
Conchyliol,

Conchol,

Egypt. med. Assoc.
Elisha Mitchell sci. Soc.
exp. Biol,

exp. mar. Biol, Ecol.

us

SS US

5

Fish. Res. Bd. Can.

Fla. Acad. Sci.

Geol,

Immunol,

invert. Pathol.

Linn. Soc.

malacol. Soc. Austr.
Mammal,

may. biol. Assoc. U.K.

SS SS

may. Res,

Morphol,

natuv. Hist.

Paleont.

Payasitol.

Proc. Asiatic Soc. Beng.

LESS Sessa

J. Roy. пистозс. Soc.
J. Sci. Hirosh. Univ., Ser. B.

420 MALACOLOGIA

Journal of the Shimonoseki College of Fisheries
Journal of Tropical Medicine and Hygiene
Journal of the Washington Academy of Science
Journal of the Zoological Society of India

Kansas University Science Bulletin

Kieler Meeresforschungen

Kongelige Danske videnskabernes selskabs
Skrifter

Konelige Norske videnskabernes selskabs
forhandlinger

Kromosomo

Kungliga Svenska vetenskapsakademiens
handlingar

Lavori della Societa malacologica Italiana

Leaflets in Malacology

Leidsche geologische mededelingen

Lethaia

Limnologica

Los Angeles County Museum of Natural History
Contributions in Science

Malacologia

Malacological Review

Malakologische Abhandlungen, Staatliches Museum
für Tierkunde in Dresden

Malakozoologische Blatter

Meddelelser om Grgnland

Meddelelser fra Kommissionen for
Havundersggelser

Mémoires de l’Institut royal des sciences
naturelles de Belgique

Mémoires du Musée royal d’histoire naturelle
de Belgique

Mémoires du Muséum national d’histoire
naturelle

Mémoires de la Société géologique et
minéralogique de Bretagne

Mémoires de la Société zoologique de France

Memoirs of the Carnegie Museum

Memoirs. Cornell University Agricultural
Experiment Station

Memoirs. Geological Society of America

Memoirs of the Geological Survey Branch,
Department of Mines, Canada

Memoirs of the Indian Museum

Minutes of the Conchological Club of
Southern California

Miscellaneous Publications of the Museum of
Zoology, University of Michigan

Mitteilungen des Badischen Landesvereins
fiir Naturkunde.

Monitore zoologico italiano

Museum of Zoology, University of Michigan,
Circular

J. Shimonoseki Coll. Fish.

J. trop. Med. Hyg.

J. Wash, Acad, Sci.

J. zool. Soc. India

Kans. Univ, Sci. Bull,

Kieler Meeresforsch.

К. danske Vidensk. Selsk. Skr.

К. norske Vidensk. Selsk. Forh.

Kromosomo
К. svenska Vetenskapsakad. Handl.

Lav. Soc. malacol, ital.

Leafl. Malacol.

Leid, geol. Meded.

Lethaia

Limnologica

L.A. Co. Mus. natur. Hist. Contr.
Sci.

Malacologia

Malacol. Rev.

Malakol.Abh., staatl. Mus, Tierk. Dresden
Malakozool. Blatt.

Medd. Grant.

Medd. Komm, Havunders.

Mém. Inst. roy. Sci. natur. Belg.
Mem. Mus. roy. Hist. natur. Belg.
Mem. Mus. natn. Hist. natur.
Mem. Soc. géol. minér. Bretagne
Mem. Soc. zool. Fr.

Mem. Carnegie Mus.

Mem., Cornell Univ. agr. Exp. Sta.

Mem., geol. Soc. Amer,
Mem. geol. Surv. Branch, Can.

Мет. Indian Mus.
Minut. conchol, Club $. Calif.

Misc. Publs. Mus. Zool., Univ. Mich.
Mitt, bad. Landesver. Naturk.

Monitore zool. ital.
Mus. Zool., Univ. Mich., Cire.

ABBREVIATIONS

Natural Science and Museums

Nature

Naturwissenschaften

Nautilus

Netherlands Journal of Zoology

New Harmony Disseminator of Useful Knowledge

New Zealand Journal of Marine and Freshwater
Research

Northwest Science

Notulae Naturae

Nucleus

Nyt magazin for naturvidenskaberne

Occasional Papers of the Bernice P. Bishop
Museum

Occasional Papers on Mollusks

Occasional Papers of the Museum of Zoology,
University of Michigan

Oceanography and Marine Biology

Oecologia

Ohio Journal of Science

Oikos

Pacific Science

Palaeontology

Papers of the Michigan Academy of Science,
Arts, and Letters

Papua and New Guinea Scientific Society Annual
Report and Proceedings

Parasitology

Pfliigers Archiv fiir die gesamte Physiologie des
Menschen und der Tiere

Philosophical Transactions of the Royal Society

Proceedings of the Academy of Natural Sciences
of Philadelphia

Proceedings of the American Philosophical Society

Proceedings of the Biological Society of
Washington

Proceedings of the Boston Society for Natural
History

Proceedings of the California Academy of Sciences

Proceedings of the Egyptian Academy of Sciences

Proceedings of the Helminthological Society of
Washington

Proceedings of the Indiana Academy of Science

Proceedings of the Iowa Academy of Science

Proceedings. Koniklijke Nederlandse Akademie
van Wetenschappen

Proceedings of the Linnean Society of New
South Wales

Proceedings of the Malacological Society of
London

Proceedings of the National Shellfisheries
Association

Natur. Sci. & Mus.

Nature

Naturwissenschaften

Nautilus

Neth. J. Zool,

N. Harmony Dissem. useful Knowl.

N.Z. J. mar. freshw. Res.

N.W. Sci.

Notulae Natur.

Nucleus

Nyt Mag. Naturvidensk,

Occ. Paps. Bernice P. Bishop Mus.

Occ. Paps. Molls.
Occ. Paps. Mus. Zool., Univ. Mich.

Oceanogr. mar, Biol.
Oecologia

Ohio J. Sci.

Oikos

Рас. Sci.
Palaeontology
Pap. Mich, Acad. Sci., Arts & Lett.

Papua N. Guin. sci. Soc. ann. Rep.
Proc.

Pavasitology

Pflugers Arch. ges. Physiol.

Phil. Trans. Roy. Soc.
Proc. Acad, natur, Sci. Philad.

Proc.
Proc,

Amer, phil. Soc.
biol. Soc. Wash.

Proc. Bost. Soc. natur. Hist.

Proc,
Proc,
Proc.

Calif. Acad. Sci.
Egypt. Acad. Sci.
helminthol. Soc. Wash.

Proc. Ind. Acad. Sci.
Proc. Iowa Acad. Sci.
Proc. K. ned. Akad. Wetensch.

Proc. Linn. Soc. N.S.W.

Proc. malacol. Soc. Lond.

Proc. natn. Shellfish. Assoc.

421

422

Proceedings of the Oklahoma Academy of Science

Proceedings of the Pennsylvania Academy of Science

Proceedings of the Royal Irish Academy

Proceedings of the Royal Society

Proceedings of the Royal Society of Edinburgh

Proceedings of the Society for Experimental
Biology and Medicine

Proceedings of the United States National Museum

Proceedings of the Utah Academy of Sciences

Proceedings of the Washington Academy of
Sciences

Proceedings of the Zoological Society of London

Professional Papers. United States Geological
Survey

Public Health Reports

Publications. Carnegie Institution of Washington

Publications of the Seto Marine Biological
Laboratory

Quarterly Journal of Microscopical Science

Record of the Auckland Institute and Museum

Record of the Australian Museum

Record of the Dominion Museum

Record of the Indian Museum

Record of the South Australian Museum

Recueil des travaux de la Station marine
d’Endoume, Faculté des sciences de Marseille

Report. Bernice Pauahi Bishop Museum of
Polynesian Ethnology and Natural History

Report of the Danish Biological Station to the
Board of Agriculture

Revista brasileira de biologia

Revue suisse de zoologie

Revue de zoologie et de botanique africaines

Sarsia

Schweizerische medizinische Wochenschrift

Science

Scientific Publications. Freshwater Biological
Association

Scottish Naturalist

Smithsonian Contributions to Knowledge

Smithsonian Miscellaneous Collections

South African Journal of Science

Southwestern Naturalist

Special Papers of the Geological Society of
America

Stain Technology

State Geological Survey of Kansas, Bulletin,
University of Kansas Publications

Sterkiana

Symposia of the Zoological Society of London

Systematic Zoology

MALACOLOGIA

Proc. Okla. Acad. Sci.
Proc. Penn. Acad, Sci.
Proc. Roy. Irish Acad.
Proc. Roy. Soc.

Proc. Roy. Soc. Edinb.
Proc. Soc. exp. Biol. Med.

Proc. U.S. natn. Mus.
Proc. Utah Acad, Sci.
Proc. Wash. Acad. Sci.

Proc. 2001. Soc. Lond.
Prof. Paps., U.S. Geol. Surv.

Publ, Hlth. Reps.
Publs., Carnegie Inst. Wash.
Publs. Seto mar. biol, Lab.

Quart, J. microsc. Sci.

Rec. Auck. Inst. & Mus.

Rec. Austr. Mus.

Rec. Dominion Mus.

Rec. Indian Mus.

Rec. S. Austr. Mus.

Rec. Trav. Sta. тат. Endoume

Rep., Bernice P. Bishop Mus.
Rep. Dan. biol. Sta.

Rev. bras. Biol.
Rev. suisse Zool.
Rev. Zool. Bot. afr.

Sarsia

Schweiz, med, Wochenschr.
Science

Sci. Publs., Freshw. biol. Assoc.

Scot. Natur.

Smithson. Contr. Knowl.
Smithson. misc. Collect.

5$. Alfred. Sci.

Southwest, Natur.

Spec. Paps. geol. Soc. Amer.

Stain Technol.

Geol. Surv. Kans, Bull., Univ. Kans.

Publs.
Sterkiana
Symp. zool. Soc. Lond.
Syst. Zool.

ABBREVIATIONS 423

Tethys

Tierwelt der Nord- und Ostsee

Tijdschrift der Nederlandsche dierkundige
vereeniging

Tohoku Journal of Agricultural Research

Torreia

Transactions of the American Microscopical
Society

Transactions of the Illinois State Academy of
Science

Transactions of the Kansas Academy of Science

Transactions of the Linnean Society of London

Transactions of the New Zealand Institute

Transactions of the Royal Society of Edinburgh

Transactions of the Royal Society of New Zealand

Transactions of the Royal Society of Tropical
Medicine and Hygiene

Transactions of the Wisconsin Academy of Science,
Arts, and Letters

Transactions of the Zoological Society of London

Travaux, Faculté des sciences, Université de
Rennes: Série océanographie biologique

Travaux de la Société de pharmacie de
Montpellier

Travaux de la Station biologique de Roscoff

Troms¢ museums arshefter

Umschau

University of California Publications in Geological
Sciences

University of California Publications in Zoology

University of Colorado Studies

University of Kansas Paleontological
Contributions

University of Kansas Publications of the Museum
of Natural History

Vegetatio

Veliger

Venus

Verhandlungen der Deutschen Zoologischen
Gesellschaft

Verhandlungen der Zoologisch-botanischen
Gesellschaft in Wien

Victoria Naturalist

Videnskabelige Meddelelser fra Dansk
naturhistorik Forening 1 Kjgbenhavn

Vie et milieu

Water Resources
Wilson Bulletin

Zeitschrift für Biologie
Zeitschrift für induktive Abstammungs- u.
Vererbungslehre

Tethys
Tierwelt N.- u. Ostsee
Tijdschr, ned. dierk. Ver.

Tohoku J. agr. Res.
Torreia
Trans, Amer, micvosc. Soc.

Trans. Ill. St. Acad. Sci.

Trans. Kans. Acad. Sci.

Trans. Linn. Soc. Lond.

Trans. N.Z. Inst.

Trans. Roy. Soc. Edinb.

Trans. Roy. Soc. N.Z.

Trans. Roy. Soc. trop. Med. Hyg.

Trans. Wisc. Acad, Sci., Arts & Lett.

Trans. 2001. Soc. Lond.

Trav. Fac, Sci. Rennes, Ser. Océanogr.
biol,

Trav. Soc. Pharm. Montpellier

Trav. Sta. biol. Rosc.
Troms@ Mus. Arsh.

Umschau
Univ. Calif. Publs. geol. Sci.

Univ. Calif. Publs. Zool.
Univ. Colo. Stud,

Univ. Kans. paleont. Contr.

Univ. Kans. Publs. Mus. natur. Hist.

Vegetatio

Veliger

Venus

Verh. dtsch, Zool. Ges.

Verh, zool.-bot. Ges. Wien

Vict. Natur.
Vidensk. Medd. dansk naturhist. Foren.

Vie et Milieu

Water Resourc.
Wilson Bull.

Z. Biol.
Z. indukt. Abstamm.- u. Vererbungsl.

424 MALACOLOGIA

Zeitschrift fiir Tropenmedizin und Parasitologie Z. Tropenmed. Parasitol.

Zeitschrift für vergleichende Physiologie Z. vergl. Physiol.

Zeitschrift für Zellforschung und mikroskopische Z. Zellforsch. mikrosk. Anat.
Anatomie

Zeitschrift für zoologische Systematik und Z. zool. Syst. Evolut.-forsch.
Evolutionsforschung

Zentralblatt für Bakteriologie, Parasitenkunde, Zentrabl. Bakteriol. Parasitenk.
Infektionskrankheiten und Hygiene

Zitteliana Zitteliana

Zoe Zoe

Zoologica Zoologica

Zoologica Africana Zool. Afr.

Zoologicheskii zhurnal Zool. Zh,

Zoologische Beitráge Zool. Beitr.

Zoologische Jahrbúcher (Anatomie...) Zool. Jahrb. (Anat.)

Zoologische Jahrbücher (Systematik...) Zool, Jahrb. (Syst.)

Zoologische mededeelingen Zool. Meded,

Zoologischer Anzeiger Zool. Anz.

Zoologiska bidrag fran Uppsala Zool. Bidr. Upps.

Geographical Abbreviations

Countries, territories and major geographical regions, including oceans and seas

Africa Formosa (Taiwan)
America France

Arctic Germany (Deutschland)
Argentina Great Britain

Asia Greece

Atlantic Greenland (Grgnland)
Australasia Hungary

Australia Iceland

Austria (Osterreich) India

Belgium Indonesia

Brazil (Brasil) Iran

Britain Iraq

British Guiana Ireland

Bulgaria Israel

Canada Italy

Caribbean Japan

Ceylon Korea

Chile Lebanon

China Liberia

Colombia Lithuania

Congo Madagascar
Czechoslovakia Malaya

Denmark (Danmark) Malaysia
Deutschland (Germany) Mediterranean

East Africa Mexico

Egypt Mozambique

England Netherlands (Nederland)
Ethiopia New Caledonia
Europe New England

Finland New Guinea

New Hebrides
New Zealand
Nicaragua
Nigeria
Northern Ireland
North America
North Wales
Norway
Oceania
Pacific
Pakistan
Papua
Philippines
Poland
Portugal
Rhodesia

Rumania (Romania)

Russia
Senegal
Scandinavia
Scotland

Alabama
Alaska
Alberta
Arizona
Arkansas
Bengal
California
Colorado
Connecticut
Delaware
Florida
Georgia
Hawaii
Hiroshima
Hokkaido
Idaho
Illinois
Indiana
Iowa
Kansas
Kentucky
Kyushu
Louisiana
Maine
Manitoba
Maryland
Massachusetts
Michigan
Minnesota
Mississippi
Missouri
Montana

ABBREVIATIONS 425

South Africa

South America

Spain (Españia)
Sweden

Switzerland

Taïwan (Formosa)
Trinidad

Turkey

Uganda

Union of Soviet Socialist Republics
United Arab Republics
United Kingdom

United Nations

United States

United States of America
Uruguay

Venezuela

Wales

West Africa

Yugoslavia

States and provinces

Natal

Nebraska

Nevada

New Brunswick
Newfoundland

New Hampshire

New Jersey

New Mexico

New South Wales
New York

North Carolina
North Dakota
Northern Territory (Austr.)
Northwest Territory (Can.)
Nova Scotia

Ohio

Oklahoma

Ontario

Oregon

Osaka

Pennsylvania

Prince Edward Island
Punjab

Quebec

Queensland

Rhode Island
Saskatchewan

Sonora

South Australia
South Carolina

South Dakota

Tamil Nadu (Madras)

Tasmania
Tennessee
Texas
Transvaal
Utah
Vermont
Victoria

Alexandria
Amsterdam
Auckland
Bangkok
Basel
Berlin
Bombay
Bordeaux
Boston

Bristol
Brookhaven
Brooklyn

MALACOLOGIA

Cities, counties, parishes

Brussels (Bruxelles)

Budapest
Calcutta
Cambridge
Canberra
Cherbourg
Cheshire
Chicago

Cold Spring Harbor
Copenhagen
Detroit
Drottningholm
Dublin
Edinburgh
Frankfurt am Main
Glasgow
Hamburg
Hiroshima
Kiev

Kyoto

Leeds
Leningrad
Lisbon
Liverpool
London

Los Angeles
Lucknow

Lyon

Madras

Virginia
Washington
Western Australia
West Virginia
Wisconsin
Wyoming

Yukon Territory

and districts

Madrid
Manchester
Marseille
Melbourne
Milan (Milano)
Minneapolis
Montevideo
Montreal
Moscow (Moskva)
Munich (München)
Naples (Napoli)
New Delhi
Norfolk
Northumberland
Norwich

Osaka

Ottawa

Paris

Peking
Philadelphia
Pittsburg
Prague (Praha)
Recife

Rome (Roma)
Roscoff

San Francisco
Säo Paulo
Seoul
Singapore
Shanghai
Stellenbosch
Stockholm
Stuttgart
Sydney

Tokyo

Toronto
Uppsala
Washington, D.C.
Wien(Vienna)
Woods Hole
Würzburg

TOM 11 МАЛАКОЛОГИА 1971-72

ОГЛАВЛЕНИЕ
Ф.Р.БЕРНАР
Род Thyasira у западной Канады (Bivalvia: Lucinacea). ................ 365
Д.БОЛТОВСКОЙ
Pteropoda Thecosomata югозападной части атлантического океана..... Aza

Д.БРОУН, Г.ОБЕРХОЛЦЕР И ДЖ.ВАН VIEH
Комплекс Bulinus natalensis tropicus (Basommatophora: Planorbidae)
из юго-восточной африки
1. Раковина, мантия, копулятивные органы и число хромосом...... 141

Д.БРОУН, Г.ОБЕРХОЛЦЕР И ДЖ.ВАН ИДЕН

Комплекс “Bulinus natalensis tropicus” (Basommatophora: Planorbidae)

из юго-восточной африки

П. Некоторве биологические наблюдения, систематика и

COMEN ACE ASH обо бо обо зоо ee во бо осо вооон НЫЕ
П.ЧЕНЛИ И ДЖ.ЭНДРЮС

Пособие для определения личинок двустворчатых моллюсков
MNT RUE ee Go оо ооо о о ee cie ee eee cie oO 8.0.9 00 60 ala Ga Gado od 45

А.ИЛВЕЛЛ И М. УЛМЕР

Заметки по биологии Anguispiva alternata (Stylommatophora:

Endodontidae O oat ae vers: «te Bierce А Мы ee node ое te RTE UNS 19
Р. ФЕЛЬДМАН

Первое сообщение о Hercoglossa ulrichi (White, 1882) (Cephalopoda:

Nautilida) из формаций каннонболл (палеоцен) северной

ЕЕ О ТИВ MOINE ve) ar оо eee ее ое elle ele Sus о O ES nC ed 407
Ю.А. ФИЛИППОВА

Новые данные о кальмарах (Cephalopoda: Oegopsida) из моря

Go НатТи а ec do a eres. одре ME оо ое II 391
’ А.Н. ГОЛИКОВ И 0. Г. КУСАКИН

К экологии морских блюдечек семейства Tecturidae (Gastropoda:
Docoglossa) и систематическому положению его подразделений....... 287

ЭЛЕН М. JIOYC

Хромосомы некоторых австрало-азиатских Paryphantidae ............. ЧЕТ

UMA-TCOHT-JIO

Совместимость и отношения хозяин-паразит между видами рода,
Bulinus (Basommatophora: Planorbidae) и египетской линией Schistosoma
haematobium (Trematoda: Digenea)...... Ruse: aia MERON EEE, BOS

МАЛАКОЛОГИА

В.Ф. ПОНДЕР

Морфология некоторых митридообразных Gastropoda (Neogastropoda),

особенно их пищеварительной и половой систем. ..... eee ses 295
Д.БАЛАКРИШНА-РАО, M.BEHKATACYBAMA, Р.САРВАДЖАГАННАДХА-РЕДДИ,

А.НАРА-ЗИМХА-РАДЖУ, П.ВЕНКАТЕСВАРА-РАО, К. СВАМИ

Метаболизм у молоди моллюсков, вынашиваемых взрослыми

прудовиками Viviparus bengalensis (L.) во время периода их эстивации...281
К. СТОБЕР

Распространение и возраст Margaritifera margaritifera на

мотлюсковых банках р. Мэдисон (CA) „Ks иль E SG Oo Gets}
П.ИОКЛИ

Образ жизни Pleuronema cordatum (Rafinesque, 1820)

(Bivalva: Unionacea) .............: ON ее ев cal
K.M. MOHT

О функциональной морфологии и адаптивной радиации y Saxicavacea
(Hiatella (Saxicava), Saxicavella, Panomya, Panope, Cyrtodaria). ........ SE ol

vi

INDEX TO SCIENTIFIC NAMES

abbreviata, Panope, 24
abyssicola, Bathyteuthis, 403
abyssinicus, Bulinus, 235, 239
acicula, Clio, 121
acicula, Creseis, 122, 135
Acmaea, 287, 288, 290-294
apicina, 290
mitra, 288, 291
pallida, 288
sybaritica,
Acroloxidae,
Acroloxus,
lacustris,
aculeata, Anomia,
Adesmacea, 16, 37
adriatica, Modiola,
adriatica, Modiolus,
Adula, 77
simpsoni, 77
Aequipecten, 47, 48, 51, 56, 60-66,
69-71, 73, 78, 79, 82, 84
irvadians, 47, 48, 51, 56, 60, 61,
69-71, 73, 78, 79, 82, 84
aequatorialis, Moroteuthis, 393
africanus, Bulinus, 150, 172, 225-226,
229, 231, 235-237, 239, 240, 242,
276-278
africanus ovoideus, Bulinus, 236
agilis, Tellina, 48, 51, 53, 58, 60, 61,
69-73, 88, 89, 91, 94, 95, 97, 103
109
agilis tenera, Tellina,
Alcithoe, 297, 309, 314
aldrovandi, Panope, 24
Allogona, 206
profunda, 206
Alluroteuthis, 403
antarcticus, 403
alternata, Anguispira,
Ambleminae, 351
Amphidesma, 365, 382
flexuosa, 365, 382
ampla, Panomya, 1, 18-21, 23, 41-44
Amygdalum, -60
papyria, 60
Anadara, 48, 51, 56, 60-73, 77
broughtonii, 73
granosa, 13
ovalis, 60
subcrenata,
transversa,
69-73, 77

287, 290, 292-294
221, 222

221, 222

221, 222

85

Gl
77

94

139-215

73
48, 51, 56, 60-61,

anceotata, Euclio pyramidata, 133
Ancylidae, 221, 222
anechoensis, Bankia,
Anguispiva, 199-215
alternata, 199-215
angulata, Crassostrea,
angulatus, Axinus, 366
angusta, Panope, 24
annularis, Pomaxis,
Anodonta, 358
Anomia,
85, 86, 89, 100
aculeata, 85
lischkei, 85
patelliformis,
simplex,
73, 85, 86, 89, 100

105

86

361

85

simplex ephippium, 85
squamula, 85
Anomiidae, 85
antarctica, Limacina, 126

403
403

antarctica, Teuthowenia,
antarcticus, Alluroteuthis,

antarcticus, Gonatus, 403
apicina, Acmaea, 290
Arca, 13

noae, 73
Architeuthis, 403
Arcidae, 60, 69, 72,\73
arctica, Hiatella, 4, 18
arctica, Panomya, 18, 21
ardens, Lepomis, 361

ardens, Notropis,
arenavia, Catinella, 222
avenaria japonica, Mya,

arenaria, Mya,

101

armata, Galiteuthis, 401, 402

Artemia, 281

Salina, 281

aspera, Galiteuthis, 391, 400-403,
405-406

aspera, Helix, 210, 222

astricta, Mitra, 296

Atilia, 312

rubiginosum, 312

Atlanta, 132, 133

bulimoides, 133

inflata, 132

atramentaria, Victaphanta, 217, 218,
220-224

auratus, Cricetus, 227

auriculoides, Strigatella, 296

(427)

48, 52, 57, 60-66, 69-71, 83,

48, 52, 57, 60-61, 69-71,

351, 359, 362-364

48, 54, 59-61, 69-73, 101

428 MALACOLOGIA

australis, Limacina retroversa, 127
australis, Microvoluta, 330, 334
australis, Panope, 24
Austromitra, 295, 296, 312, 314, 315,
319-323, 327, 330, 331, 334, 337,
340-342
rubiginosa, 295, 296, 312, 315, 319,
320, 331, 340-342
rubiradix, 312, 314, 315
Axinulus, 365
Axinus, 365-367, 382
angulatus, 366
flexuosus, 382
gouldii, 382
sarsi, 367, 382
sinuatus, 366
Babinka, 368
balaustria, Tellina, 94
balea, Limacina, 126
balea, Limacina retroversa, 127
balthica, Macoma, 60, 94
Bankia, 60, 105
anechoensis, 105
gouldi, 60, 105
indica, 105
setacea, 105
banksi, Onychoteuthis, 403
barbarensis, Cryptodon, 382
barbarensis, Thyasiva, 382-384
Barnea, 46, 48, 51, 54, 59-73, 101-105
candida, 101
parva, 101
truncata, 46, 48, 51, 59-61, 69-73
Bartlettia, 9
bartschi, Teredo, 105
Basommatophora, 141, 167-169, 171,
195-198, 225, 276-278
Bathyteuthis, 403
abyssicola, 403
Batoteuthis, 403
scolops, 403
beccarii, Bulinus, 238
bengalensis, Viviparus, 281-283, 285,
286
beringiana, Panomya, 18
biconica, Microvoluta, 325, 329-331
biconica, Pusia, 328
biconica, Vulpecula, 328

bidentatus lineatus, Melampus, 221, 222

bidentatus, Melampus, 221, 222
Biomphalaria, 188, 261, 262, 264-266,
270

glabrata, 261, 262, 265, 266, 270
pfeifferi, 188, 264
binghami, Sphenia, 13
biparia, Hartmannella, 225, 241, 276-277,
279
biplicata, Ptychina, 366, 282
bisecta, Cyprina, 368
bisecta, Cryptodon, 368, 372
bisecta omarui, Conchocelle, 370
bisecta omarui, Thyasira, 370
bisecta, Thyasira, 365, 366, 368-370,
372, 373, 375, 377
bisecta, Venus, 365, 368
bisectus, Cryptodon, 368, 372
bisinuatus, Cryptodon, 366
bitruncata, Panope, 24
Bivalvia, 2, 351, 363-366, 388, 389
Blarina, 210
brevicauda talpoides, 210
Borsoniinae, 338
Botula, 6
bovis, Schistosoma, 178, 227, 242, 264,
269
Brachidontes, 60, 77
vecurvus, 60
senhausi, 77
Brachiopoda, 367
Brachioteuthidae, 400
Brachioteuthis, 391, 400, 403, 405, 406,
riisei, 391, 400, 403, 405, 406
brevicauda talpoides, Blarina, 210
broughtonii, Anadara, 73
bubalus, Ictiobus, 361
Buccinacea, 333
Buccinidae, 335
Buccinum, 297, 312, 335
bulimoides, Atlanta, 133
bulimoides, Limacina, 121-124, 128-131,
133, 136, 139, 140
bulimoides, Munthea, 133
Bulininae, 227
Bulinus, 141-143, 149-182, 184-191,
195-198, 225-247, 249-270, 276-278
abyssinicus, 235, 239
africanus, 150, 172, 225, 226, 229, 231,
235-237, 239, 240, 242, 276-278
africanus ovoideus, 236
beccarii, 238
cernicus, 233, 238, 239
comptus, 175, 179, 180
contortus, 142, 165, 166
corneus, 179, 180

INDEX, VOL. 11 429

coulboisi, 190, 191, 225, 227, 229, 164. 168-173, 175-177, 179-182,
230, 234-237, 240, 243, 251, 184, 189, 195-198
254-258, 263, 268, 270, 276-278 ` buntingi, Nephrops, 411

craveni, 175, 179, 180 busbyi, Paryphanta, 217, 218, 221

depressus, 163, 179, 180, 190, 237, 242 calcarea, Macoma, 94

diaphanus, 175, 180 californianus, Mytilus, 77

didieri, 239 Calliteuthis, 403

examia, 239 miranda, 403

forskalii, 172, 179, 225, 226, 229-231 Campaniclava, 134
233-239, 276-278 cleodorae, 134

globosus, 150, 182, 188, 189, 225, campechiensis, Mercenaria, 91
229, 230, 234-237, 239-242, 244, Cancilla, 334
251, 254, 255, 263-265, 268, candida, Barnea, 101
276-279 capense, Schistosoma, 227

globosus ugandae, 239 caprodes, Percina, 361

guernei, 225-227, 229-237, 239, 240, Cardiidae, 89
242-247, 249-270, 276-279 Cardita, 14

hemprichii, 179 variegata, 14

hemprichii depressus, 179 ventricosa, 14

mariei, 238 Carditacea, 14

nasutus, 236 Cardium, 46, 89

natalensis, 141-143, 149-182, 184- echinatum, 89
191, 195-198, 242 edule, 89

nyassanus, 186, 188 exiguun, 89

reticulatus, 237, 238 exiguun pygmeun, 89

scalaris, 225, 229, 230, 234, 237, 239, minimum, 89
241, 244, 276-278 ovale, 89

senegalensis, 237-239 ovale fasciatum, 89

sericinus, 225, 229, 230, 234, 238, scabrum, 89
240, 242, 243, 251, 253-263, 265, -cassis, Collisella, 291
268, 270, 276-278 Catinella, 222

succinoides, 186, 188 avenaria, 222

transversalis, 186 gabbi, 222

trigonus, 239 votundata, 222

tropicus, 141-143, 149, 151-182, texana, 222
184-191, 195-198, 225-228, 230, vermeta, 222
234-237, 239-242, 244, 276 Cavolina, 121-124, 129, 135, 139-140

truncatus, 141-143, 161, 164, 166-169, inflexa, 121
171-173, 177, 179-180, 186, 190- Cavoliniidae, 122, 133
191, 195-198, 225-230, 233-244, Cephalopoda, 391, 405-408, 413
246, 247, 251, 253-265, 268, 270, cernicus, Bulinus, 233, 238, 239

276-279 Chamidae, 9
truncatus rohlfsi, 225, 228, 234-236 Charitodoron, 334
238, 240, 242, 243, 251, 255, Chlamydephoridae, 221
258-261, 270, 276-279 Chlamys, 84
truncatus sericinus, 240 striatus, 84
truncatus trigonus, 186, 190, 236 chrysostoma, Mitra, 311
truncatus truncatus, 190, 225, 228, cinerea, Urosalpinx, 298
230, 233, 234, 240, 243, 251, Clausina, 366
253-263, 265, 268, 270, 276-279 Cleodora, 133, 134
ugandae, 235-237, 239 cuspidata, 134

zuluensis, 141-142, 151, 161, 162, pyramidata, 133

430

pyramidata lata, 133
cleodorae, Campaniclava, 134
Clio, 121-124, 126, 128-131, 133, 134,
136, 139, 140
acicula, 121
cuspidata, 121-124, 129, 134, 136,
139, 140
helicina, 126
pyramidata, 121-124, 128-131, 133,
134, 139, 140
pyramidata lanceolata,
Codakiacea, 365
Collembola, 211
Collisella, 287, 288, 290-294
cassis, 291
Columbella, 312
rubiginosum, 312
commercialis, Crassostrea, 86
compta, Isidora, 179
comptus, Bulinus, 175, 179, 180
Conchocele, 365, 366, 368, 370, 372
bisecta omarui, 370
disjuncta, 365, 366, 368, 372
investigatoris, 366
concinna, Notoacmea,
Congeria, 60
leucophaeta, 60
conica, Imbricaria,
conovula, Imbricaria,
conovula, Mitra, 310
consanguinea, Pusia,
contortus, Bulinus,
conularis, Imbricaria,
conularis, Mitra, 310
corallina, Mactra, 99
cordatum, Pleurobema,
359, 360, 362-364
cornea, Physa, 179
corneus, Bulinus, 179, 180
costata, Cyrtopleura, 48, 51, 54, 59-61
69-73, 103, 106-108
coulboisi, Bulinus, 190, 191, 225, 229,
230, 234-237, 240, 243, 251, 254-
258, 263, 268, 270, 276-278
Cranchiidae, 400
crassa, Tellina, 94
crassistesta, Mytilus, 77
crassium, Laevicardium, 89, 90
Crassostrea, 47, 48, 52, 57, 60-73,
80, 81, 86, 100, 102, 103
angulata, 86
commercialis, 86

133

291
311
299, 310, 311, 331
296, 334

142, 165, 166
307, 310, 311

351-354, 357,

MALACOLOGIA

gigas, 86
rhizophorae, 86
virginica, 48, 52, 57, 60, 61, 69-73,

80, 81, 86, 100, 102, 103
craveni, Bulinus, 175, 179, 180

craveni, Physa, 178
Crenella, 77
decussata, 77
crenulata, Mitra, 296

crenulata, Pterygia, 296, 302, 335
Creseis, 121-124, 128, 135, 139, 140
acicula, 122, 135
virgula, 122, 135
Cricetus, 227
auratus, 227
crispata, Zirfaea, 101
Cryptodon, 365, 366, 368, 372, 382
barbarensis, 382
bisecta, 368, 272
bisectus, 368, 372
bisinuatus, 366
flexuosum, 382,
flexuosus, 382
gouldii, 382
crytonota, Physa,
Crystalloteuthis,
glacilialis, 403
cucumerina, Mitra, 302
cuneata, Rangia, 46-48, 51, 54, 60, 61,
69, 70, 73, 99-102
Cuspidaria, 368, 378
cuspidata, Cleodora, 134
cuspidata, Clio, 121-124, 129, 134, 136,
139, 140
cuspidata, Euclio,
cuspidata, Hyalea,
Cutellus, 97
pellucidus, 97
cuvierensis, Microvoluta,
cyanellus, Lepomis, 361
cygnus, Thyasiva, 365, 368, 370, 371, 374

178
403

134
134

330

Cylindra, 333, 334
Cylindrinae, 333
Cylindromitrinae, 334, 335, 338
Cyprina, 368
bisecta, 368
Cyrtodaria, 1-3, 31-39, 41-44
kurriana, 31
siliqua, 1, 31-36, 39, 41-44
Cyrtopleura, 48, 51, 54, 59-73, 103,
106-108
costata, 48, 51, 54, 59-61, 69-73,

INDEX, VOL. 11

103, 106-108
dactylus, Pholas, 101
danica, Hercoglossa, 410
decussata, Crenella, 77
demissus, Modiolus, 49, 51, 56, 60-61,
69, 10, 1231331111, °80
denselamellosa, Ostrea, 87
depressus, Bulinus, 163, 179, 180, 190,
237, 242
depressus, Bulinus hemprichii, 179
desjardini, Marginella, 328
Diacria, 121-124, 130, 135, 139, 140
trispinosa, 135
diaphana, Physa, 178
diaphanus, Bulinus, 175, 180
didieri, Bulinus, 239
Digenea, 225, 276-278
Diplodonta, 372
directus, Ensis, 48, 53, 58, 60-67,
69-73, 93-95, 97, 99, 101
discors, Modiolaria, 77
discors, Musculus, 17
disjuncta, Conchocele,
372
disjuncta, Thyasira, 365, 366, 368-370,
372, 375, 377, 378, 380, 382, 385
Docoglossa, 287, 288, 292-294
dolomieui, Micropterus, 361
Donacidae, 96
donacina, Tellina, 94
Donax, 33, 46, 48, 51, 53, 58, 60-66,
69-72, 90-92, 96, 109
variabilis, 46, 48, 51, 53, 58, 60-61,
69-72, 90-92, 96, 109
venustus, 96
vittatus, 96
douthitti, Schistosomatium, 233
Dreissenacea, 3, 16
Drepanochilus, 411
dunniae, Rhytida,
echinatum, Cardium, 89
edule, Cardium, 89
edulis, Mytilus, 48, 51, 56, 60, 61,
69, 70, 72, 73, 76, 77, 82
edulis, Ostrea, 87
elliptica, Spisula, 99

365, 366, 368,

Ellobiidae, 221, 222
elvae, Trichobilharzia, 233
Enclimatoceras, 408, 410

ulrichi, 408
hyatti, 410

Endodontidae, 199, 213-215

2170218, 29109020224

431

48, 53, 58, 60-67, 69-73, 93-95,
97, 99, 101
directus, 48, 53, 58, 60, 61, 69-73,
93-95, 97, 99, 101
ensis, 97
siliqua, 97
ensis, Ensis, 97
Entodesma, 16
ephippium, Anomia simplex, 85
episcopales, Mitra, 296
equestris, Ostrea, 87
eremitarum, Mitra, 311, 312
erinacea, Ocenebra, 321
Etheostoma, 361
simoterum, 361
Etheriidae, 35
Euclio, 133, 134
cuspidata, 134
pyramidata, 133
pyramidata lanceotata, 133
Eumitra, 311
nigra, 311
Euphausia, 398
superba, 398
Euthecosomata, 126
excavata, Thyasira, 366
exiguun, Cardium, 89
exiguun pygmeum, Cardium, 89
eximia, Bulinus, 239
fabula, Tellina, 94
fasciatum, Cardium ovale, 89
Fasciolariidae, 338
ferruginosa, Kellia, 366
filaria, Mitra, 296
flexuosa, Amphidesma,
flexuosa, Lucina, 382
flexuosa, Tellina, 366, 382, 384
flexuosa, Thyasira, 365, 366, 368, 371,
376, 382, 384
flexuosum, Cryptodon, 382
flexuosus, Axinus, 382
flexuosus, Cryptodon, 382
floridana, Thala, 338
forskalii, Bulinus, 172, 179, 225, 226,
229-231, 233-239, 276-278
fragilis, Gastrana, 94
frons, Ostrea, 87
Fulvia, 90
mutica, 90
fuscus, Laevapex, 221, 222
gabbi, Catinella, 222
Galiteuthis, 391, 400-403, 405, 406

Ensis,

365, 382

432

401, 402
aspera, 391, 400-403, 405, 406
suhmi, 402
gallicana, Hiatella, 4
gallicana rugosa, Hiatella, 4
gallina, Venus, 91
gardnerae, Hercoglossa,
Gastrana, 94
fragilis, 94
Gastrochaenidae, 5

aymata,

411

Gastropoda, 287, 292-294, 342
gawleri, Strangesta, 217, 218, 220,
223, 224

Gemma, 48, 51, 55, 58, 60, 61, 69-71,

86, 91, 92, 107, 109
gemma, 48, 51, 55, 58, 60, 61, 69-71,

86, 91, 92, 107, 109

gemma, Gemma, 48, 51, 55, 58, 60, 61,
69-71, 86, 91, 92, 107, 109

generosa, Panope, 1, 20, 24-31, 41-44

giganteus, Saxidomus, 91

gigas, Crassostrea, 86

glabrata, Biomphalaria,
266, 270

glacialis, Psychroteuthis,
403, 405, 406

glacilialis, Crystalloteuthis,

globosa, Nototeredo, 411

globosa, Panope, 24

globosus, Bulinus, 150, 182, 188, 189,
225, 229, 230, 234-237, 239-242,
244, 251, 254, 255, 263-265, 268,
276-279

globosus ugandae, Bulinus,

Glossus, 9

Glycymeris, 32

261, 262, 265,
391, 398-400,

403

239

siliqua, 32
glycymeris, Panope, 24
Gonatus, 403

antarcticus, 403
gouldi, Bankia, 60, 105

gouldi, Solen, 97
gouldi, Thyasira,
Gouldia, 91
minima, 91
gouldiana, Pandora,
gouldii, Axinus, 382
gouldii, Cryptodon, 382
gouldii, Lucina, 382, 384
gouldii, Thyasira, 382
grandis, Pecten, 84
granosa, Anadara, 13

384

107

MALACOLOGIA

greeri, Succinea, 222
grgnlandica, Volutomitra,
gvosvenori, Succinea, 222
guernei, Bulinus, 225-227, 229-237,
239, 240, 242-247, 249-270, 276-279
haematobium, Schistosoma, 142, 172,
173, 178, 190, 195-198, 225-227,
231, 233-235, 240-243, 245-252,
255, 262, 264-270, 277, 278
hamiltoni, Mesonychoteuthis, 403
Haplotrema, 217, 221
sportella, 217
vancouverense, 217
Haplotrematidae, 217, 221
Hartmannella, 225, 241, 276, 277, 279
biparia, 225, 241, 276, 277, 279
hebes, Vexillum, 296
hedleyi, Peculator, 295, 296, 322, 323,
325, 329, 331, 340-342
hedleyi, Pusia, 322
hedleyi, Velpecula,
Helicidae, 222
helicina, Clio, 126
helicina, Limacina, 121-124, 126-133,
135, 136, 139, 140
helicina, Spiratella, 121
helicis, Postharmostmum,
213-215
210, 217, 220-224
210, 222

334

322

199, 200, 211,

Helix,
aspersa,
pomatia, 217, 221-224

hemprichii, Bulinus, 179

hemprichii depressus, Bulinus, 179

Hercoglossa, 407, 408, 410, 411, 413
danica, 410
gardnerae, 411
orbiculata, 411
ulrichi, 407, 408, 410-413

Hercoglossidae, 408

Heterodonta, 365, 368, 388, 389

Heterofursus, 126
vetroversus, 126

Hiatella, 1-4, 6-9, 11-18, 21-24, 30, 31,

37-39, 41-44
arctica, 4, 18
gallicana, 4
gallicana rugosa, 4
pholadis, 4

hirasei, Succinea, 222
horticola, Succinea, 222
Hyalea, 133, 134
cuspidata, 134

INDEX, VOL. 11

lanceolata, 133

hyalina, Lyonsia, 46, 48, 51, 55, 60, 61,

69, 70, 107-109
hyatti, Enclimatoceras, 410
hyotis, Pycnodonta, 88
Ictalurus, 361
melas, 361
Ictiobus, 361
bubalus, 361
idae, Mitra, 296
Imbricaria, 299, 302, 307, 310, 311,
331, 333, 334, 337
conica, 311
conovula, 299, 310, 311, 331
conularis, 307, 310, 311
Imbricariinae, 333, 334
inaequalis, Thyasiva, 384
inaequivalvis, Pandora, 107
indica, Bankia, 105
inflata, Atlanta, 132
inflata, Limacina, 121-124, 128-133,
135, 139, 140
inflata, Thilea, 132
inflexa, Cavolina, 121
ingens, Moroteuthis, 392, 393, 403
inadians, Aequipecten, 47, 48, 51, 56,
60, 61, 69-71, 73, 78, 79, 82, 84
intercalatum, Schistosoma, 227
investigatoris, Conchocele, 366
irradians, Pecten, 82
Isidova, 179
compta, 179
Isocardia, 9
japonica, Mya arenaria, 101
japonica, Panope, 24
japonica, Teredo, 105
japonicum, Schistosoma, 265, 270
jeffreysi, Saxicavella, 1, 12-18, 39,
41-44
Juncus, 163, 186
jurtina, Maniola, 188
juvenalis, Tellina, 95
Kellia, 366
ferruginosa, 366

knipovitchi, Moroteuthis, 391-395, 403,

405, 406

Kondokovia, 391, 395-398, 403, 405, 406

longimana, 391, 395-398, 403, 405,
406
kurriana, Cyrtodaria, 31
lacustris, Acroloxus, 221, 222
Laevapex, 221, 222

fuscus, 221, 222
Laevicardium, 48, 52, 57, 60-67, 69-73,
82, 83, 89, 90, 94, 95, 101

crassium, 89, 90
mortoni, 48, 52, 57, 60, 61, 69-73,
82, 83, 94, 95, 101
lanceolata, Clio pyramidata, 133
lanceolata, Hyalea, 133
lata, Cleodora pyramidata, 133
lateralis, Mulinia, 47, 48, 54, 59-61,
69-73, 86, 98, 99, 101
Lepomis, 361
ardens, 361
cyanellus, 361
macrochiris, 361
megalotis, 361
Leptonacea, 368
leucophaeta, Congeria, 60
leucopus, Peromyscus, 210
Lima, 84
Limacina, 121-133, 135, 136, 139, 140
antarctica, 126
balea, 126
bulimoides, 121-124, 128-131, 133,
136, 139, 140
helicina, 121-124, 126-133, 135, 136,
139, 140
inflata, 121-124, 128-133, 135, 139,
140
vetroversa, 121-124, 126, 128-132,
135, 136, 139, 140
vetroversa australis, 127
retroversa balea, 127
vetroversa vetroversa, 127
Limacinidae, 122, 126
lineatus, Melampus bidentatus, 221, 222
lirata, Physa, 178
lischkei, Anomia, 85
Lithophaga, 38
lithophaga, Petricola, 94
longimana, Kondakovia, 391, 395-398,
403, 405, 406
lonnbergii, Moroteuthis, 393
lorigera, Oregoniateuthis, 403
loscombiana, Pholadidea, 101
Lucina, 366, 382, 384
flexuosa, 382
gouldii, 382, 384
sinuata, 366, 382
Lucinacea, 9, 365-367, 388, 389
Lucinidae, 368
luculenta, Mitra, 296, 320

433

434 MALACOLOGIA

luculenta, Pusia, 320
luculentum, Vexillum, 296, 315, 319-
322
lurida, Ostrea, 87
lusoria, Meretrix, 91
lutaria, Ostrea, 88
Lutraria, 39, 99
lutraria, 99
lutraria, Lutraria, 99
Lymnaea, 164, 185, 186, 188
natalensis, 188
peregra, 164, 185, 186
stagnalis, 186, 188
Lyonsia, 46, 48, 51, 55, 60, 61, 69, 70,
107-109
hyalina, 46, 48, 51, 55, 60, 61, 69,
70, 107-109
norwegica, 107
Lyonsidae, 107
Lyrodus, 106
pedicellata, 106
Macoma, 60, 94
balthica, 60, 94
calcarea, 94
phenax, 60
tenta, 60
macrochiris, Lepomis, 361
Mactra, 99
corallina, 99
sachalinensis, 99
sulcatoria, 99
veneriformis, 99
Mactracea, 39
Mactridae, 99
magellanicus, Plapecten, 84
maniculatus, Peromyscus, 210
Maniola, 188
jurtina, 188
mansoni, Schistosoma, 233, 246-248,
262, 264, 265, 270
Margaritifera, 343, 344, 347-350
margaritifera, 343, 344, 347-350
margaritifera, Margaritifera, 343,
344, 347-350
marginata, Microvoluta, 328, 330
marginata, Turricula, 328
Marginella, 328
desjardini, 328
Marginellidae, 338
maviei, Bulinus, 238
marmorata, Modiolaria, 77
marmorata, Modiolus, 77

mattheei, Schistosoma, 17
megalotis, Lepomis, 361
megotara, Teredo, 105
Melampus, 221, 222
bidentatus, 221, 222

bidentatus lineatus,

melas, Ictalurus, 361
Mercenaria, 48, 52, 57, 60-62, 64-66,
69, 70, 72, 84, 85, 91; 94,95
campechiensis, 91

mercenaria,

48, 52, 57,

8, 227, 242

221, 222

60, 61, 69,

70, 72, 84, 85, 91, 94; 99
mercenaria, Mercenaria,

60, 61, 69, 70, 72, 84, 85, 91, 94, 99

Meretrix, 91
lusoria, 91
meretrix, 91
vudis, 91

meretrix, Meretrix, 91

Mesodon, 206

thyroidus, 206
Mesonychoteuthis, 403
hamiltoni, 403
Micropterus, 361
dolomieui, 361
salmoides, 361

Microvoluta, 295, 325, 328-331, 333-335,

337, 341, 342
australis, 330, 334
biconica, 325, 329-331

cuvierensis,

330

marginata, 328, 330

Microvolutidae,

334, 335

microzonias, Mitra, 296
micvozonias, Pusia, 334
minima, Gouldia, 91
minimum, Cardium, 89
miranda, Calliteuthis, 403

Mitra, 296-298, 302, 310-312, 320, 331,

333, 334, 337

astricta, 296
chrysostoma,

311

conovula, 310
conularis, 310
crenulata, 296

cucumerina,
episcopales,
eremitarum,
filaria, 296
idae, 296

302
296
311. 312

luculenta, 296, 320

microzonias,

296

48, 52, 57,

INDEX, VOL. 11

mitra, 296-298, 311, 312, 331
nigra, 311, 312
nodulosa, 337
vetusa, 296
scutulata, 296
Sizetica, 311,312
Zonata, 296, 297
mitra, Acmaea, 288, 291
mitra, Mitra, 296-298, 311, 312, 331
Mitracea, 333
Mitridae, 295, 333-337, 340-342
Mitrinae, 333-335, 338
Modiola, 77
adriatica, 77
Modiolaria, 77
discors, 77
marmorata, 77
niger, 11
Modiolus, 48, 51, 56, 60-70, 72, 73,
27480
adriatica, 77
demissus, 48, 51, 56, 60, 61, 69, 70,
Hat, 11, 80
marmorata, “7
modiolus, 77
niger, 77
Monia, 85
squama, 85
Moroteuthis,
405, 406
aequatorialis, 393
ingens, 392, 393, 403
knipovitchi, 391-395, 403, 405, 406
lonnbergii, 393
robsoni, 393
robusta, 393
morrhuana, Pitar, 48, 52, 57, 60, 61,
69-73, 91, 93, 101
mortoni, Laevicardium, 48, 52, 57, 60,
61, 69-73, 82, 83, 94, 95, 101
moskalevi, Problacmaea, 287, 288,
290-294

391-395, 397, 398, 403,

Mulinia, 47, 48, 54, 59-73, 86, 98, 99,
101
lateralis, 47, 48, 54, 59-61, 69-73,

86, 98, 99, 101
Munthea, 133
bulimoides, 133
Muricacea, 333
Muricidae, 335
Mus, 310
Musculus, 77

435

discors, 77
mutica, Fulvia, 90
Mya, 19, 39, 48, 54, 59-66, 69-73, 101
avenavia, 48, 54, 59-61, 69-73, 101
avenaria japonica, 101
truncata, 19, 101
Myacea, 16, 39
Myacidae, 101
Myonera, 368
Mytilacea, 3, 16
Mytilidae, 60, 72, 77
Mytilus,
82
californianus, 77
crassistesta, 77
edulis, 48, 51, 56, 60, 61, 69, 70, 72,
13,16, u, 82
Myxophyllum, 212
steenstrupi, 212
Nassarius, 204
obsoletus, 204
Nassidae, 333
nasutus, Bulinus, 236
natalensis, Bulinus, 141-143, 149-182,
184-191, 195-198, 242
natalensis, Lymnaea, 188
natalensis, Panope, 24
natalensis, Physa, 178
Nautilaceae, 408
Nautilida, 407, 408, 413
Nautiloidea, 408
Nautilus, 408
texanus, 408
ulrichi, 408
navalis, Teredo, 48, 55, 60, 61, 69, 70,
72, 73, 103, 105, 106
Neocancilla, 334
Neogastropoda, 295, 309, 316, 335,
340-342
Neoteuthis, 403
Neotiidae, 75
Nephrops, 411
buntingi, 411
niger, Modiolaria, 77
nigev, Modiolus, 77
nigra, Eumitra, 311
nigra, Mitra, 311, 312
nigromaculatus, Pomoxis, 361
noae, Arca, 13
nodulosa, Mitra, 337
Noetia, 46, 48, 51, 56, 60-66, 69-75
ponderosa,

48, 51, 56, 60-70, 72, 73, 76, 77,

46, 48, 51, 56, 60, 61, 69-75

436 MALACOLOGIA

norvegica, Panopea, 18
norwegica, Lyonsia, 107
norwegica, Panopea, 19
norwegica, Teredo, 106
nosophora, Oncomelania, 269
Notoacmea, 287, 288, 290-294
concinna, 291
Nototeredo, 411
globosa, 411
Notropis, 351, 359, 362-364
ardens, 351, 359, 362-364

novoseelandica, Schizoglossa, 217, 218

223, 224
Nucella, 309, 312, 335
nyassanus, Bulinus, 186, 188
obsoletus, Nassarius, 204
Ocenebra, 317, 321
erinacea, 321
Oegopsida, 391, 405, 406
Oliva, 321
sayana, 321
Olividae, 335, 338
omarui, Conchocele bisecta, 370
omarui, Thyasira bisecta, 370
Oncomelania, 265, 269
nosophora, 269
Onychoteuthidae, 391, 392, 405, 406
Onychoteuthis, 403
banksi, 403
opercularis, Pecten, 84
orbiculata, Hercoglossa, 411
Oregoniateuthis, 403
lorigera, 403
Ostrea, 87, 88
denselamellosa, 87
edulis, 87
equestris, 87
frons, 87
lurida, 87
lutaria, 88
taurica, 88
Ostreidae, 69, 86
ovale, Cardium, 89
ovale fasciatum, Cardium, 89
ovalis, Anadara, 60
ovata, Venus, 91
ovoideus, Bulinus africanus, 236
pallida, Acmaea, 288
Pandora, 107
gouldiana, 107
inaequivalvis, 107
Pandoracea, 93, 107

Pandoridae, 107

Panomya, 1-3, 16, 18-21, 23, 24, 26,
28-31, 33, 35-39, 41-44

ampla, 1, 18-21, 23, 41-44

arctica, 18, 21

beringiana, 18

spengleri, 18

turgida, 18

Panope, 1-3, 9, 20, 24-31, 33, 35-39,
41-44

abbreviata, 24

aldrovandi, 24

angusta, 24

australis, 24

bitruncata, 24

generosa, 1, 20, 24-31, 41-44

globosa, 24

glycymeris, 24

japonica, 24

natalensis, 24

rugosa, 24

smithae, 24, 25

zelandica, 24

Panopea, 3, 14, 18

norvegica, 18

norwegica, 19

plicata, 14

Paphia; 91

philippinorum, 91

staminea, 91

papyria, Amygdalum, 60

Paradmete, 334

Parapholas, 101

quadrizonata, 101

parva, Barnea, 101

Paryphanta, 217, 218, 221

busbyi, 217, 218, 221

Paryphantidae, 217, 218, 220-222

patelliformis, Anomia, 85

Patelloida, 287, 290-294

saccharina, 291

Patelloidinae, 291-294

paupercula, Strigatella, 295, 296, 299,
301-303, 306-308, 311, 319, 331,
340-342

paupercula, Voluta, 296

pavo, Taonius, 403

Pecten, 82, 84

ivvadians, 82

grandis, 84

opercularis, 84

septemradiatus, 84

INDEX, VOL. 11 437

striatus, 84 virens, 282 -
tenuicostatus, 84 Pitar, 48, 52, 57, 60-65, 69-73, 91,
tigrinum, 84 93, 101
Pectinidae, 82 morrhuana, 48, 52, 57, 60, 61, 69-73,
Peculator, 295, 296, 322, 323, 325, 915493, “101
329-335, 340-342 Placopecten, 84
hedleyi, 295, 296, 322, 323, 325, 329, magellanicus, 84
331, 340-342 plana, Thyasira, 384
verconis, 334 Planorbidae, 141, 167-169, 171, 195-198,
Peculatoridae, 334 225, 227, 276-278
pedicellata, Lyrodus, 106 Platydon, 38
pedicellata, Teredo, 106 plebeius, Tagelus, 60
pellucidus, Cutellus, 97 Pleurobema, 351-354, 357, 359, 360,
Percina, 361 362-364
caprodes, 361 cordatum, 351-354, 357, 359, 360,
peregra, Lymnaea, 164, 185, 186 362-364
Peromyscus, 210 plicaria, Voluta, 321
leucopus, 210 plicarium, Vexillum, 315, 319-321, 331
maniculatus, 210 plicata, Panopea, 14
peroniana, Prothyasiva, 366 plicata, Saxicava, 14
Petricola, 48, 53, 58, 60-65, 69-72, Polysyringia, 368
87, 88, 94, 101 pomatia, Helix, 217, 221-224
lithophaga, 94 Pomoxis, 361
pholadiformis, 48, 53, 58, 60, 61, annularis, 361
69-72, 87, 88, 94, 101 nigromaculatus, 361
Petricolidae, 94 ponderosa, Noetia, 46, 48, 51, 56,
pfeifferi, Biomphalaria, 188, 264 60, 61, 69-75
phenax, Macoma, 60 Poromya, 368
philippinorum, Paphia, 91 Postharmostmum, 199, 200, 211, 213-215
philippinorm, Venerupis, 91 helicis, 199, 200, 211, 213-215
Pholadidae, 5, 101, 109 Problacmaea, 287, 288, 290-294
Pholadidea, 101 moskalevi, 287, 288, 290-294
loscombiana, 101 sybaritica, 287, 288, 291-294
pholadiformis, Petricola, 48, 53, 58, Proclio, 121
60, 61, 69-72, 87, 88, 94, 101 subteres, 121
pholadis, Itiatella, 4 proclivis, Tapes, 91
Pholas, 101 Procymbulia, 121
dactylus, 101 valdiviae, 121
Phragmites, 163 profunda, Allogona, 206
Physe, 118,179 Prolucina, 368
cornea, 179 Promachoteuthis, 403
craven, 178 Prothyasiva, 366
crytonota, 178 peroniana, 366
diaphana, 178 Psychroteuthidae, 398
lirata, 178 Psychroteuthis, 391, 398-400, 403,
natalensis, 178 405, 406
tropica, 178 glacialis, 391, 398-400, 403, 405, 406
verreauxii, 178 Pterygia, 296, 302, 334, 335
zuluensis, 179 crenulata, 296, 302, 335
physellae, Trichobilharzia, 233 Ptychina, 366, 382
Physopsis, 239 biplicata, 366, 382

Pila, 282 pullastra, Venerupis, 91

438 MALACOLOGIA

Purpuridae, 333
Pusia, 296, 320, 322, 328, 333, 334
biconica, 328
consanguinea,
hedleyi, 322
luculenta, 320
microzonias, 334
Pycnodonta, 88
hyotis, 88
pygmeum, Cardium exiguun, 89
pyramidata anceotata, Euclio, 133
pyramidata, Cleodora, 133
pyramidata, Clio, 121-124, 128-131,
133, 134, 139, 140
pyramidata, Euclio, 133
pyramidata lanceolata, Clio, 133
pyramidata lata, Cleodora, 133
quadrizonata, Pavapholas, 101
Rangia, 46-48, 51, 54, 60-64, 69, 70,
73, 99-102
cuneata, 46-48, 51, 54, 60, 61, 69,
70, 73, 99-102
recurvus, Brachidontes, 60
reticulatus, Bulinus, 237, 238
vetroversa australis, Limacina, 127
retroversa balea, Limacina, 127
retroversus, Heterofursus, 126
retroversa, Limacina, 121-124, 126,
128-132, 135, 136, 139, 140
retroversa, Limacina retroversa, 127
retroversa vetroversa, Limacina, 127
retusa, Mitra, 296
retusa, Strigatella, 296
rhizophorae, Crassostrea, 86
Rhodopetala, 287, 288, 291-294
yosea, 287, 288, 291-294
Rhytida, 217, 218, 221, 223, 224
dunniae, 217, 218, 221, 223, 224
riisei, Brachioteuthis, 391, 400, 403,
405, 406
robsoni, Moroteuthis, 393
robusta, Moroteuthis, 393
rohlfsi, Bulinus truncatus, 225, 228,
230, 234-236, 238, 240, 242, 243,
251, 255, 258-261, 270, 276-279
rosea, Rhodopetala, 287, 288, 291-294
rotundata, Catinella, 222
rubella, Tectura, 287, 288
rubiginosa, Austromitra, 295, 296, 312,
315, 319, 320, 331, 340-342
rubiginosum, Atilia, 312
rubiginosum, Columbella, 312

296, 334

rubignosum, Vexillum, 312
rubiradix, Austromitra, 312, 314, 315
vudis, Meretrix, 91

rugosa, Hiatella gallicana, 4
rugosa, Panope, 24

rugosa, Saxicava, 10
saccharina, Patelloidea, 291
sachalinensis, Mactra, 99
salina, Artemia, 281
salmoides, Micropterus, 361
sarsi, Axinus, 367, 382
sarsi, Thyasiva, 384

Saxicava, 1, 3, 9, 10, 12-14, 18, 41-44
plicata, 14
vugosa, 10
Saxicavacea, 1-4, 9, 11, 13, 16, 29, 31,
36-38, 41-44
Saxicavella, 1-3, 13-18, 29, 31, 37-39,
41-44
jeffreysi, 1, 12-18, 39, 41-44

Saxidomus, 91
giganteus, 91
sayana, Oliva, 321
Scabricola, 334
scabrum, Cardium, 89
scalaris, Bulinus, 225, 229, 230, 234,
237, 239, 241, 244, 276-278
Scaphella, 334
Schistosoma, 142, 171-173, 178, 190,
195-198, 225-227, 231, 233-235,
240-243, 245-252, 255, 262,
264-270, 276-279
bovis, 178, 227, 242, 264, 269
capense, 227
haematobium, 142, 172, 173, 178, 190,
195-198, 225-227, 231, 233-235,
240-243, 245-252, 255, 262,
264-270, 277, 278
intercalatum, 227

japonicum, 265, 270

mansoni, 233, 246-248, 262, 264, 265,
270

mattheei, 178, 227, 242

Schistosomatium, 233
douthitti, 233
Schizoglossa, 217, 218, 223, 224
novoseelandica, 217, 218, 223, 224
Schizothaerus, 39, 366
scolops, Batoteuthis, 403
scutulata, Mitra, 296
scutulata, Strigatella, 296
semidecussata, Tapes, 91

INDEX, VOL. 11

senegalensis, Bulinus, 237-239
senhausi, Brachidontes, 7
septemradiatus, Pecten, 84
Septibranchia, 368
sericinus, Bulinus, 225, 229, 230, 234,
238, 240, 242, 243, 251, 253-263,
265, 268, 270, 276-278
sericinus, Bulinus truncatus, 240
setacea, Bankia, 105
siliqua, Cyrtodaria,
siliqua, Ensis, 97
siliqua, Glycymeris, 32
simoterum, Etheostoma, 361
simplex, Anomia, 48, 52, 57, 60, 61,
69-71, 73, 85, 86, 89, 100
simplex ephippium, Anomia, 85
simpsoni, Adula, 77
sinuata, Lucina, 366, 382
sinuatus, Axinus, 366
sinuosa, Venus, 366, 382
smithae, Panope, 24, 25
Solecurtus, 10, 33
Solen, 97
gouldi, 97
Solenacea, 3
Solenidae, 97
solidissima, Spisula, 48, 53, 59-61,
69-73, 96, 97, 99
spengleri, Panomya, 18
Sphenia, 13, 16
binghami, 13
Spiratella, 121
helicina, 121
Spisula, 13, 48, 53, 59-67, 69-73, 96,
97, 99
elliptica, 99
solidissima,
96, 97, 99
subtruncata, 99
sportella, Haplotrema, 217
squama, Monia, 85
squamula, Anomia, 85
stagnalis, Lymnaea, 186, 188
staminea, Paphia, 91
steenstrupi, Myxophyllum, 212
Stenoglossa, 333
stictica, Mitra, 311, 312
Strangesta, 217, 218, 220, 223, 224
gawleri, 217, 218, 220, 223, 224
tumidula, 217, 218, 220, 223, 224
Streptaxacea, 217, 221

Streptaxidae, 221

1, 31-36, 41-44

48, 53, 59-61, 69-73,

439

Striatula, Venus, 91

striatus, Chlamys, 84

striatus, Pecten, 84

striatus, Tamias, 210

Strigatella, 295, 296, 299, 301-303,
306-308, 310-312, 314, 317-319,
321, 322, 327, 331, 333, 334,

340-342
auriculoides, 296
paupercula, 295, 296, 299, 301-303,

306-308, 311, 319, 331, 340-342
vetusa, 296
scutulata, 296
Stylommatophora, 199, 213-215
subcrenata, Anadara, “13
subteres, Proclio, 121
subtruncata, Spisula, 99
Succinea, 222
greeri, 222
gvosvenori, 222
hivasei, 222
horticola, 222
urbana, 222
Succineidae, 222
succinoides, Bulinus, 186, 188
suhmi, Galiteuthis, 402
sulcatoria, Mactra, 99
superba, Euphausia, 398
Swainsonia, 334
sybaritica, Acmaea,
sybaritica, Problacmaea,
291-294
Tagelus, 60
plebeius, 60
talpoides, Blarina brevicauda, 210
Tamias, 210
striatus, 210
Tapes, 91
proclivis, 91
semidecussata, 91
variegata, 91
Taonius, 403
pavo, 403
taurica, Ostrea, 88
Tectura, 287, 288, 290-294
rubella, 287, 288
virginea, 288
Tecturidae, 287, 288, 292-294
Tecturinae, 291, 292
Tellina, 48, 51, 53, 58, 60-67, 69-13,
88, 89, 91, 94, 95, 97, 103, 109,
366, 382, 384

287, 290, 292-294
287, 288,

440

agilis, 48, 51, 53, 58, 60, 61, 69-73,

88, 89, 91, 94, 95, 97, 103, 109
agilis tenera, 94
balaustria, 94
crassa, 94
donacina, 94

MALACOLOGIA

flexuosa, 365, 366, 368, 371, 376,
382, 384

gouldi, 384

gouldii, 382

inaequalis, 384

plana, 384

sarsi, 384
trisinuata, 365, 366, 388, 389
Thyasiridae, 365, 366, 368
Thyassira, 366
Thyatira, 366
thyroidus, Mesodon, 206
tigrinum, Pecten, 84
thomsoni, Teredo, 106
Toxoglossa, 322, 333
transversa, Anadara, 48, 51, 56, 60, 61,
69-73, 77
transversalis, Bulinus, 186
Trematoda, 225, 276-278
Tresus, 39
Trichobilharzia, 233
elvae, 233
physellae, 233
navalis, 48, 55, 60, 61, 69, 70, 72, trigonus, Bulinus, 239
73, 103, 105, 106 trigonus, Bulinus truncatus, 186, 190,
norwegica, 106 236
pedicellata, 106 trisinuata, Thyasiva, 365, 366, 388, 389
thomsoni, 106 trispinosa, Diacria, 135
tesselata, Testudinalia, 291 tropica, Physa, 178
Testudinalia, 287, 288, 290-294 tropicus, Bulinus, 141-143, 149, 151-182,
tesselata, 291 184-191, 195-198, 225-228, 230,
texana, Catinella, 222 234-237, 239-242, 244, 276
texanus, Nautilus, 408 truncata, Barnea, 46, 48, 51, 59-61,
Thala, 338 69-73
floridana, 338 truncata, Mya, 19, 101
Thecosomata, 126 truncatus, Bulinus, 141-143, 161, 164,
Thiatisa, 366 166-169, 171-173, 177, 179, 180,
Thiatyra, 366 186, 190, 191, 195-198, 225-230,
Thilea, 132 233-244, 246, 247, 251, 253-265,
inflata, 132 268, 270, 276-279
Thyarsiva, 366 truncatus, Bulinus truncatus, 190, 225,
Thyaseiva, 366 228, 230, 233, 234, 240, 243, 251,
Thyasira, 365, 366, 368-378, 380, 382, 253-263, 265, 268, 270, 276-279
384, 385, 388, 389 truncatus rohlfsi, Bulinus, 225, 228,
barbarensis, 382, 384 230, 234-236, 238, 240, 242, 243,
bisecta, 365, 366, 368-370, 372, 373, 251, 255, 258-261, 270, 276-279

fabula, 94

flexuosa, 366, 382, 384

juvenalis, 95
Tellinacea, 33
Tellinidae, 94
tenera, Tellina agilis, 94
tenta, Macoma, 60
Teuthowenia, 403

antarctica, 403
tenuicostatus, Pecten, 84
Terebridae, 335
Teredinidae, 37, 69, 105, 109,
Teredo, 48, 55, 60-66, 69, 70, 72, 73,

103, 105, 106

bartschi, 105

japonica, 105

megotara, 105

375, 377 5 truncatus sericinus, Bulinus, 240
bisecta omarui, 370 truncatus trigonus, Bulinus, 186, 190,
cygnus, 365, 368, 370, 371, 374 236

truncatus truncatus, Bulinus, 190, 225,
228, 230, 233, 234, 240, 243, 251,
253-263, 265, 268, 270, 276-279

disjuncta, 365, 366, 368-370, 372,
375, 377, 378, 380, 382, 385
excavata, 366

tumidula, Strangesta,

223, 224

Turbinellidae, 338
turgida, Panomya, 18

Turricula, 328

marginata, 328

Turridae, 338
ugandae, Bulinus,

ugandae, Bulinus globosus,

217, 218, 220,

INDEX, VOL. 11 441

235-237, 239

ulrichi, Enclimatoceras,
ulrichi, Hercoglossa,

ulrichi, Nautil:s,

408

407, 408, 410-413

408

Unionacea, 351, 363, 364

Unionidae, 351

Unguilinidae, 365, 367
222

urbana, Succinea,
Urosalpinx, 298
cinerea, 298

valdiviae, Procymbulia,

Vallisneria, 186

121

vancouverense, Haplotrema,

variabilis, Donax,

46, 48, 51, 53, 60,

239

217

61, 69-72, 90-92, 96, 109

variegata, Cardita,

variegata, Tapes,
Velpecula, 322
hedleyi, 322
Veneracea, 9
Veneridae, 91

91

veneriformis, Mactra,
Veneroidea, 365, 366

Venerupis, 91
philippinorm,
pullastra, 91

91

ventricosa, Cardita,

Venus, 91, 365, 366, 368, 382

bisecta, 365, 368

gallina, 91
ovata, 91

sinuosa, 366, 382

striatula, 91
venustus, Donax,

96

14

14

99

verconis, Peculator, 334
vermeta, Catinella, 222
veyreauxii, Physa, 178
Verticordidae, 368
Vexillidae, 295, 333-337, 340-342
Vexillinae, 333, 334
Vexillum, 296, 312, 313, 315, 319-322,
331, 333, 334, 337, 338
hebes, 296
luculentum, 296, 215, 219-322
plicarium, 315, 319-321, 331
vubiginosum, 312
Victaphanta, 217, 218, 220-224
atramentaria, 217, 218, 220-224
virens, Pila, 282
virginea, Tectura, 288
virginica, Crassostrea, 48, 52, 57, 60,
61, 69-73, 80, 81, 86, 100, 102, 103
virgula, Creseis, 122, 135
vittatus, Donax, 96
Viviparus, 281-283, 285, 286
bengalensis, 281-283, 285, 286
Voluta, 296, 321
paupercula, 296
plicaria, 321
Volutacea, 333, 334
Volutidae, 334, 335, 338
Volutomitra, 334
gvénlandica, 334
Volutomitridae, 295, 333-338, 340-342
Volutomitrinae, 334
Vulpecula, 328
biconica, 328
Zirfaea, 101
crispata, 101
zelandica, Panope, 24
zonata, Mitra, 296, 297
zuluensis, Bulinus, 141, 142, 151, 161,
162, 164, 168-173, 175-177,
179-182, 184, 189, 195-198
zuluensis, Physa, 179

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